Responses of vascular plant fine roots and associated microbial communities to whole-ecosystem warming and elevated CO2 in northern peatlands.

Warming and elevated CO2 (eCO2) are expected to facilitate vascular plant encroachment in peatlands. The rhizosphere, where microbial activity is fueled by root turnover and exudates, plays a crucial role in biogeochemical cycling, and will likely at least partially dictate the response of the belowground carbon cycle to climate changes. We leveraged the Spruce and Peatland Responses Under Changing Environments (SPRUCE) experiment, to explore the effects of a whole-ecosystem warming gradient (+0°C to 9°C) and eCO2 on vascular plant fine roots and their associated microbes. We combined trait-based approaches with the profiling of fungal and prokaryote communities in plant roots and rhizospheres, through amplicon sequencing. Warming promoted self-reliance for resource uptake in trees and shrubs, while saprophytic fungi and putative chemoorganoheterotrophic bacteria utilizing plant-derived carbon substrates were favored in the root zone. Conversely, eCO2 promoted associations between trees and ectomycorrhizal fungi. Trees mostly associated with short-distance exploration-type fungi that preferentially use labile soil N. Additionally, eCO2 decreased the relative abundance of saprotrophs in tree roots. Our results indicate that plant fine-root trait variation is a crucial mechanism through which vascular plants in peatlands respond to climate change via their influence on microbial communities that regulate biogeochemical cycles.

Climate drivers alter nitrogen availability in surface peat and decouple N2 fixation from CH4 oxidation in the Sphagnum moss microbiome.

Peat mosses (Sphagnum spp.) are keystone species in boreal peatlands, where they dominate net primary productivity and facilitate the accumulation of carbon in thick peat deposits. Sphagnum mosses harbor a diverse assemblage of microbial partners, including N2 -fixing (diazotrophic) and CH4 -oxidizing (methanotrophic) taxa that support ecosystem function by regulating transformations of carbon and nitrogen. Here, we investigate the response of the Sphagnum phytobiome (plant + constituent microbiome + environment) to a gradient of experimental warming (+0°C to +9°C) and elevated CO2 (+500 ppm) in an ombrotrophic peatland in northern Minnesota (USA). By tracking changes in carbon (CH4 , CO2 ) and nitrogen (NH4 -N) cycling from the belowground environment up to Sphagnum and its associated microbiome, we identified a series of cascading impacts to the Sphagnum phytobiome triggered by warming and elevated CO2 . Under ambient CO2 , warming increased plant-available NH4 -N in surface peat, excess N accumulated in Sphagnum tissue, and N2 fixation activity decreased. Elevated CO2 offset the effects of warming, disrupting the accumulation of N in peat and Sphagnum tissue. Methane concentrations in porewater increased with warming irrespective of CO2 treatment, resulting in a ~10× rise in methanotrophic activity within Sphagnum from the +9°C enclosures. Warming's divergent impacts on diazotrophy and methanotrophy caused these processes to become decoupled at warmer temperatures, as evidenced by declining rates of methane-induced N2 fixation and significant losses of keystone microbial taxa. In addition to changes in the Sphagnum microbiome, we observed ~94% mortality of Sphagnum between the +0°C and +9°C treatments, possibly due to the interactive effects of warming on N-availability and competition from vascular plant species. Collectively, these results highlight the vulnerability of the Sphagnum phytobiome to rising temperatures and atmospheric CO2 concentrations, with significant implications for carbon and nitrogen cycling in boreal peatlands.

Forest stand and canopy development unaltered by 12 years of CO2 enrichment.

Canopy structure-the size and distribution of tree crowns and the spatial and temporal distribution of leaves within them-exerts dominant control over primary productivity, transpiration and energy exchange. Stand structure-the spatial arrangement of trees in the forest (height, basal area and spacing)-has a strong influence on forest growth, allocation and resource use. Forest response to elevated atmospheric CO2 is likely to be dependent on the canopy and stand structure. Here, we investigated elevated CO2 effects on the forest structure of a Liquidambar styraciflua L. stand in a free-air CO2 enrichment experiment, considering leaves, tree crowns, forest canopy and stand structure. During the 12-year experiment, the trees increased in height by 5 m and basal area increased by 37%. Basal area distribution among trees shifted from a relatively narrow distribution to a much broader one, but there was little evidence of a CO2 effect on height growth or basal area distribution. The differentiation into crown classes over time led to an increase in the number of unproductive intermediate and suppressed trees and to a greater concentration of stand basal area in the largest trees. A whole-tree harvest at the end of the experiment permitted detailed analysis of canopy structure. There was little effect of CO2 enrichment on the relative leaf area distribution within tree crowns and there was little change from 1998 to 2009. Leaf characteristics (leaf mass per unit area and nitrogen content) varied with crown depth; any effects of elevated CO2 were much smaller than the variation within the crown and were consistent throughout the crown. In this young, even-aged, monoculture plantation forest, there was little evidence that elevated CO2 accelerated tree and stand development, and there were remarkably small changes in canopy structure. Questions remain as to whether a more diverse, mixed species forest would respond similarly.

