Elevated atmospheric CO2: effects on phytochemistry, insect performance and insect-parasitoid interactions

This study was conducted to examine the effects of CO₂-mediated changes in tree chemistry on the performance of the gypsy moth ((Lymantria dispar L.) and the parasitold Cotesia melanoscela (Ratz.). We used carbon-nutrient balance theory to develop hypotheses regarding changes in tree chemistry and the performance of both insects under elevated CO₂. As predicted, levels of foliar nitrogen declined and concentrations of carbon-based compounds (e.g. starch and phenolics) increased under elevated CO₂. Gypsy moth performance (e.g. growth, development) was altered by CO₂-mediated changes in foliar chemistry, but the magnitude was small and varied across tree species. Larvae feeding on high CO₂ aspen exhibited the largest reduction in performance, relative to larvae feeding on birch, oak, or maple. Parasitism by C. melanoscela significantly prolonged gypsy moth development and reduced growth rates. Overall, the effect of parasitism on gypsy moth performance did not differ between CO₂ treatments. Altered gypsy moth performance on high CO₂ foliage in turn affected parasitoid performance, but the response was variable: parasitoid mortality increased and adult female size declined slightly under high CO₂, while development time and adult male size were unaffected. Our results suggest that CO₂-induced changes in plant chemistry were buffered to the extent that effects on third trophic level interactions were weak to non-existent for the system examined in this study.     

Effects of elevated CO2 and temperature-grown red and sugar maple on gypsy moth performance

Few studies have investigated how tree species grown under elevated CO₂ and elevated temperature alter the performance of leaf‐feeding insects. The indirect effects of an elevated CO₂ concentration and temperature on leaf phytochemistry, along with potential direct effects on insect growth and consumption, may independently or interactively affect insects. To investigate this, we bagged larvae of the gypsy moth on leaves of red and sugar maple growing in open‐top chambers in four CO₂/temperature treatment combinations: (i) ambient temperature, ambient CO₂; (ii) ambient temperature, elevated CO₂ (+ 300 μL L^?1 CO₂); (iii) elevated temperature (+ 3.5°C), ambient CO₂; and (iv) elevated temperature, elevated CO₂. For both tree species, leaves grown at elevated CO₂ concentration were significantly reduced in leaf nitrogen concentration and increased in C: N ratio, while neither temperature nor its interaction with CO₂ concentration had any effect. Depending on the tree species, leaf water content declined (red maple) and carbon‐based phenolics increased (sugar maple) on plants grown in an enriched CO₂ atmosphere. The only observed effect of elevated temperature on leaf phytochemistry was a reduction in leaf water content of sugar maple leaves. Gypsy moth larval responses were dependent on tree species. Larvae feeding on elevated CO₂‐grown red maple leaves had reduced growth, while temperature had no effect on the growth or consumption of larvae. No significant effects of either temperature or CO₂ concentration were observed for larvae feeding on sugar maple leaves. Our data demonstrate strong effects of CO₂ enrichment on leaf phytochemical constituents important to folivorous insects, while an elevated temperature largely has little effect. We conclude that alterations in leaf chemistry due to an elevated CO₂ atmosphere are more important in this plant–folivorous insect system than either the direct short‐term effects of temperature on insect performance or its indirect effects on leaf chemistry.     

Leaf age effects of elevated CO2-grown white oak leaves on spring-feeding lepidopterans

Folivorous insect responses to elevated CO₂-grown tree species may be complicated by phytochemical changes as leaves age. For example, young expanding leaves in tree species may be less affected by enriched CO₂-alterations in leaf phytochemistry than older mature leaves due to shorter exposure times to elevated CO₂ atmospheres. This, in turn, could result in different effects on early vs. late instar larvae of herbivorous insects. To address this, seedlings of white oak (Quercus alba L.), grown in open-top chambers under ambient and elevated CO₂, were fed to two important early spring feeding herbivores; gypsy moth (Lymantria dispar L.), and forest tent caterpillar (Malacosoma disstria Hübner). Young, expanding leaves were presented to early instar larvae, and older fully expanded or mature leaves to late instar larvae. Young leaves had significantly lower leaf nitrogen content and significantly higher total nonstructural carbohydrate:nitrogen ratio as plant CO₂ concentration rose, while nonstructural carbohydrates and total carbon-based phenolics were unaffected by plant CO₂ treatment. These phytochemical changes contributed to a significant reduction in the growth rate of early instar gypsy moth larvae, while growth rates of forest tent caterpillar were unaffected. The differences in insect responses were attributed to an increase in the nitrogen utilization efficiency (NUE) of early instar forest tent caterpillar larvae feeding on elevated CO₂-grown leaves, while early instar gypsy moth larval NUE remained unchanged among the treatments. Later instar larvae of both insect species experienced larger reductions in foliage quality on elevated CO₂-grown leaves than earlier instars, as the carbohydrate:nitrogen ratio of leaves substantially increased. Despite this, neither insect species exhibited changes in growth or consumption rates between CO₂ treatments in the later instar. An increase in NUE was apparently responsible for offsetting reduced foliar nitrogen for the late instar larvae of both species.     

