Inter-annual changes in detritus-based food chains can enhance plant growth response to elevated atmospheric CO2.

Elevated atmospheric CO2 generally enhances plant growth, but the magnitude of the effects depend, in part, on nutrient availability and plant photosynthetic pathway. Due to their pivotal role in nutrient cycling, changes in abundance of detritivores could influence the effects of elevated atmospheric CO2 on essential ecosystem processes, such as decomposition and primary production. We conducted a field survey and a microcosm experiment to test the influence of changes in detritus-based food chains on litter mass loss and plant growth response to elevated atmospheric CO2 using two wetland plants: a C3 sedge (Scirpus olneyi) and a C4 grass (Spartina patens). Our field study revealed that organism's sensitivity to climate increased with trophic level resulting in strong inter-annual variation in detritus-based food chain length. Our microcosm experiment demonstrated that increased detritivore abundance could not only enhance decomposition rates, but also enhance plant growth of S. olneyi in elevated atmospheric CO2 conditions. In contrast, we found no evidence that changes in the detritus-based food chains influenced the growth of S. patens. Considered together, these results emphasize the importance of approaches that unite traditionally subdivided food web compartments and plant physiological processes to understand inter-annual variation in plant production response to elevated atmospheric CO2.

Rising sea level, temperature, and precipitation impact plant and ecosystem responses to elevated CO2 on a Chesapeake Bay wetland: review of a 28-year study.

An ongoing field study of the effects of elevated atmospheric CO2 on a brackish wetland on Chesapeake Bay, started in 1987, is unique as the longest continually running investigation of the effects of elevated CO2 on an ecosystem. Since the beginning of the study, atmospheric CO2 increased 18%, sea level rose 20 cm, and growing season temperature varied with approximately the same range as predicted for global warming in the 21st century. This review looks back at this study for clues about how the effects of rising sea level, temperature, and precipitation interact with high atmospheric CO2 to alter the physiology of C3 and C4 photosynthetic species, carbon assimilation, evapotranspiration, plant and ecosystem nitrogen, and distribution of plant communities in this brackish wetland. Rising sea level caused a shift to higher elevations in the Scirpus olneyi C3 populations on the wetland, displacing the Spartina patens C4 populations. Elevated CO2 stimulated carbon assimilation in the Scirpus C3 species measured by increased shoot and root density and biomass, net ecosystem production, dissolved organic and inorganic carbon, and methane production. But elevated CO2 also decreased biomass of the grass, S. patens C4. The elevated CO2 treatment reduced tissue nitrogen concentration in shoots, roots, and total canopy nitrogen, which was associated with reduced ecosystem respiration. Net ecosystem production was mediated by precipitation through soil salinity: high salinity reduced the CO2 effect on net ecosystem production, which was zero in years of severe drought. The elevated CO2 stimulation of shoot density in the Scirpus C3 species was sustained throughout the 28 years of the study. Results from this study suggest that rising CO2 can add substantial amounts of carbon to ecosystems through stimulation of carbon assimilation, increased root exudates to supply nitrogen fixation, reduced dark respiration, and improved water and nitrogen use efficiency.

Fire, hurricane and carbon dioxide: effects on net primary production of a subtropical woodland.

Disturbance affects most terrestrial ecosystems and has the potential to shape their responses to chronic environmental change. Scrub-oak vegetation regenerating from fire disturbance in subtropical Florida was exposed to experimentally elevated carbon dioxide (CO2) concentration (+350 µl l(-1)) using open-top chambers for 11 yr, punctuated by hurricane disturbance in year 8. Here, we report the effects of elevated CO2 on aboveground and belowground net primary productivity (NPP) and nitrogen (N) cycling during this experiment. The stimulation of NPP and N uptake by elevated CO2 peaked within 2 yr after disturbance by fire and hurricane, when soil nutrient availability was high. The stimulation subsequently declined and disappeared, coincident with low soil nutrient availability and with a CO2 -induced reduction in the N concentration of oak stems. These findings show that strong growth responses to elevated CO2 can be transient, are consistent with a progressively limited response to elevated CO2 interrupted by disturbance, and illustrate the importance of biogeochemical responses to extreme events in modulating ecosystem responses to global environmental change.

