Genetic variation in germination, growth, and survivorship of red maple in response to subambient through elevated atmospheric CO2

Genetic variation in plant response to atmospheric carbon dioxide (CO₂) may have influenced paleo‐vegetation dynamics and could determine how future elevated CO₂ drives plant evolution and ecosystem productivity. We established how levels of relatedness – the maternal family, population, and provenance – affect variation in the CO₂ response of a species. This 2‐year growth chamber experiment focused on the germination, growth, biomass allocation, and survivorship responses of Acer rubrum to four concentrations of CO₂: 180, 270, 360, and 600 μL L^?1– representing Pleistocene through potential future conditions. We found that all levels of relatedness interacted with CO₂ to contribute to variation in response. Germination responses to CO₂ varied among families and populations, growth responses depended on families and regions of origin, and survivorship responses to CO₂ were particularly affected by regional identities. Differences among geographic regions accounted for 23% of the variation in biomass response to CO₂. If seeds produced under subambient CO₂ conditions behave similarly, our results suggest that A. rubrum may have experienced strong selection on seedling survivorship at Pleistocene CO₂ levels. Further, this species may evolve in response to globally rising CO₂ so as to increase productivity above that experimentally observed today. Species responses to future atmospheric CO₂ and the accompanying biotic effects on the global carbon cycle will vary among families, populations, and provenances.     

Below-ground respiratory responses of sugar maple and red maple saplings to atmospheric CO2 enrichment and elevated air temperature

The research described in this paper represents a part of a much broader research project with the general objective of describing the effects of elevated [CO2] and temperature on tree growth, physiological processes, and ecosystem-level processes. The specific objective of this research was to examine the below-ground respiratory responses of sugar maple (Acer saccharum Marsh.) and red maple (Acer rubrum L.) seedlings to elevated atmospheric [CO2] and temperature. Red maple and sugar maple seedlings were planted in the ground in each of 12 open-top chambers and exposed from 1994 through 1997 to ambient air or air enriched with 30 Pa CO2,< in combination with ambient or elevated (+4 °C) air temperatures. Carbon dioxide efflux was measured around the base of the seedlings and from root-exclusion zones at intervals during 1995 and 1996 and early 1997. The CO2 efflux rates averaged 0.4 μmol CO2 m-2 s-1 in the root-exclusion zones and 0.75 μmol CO2 m-2 s-1 around the base of the seedlings. Mineral soil respiration in root-exclusion zones averaged 12% higher in the high temperature treatments than at ambient temperature, but was not affected by CO2 treatments. The fraction of total efflux attributable to root + rhizosphere respiration ranged from 14 to 61% in measurements made around red maple plants, and from 35 to 62% around sugar maple plants. Root respiration rates ranged from 0 to 0.94 μmol CO2 s-1 m-2 of soil surface in red maple and from 0 to 1.02 in sugar maple. In both 1995 and 1996 root respiration rates of red maple were highest in high-CO2 treatments and lowest in high temperature treatments. Specific red maple root respiration rates of excised roots from near the soil surface in 1996 were also highest under CO2 enrichment and lowest in high temperature treatments. In sugar maple the highest rates of CO2 efflux were from around the base of plants exposed to both high temperature and high-CO2, even though specific respiration rates were< lowest for this species under the high temperature and CO2 enrichment regime. In both species, patterns of response to treatments were similar in root respiration and root mass, indicating that the root respiration responses were due in part to differences in root mass. The results underscore the need for separating the processes occurring in the roots from those in the forest floor and mineral soil in order to increase our understanding of the effects of global climate change on carbon sequestration and cycling in the below-ground systems of forests.     

