Brian J. Kopper

Altered performance of forest pests under atmospheres enriched by CO2 and O3

Human activity causes increasing background concentrations of the greenhouse gases CO2 and O3. Increased levels of CO2 can be found in all terrestrial ecosystems. Damaging O3 concentrations currently occur over 29% of the worlds temperate and subpolar forests but are predicted to affect fully 60% by 2100 (ref. 3). Although individual effects of CO2 and O3 on vegetation have been widely investigated, very little is known about their interaction, and long-term studies on mature trees and higher trophic levels are extremely rare. Here we present evidence from the most widely distributed North American tree species, Populus tremuloides, showing that CO2 and O3, singly and in combination, affected productivity, physical and chemical leaf defences and, because of changes in plant quality, insect and disease populations. Our data show that feedbacks to plant growth from changes induced by CO2 and O3 in plant quality and pest performance are likely. Assessments of global change effects on forest ecosystems must therefore consider the interacting effects of CO2 and O3 on plant performance, as well as the implications of increased pest activity.

Consequences of elevated carbon dioxide and ozone for foliar chemical composition and dynamics in trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera).

Atmospheric chemical composition affects foliar chemical composition, which in turn influences the dynamics of both herbivory and decomposition in ecosystems. We assessed the independent and interactive effects of CO2 and O3 fumigation on foliar chemistry of quaking aspen (Populus tremuloides) and paper birch (Betula papyrifera) at a Free-Air CO2 Enrichment (FACE) facility in northern Wisconsin. Leaf samples were collected at five time periods during a single growing season, and analyzed for nitrogen. starch and condensed tannin concentrations, nitrogen resorption efficiencies (NREs), and C:N ratios. Enriched CO2 reduced foliar nitrogen concentrations in aspen and birch; O3 only marginally reduced nitrogen concentrations. NREs were unaffected by pollution treatment in aspen, declined with 03 exposure in birch, and this decline was ameliorated by enriched CO2. C:N ratios of abscised leaves increased in response to enriched CO2 in both tree species. O3 did not significantly alter C:N ratios in aspen, although values tended to be higher in + CO2 + O3 leaves. For birch, O3 decreased C:N ratios under ambient CO2 and increased C:N ratios under elevated CO2. Thus, under the combined pollutants, the C:N ratios of both aspen and birch leaves were elevated above the averaged responses to the individual and independent trace gas treatments. Starch concentrations were largely unresponsive to CO2 and O3 treatments in aspen. but increased in response to elevated CO2 in birch. Levels of condensed tannins were negligibly affected by CO2 and O3 treatments in aspen, but increased in response to enriched CO2 in birch. Results from this work suggest that changes in foliar chemical composition elicited by enriched CO2 are likely to impact herbivory and decomposition, whereas the effects of O3 are likely to be minor, except in cases where they influence plant response to CO2.

Effects of Diterpene Acids on Components of a Conifer Bark Beetle–Fungal Interaction: Tolerance by Ips pini and Sensitivity by Its Associate Ophiostoma ips

Abstract Conifer resin and phloem tissue contain several phytochemical groups, composed primarily of monoterpenes, diterpene acids, and stilbene phenolics. The effects of monoterpenes and phenolics on stem-colonizing bark beetles and their associated microorganisms have been studied to some extent, but the roles of diterpene acids are largely unknown. Diterpene acids are known to have substantial feeding deterrent and growth inhibiting effects on a variety of insect groups and are known to inhibit a variety of fungi. We tested three diterpene acids present in red pine, Pinus resinosa, at various concentrations, on several life history components of the bark beetle Ips pini and the fungus Ophiostoma ips. No diterpene acid affected the host acceptance behavior or larval survival of Ips pini. In contrast, abietic acid and isopimaric acid strongly inhibited spore germination of O. ips, and abietic acid strongly inhibited mycelial growth. The levels of inhibition observed were higher than with any previous assays of monoterpenes or phenolics in this system. These results support the view that conifer defenses against bark beetle–fungal complexes are multifaceted, with all three phytochemical groups being important to P. resinosa, but each with varying relative activity against the beetles and fungi.

