Links across ecological scales: Plant biomass responses to elevated CO2.

The degree to which elevated CO2 concentrations (e[CO2 ]) increase the amount of carbon (C) assimilated by vegetation plays a key role in climate change. However, due to the short-term nature of CO2 enrichment experiments and the lack of reconciliation between different ecological scales, the effect of e[CO2 ] on plant biomass stocks remains a major uncertainty in future climate projections. Here, we review the effect of e[CO2 ] on plant biomass across multiple levels of ecological organization, scaling from physiological responses to changes in population-, community-, ecosystem-, and global-scale dynamics. We find that evidence for a sustained biomass response to e[CO2 ] varies across ecological scales, leading to diverging conclusions about the responses of individuals, populations, communities, and ecosystems. While the distinct focus of every scale reveals new mechanisms driving biomass accumulation under e[CO2 ], none of them provides a full picture of all relevant processes. For example, while physiological evidence suggests a possible long-term basis for increased biomass accumulation under e[CO2 ] through sustained photosynthetic stimulation, population-scale evidence indicates that a possible e[CO2 ]-induced increase in mortality rates might potentially outweigh the effect of increases in plant growth rates on biomass levels. Evidence at the global scale may indicate that e[CO2 ] has contributed to increased biomass cover over recent decades, but due to the difficulty to disentangle the effect of e[CO2 ] from a variety of climatic and land-use-related drivers of plant biomass stocks, it remains unclear whether nutrient limitations or other ecological mechanisms operating at finer scales will dampen the e[CO2 ] effect over time. By exploring these discrepancies, we identify key research gaps in our understanding of the effect of e[CO2 ] on plant biomass and highlight the need to integrate knowledge across scales of ecological organization so that large-scale modeling can represent the finer-scale mechanisms needed to constrain our understanding of future terrestrial C storage.

Patterns of free amino acids in tundra soils reflect mycorrhizal type, shrubification, and warming.

The soil nitrogen (N) cycle in cold terrestrial ecosystems is slow and organically bound N is an important source of N for plants in these ecosystems. Many plant species can take up free amino acids from these infertile soils, either directly or indirectly via their mycorrhizal fungi. We hypothesized that plant community changes and local plant community differences will alter the soil free amino acid pool and composition; and that long-term warming could enhance this effect. To test this, we studied the composition of extractable free amino acids at five separate heath, meadow, and bog locations in subarctic and alpine Scandinavia, with long-term (13 to 24 years) warming manipulations. The plant communities all included a mixture of ecto-, ericoid-, and arbuscular mycorrhizal plant species. Vegetation dominated by grasses and forbs with arbuscular and non-mycorrhizal associations showed highest soil free amino acid content, distinguishing them from the sites dominated by shrubs with ecto- and ericoid-mycorrhizal associations. Warming increased shrub and decreased moss cover at two sites, and by using redundancy analysis, we found that altered soil free amino acid composition was related to this plant cover change. From this, we conclude that the mycorrhizal type is important in controlling soil N cycling and that expansion of shrubs with ectomycorrhiza (and to some extent ericoid mycorrhiza) can help retain N within the ecosystems by tightening the N cycle.

Biomass responses in a temperate European grassland through 17 years of elevated CO2.

Future increase in atmospheric CO2 concentrations will potentially enhance grassland biomass production and shift the functional group composition with consequences for ecosystem functioning. In the "GiFACE" experiment (Giessen Free Air Carbon dioxide Enrichment), fertilized grassland plots were fumigated with elevated CO2 (eCO2 ) year-round during daylight hours since 1998, at a level of +20% relative to ambient concentrations (in 1998, aCO2 was 364 ppm and eCO2 399 ppm; in 2014, aCO2 was 397 ppm and eCO2 518 ppm). Harvests were conducted twice annually through 23 years including 17 years with eCO2 (1998 to 2014). Biomass consisted of C3 grasses and forbs, with a small proportion of legumes. The total aboveground biomass (TAB) was significantly increased under eCO2 (p = .045 and .025, at first and second harvest). The dominant plant functional group grasses responded positively at the start, but for forbs, the effect of eCO2 started out as a negative response. The increase in TAB in response to eCO2 was approximately 15% during the period from 2006 to 2014, suggesting that there was no attenuation of eCO2 effects over time, tentatively a consequence of the fertilization management. Biomass and soil moisture responses were closely linked. The soil moisture surplus (c. 3%) in eCO2 manifested in the latter years was associated with a positive biomass response of both functional groups. The direction of the biomass response of the functional group forbs changed over the experimental duration, intensified by extreme weather conditions, pointing to the need of long-term field studies for obtaining reliable responses of perennial ecosystems to eCO2 and as a basis for model development.