Nonlinearity of photosynthetic responses to growth in rising atmospheric CO2: an experimental and modelling study

Nonlinear responses of photosynthesis to the CO₂ concentration at which plants were grown (C_g) have been often reported in the literature. This study was designed to develop mechanistic understanding of the nonlinear responses with both experimental and modelling approaches. Soybean (Glycine max) was grown in five levels of C_g (280, 350, 525, 700, 1000 ppm) with either a high or low rate of nitrogen fertilization. When the rate of nitrogen fertilization was high, the photosynthetic rate measured at C_g was highest in plants from the 700 ppm CO₂ treatment. When the rate of nitrogen fertilization was low, little variation was observed in the photosynthetic rates of plants from the different treatments measured at their respective C_g. Measurements of CO₂-induced changes in mass-based leaf nitrogen concentration (n_m, an index of changes in biochemical processes) and leaf mass per unit area (h, an index of morphological properties) were used in a model and indicate that the nonlinearity of photosynthetic responses to C_g is largely determined by relative changes in photosynthetic sensitivity, biochemical downregulation, and morphological upregulation. In order to further understand the nonlinear responses, we compiled data from the literature on CO₂-induced changes in n_m and h. These compiled data indicate that h generally increases and n_m usually decreases with increasing C_g, but that the trajectories and magnitudes of the changes in h and n_m vary with species and growth environments. Integration of these variables (n_m and h) into a biochemically based model of photosynthesis enabled us to predict diverse responses of photosynthesis to C_g. Thus a general mechanism is suggested for the highly variable, nonlinear responses of photosynthesis to C_g reported in the literature.     

Effects of elevated ozone on CO2 uptake and leaf structure in sugar maple under two light environments

The interactive effects of ozone and light on leaf structure, carbon dioxide uptake and short-term carbon allocation of sugar maple ( Acer saccharum Marsh.) seedlings were examined using gas exchange measurements and ¹⁴C-macroautoradiographic techniques. Two-year-old sugar maple seedlings were fumigated from budbreak for 5 months with ambient or 3 × ambient ozone in open-top chambers, receiving either 35% (high light) or 15% (low light) of full sunlight. Ozone accelerated leaf senescence, and reduced net photosynthesis, ¹⁴CO₂ uptake and stomatal conductance, with the effects being most pronounced under low light. The proportion of intercellular space increased in leaves of seedlings grown under elevated ozone and low light, possibly enhancing the susceptibility of mesophyll cells to ozone by increasing the cumulative dose per mesophyll cell. Indeed, damage to spongy mesophyll cells in the elevated ozone × low light treatment was especially frequent. ¹⁴C macroautoradioraphy revealed heterogeneous uptake of ¹⁴CO₂ in well defined areole regions, suggesting patchy stomatal behaviour in all treatments. However, in seedlings grown under elevated ozone and low light, the highest ¹⁴CO₂ uptake occurred along larger veins, while interveinal regions exhibited little or no uptake. Although visible symptoms of ozone injury were not apparent in these seedlings, the cellular damage, reduced photosynthetic rates and reduced whole-leaf chlorophyll levels corroborate the visual scaling of whole-plant senescence, suggesting that the ozone × low light treatment accelerated senescence or senescence-like injury in sugar maple.     

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.     

Enriched atmospheric CO2 and defoliation: effects on tree chemistry and insect performance

We examined the effects of CO₂ and defoliation on tree chemistry and performance of the forest tent caterpillar, Malacosoma disstria. Quaking aspen (Populus tremuloides) and sugar maple (Acer saccharum) trees were grown in open-top chambers under ambient or elevated concentrations of CO₂. During the second year of growth, half of the trees were exposed to free-feeding forest tent caterpillars, while the remaining trees served as nondefoliated controls. Foliage was collected weekly for phytochemical analysis. Insect performance was evaluated on foliage from each of the treatments. At the sampling date coincident with insect bioassays, levels of foliar nitrogen and starch were lower and higher, respectively, in high CO₂ foliage, and this trend persisted throughout the study. CO₂-mediated increases in secondary compounds were observed for condensed tannins in aspen and gallotannins in maple. Defoliation reduced levels of water and nitrogen in aspen but had no effect on primary metabolites in maple. Similarly, defoliation induced accumulations of secondary compounds in aspen but not in maple. Larvae fed foliage from the enriched CO₂ or defoliated treatments exhibited reduced growth and food processing efficiencies, relative to larvae on ambient CO₂ or nondefoliated diets, but the patterns were host species-specific. Overall, CO₂ and defoliation appeared to exert independent effects on foliar chemistry and forest tent caterpillar performance.     