Responses of trembling aspen (Populus tremuloides) phytochemistry and aspen blotch leafminer (Phyllonorycter tremuloidiella) performance to elevated levels of atmospheric CO2 and O3

1 This research was conducted at the Aspen FACE (Free Air CO2 Enrichment) site located in northern Wisconsin, U.S.A. where trembling aspen (Populus tremuloides Michaux) trees were exposed to one of four atmospheric treatments: elevated carbon dioxide (CO2; 560 µL/L), elevated ozone (O3; ambient × 1.5), elevated CO2 and O3, or ambient air. We evaluated the effects of these fumigants on aspen foliar quality and the performance of aspen blotch leafminer (Phyllonorycter tremuloidiella Braun).

Components of Antagonism and Mutualism in Ips pini–Fungal Interactions: Relationship to a Life History of Colonizing Highly Stressed and Dead Trees

Abstract Efforts to describe the complex relationships between bark beetles and the ophiostomatoid (stain) fungi they transport have largely resulted in a dichotomous classification. These symbioses have been viewed as either mutualistic (i.e., fungi help bark beetles colonize living trees by overcoming tree defenses or by providing nutrients after colonization in return for transport to a host) or antagonistic (i.e., fungi compete for a limited resource and reduce brood development with no apparent benefit to the beetle). We investigated several components of one beetle–fungus interaction. Specifically, we addressed whether beetle entry into, and development within, a host tree vary with the degree of colonization by ophiostomatoid fungi. Ips pini (Say) transports several species of ophiostomatoid fungi, the most common being Ophiostoma ips (Rumbold) Nannfeldt, in the process of colonizing its host, Pinus resinosa Aitman. We introduced this fungus 0, 3, 7, and 10 d before beetle entry to characterize its effects on I. pini colonization and development. This sequence allowed quantification of temporal effects and comparison of results with other systems. Fungal growth was greatest when inoculated before beetle colonization. Fungal colonization reduced beetle entry into logs, but increased brood production. Mate capture was not significantly affected by fungal growth. The benefits imparted by O. ips to its beetle vector during brood development are compared with results from other systems. This difference may in part be related to the exploitation of highly stressed and dead trees, rather than vigorous hosts, by I. pini.

Co2 and O3 Effects on Paper Birch (Betulaceae: Betula papyrifera) Phytochemistry and Whitemarked Tussock Moth (Lymantriidae: Orgyia leucostigma) Performance

Abstract Elevated atmospheric concentrations of CO2 and O3 are known to alter the chemical composition of foliage, which in turn may affect the performance of herbivorous insects. We investigated the independent and interactive effects of CO2 and O3 on foliar quality of paper birch (Betula papyrifera Marshall) and the consequences of chemical changes for performance of the whitemarked tussock moth Orgyia leucostigma (J. E. Smith). The experimental design was a 2 by 2 factorial, with ambient and elevated levels of CO2 and O3, respectively. Foliage was analyzed for concentrations of nitrogen, starch, and condensed tannins. CO2 and O3 independently and interactively affected nitrogen concentrations, with the elevated CO2 + O3 treatment reducing nitrogen concentrations more than either treatment alone. Elevated CO2 and O3 had no significant effect on starch and tannin concentrations when administered alone but increased starch concentrations by 17% over ambient when administered together. Larvae were reared on experimental trees from egg hatch through pupation to determine treatment effects on development time and pupal mass. Larval performance measures were not statistically different among fumigation treatments, although females tended to have reduced pupal mass under the elevated CO2 + O3 treatment. These results demonstrate that chemical responses of some plant species to elevated levels of CO2 (560 μl L−1) and O3 (1.5 × ambient) may be of insufficient magnitude to significantly alter standard measures of individual insect performance.

Effects of Paper Birch Condensed Tannin on Whitemarked Tussock Moth (Lepidoptera: Lymantriidae) Performance

Abstract This research tested the effects of paper birch, Betula papyrifera Marshall, condensed tannin on larval performance of the whitemarked tussock moth, Orgyia leucostigma (J. E. Smith). We conducted laboratory bioassays on fifth stadium larvae. Larvae were reared on one of three diets: control (no condensed tannin), moderate condensed tannin (8.8% dry mass), and high condensed tannin (17.6% dry mass). Although survivorship was not different between the treatments, larvae fed diets amended with condensed tannin exhibited increased stadium duration, decreased relative growth rate, and decreased food conversion efficiencies. Prolonged development times enabled larvae to compensate for low consumption and growth rates such that insects on tannin diets ate more and grew larger than insects on the control diet. Analysis of tannin levels in food, frass, and body tissue indicated that larvae do not metabolize condensed tannin, but concentrate and egest it. Our results show that paper birch condensed tannin has both positive and negative effects on the performance indices of whitemarked tussock moths. However, whether the benefits of increased final size (and possibly fecundity) outweigh the risks of increased development time and prolonged exposure to natural enemies remains unclear.