Organic matter flow in the food web at a temperate heath under multifactorial climate change.

The rising atmospheric CO(2) concentration, increasing temperature and changed patterns of precipitation currently expose terrestrial ecosystems to altered environmental conditions. This may affect belowground nutrient cycling through its intimate relationship with the belowground decomposers. Three climate change factors (elevated CO(2), increased temperature and drought) were investigated in a full factorial field experiment at a temperate heathland location. The combined effect of biotic and abiotic factors on nitrogen and carbon flows was traced in plant root → litter → microbe → detritivore/omnivore → predator food-web for one year after amendment with (15)N(13)C(2)-glycine. Isotope ratio mass spectrometry (IRMS) measurement of (15)N/(14)N and (13)C/(12)C in soil extracts and functional ecosystem compartments revealed that the recovery of (15)N sometimes decreased through the chain of consumption, with the largest amount of bioactive (15)N label pool accumulated in the microbial biomass. The elevated CO(2) concentration at the site for 2 years increased the biomass, the (15)N enrichment and the (15)N recovery in detritivores. This suggests that detritivore consumption was controlled by both the availability of the microbial biomass, a likely major food source, and the climatic factors. Furthermore, the natural abundance δ(13)C of enchytraeids was significantly altered in CO(2)-fumigated plots, showing that even small changes in δ(13)C-CO(2) can be used to detect transfer of carbon from primary producers to detritivores. We conclude that, in the short term, the climate change treatments affected soil organism activity, possibly with labile carbohydrate production controlling the microbial and detritivore biomass, with potential consequences for the decomposition of detritus and nutrient cycling. Hence, there appears to be a strong coupling of responses in carbon and nitrogen cycling at this temperate heath.

Globally consistent influences of seasonal precipitation limit grassland biomass response to elevated CO2.

Rising atmospheric carbon dioxide concentration should stimulate biomass production directly via biochemical stimulation of carbon assimilation, and indirectly via water savings caused by increased plant water-use efficiency. Because of these water savings, the CO2 fertilization effect (CFE) should be stronger at drier sites, yet large differences among experiments in grassland biomass response to elevated CO2 appear to be unrelated to annual precipitation, preventing useful generalizations. Here, we show that, as predicted, the impact of elevated CO2 on biomass production in 19 globally distributed temperate grassland experiments reduces as mean precipitation in seasons other than spring increases, but that it rises unexpectedly as mean spring precipitation increases. Moreover, because sites with high spring precipitation also tend to have high precipitation at other times, these effects of spring and non-spring precipitation on the CO2 response offset each other, constraining the response of ecosystem productivity to rising CO2. This explains why previous analyses were unable to discern a reliable trend between site dryness and the CFE. Thus, the CFE in temperate grasslands worldwide will be constrained by their natural rainfall seasonality such that the stimulation of biomass by rising CO2 could be substantially less than anticipated.

Long-term and realistic global change manipulations had low impact on diversity of soil biota in temperate heathland.