The effects of 11 yr of CO2 enrichment on roots in a Florida scrub-oak ecosystem.

Uncertainty surrounds belowground plant responses to rising atmospheric CO2 because roots are difficult to measure, requiring frequent monitoring as a result of fine root dynamics and long-term monitoring as a result of sensitivity to resource availability. We report belowground plant responses of a scrub-oak ecosystem in Florida exposed to 11 yr of elevated atmospheric CO2 using open-top chambers. We measured fine root production, turnover and biomass using minirhizotrons, coarse root biomass using ground-penetrating radar and total root biomass using soil cores. Total root biomass was greater in elevated than in ambient plots, and the absolute difference was larger than the difference aboveground. Fine root biomass fluctuated by more than a factor of two, with no unidirectional temporal trend, whereas leaf biomass accumulated monotonically. Strong increases in fine root biomass with elevated CO2 occurred after fire and hurricane disturbance. Leaf biomass also exhibited stronger responses following hurricanes. Responses after fire and hurricanes suggest that disturbance promotes the growth responses of plants to elevated CO2. Increased resource availability associated with disturbance (nutrients, water, space) may facilitate greater responses of roots to elevated CO2. The disappearance of responses in fine roots suggests limits on the capacity of root systems to respond to CO2 enrichment.

Direct and indirect effects of elevated atmospheric CO2 on net ecosystem production in a Chesapeake Bay tidal wetland.

The rapid increase in atmospheric CO2 concentrations (Ca ) has resulted in extensive research efforts to understand its impact on terrestrial ecosystems, especially carbon balance. Despite these efforts, there are relatively few data comparing net ecosystem exchange of CO2 between the atmosphere and the biosphere (NEE), under both ambient and elevated Ca . Here we report data on annual sums of CO2 (NEE(net) ) for 19 years on a Chesapeake Bay tidal wetland for Scirpus olneyi (C3 photosynthetic pathway)- and Spartina patens (C4 photosynthetic pathway)-dominated high marsh communities exposed to ambient and elevated Ca (ambient + 340 ppm). Our objectives were to (i) quantify effects of elevated Ca on seasonally integrated CO2 assimilation (NEE(net) = NEE(day) + NEE(night) , kg C m(-2) y(-1) ) for the two communities; and (ii) quantify effects of altered canopy N content on ecosystem photosynthesis and respiration. Across all years, NEE(net) averaged 1.9 kg m(-2) y(-1) in ambient Ca and 2.5 kg m(-2) y(-1) in elevated Ca , for the C3 -dominated community. Similarly, elevated Ca significantly (P < 0.01) increased carbon uptake in the C4 -dominated community, as NEE(net) averaged 1.5 kg m(-2) y(-1) in ambient Ca and 1.7 kg m(-2) y(-1) in elevated Ca . This resulted in an average CO2 stimulation of 32% and 13% of seasonally integrated NEE(net) for the C3 - and C4 -dominated communities, respectively. Increased NEE(day) was correlated with increased efficiencies of light and nitrogen use for net carbon assimilation under elevated Ca , while decreased NEE(night) was associated with lower canopy nitrogen content. These results suggest that rising Ca may increase carbon assimilation in both C3 - and C4 -dominated wetland communities. The challenge remains to identify the fate of the assimilated carbon.

Plant-soil distribution of potentially toxic elements in response to elevated atmospheric CO2.

The distribution of contaminant elements within ecosystems is an environmental concern because of these elements' potential toxicity to animals and plants and their ability to hinder microbial ecosystem services. As with nutrients, contaminants are cycled within and through ecosystems. Elevated atmospheric CO2 generally increases plant productivity and alters nutrient element cycling, but whether CO2 causes similar effects on the cycling of contaminant elements is unknown. Here we show that 11 years of experimental CO2 enrichment in a sandy soil with low organic matter content causes plants to accumulate contaminants in plant biomass, with declines in the extractable contaminant element pools in surface soils. These results indicate that CO2 alters the distribution of contaminant elements in ecosystems, with plant element accumulation and declining soil availability both likely explained by the CO2 stimulation of plant biomass. Our results highlight the interdependence of element cycles and the importance of taking a broad view of the periodic table when the effects of global environmental change on ecosystem biogeochemistry are considered.