Response of quaking aspen genotypes to enriched CO2: foliar chemistry and tussock moth performance

Abstract 1 Genetic variation in the phytochemical responses of plants to CO2 enrichment is likely to alter trophic dynamics, and to shift intraspecific selection pressures on plant populations. We evaluated the independent and interactive effects of atmospheric CO2 and quaking aspen (Populus tremuloides Michx.) genotype on chemical composition of foliage and performance of the whitemarked tussock moth (Orgyia leucostigma J. E. Sm.). 2 This research was conducted at the Aspen FACE (Free Air CO2 Enrichment) site in northern Wisconsin, U.S.A. Leaf samples were collected periodically from each of three genetically variable aspen genotypes growing under ambient and elevated CO2, and analysed for levels of primary and secondary metabolites. Tussock moth larvae were reared in situ on experimental trees, and development times and pupal masses were recorded. 3 Foliar chemical composition varied among aspen genotypes and in response to CO2 enrichment. However, chemical responses of trees to elevated CO2 were generally consistent across genotypes. 4 Larval development times varied among host genotypes and increased slightly for insects on high‐CO2 plants. Enriched CO2 tended to reduce insect pupal masses, particularly for females on one of the three aspen genotypes. 5 CO2 × genotype interactions observed for plant chemistry and insect performance in this study with a small number of genotypes are probably too few, and too weak, to shift selection pressures in aspen populations. These results differ, however, from earlier work in which more substantial CO2 × genotype interactions were observed for plant chemistry.

Rapid Analysis of Abietanes in Conifers

Diterpene resin acids are major constituents of conifer oleoresin and play important roles in tree defense against insects and microbial pathogens. The tricyclic C-20 carboxylic acids are generally classified into two groups, the abietanes and the pimaranes. The abietanes have conjugated double bonds and exhibit characteristic UV spectra. Here, we report the analysis of abietanes by reversed-phase high-performance liquid chromatography using multiwavelength detection to optimize quantification of underivatized abietic, neoabietic, palustric, levopimaric, and dehydroabietic acids. The utility of the method is demonstrated with methanol extracts of white spruce (Picea glauca) phloem, and representative concentrations are reported.

Contrasting Patterns of Diterpene Acid Induction by Red Pine and White Spruce to Simulated Bark Beetle Attack, and Interspecific Differences in Sensitivity Among Fungal Associates

Conifers possess a suite of physiochemical defenses that protect their subcortical tissues from bark beetle - fungal complexes. These defenses include rapid induction of terpenoids and phenolics at the site of attack. Studies of the distribution, induction, and bioactivity of conifer terpenoids have focused heavily on monoterpenes. We assessed induction of diterpene acids in white spruce (Picea glauca) and red pine (Pinus resinosa) to fungal associates of two bark beetles, and the responses of four spruce beetle (Dendroctonus rufipennis)—associated fungi to three diterpene acids. Constitutive phloem contents differed between species, in that red pine had extremely low concentrations of diterpene acids, whereas white spruce had substantial constitutive levels. Induction differed quantitatively. Both red pine and white spruce exhibited marked increases, but red pine underwent greater increases and achieved higher concentrations than white spruce. Induction also differed qualitatively in that red pine showed lower diversity and fewer compositional changes during induction than white spruce. In red pine,fungal inoculation accompanying wounding elicited greater increases than wounding alone, but in white spruce total concentrations were higher following wounding alone. Spruce beetle fungal symbiont growth varied among species and compounds. Some diterpenes elicited both stimulatory and inhibitory effects on fungi, depending on concentration. All four fungi exhibited higher tolerances compared to those associated with pine bark beetles in previous studies. Variation in tolerances to, and potentially metabolism of, diterpene acids by symbionts may reflect differences in constitutive levels between spruce and pine, and partially explain differences in concentrations achieved during induction.