Photosynthesis and conductance of spring-wheat leaves: field response to continuous free-air atmospheric CO2 enrichment

Spring wheat was grown from emergence to grain maturity in two partial pressures of CO₂ (pCO₂): ambient air of nominally 37 Pa and air enriched with CO₂ to 55 Pa using a free-air CO₂ enrichment (FACE) apparatus. This experiment was the first of its kind to be conducted within a cereal field without the modifications or disturbance of microclimate and rooting environment that accompanied previous studies. It provided a unique opportunity to examine the hypothesis that continuous exposure of wheat to elevated pCO₂ will lead to acclimatory loss of photosynthetic capacity. The diurnal courses of photosynthesis and conductance for upper canopy leaves were followed throughout the development of the crop and compared to model-predicted rates of photosynthesis. The seasonal average of midday photosynthesis rates was 28% greater in plants exposed to elevated pCO₂ than in contols and the seasonal average of the daily integrals of photosynthesis was 21% greater in elevated pCO₂ than in ambient air. The mean conductance at midday was reduced by 36%. The observed enhancement of photosynthesis in elevated pCO₂ agreed closely with that predicted from a mechanistic biochemical model that assumed no acclimation of photosynthetic capacity. Measured values fell below predicted only in the flag leaves in the mid afternoon before the onset of grain-filling and over the whole diurnal course at the end of grain-filling. The loss of enhancement at this final stage was attributed to the earlier senescence of flag leaves in elevated pCO₂. In contrast to some controlled-environment and field-enclosure studies, this field-scale study of wheat using free-air CO₂ enrichment found little evidence of acclimatory loss of photosynthetic capacity with growth in elevated pCO₂ and a significant and substantial increase in leaf photosynthesis throughout the life of the crop.     

The response of two Glomus mycorrhizal fungi and a fine endophyte to elevated atmospheric CO2, soil warming and drought

Plantago lanceolata plants were grown under various environmental conditions in association with the mycorrhizal fungi Glomus mosseae, G. caledonium and a fine endophyte either individually or all together. Using a time‐course approach, we investigated the effects of elevated atmospheric CO₂ (eCO₂), soil warming and drought and their interactions on root length colonized (RLC) by mycorrhizal fungi and extraradical mycorrhizal hyphal (EMH) production. Plant growth responded as would be expected to the environmental manipulations. There was no plant growth‐independent effect of eCO₂ on mycorrhizal colonization; however, EMH production was stimulated by eCO₂, i.e. there was increased partitioning of below‐ground carbon to the EMH. Soil warming directly stimulated both percent RLC by the Glomus species and EMH density; soil warming did not affect RLC by the fine endophyte. Drought decreased percent RLC for the fine endophyte, but not for the Glomus species. The presence of one mycorrhizal fungus did not affect the response of another to the environmental variables. There was no evidence of any interactive effects of the environmental variables on RLC, but there were significant environmental interactions on EMH production. In particular, the stimulatory effects of eCO₂ and soil warming on EMH density were not additive. The results are discussed in terms of the soil carbon cycle, highlighting some crucial gaps in our knowledge. If future environmental changes affect mycorrhizal fungal turnover and respiration, then this could have important implications for the terrestrial carbon cycle.     