Soil CO2 efflux in a boreal pine forest under atmospheric CO2 enrichment and air warming

The response of forest soil CO₂ efflux to the elevation of two climatic factors, the atmospheric concentration of CO₂ (↑CO₂ of 700 μmol mol⁻¹) and air temperature (↑ T with average annual increase of 5°C), and their combination (↑CO₂+↑ T ) was investigated in a 4-year, full-factorial field experiment consisting of closed chambers built around 20-year-old Scots pines ( Pinus sylvestris L.) in the boreal zone of Finland. Mean soil CO₂ efflux in May–October increased with elevated CO₂ by 23–37%, with elevated temperature by 27–43%, and with the combined treatment by 35–59%. Temperature elevation was a significant factor in the combined 4-year efflux data, whereas the effect of elevated CO₂ was not as evident. Elevated temperature had the most pronounced impact early and late in the season, while the influence of elevated CO₂ alone was especially notable late in the season. Needle area was found to be a significant predictor of soil CO₂ efflux, particularly in August, a month of high root growth, thus supporting the assumption of a close link between whole-tree physiology and soil CO₂ emissions. The decrease in the temperature sensitivity of soil CO₂ efflux observed in the elevated temperature treatments in the second year nevertheless suggests the existence of soil response mechanisms that may be independent of the assimilating component of the forest ecosystem. In conclusion, elevated atmospheric CO₂ and air temperature consistently increased forest soil CO₂ efflux over the 4-year period, their combined effect being additive, with no apparent interaction.     

The relationship between leaf composition and morphology at elevated CO2 concentrations

The composition and morphology of leaves exposed to elevated [CO₂] usually change so that the leaf nitrogen (N) per unit dry mass decreases and the leaf dry mass per unit area increases. However, at ambient [CO₂], leaves with a high leaf dry mass per unit area usually have low leaf N per unit dry mass. Whether the changes in leaf properties induced by elevated [CO₂] follow the same overall pattern as that at ambient [CO₂] has not previously been addressed. Here we address this issue by using leaf measurements made at ambient [CO₂] to develop an empirical model of the composition and morphology of leaves. Predictions from that model are then compared with a global database of leaf measurements made at ambient [CO₂]. Those predictions are also compared with measurements showing the impact of elevated [CO₂]. In the empirical model both the leaf dry mass and liquid mass per unit area are positively correlated with leaf thickness, whereas the mass of C per unit dry mass and the mass of N per unit liquid mass are constant. Consequently, both the N:C ratio and the surface area:volume ratio of leaves are positively correlated with the liquid content. Predictions from that model were consistent with measurements of leaf properties made at ambient [CO₂] from around the world. The changes induced by elevated [CO₂] follow the same overall trajectory. It is concluded that elevated [CO₂] enhances the rate at which dry matter is accumulated but the overall trajectory of leaf development is conserved.     