Effect of elevated CO2 on coarse-root biomass in Florida scrub detected by ground-penetrating radar.

Growth and distribution of coarse roots in time and space represent a gap in our understanding of belowground ecology. Large roots may play a critical role in carbon sequestration belowground. Using ground-penetrating radar (GPR), we quantified coarse-root biomass from an open-top chamber experiment in a scrub-oak ecosystem at Kennedy Space Center, Florida, USA. GPR propagates electromagnetic waves directly into the soil and reflects a portion of the energy when a buried object is contacted. In our study, we utilized a 1500 MHz antenna to establish correlations between GPR signals and root biomass. A significant relationship was found between GPR signal reflectance and biomass (R2 = 0.68). This correlation was applied to multiple GPR scans taken from each open-top chamber (elevated and ambient CO2). Our results showed that plots receiving elevated CO2 had significantly (P = 0.049) greater coarse-root biomass compared to ambient plots, suggesting that coarse roots may play a large role in carbon sequestration in scrub-oak ecosystems. This nondestructive method holds much promise for rapid and repeatable quantification of coarse roots, which are currently the most elusive aspect of long-term belowground studies.

Nitrogen cycling during seven years of atmospheric CO2 enrichment in a scrub oak woodland.

Experimentally increasing atmospheric CO2 often stimulates plant growth and ecosystem carbon (C) uptake. Biogeochemical theory predicts that these initial responses will immobilize nitrogen (N) in plant biomass and soil organic matter, causing N availability to plants to decline, and reducing the long-term CO2-stimulation of C storage in N limited ecosystems. While many experiments have examined changes in N cycling in response to elevated CO2, empirical tests of this theoretical prediction are scarce. During seven years of postfire recovery in a scrub oak ecosystem, elevated CO2 initially increased plant N accumulation and plant uptake of tracer 15N, peaking after four years of CO2 enrichment. Between years four and seven, these responses to CO2 declined. Elevated CO2 also increased N and tracer 15N accumulation in the O horizon, and reduced 15N recovery in underlying mineral soil. These responses are consistent with progressive N limitation: the initial CO2 stimulation of plant growth immobilized N in plant biomass and in the O horizon, progressively reducing N availability to plants. Litterfall production (one measure of aboveground primary productivity) increased initially in response to elevated CO2, but the CO2 stimulation declined during years five through seven, concurrent with the accumulation of N in the O horizon and the apparent restriction of plant N availability. Yet, at the level of aboveground plant biomass (estimated by allometry), progressive N limitation was less apparent, initially because of increased N acquisition from soil and later because of reduced N concentration in biomass as N availability declined. Over this seven-year period, elevated CO2 caused a redistribution of N within the ecosystem, from mineral soils, to plants, to surface organic matter. In N limited ecosystems, such changes in N cycling are likely to reduce the response of plant production to elevated CO2.

EFFECTS OF ELEVATED ATMOSPHERIC CO(2) ON WATER CHEMISTRY AND MOSQUITO (DIPTERA: CULICIDAE) GROWTH UNDER COMPETITIVE CONDITIONS IN CONTAINER HABITATS.

We investigated the direct and indirect effects of elevated atmospheric CO(2) on freshwater container habitats and their larval mosquito occupants. We predicted that a doubling of atmospheric CO(2) would (1) alter the chemical properties of water in this system, (2) slow degradation of leaf litter, and (3) decrease larval growth of Aedes albopictus (Skuse) mosquitoes raised on that litter under competitive conditions. Effects of elevated CO(2) on water quality parameters were not detected, but the presence of leaf litter significantly reduced pH and dissolved oxygen relative to water-filled containers without litter. Degradation rates of oak leaf litter from plants grown under elevated CO(2) atmospheres did not differ from breakdown rates of litter from ambient CO(2) conditions. Litter from plants grown in an elevated CO(2) atmospheres did not influence mosquito population growth, but mosquito production decreased significantly with increasing larval density. Differences among mosquito density treatments influenced survivorship most strongly among male Ae. albopictus and time to emergence most strongly among females, suggesting fundamental sex-determined differences in response to competition. Results of this and other studies indicate that direct and indirect effects of doubled atmospheric CO(2) are minimal in artificial containers with freshwater.