Bringing function to structure: Root-soil interactions shaping phosphatase activity throughout a soil profile in Puerto Rico.

Large areas of highly productive tropical forests occur on weathered soils with low concentrations of available phosphorus (P). In such forests, root and microbial production of acid phosphatase enzymes capable of mineralizing organic phosphorus is considered vital to increasing available P for plant uptake.We measured both root and soil phosphatase throughout depth and alongside a variety of root and soil factors to better understand the potential of roots and soil biota to increase P availability and to constrain estimates of the biochemical mineralization within ecosystem models.We measured soil phosphatase down to 1 m, root phosphatase to 30 cm, and collected data on fine-root mass density, specific root length, soil P, bulk density, and soil texture using soil cores in four tropical forests within the Luquillo Experimental Forest in Puerto Rico.We found that soil phosphatase decreased with soil depth, but not root phosphatase. Furthermore, when both soil and root phosphatase were expressed per soil volume, soil phosphatase was 100-fold higher that root phosphatase.Both root and soil factors influenced soil and root phosphatase. Soil phosphatase increased with fine-root mass density and organic P, which together explained over 50% of the variation in soil phosphatase. Over 80% of the variation in root phosphatase per unit root mass was attributed to specific root length (positive correlation) and available (resin) P (negative correlation). Synthesis: Fine-root traits and soil P data are necessary to understand and represent soil and root phosphatase activity throughout the soil column and across sites with different soil conditions and tree species. These findings can be used to parameterize or benchmark estimates of biochemical mineralization in ecosystem models that contain fine-root biomass and soil P distributions throughout depth.

Divergent species-specific impacts of whole ecosystem warming and elevated CO2 on vegetation water relations in an ombrotrophic peatland.

Boreal peatland forests have relatively low species diversity and thus impacts of climate change on one or more dominant species could shift ecosystem function. Despite abundant soil water availability, shallowly rooted vascular plants within peatlands may not be able to meet foliar demand for water under drought or heat events that increase vapor pressure deficits while reducing near surface water availability, although concurrent increases in atmospheric CO2 could buffer resultant hydraulic stress. We assessed plant water relations of co-occurring shrub (primarily Rhododendron groenlandicum and Chamaedaphne calyculata) and tree (Picea mariana and Larix laricina) species prior to, and in response to whole ecosystem warming (0 to +9°C) and elevated CO2 using 12.8-m diameter open-top enclosures installed within an ombrotrophic bog. Water relations (water potential [Ψ], turgor loss point, foliar and root hydraulic conductivity) were assessed prior to treatment initiation, then Ψ and peak sap flow (trees only) assessed after 1 or 2 years of treatments. Under the higher temperature treatments, L. laricina Ψ exceeded its turgor loss point, increased its peak sap flow, and was not able to recover Ψ overnight. In contrast, P. mariana operated below its turgor loss point and maintained constant Ψ and sap flow across warming treatments. Similarly, C. calyculata Ψ stress increased with temperature while R. groenlandicum Ψ remained at pretreatment levels. The more anisohydric behavior of L. laricina and C. calyculata may provide greater net C uptake with warming, while the more conservative P. mariana and R. groenlandicum maintained greater hydraulic safety. These latter species also responded to elevated CO2 by reduced Ψ stress, which may also help limit hydraulic failure during periods of extreme drought or heat in the future. Along with Sphagnum moss, the species-specific responses of peatland vascular communities to drier or hotter conditions will shape boreal peatland composition and function in the future.

Nitrogen and phosphorus cycling in an ombrotrophic peatland: a benchmark for assessing change.