In a dry heathland ecosystem we manipulated temperature (warming), precipitation (drought) and atmospheric concentration of CO2 in a full-factorial experiment in order to investigate changes in below-ground biodiversity as a result of future climate change. We investigated the responses in community diversity of nematodes, enchytraeids, collembolans and oribatid mites at two and eight years of manipulations. We used a structural equation modelling (SEM) approach analyzing the three manipulations, soil moisture and temperature, and seven soil biological and chemical variables. The analysis revealed a persistent and positive effect of elevated CO2 on litter C:N ratio. After two years of treatment, the fungi to bacteria ratio was increased by warming, and the diversities within oribatid mites, collembolans and nematode groups were all affected by elevated CO2 mediated through increased litter C:N ratio. After eight years of treatment, however, the CO2-increased litter C:N ratio did not influence the diversity in any of the four fauna groups. The number of significant correlations between treatments, food source quality, and soil biota diversities was reduced from six to three after two and eight years, respectively. These results suggest a remarkable resilience within the soil biota against global climate change treatments in the long term.

Bacteria and fungi respond differently to multifactorial climate change in a temperate heathland, traced with 13C-glycine and FACE CO2.

It is vital to understand responses of soil microorganisms to predicted climate changes, as these directly control soil carbon (C) dynamics. The rate of turnover of soil organic carbon is mediated by soil microorganisms whose activity may be affected by climate change. After one year of multifactorial climate change treatments, at an undisturbed temperate heathland, soil microbial community dynamics were investigated by injection of a very small concentration (5.12 µg C g(-1) soil) of (13)C-labeled glycine ((13)C2, 99 atom %) to soils in situ. Plots were treated with elevated temperature (+1°C, T), summer drought (D) and elevated atmospheric carbon dioxide (510 ppm [CO2]), as well as combined treatments (TD, TCO2, DCO2 and TDCO2). The (13)C enrichment of respired CO2 and of phospholipid fatty acids (PLFAs) was determined after 24 h. (13)C-glycine incorporation into the biomarker PLFAs for specific microbial groups (Gram positive bacteria, Gram negative bacteria, actinobacteria and fungi) was quantified using gas chromatography-combustion-stable isotope ratio mass spectrometry (GC-C-IRMS). Gram positive bacteria opportunistically utilized the freshly added glycine substrate, i.e. incorporated (13)C in all treatments, whereas fungi had minor or no glycine derived (13)C-enrichment, hence slowly reacting to a new substrate. The effects of elevated CO2 did suggest increased direct incorporation of glycine in microbial biomass, in particular in G(+) bacteria, in an ecosystem subjected to elevated CO2. Warming decreased the concentration of PLFAs in general. The FACE CO2 was (13)C-depleted (δ(13)C = 12.2‰) compared to ambient (δ(13)C = ∼-8‰), and this enabled observation of the integrated longer term responses of soil microorganisms to the FACE over one year. All together, the bacterial (and not fungal) utilization of glycine indicates substrate preference and resource partitioning in the microbial community, and therefore suggests a diversified response pattern to future changes in substrate availability and climatic factors.

Off-season uptake of nitrogen in temperate heath vegetation.

In this field study we show that temperate coastal heath vegetation has a significant off-season uptake potential for nitrogen, both in the form of ammonium and as glycine, throughout winter. We injected 15N-ammonium and 15N 2x(13C)-glycine into the soil twice during winter and once at spring. The winter temperatures were similar to those of an average winter in the northern temperate region of Europe, with only few days of soil temperatures below zero or above 5 degrees C. The vegetation, consisting of the evergreen dwarf shrub Calluna vulgaris, the deciduous dwarf shrub Salix arenaria, and the graminoids Carex arenaria and Deschampsia flexuosa, showed high root uptake of both forms of nitrogen, both 1 day after labelling and after a month, in species specific temporal patterns. Plant uptake of 13C was not significant, providing no further evidence of intact uptake of glycine. Translocation of the labelled nitrogen to shoots was generally evident after 1 month and increased as spring approached, with different translocation strategies in the three plant functional types. Furthermore, only the graminoids showed shoot growth during winter. Increasing plant nitrogen concentration from fall to spring at temperate heaths may, hence, be due to nitrogen uptake. Our results suggest that the potential for nitrogen uptake in plants at winter is of the same order of magnitude as at summer. Hence, winter nitrogen uptake in ecosystems in the temperate/boreal region should be considered when making annual nitrogen budgets of heath ecosystems, and the view of plant nutrient uptake as low in this climatic region during winter should be revised.