Light response characteristics of net CO2 exchange in brackish wetland plant communities.

Photosynthetic responses to incident photon flux density (400-700 nm; PPFD) was studied in a grass community consisting of Spartina patens and Distichlis spicata and a mixed community having the two grasses and a sedge, Scirpus Olneyi. Net community CO2 exchange and incident PPFD were monitored from dawn to dusk in a large open gas exchange system, and a hyperbolic light response model was fit to the data for each day. Light response curves from five growing seasons were evaluated for seasonal trends in the compensation value, initial slope, and maximum net CO2 exchange rate calculated from the model at PPFD=1670 µmol m-2s-1.All response curves were curvilinear. Data from approximately 30% of the 113 days studied fit saturation curves which occurred primarily in spring and fall. Approximately 5% of all curves constructed required a different response curve for the morning and afternoon. These occurred during mid-summer and were interpreted to be evidence of water stress.The compensation flux density was very high early in the growing season, but rapidly decreased and during the months June, July and August, it averaged near 100 and 120 µmol m-2s-1 in the mixed and grass communities. The initial slope and maximum net CO2 exchange rate increased from early May to maxima in July and declined thereafter. Mid-summer mean values for the mixed and grass communities respectively were 34.3±10.3 mmol mol-1 and 39.1±9.1 mmol mol-1 for the initial slope and 20.3±4.2 µmol m-2s-1 and 23.0±3.8 µmol m-2s-1 for maximum net CO2 exchange. Daytime respiration accounted for approximately 20% of maximum gross photosynthesis in both communities.Photosynthetic efficiency, CO2 assimilated per unit total incident solar radiation, was approximately 4.1% and 4.7% at dawn or dusk and 2.3% and 2.6% at midday for the mixed and grass community. Gross photosynthesis, maximum photosynthesis plus midday respiration, accounted for 2.7% and 3.0% of total incident solar radiation in the mixed and grass communities.

Effects of elevated CO2 on growth and carbon/nutrient balance in the deciduous woody shrub Lindera benzoin (L.) Blume (Lauraceae).

We examined the effects of elevated CO2 on growth and carbon/nutrient balance in a natural population of the deciduous temperate zone shrub Lindera benzoin. Our data concern whole plant, leaf, and stem growth for the first two seasons of a long-term field experiment in which CO2 levels were manipulated in situ. In addition to growth parameters, we evaluated changes in leaf and stem chemistry, including total nitrogen, nonstructural carbohydrates, and total phenolics. Over the course of this study, L. benzoin appeared to respond to elevated CO2 primarily by physiological and biochemical changes, with only a slight enhancement in aboveground growth (ramet height). Positive effects on aboveground growth were primarily evident in young (nonreproductive) ramets. Our results suggest that nitrogen limitation may have constrained plants to allocate carbohydrates produced in response to elevated CO2 primarily to storage and belowground growth, and perhaps to increased secondary chemical production, rather than to increased stem and leaf growth. We discuss our results in terms of changes in carbon/nutrient balance induced by elevated CO2, and provide predictions for future changes in this system based upon constraints imposed by intrinsic and extrinsic factors and their potential effects on the reallocation of stored reserves.

Long-term photosynthetic response in single leaves of A C3 and C4 salt marsh species grown at elevated atmospheric CO2 in situ.

Mono-specific communities of the C3 sedge, Scirpus olneyi and the C4 grass, Spartina patens, were exposed to normal ambient or elevated CO2, (ca. 680 µl l-1) throughout the 1987 and 1988 growing seasons in open-top field chambers located on a tidal marsh. Single stems of C3 plants grown in ambient or elevated CO2 showed an increased photosynthetic rate when tested at elevated CO2 for both seasons. This increase in photosynthetic response in the C3 species was maintained throughout the 1987 and 1988 growing season. The stimulation of photosynthesis with elevated CO2 appeared to increase as temperature increased and decreased as photosynthetic photon flux (PPF) increased. Analysis of the photosynthetic response of the C3 species during the 1988 season indicated that significant differences in light-saturated photosynthetic rate between ambient and elevated CO2 conditions continued until October. In contrast to the C3 sedge, the C4 grass showed no significant photosynthetic increase to elevated CO2 except at the beginning of the 1988 season.