Aims: Slow decomposition and isolation from groundwater mean that ombrotrophic peatlands store a large amount of soil carbon (C) but have low availability of nitrogen (N) and phosphorus (P). To better understand the role these limiting nutrients play in determining the C balance of peatland ecosystems, we compile comprehensive N and P budgets for a forested bog in northern Minnesota, USA. Methods: N and P within plants, soils, and water are quantified based on field measurements. The resulting empirical dataset are then compared to modern-day, site-level simulations from the peatland land surface version of the Energy Exascale Earth System Model (ELM-SPRUCE). Results: Our results reveal N is accumulating in the ecosystem at 0.2 ± 0.1 g N m-2 year-1 but annual P inputs to this ecosystem are balanced by losses. Biomass stoichiometry indicates that plant functional types differ in N versus P limitation, with trees exhibiting a stronger N limitation than ericaceous shrubs or Sphagnum moss. High biomass and productivity of Sphagnum results in the moss layer storing and cycling a large proportion of plant N and P. Comparing our empirically-derived nutrient budgets to ELM-SPRUCE shows the model captures N cycling within dominant plant functional types well. Conclusions: The nutrient budgets and stoichiometry presented serve as a baseline for quantifying the nutrient cycling response of peatland ecosystems to both observed and simulated climate change. Our analysis improves our understanding of N and P dynamics within nutrient-limited peatlands and represents a crucial step toward improving C-cycle projections into the twenty-first century.

Peatland warming strongly increases fine-root growth.

Belowground climate change responses remain a key unknown in the Earth system. Plant fine-root response is especially important to understand because fine roots respond quickly to environmental change, are responsible for nutrient and water uptake, and influence carbon cycling. However, fine-root responses to climate change are poorly constrained, especially in northern peatlands, which contain up to two-thirds of the world's soil carbon. We present fine-root responses to warming between +2 °C and 9 °C above ambient conditions in a whole-ecosystem peatland experiment. Warming strongly increased fine-root growth by over an order of magnitude in the warmest treatment, with stronger responses in shrubs than in trees or graminoids. In the first year of treatment, the control (+0 °C) shrub fine-root growth of 0.9 km m-2 y-1 increased linearly by 1.2 km m-2 y-1 (130%) for every degree increase in soil temperature. An extended belowground growing season accounted for 20% of this dramatic increase. In the second growing season of treatment, the shrub warming response rate increased to 2.54 km m-2 °C-1 Soil moisture was negatively correlated with fine-root growth, highlighting that drying of these typically water-saturated ecosystems can fuel a surprising burst in shrub belowground productivity, one possible mechanism explaining the "shrubification" of northern peatlands in response to global change. This previously unrecognized mechanism sheds light on how peatland fine-root response to warming and drying could be strong and rapid, with consequences for the belowground growing season duration, microtopography, vegetation composition, and ultimately, carbon function of these globally relevant carbon sinks.

Rapid loss of an ecosystem engineer: Sphagnum decline in an experimentally warmed bog.

Sphagnum mosses are keystone components of peatland ecosystems. They facilitate the accumulation of carbon in peat deposits, but climate change is predicted to expose peatland ecosystem to sustained and unprecedented warming leading to a significant release of carbon to the atmosphere. Sphagnum responses to climate change, and their interaction with other components of the ecosystem, will determine the future trajectory of carbon fluxes in peatlands. We measured the growth and productivity of Sphagnum in an ombrotrophic bog in northern Minnesota, where ten 12.8-m-diameter plots were exposed to a range of whole-ecosystem (air and soil) warming treatments (+0 to +9°C) in ambient or elevated (+500 ppm) CO2. The experiment is unique in its spatial and temporal scale, a focus on response surface analysis encompassing the range of elevated temperature predicted to occur this century, and consideration of an effect of co-occurring CO2 altering the temperature response surface. In the second year of warming, dry matter increment of Sphagnum increased with modest warming to a maximum at 5°C above ambient and decreased with additional warming. Sphagnum cover declined from close to 100% of the ground area to <50% in the warmest enclosures. After three years of warming, annual Sphagnum productivity declined linearly with increasing temperature (13-29 g C/m2 per °C warming) due to widespread desiccation and loss of Sphagnum. Productivity was less in elevated CO2 enclosures, which we attribute to increased shading by shrubs. Sphagnum desiccation and growth responses were associated with the effects of warming on hydrology. The rapid decline of the Sphagnum community with sustained warming, which appears to be irreversible, can be expected to have many follow-on consequences to the structure and function of this and similar ecosystems, with significant feedbacks to the global carbon cycle and climate change.