Respiratory responses of higher plants to atmospheric CO2 enrichment

Although the respiratory response of native and agricultural plants to atmospheric CO₂ enrichment has been reported over the past 75 years, only recently have these effects emerged as prominent measures of plant and ecosystem response to the earth's changing climate. In this review we discuss this rapidly expanding field of study and propose that both increasing and decreasing rates of leaf and whole-plant respiration are likely to occur in response to rising CO₂ concentrations. While the stimulatory effects of CO₂ on respiration are consistent with our knowledge of leaf carbohydrate status and plant metabolism, we wish to emphasize the rather surprising short-term inhibition of leaf respiration by elevated CO₂ and the reported effects of long-term CO₂ exposure on growth and maintenance respiration. As is being found in many studies, it is easier to document the respiratory response of higher plants to elevated CO₂ than it is to assign a mechanistic basis for the observed effects. Despite this gap in our understanding of how respiration is affected by CO₂ enrichment, data are sufficient to suggest that changes in leaf and whole-plant respiration may be important considerations in the carbon dynamics of terrestrial ecosystems as global CO₂ continues to rise. Suggestions for future research that would enable these and other effects of CO₂ on respiration to be unravelled are presented.     

Allocation responses to CO2 enrichment and defoliation by a native annual plant Heterotheca subaxillaris

Among plants grown under enriched atmospheric CO₂, root:shoot balance (RSB) theory predicts a proportionately greater allocation of assimilate to roots than among ambient‐grown plants. Conversely, defoliation, which decreases the plant's capacity to assimilate carbon, is predicted to increase allocation to shoot. We tested these RSB predictions, and whether responses to CO₂ enrichment were modified by defoliation, using Heterotheca subaxillaris, an annual plant native to south‐eastern USA. Plants were grown under near‐ambient (400 μmol mol^?1) and enriched (700 μmol mol^?1) levels of atmospheric CO₂. Defoliation consisted of the weekly removal of 25% of each new fully expanded, but not previously defoliated, leaf from either rosette or bolted plants. In addition to dry mass measurements of leaves, stems, and roots, Kjeldahl N, protein, starch and soluble sugars were analysed in these plant components to test the hypothesis that changes in C:N uptake ratio drive shifts in root:shoot ratio. Young, rapidly growing CO₂‐enriched plants conformed to the predictions of RSB, with higher root:shoot ratio than ambient‐grown plants (P < 0.02), whereas older, slower growing plants did not show a CO₂ effect on root:shoot ratio. Defoliation resulted in smaller plants, among which both root and shoot biomass were reduced, irrespective of CO₂ treatment (P < 0.03). However, H. subaxillaris plants were able to compensate for leaf area removal through flexible shoot allocation to more leaves vs. stem (P < 0.01). Increased carbon availability through CO₂ enrichment did not enhance the response to defoliation, apparently because of complete growth compensation for defoliation, even under ambient conditions. CO₂‐enriched plants had higher rates of photosynthesis (P < 0.0001), but this did not translate into increased final biomass accumulation. On the other hand, earlier and more abundant yield of flower biomass was an important consequence of growth under CO₂ enrichment.     

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.     

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.     

Changes in net photosynthesis and growth of Pinus eldarica seedlings in response to atmospheric CO2 enrichment

Pinus eldarica L. trees, rooted in the natural soil of an agricultural field at Phoenix, Arizona, were grown from the seedling stage in clear-plastic-wall open-top enclosures maintained at four different atmospheric CO₂ concentrations for 15 months. Light response functions were determined for one tree from each treatment by means of whole-tree net CO₂ exchange measurements at the end of this period, after which rates of carbon assimilation of an ambient-treatment tree were measured across a range of atmospheric CO₂ concentrations. The first of these data sets incorporates the consequences of both the CO₂-induced enhancement of net photosynthesis per unit needle area and the CO₂-induced enhancement of needle area itself (due primarily to the production of more needles), whereas the second data set reflects only the first of these effects. Hence the division of the normalized results of the first data set by the normalized results of the second set yields a representation of the increase in whole-tree net photosynthesis due to enhanced needle production caused by atmospheric CO₂ enrichment. In the solitary trees we studied, the relative contribution of this effect increased rapidly with the CO₂ concentration of the air to increase whole-tree net photosynthesis by nearly 50% at a CO₂ concentration approximately 300 μmol mol⁻¹ above ambient.