Water savings in mature deciduous forest trees under elevated CO2

Stomatal conductance of plants exposed to elevated CO₂ is often reduced. Whether this leads to water savings in tall forest‐trees under future CO₂ concentrations is largely unknown but could have significant implications for climate and hydrology. We used three different sets of measurements (sap flow, soil moisture and canopy temperature) to quantify potential water savings under elevated CO₂ in a ca. 35 m tall, ca. 100 years old mixed deciduous forest. Part of the forest canopy was exposed to 540 ppm CO₂ during daylight hours using free air CO₂ enrichment (FACE) and the Swiss Canopy Crane (SCC). Across species and a wide range of weather conditions, sap flow was reduced by 14% in trees subjected to elevated CO₂, yielding ca. 10% reduction in evapotranspiration. This signal is likely to diminish as atmospheric feedback through reduced moistening of the air comes into play at landscape scale. Vapour pressure deficit (VPD)‐sap flow response curves show that the CO₂ effect is greatest at low VPD, and that sap flow saturation tends to occur at lower VPD in CO₂‐treated trees. Matching stomatal response data, the CO₂ effect was largely produced by Carpinus and Fagus, with Quercus contributing little. In line with these findings, soil moisture at 10 cm depth decreased at a slower rate under high‐CO₂ trees than under control trees during rainless periods, with a reversal of this trend during prolonged drought when CO₂‐treated trees take advantage from initial water savings. High‐resolution thermal images taken at different heights above the forest canopy did detect reduced water loss through altered energy balance only at <5 m distance (0.44 K leaf warming of CO₂‐treated Fagus trees). Short discontinuations of CO₂ supply during morning hours had no measurable canopy temperature effects, most likely because the stomatal effects were small compared with the aerodynamic constraints in these dense, broad‐leaved canopies. Hence, on a seasonal basis, these data suggest a <10% reduction in water consumption in this type of forest when the atmosphere reaches 540% ppm CO₂.     

Effects of elevated CO2 on the chrysanthemum leaf-miner, Chromatomyia syngenesiae: a greenhouse study

Although feeding behaviour of Chromatomyia syngenesiae on plants grown in elevated CO₂ (ambient + 200ppm) was unaffected, leaf-miner development was slower in elevated compared to ambient CO₂ atmospheres. Pupal weight was lower at high CO₂ and correlated with the area of leaf mined; no such correlation existed in ambient CO₂. There appears to be no compensatory feeding by the leaf-miner for the reduced food quality of plants growing in elevated CO₂. The implications of these findings are discussed.     

Modifications of the leaf surface structures of Quercus ilex L. in open, naturally CO2-enriched environments

Two Italian CO₂ springs allowed us to study the long-term effect of a 350–2600 μ mol mol^–1 increase in CO₂ concentrations on the surface structures of leaves of Quercus ilex L. Carbon dioxide increased the quantity of cuticular waxes, above an apparent threshold of 750 μ mol mol^–1 CO₂. Leaf wettability was not modified by CO₂ concentrations. Reduction in stomatal frequency was observable up to 750 μ mol mol^–1 CO₂, the slope being almost the same as that estimated for the increase in CO₂ concentration from pre-industrial times to the present. At higher concentrations, CO₂ seemed to exert no more impact on stomatal frequency.     

Influence of atmospheric CO2 enrichment on methane consumption in a temperate forest soil

Rates of atmospheric CH₄ consumption of soils in temperate forest were compared in plots continuously enriched with CO₂ at 200 µL L^?1 above ambient and in control plots exposed to the ambient atmosphere of 360 µL CO₂ L^?1. The purpose was to determine if ecosystem atmospheric CO₂ enrichment would alter soil microbial CH₄ consumption at the forest floor and if the effect of CO₂ would change with time or with environmental conditions. Reduced CH₄ consumption was observed in CO₂‐enriched plots relative to control plots on 46 out of 48 sampling dates, such that CO₂‐enriched plots showed annual reductions in CH₄ consumption of 16% in 1998 and 30% in 1999. No significant differences were observed in soil moisture, temperature, pH, inorganic‐N or rates of N‐mineralization between CO₂‐enriched and control plots, indicating that differences in CH₄ consumption between treatments were likely the result of changes in the composition or size of the CH₄‐oxidizing microbial community. A repeated measures analysis of variance that included soil moisture, soil temperature (from 0 to 30 cm), and time as covariates indicated that the reduction of CH₄ consumption under elevated CO₂ was enhanced at higher soil temperatures. Additionally, the effect of elevated CO₂ on CH₄ consumption increased with time during the two‐year study. Overall, these data suggest that rising atmospheric CO₂ will reduce atmospheric CH₄ consumption in temperate forests and that the effect will be greater in warmer climates. A 30% reduction in atmospheric CH₄ consumption by temperate forest soils in response to rising atmospheric CO₂ will result in a 10% reduction in the sink strength of temperate forest soils in the atmospheric CH₄ budget and a positive feedback to the greenhouse effect.     