Root and Rhizosphere Bacterial Phosphatase Activity Varies with Tree Species and Soil Phosphorus Availability in Puerto Rico Tropical Forest.

Tropical forests generally occur on highly weathered soils that, in combination with the immobility of phosphorus (P), often result in soils lacking orthophosphate, the form of P most easily metabolized by plants and microbes. In these soils, mineralization of organic P can be the major source for orthophosphate. Both plants and microbes encode for phosphatases capable of mineralizing a range of organic P compounds. However, the activity of these enzymes depends on several edaphic factors including P availability, tree species, and microbial communities. Thus, phosphatase activity in both roots and the root microbial community constitute an important role in P mineralization and P nutrient dynamics that are not well studied in tropical forests. To relate phosphatase activity of roots and bacteria in tropical forests, we measured phosphatase activity in roots and bacterial isolates as well as bacterial community composition from the rhizosphere. Three forests in the Luquillo Mountains of Puerto Rico were selected to represent a range of soil P availability as measured using the resin P method. Within each site, a minimum of three tree species were chosen to sample. Root and bacterial phosphatase activity were both measured using a colorimetric assay with para-nitrophenyl phosphate as a substrate for the phosphomonoesterase enzyme. Both root and bacterial phosphatase were chiefly influenced by tree species. Though tree species was the only significant factor in root phosphatase activity, there was a negative trend between soil P availability and phosphatase activity in linear regressions of average root phosphatase and resin P. Permutational multivariate analysis of variance of bacterial community composition based on 16S amplicon sequencing indicated that bacterial composition was strongly controlled by soil P availability (p-value < 0.05). These results indicate that although root and bacterial phosphatase activity were influenced by tree species; bacterial community composition was chiefly influenced by P availability. Although the sample size is limited given the tremendous diversity of tropical forests, our study indicates the importance of roots and bacterial function to understanding phosphatase activity. Future work will broaden the diversity of tree species and microbial members sampled to provide insight into P mineralization and model representation of tropical forests.

Needle age and season influence photosynthetic temperature response and total annual carbon uptake in mature Picea mariana trees.

BACKGROUND AND AIMS: The carbon (C) balance of boreal terrestrial ecosystems is sensitive to increasing temperature, but the direction and thresholds of responses are uncertain. Annual C uptake in Picea and other evergreen boreal conifers is dependent on seasonal- and cohort-specific photosynthetic and respiratory temperature response functions, so this study examined the physiological significance of maintaining multiple foliar cohorts for Picea mariana trees within an ombrotrophic bog ecosystem in Minnesota, USA. METHODS: Measurements were taken on multiple cohorts of needles for photosynthetic capacity, foliar respiration (Rd) and leaf biochemistry and morphology of mature trees from April to October over 4 years. The results were applied to a simple model of canopy photosynthesis in order to simulate annual C uptake by cohort age under ambient and elevated temperature scenarios. KEY RESULTS: Temperature responses of key photosynthetic parameters [i.e. light-saturated rate of CO2 assimilation (Asat), rate of Rubisco carboxylation (Vcmax) and electron transport rate (Jmax)] were dependent on season and generally less responsive in the developing current-year (Y0) needles compared with 1-year-old (Y1) or 2-year-old (Y2) foliage. Temperature optimums ranged from 18·7 to 23·7, 31·3 to 38·3 and 28·7 to 36·7 °C for Asat, Vcmax and Jmax, respectively. Foliar cohorts differed in their morphology and photosynthetic capacity, which resulted in 64 % of modelled annual stand C uptake from Y1&2 cohorts (LAI 0·67 m(2 )m(-2)) and just 36 % from Y0 cohorts (LAI 0·52 m(2 )m(-2)). Under warmer climate change scenarios, the contribution of Y0 cohorts was even less; e.g. 31 % of annual C uptake for a modelled 9 °C rise in mean summer temperatures. Results suggest that net annual C uptake by P. mariana could increase under elevated temperature, and become more dependent on older foliar cohorts. CONCLUSIONS: Collectively, this study illustrates the physiological and ecological significance of different foliar cohorts, and indicates the need for seasonal- and cohort-specific model parameterization when estimating C uptake capacity of boreal forest ecosystems under ambient or future temperature scenarios.