Element pool changes within a scrub-oak ecosystem after 11 years of exposure to elevated CO2.

The effects of elevated CO2 on ecosystem element stocks are equivocal, in part because cumulative effects of CO2 on element pools are difficult to detect. We conducted a complete above and belowground inventory of non-nitrogen macro- and micronutrient stocks in a subtropical woodland exposed to twice-ambient CO2 concentrations for 11 years. We analyzed a suite of nutrient elements and metals important for nutrient cycling in soils to a depth of ~2 m, in leaves and stems of the dominant oaks, in fine and coarse roots, and in litter. In conjunction with large biomass stimulation, elevated CO2 increased oak stem stocks of Na, Mg, P, K, V, Zn and Mo, and the aboveground pool of K and S. Elevated CO2 increased root pools of most elements, except Zn. CO2-stimulation of plant Ca was larger than the decline in the extractable Ca pool in soils, whereas for other elements, increased plant uptake matched the decline in the extractable pool in soil. We conclude that elevated CO2 caused a net transfer of a subset of nutrients from soil to plants, suggesting that ecosystems with a positive plant growth response under high CO2 will likely cause mobilization of elements from soil pools to plant biomass.

Altered soil microbial community at elevated CO(2) leads to loss of soil carbon.

Increased carbon storage in ecosystems due to elevated CO(2) may help stabilize atmospheric CO(2) concentrations and slow global warming. Many field studies have found that elevated CO(2) leads to higher carbon assimilation by plants, and others suggest that this can lead to higher carbon storage in soils, the largest and most stable terrestrial carbon pool. Here we show that 6 years of experimental CO(2) doubling reduced soil carbon in a scrub-oak ecosystem despite higher plant growth, offsetting approximately 52% of the additional carbon that had accumulated at elevated CO(2) in aboveground and coarse root biomass. The decline in soil carbon was driven by changes in soil microbial composition and activity. Soils exposed to elevated CO(2) had higher relative abundances of fungi and higher activities of a soil carbon-degrading enzyme, which led to more rapid rates of soil organic matter degradation than soils exposed to ambient CO(2). The isotopic composition of microbial fatty acids confirmed that elevated CO(2) increased microbial utilization of soil organic matter. These results show how elevated CO(2), by altering soil microbial communities, can cause a potential carbon sink to become a carbon source.

Effects of elevated CO2 on foliar quality and herbivore damage in a scrub oak ecosystem.

Atmospheric CO2 concentrations have increased exponentially over the last century and continuing increases are expected to have significant effects on ecosystems. We investigated the interactions among atmospheric CO2, foliar quality, and herbivory within a scrub oak community at the Kennedy Space Center, Florida. Sixteen plots of open-top chambers were followed; eight of which were exposed to ambient levels of CO2 (350 ppm), and eight of which were exposed to elevated levels of CO2 (700 ppm). We focused on three oak species, Quercus geminata, Quercus myrtifolia, Quercus chapmanii, and one nitrogen fixing legume, Galactia elliottii. There were declines in overall nitrogen and increases in C:N ratios under elevated CO2. Total carbon, phenolics (condensed tannins, hydrolyzable tannins, total phenolics) and fiber (cellulose, hemicellulose, lignin) did not change under elevated CO2 across plant species. Plant species differed in their relative foliar chemistries over time, however, the only consistent differences were higher nitrogen concentrations and lower C:N ratios in the nitrogen fixer when compared to the oak species. Under elevated CO2, damage by herbivores decreased for four of the six insect groups investigated. The overall declines in both foliar quality and herbivory under elevated CO2 treatments suggest that damage to plants may decline as atmospheric CO2 levels continue to rise.

Effects of elevated co2 and herbivore damage on litter quality in a scrub oak ecosystem.