Interactive effects of elevated CO2 and temperature on the leaf-miner Dialectica scalariella Zeller (Lepidoptera: Gracillariidae) in Paterson's Curse, Echium plantagineum (Boraginaceae)

Doubling of the current atmospheric CO₂ concentration, and an increase in global mean annual temperatures of 1.5–6 °C, have been predicted to occur by the end of this century. Whilst the separate effects of CO₂ and temperature on plant–insect interactions have been examined in a number of studies, few have investigated their combined impact. We carried out a factorial experiment to explore the effect of a doubling of CO₂ concentration and a 3 °C temperature increase on the development of a complete generation of the leaf‐miner, Dialectica scalariella, in the host plant Paterson's Curse, Echium plantagineum. Elevated CO₂ increased biomass, reduced leaf N and increased C:N ratios in the host plants. Leaf thickness also increased under elevated CO₂, but only in the high‐temperature treatment. Female D. scalariella did not discriminate between plants grown at the different CO₂ levels when ovipositing, despite the reduction in foliage quality under elevated CO₂. Overall, the negative response of D. scalariella to elevated CO₂ was greater than for many species of free‐living insects, presumably because of the limited mobility imposed by the leaf‐mining habit. Development was accelerated at the high temperature and slowed under elevated CO₂. The net result was a reduction in development time of ～14 days in the elevated CO₂/high temperature treatment, compared to the ambient CO₂/low temperature treatment. Larval survivorship and adult moth weight were both affected by a significant interaction between CO₂ and temperature. At the low temperature, CO₂ had little effect on survivorship, but at the high temperature, survivorship was significantly reduced under elevated CO₂. Similarly, elevated CO₂ had a stronger negative effect on adult moth weight when combined with the high‐temperature treatment. A possible explanation for these results is that the high temperature accelerated insect development to such an extent that the larvae did not have sufficient feeding time to compensate for the poorer quality of the foliage. The frequency with which interactions between CO₂ and temperature affected both plant and insect performance in this study highlights the need for caution when predicting the effects of future climate change on plant–insect interactions from single‐factor experiments.     

Elevated atmospheric CO2 lowers herbivore abundance, but increases leaf abscission rates

Increased levels of atmospheric carbon dioxide (CO₂) are likely to affect the trophic relationships that exist between plants, their herbivores and the herbivores' natural enemies. This study takes advantage of an open‐top CO₂ fertilization experiment in a Florida scrub oak community at Kennedy Space Center, Florida, consisting of eight chambers supplied with ambient CO₂ (360 ppm) and eight chambers supplied with elevated CO₂ (710 ppm). We examined the effects of elevated CO₂ on herbivore densities and levels of leaf consumption, rates of herbivore attack by natural enemies and effects on leaf abscission. Cumulative levels of herbivores and herbivore damage were significantly lower in elevated CO₂ than in ambient CO₂. This may be because leaf nitrogen levels are lower in elevated CO₂. More herbivores die of host plant‐induced death in elevated CO₂ than in ambient CO₂. Attack rates of herbivores by parasitoids are also higher in elevated CO₂, possibly because herbivores need to feed for a longer time in order to accrue sufficient nitrogen (N), thus exposing themselves longer to natural enemies. Insect herbivores cause an increase in abscission rates of leaves throughout the year. Because of the lower insect density in elevated CO₂, we thought, abscission rates would be lower in these chambers. However, abscission rates were significantly higher in elevated CO₂. Thus, the direct effects of elevated CO₂ on abscission are greater than the indirect effects on abscission mediated via lower insect densities. A consequence of increased leaf abscission in elevated CO₂ is that nutrient deposition rates to the soil surface are accelerated.     

CO2 and O3 effects on host plant preferences of the forest tent caterpillar (Malacosoma disstria)

Elevated levels of CO₂ and O₃ affect plant growth and phytochemistry, which in turn can alter physiological performance of associated herbivores. Little is known, however, about how generalist insect herbivores respond behaviorally to CO₂‐ and O₃‐mediated changes in their host plants. This research examined the effects of elevated CO₂ and O₃ levels on host plant preferences and consumption of forest tent caterpillar (FTC, Malacosoma disstria Hbn.) larvae. Dual choice feeding assays were performed with foliage from birch (Betula papyrifera Marsh.) and aspen (Populus tremuloides Michx., genotypes 216 and 259). Trees were grown at the Aspen Free Air CO₂ Enrichment (FACE) facility near Rhinelander, WI, USA, and had been exposed to ambient or elevated concentrations of CO₂ and/or O₃. Levels of nutritional and secondary compounds were quantified through phytochemical analyses. The results showed that elevated O₃ levels increased FTC larval preferences for birch compared with aspen, whereas elevated CO₂ levels had the opposite effect. In assays with the two aspen genotypes, addition of both CO₂ and O₃ caused a shift in feeding preferences from genotype 259 to genotype 216. Consumption was unaffected by experimental treatments in assays comparing aspen and birch, but were increased for larvae given high O₃ foliage in the aspen genotype assays. Elevated levels of CO₂ and O₃ altered tree phytochemistry, but did not explain shifts in feeding preferences. The results demonstrate that increased levels of CO₂ and O₃ can alter insect host plant preferences both between and within tree species. Also, consequences of altered host quality (e.g., compensatory consumption) may be buffered by partial host shifts in situations when alternative plant species are available. Environmentally induced changes in host plant preferences may have the potential to alter the distribution of herbivory across plant genotypes and species, as well as competitive interactions among them.     