Atmospheric CO(2) concentrations have increased dramatically over the last century and continuing increases are expected to have significant, though currently unpredictable, effects on ecosystems. One important process that may be affected by elevated CO(2) is leaf litter decomposition. We investigated the interactions among atmospheric CO(2), herbivory, and litter quality within a scrub oak community at the Kennedy Space Center, Florida. Leaf litter chemistry in 16 plots of open-top chambers was followed for 3 years; eight were exposed to ambient levels of CO(2), and eight were exposed to elevated levels of CO(2) (ambient + 350 ppmV). We focused on three dominant oak species, Quercus geminata, Quercus myrtifolia, and Quercus chapmanii. Condensed tannin concentrations in oak leaf litter were higher under elevated CO(2). Litter chemistry differed among all plant species except for condensed tannins. Phenolic concentrations were lower, whereas lignin concentrations and lignin/nitrogen ratios were higher in herbivore-damaged litter independent of CO(2) concentration. However, changes in litter chemistry from year to year were far larger than effects of CO(2) or insect damage, suggesting that these may have only minor effects on litter decomposition.

Influence of elevated CO(2) on the fungal community in a coastal scrub oak forest soil investigated with terminal-restriction fragment length polymorphism analysis.

Sixteen open-top chambers (diameter, 3.66 m) were established in a scrub oak habitat in central Florida where vegetation was removed in a planned burn prior to chamber installation. Eight control chambers have been continuously exposed to ambient air and eight have been continuously exposed to elevated CO(2) at twice-ambient concentration (approximately 700 ppm) for 5 years. Soil cores were collected from each chamber to examine the influence of elevated atmospheric CO(2) on the fungal community in different soil fractions. Each soil sample was physically fractionated into bulk soil, rhizosphere soil, and roots for separate analyses. Changes in relative fungal biomass were estimated by the ergosterol technique. In the bulk soil and root fractions, a significantly increased level of ergosterol was detected in the elevated CO(2) treatments relative to ambient controls. Fungal community composition was determined by terminal-restriction fragment length polymorphism (T-RFLP) analysis of the internal transcribed spacer (ITS) region. The specificities of different ITS primer sets were evaluated against plant and fungal species isolated from the experimental site. Changes in community composition were assessed by principal component analyses of T-RFLP profiles resolved by capillary electrophoresis. Fungal species richness, defined by the total number of terminal restriction fragments, was not significantly affected by either CO(2) treatment or soil fraction.

Induced defensive response of myrtle oak to foliar insect herbivory in ambient and elevated CO2.

The rising level of atmospheric CO2 has stimulated several recent studies attempting to predict the effects of increased CO2 on ecological communities. However, most of these studies have been conducted in the benign conditions of the laboratory and in the absence of herbivores. In the current study, we utilized large octagonal chambers, which enclosed portions of an intact scrub-oak community to investigate the interactive effects of CO2 and insect herbivory on myrtle oak, Quercus myrtifolia. Specifically, we assessed the effects of ambient and elevated CO2 (2x current concentrations) on percent foliar nitrogen, C:N ratio, total relative foliar tannin content, and the presence of leaf damage caused by leaf mining and leaf chewing insects that feed on myrtle oak. Total foliar N declined and C:N ratios increased significantly in oaks in elevated CO2 chambers. The percentages of leaves damaged by either leafminers or leaf chewers tended to be lower in elevated compared to ambient chambers, but they co-occurred on leaves less than expected, regardless of CO2 treatment. Leaves that had been either mined or chewed exhibited a similar wounding or defensive response; they had an average of 25 and 21% higher protein binding ability, which is correlated with tannin concentration, compared to nondamaged control leaves, respectively. While the protein-binding ability (expressed as total percent tannin) of leaves from elevated CO2 was slightly higher than from leaves grown in ambient chambers, this difference was not significant.

MORE EFFICIENT PLANTS: A Consequence of Rising Atmospheric CO2?

The primary effect of the response of plants to rising atmospheric CO2 (Ca) is to increase resource use efficiency. Elevated Ca reduces stomatal conductance and transpiration and improves water use efficiency, and at the same time it stimulates higher rates of photosynthesis and increases light-use efficiency. Acclimation of photosynthesis during long-term exposure to elevated Ca reduces key enzymes of the photosynthetic carbon reduction cycle, and this increases nutrient use efficiency. Improved soil-water balance, increased carbon uptake in the shade, greater carbon to nitrogen ratio, and reduced nutrient quality for insect and animal grazers are all possibilities that have been observed in field studies of the effects of elevated Ca. These effects have major consequences for agriculture and native ecosystems in a world of rising atmospheric Ca and climate change.