Effects of elevated CO2 and/or O3 on growth, development and physiology of wheat (Triticum aestivum L.)

Two cultivars of spring wheat (Triticum aestivum L. cvs. Alexandria and Hanno) and three cultivars of winter wheat (cvs. Riband, Mercia and Haven) were grown at two concentrations of CO₂ [ambient (355 pmol mol^?1) and elevated (708 μmol mol^?1)] under two O₃ regimes [clean air (< 5 nmol mol^?1 O₃) and polluted air (15 nmol mol^?1 O₃ at night rising to a midday maximum of 75 nmol mol^?1)] in a phytotron at the University of Newcastle-upon-Tyne. Between the two-leaf stage and anthesis, measurements of leaf gas-exchange, non-structural carbohydrate content, visible O₃ damage, growth, dry matter partitioning, yield components and root development were made in order to examine responses to elevated CO₂ and/or O₃. Growth at elevated CO₂ resulted in a sustained increase in the rate of CO₂ assimilation, but after roughly 6 weeks' exposure there was evidence of a slight decline in the photosynthetic rate (c.-15%) measured under growth conditions which was most pronounced in the winter cultivars. Enhanced rates of CO₂ assimilation were accompanied by a decrease in stomatal conductance which improved the instantaneous water use efficiency of individual leaves. CO₂ enrichment stimulated shoot and root growth to an equivalent extent, and increased tillering and yield components, however, non-structural carbohydrates still accumulated in source leaves. In contrast, long-term exposure to O₃ resulted in a decreased CO₂ assimilation rate (c. -13%), partial stomatal closure, and the accumulation of fructan and starch in leaves in the light. These effects were manifested in decreased rates of shoot and root growth, with root growth more severely affected than shoot growth. In the combined treatment growth of O₃-treated plants was enhanced by elevated CO₂, but there was little evidence that CO₂ enrichment afforded additional protection against O₃ damage. The reduction in growth induced by O₃ at elevated CO₂ was similar to that induced by O₃ at ambient CO₂ despite additive effects of the individual gases on stomatal conductance that would be expected to reduce the O₃ flux by 20%, and also CO₂-induced increases in the provision of substrates for detoxification and repair processes. These observations suggest that CO₂ enrichment may render plants more susceptible to O₃ damage at the cellular level. Possible mechanisms are discussed.     

Changes in needle quality and larch bud moth performance in response to CO2 enrichment and defoliation of treeline larches

Abstract. 1. It is hypothesised that the larch bud moth cycle is controlled by host‐tree foliage quality. In a Free Air CO₂ Enrichment (FACE) experiment at the Swiss alpine treeline (2180 m a.s.l.), the effects of elevated CO₂ and previous year defoliation on needle quality of larch and the performance of the larch bud moth were investigated. 2. Starch and lignin concentrations increased and water content decreased in elevated CO₂‐grown needles compared with ambient CO₂ concentration. Defoliation resulted in reduced N, water, starch, and sugar concentrations in needles of the next year generation. No interactions between elevated CO₂ and defoliation on needle quality were observed. 3. Needle quality changes due to needle maturation over the course of the experiment, however, were much larger than the effects of elevated CO₂ and defoliation. For example, N concentration was on average 38% lower and lignin concentration 55% higher at the end of the experiment (early July 2003) than at the beginning (mid June 2003). 4. On non‐defoliated trees, larch bud moth larvae grew somewhat more slowly under elevated CO₂ compared with ambient CO₂ concentration. If, however, trees had been defoliated, this response was reversed, with a faster growth of larch bud moth on high CO₂‐exposed trees than on control trees. Pupal weight was not affected by either CO₂ treatment or defoliation. 5. These results suggest that the larch bud moth has to cope with large changes in food quality due to needle maturation during its development, and that additional CO₂‐ and defoliation‐induced alterations in needle chemistry have comparatively minor influences on larch bud moth performance at the treeline.