The Sphagnome Project: enabling ecological and evolutionary insights through a genus-level sequencing project.

Considerable progress has been made in ecological and evolutionary genetics with studies demonstrating how genes underlying plant and microbial traits can influence adaptation and even 'extend' to influence community structure and ecosystem level processes. Progress in this area is limited to model systems with deep genetic and genomic resources that often have negligible ecological impact or interest. Thus, important linkages between genetic adaptations and their consequences at organismal and ecological scales are often lacking. Here we introduce the Sphagnome Project, which incorporates genomics into a long-running history of Sphagnum research that has documented unparalleled contributions to peatland ecology, carbon sequestration, biogeochemistry, microbiome research, niche construction, and ecosystem engineering. The Sphagnome Project encompasses a genus-level sequencing effort that represents a new type of model system driven not only by genetic tractability, but by ecologically relevant questions and hypotheses.

Rain events decrease boreal peatland net CO2 uptake through reduced light availability.

Boreal peatlands store large amounts of carbon, reflecting their important role in the global carbon cycle. The short-term exchange and the long-term storage of atmospheric carbon dioxide (CO2 ) in these ecosystems are closely associated with the permanently wet surface conditions and are susceptible to drought. Especially, the single most important peat forming plant genus, Sphagnum, depends heavily on surface wetness for its primary production. Changes in rainfall patterns are expected to affect surface wetness, but how this transient rewetting affects net ecosystem exchange of CO2 (NEE) remains unknown. This study explores how the timing and characteristics of rain events during photosynthetic active periods, that is daytime, affect peatland NEE and whether rain event associated changes in environmental conditions modify this response (e.g. water table, radiation, vapour pressure deficit, temperature). We analysed an 11-year time series of half-hourly eddy covariance and meteorological measurements from Degerö Stormyr, a boreal peatland in northern Sweden. Our results show that daytime rain events systematically decreased the sink strength of peatlands for atmospheric CO2 . The decrease was best explained by rain associated reduction in light, rather than by rain characteristics or drought length. An average daytime growing season rain event reduced net ecosystem CO2 uptake by 0.23-0.54 gC m(-2) . On an annual basis, this reduction of net CO2 uptake corresponds to 24% of the annual net CO2 uptake (NEE) of the study site, equivalent to a 4.4% reduction of gross primary production (GPP) during the growing season. We conclude that reduced light availability associated with rain events is more important in explaining the NEE response to rain events than rain characteristics and changes in water availability. This suggests that peatland CO2 uptake is highly sensitive to changes in cloud cover formation and to altered rainfall regimes, a process hitherto largely ignored.

Can frequent precipitation moderate the impact of drought on peatmoss carbon uptake in northern peatlands?

Northern peatlands represent a large global carbon store that can potentially be destabilized by summer water table drawdown. Precipitation can moderate the negative impacts of water table drawdown by rewetting peatmoss (Sphagnum spp.), the ecosystem's key species. Yet, the frequency of such rewetting required for it to be effective remains unknown. We experimentally assessed the importance of precipitation frequency for Sphagnum water supply and carbon uptake during a stepwise decrease in water tables in a growth chamber. CO2 exchange and the water balance were measured for intact cores of three peatmoss species (Sphagnum majus, Sphagnum balticum and Sphagnum fuscum) representative of three hydrologically distinct peatland microhabitats (hollow, lawn and hummock) and expected to differ in their water table-precipitation relationships. Precipitation contributed significantly to peatmoss water supply when the water table was deep, demonstrating the importance of precipitation during drought. The ability to exploit transient resources was species-specific; S. fuscum carbon uptake increased linearly with precipitation frequency for deep water tables, whereas carbon uptake by S. balticum and S. majus was depressed at intermediate precipitation frequencies. Our results highlight an important role for precipitation in carbon uptake by peatmosses. Yet, the potential to moderate the impact of drought is species-specific and dependent on the temporal distribution of precipitation.

Extremely wet summer events enhance permafrost thaw for multiple years in Siberian tundra.

Permafrost thaw can accelerate climate warming by releasing carbon from previously frozen soil in the form of greenhouse gases. Rainfall extremes have been proposed to increase permafrost thaw, but the magnitude and duration of this effect are poorly understood. Here we present empirical evidence showing that one extremely wet summer (+100 mm; 120% increase relative to average June-August rainfall) enhanced thaw depth by up to 35% in a controlled irrigation experiment in an ice-rich Siberian tundra site. The effect persisted over two subsequent summers, demonstrating a carry-over effect of extremely wet summers. Using soil thermal hydrological modelling, we show that rainfall extremes delayed autumn freeze-up and rainfall-induced increases in thaw were most pronounced for warm summers with mid-summer precipitation rainfall extremes. Our results suggest that, with rainfall and temperature both increasing in the Arctic, permafrost will likely degrade and disappear faster than is currently anticipated based on rising air temperatures alone.

Global CO2 fertilization of Sphagnum peat mosses via suppression of photorespiration during the twentieth century.

Natural peatlands contribute significantly to global carbon sequestration and storage of biomass, most of which derives from Sphagnum peat mosses. Atmospheric CO2 levels have increased dramatically during the twentieth century, from 280 to > 400 ppm, which has affected plant carbon dynamics. Net carbon assimilation is strongly reduced by photorespiration, a process that depends on the CO2 to O2 ratio. Here we investigate the response of the photorespiration to photosynthesis ratio in Sphagnum mosses to recent CO2 increases by comparing deuterium isotopomers of historical and contemporary Sphagnum tissues collected from 36 peat cores from five continents. Rising CO2 levels generally suppressed photorespiration relative to photosynthesis but the magnitude of suppression depended on the current water table depth. By estimating the changes in water table depth, temperature, and precipitation during the twentieth century, we excluded potential effects of these climate parameters on the observed isotopomer responses. Further, we showed that the photorespiration to photosynthesis ratio varied between Sphagnum subgenera, indicating differences in their photosynthetic capacity. The global suppression of photorespiration in Sphagnum suggests an increased net primary production potential in response to the ongoing rise in atmospheric CO2, in particular for mire structures with intermediate water table depths.

Peatland vegetation composition and phenology drive the seasonal trajectory of maximum gross primary production.

Gross primary production (GPP) is a key driver of the peatland carbon cycle. Although many studies have explored the apparent GPP under natural light conditions, knowledge of the maximum GPP at light-saturation (GPPmax) and its spatio-temporal variation is limited. This information, however, is crucial since GPPmax essentially constrains the upper boundary for apparent GPP. Using chamber measurements combined with an external light source across experimental plots where vegetation composition was altered through long-term (20-year) nitrogen addition and artificial warming, we could quantify GPPmax in-situ and disentangle its biotic and abiotic controls in a boreal peatland. We found large spatial and temporal variations in the magnitudes of GPPmax which were related to vegetation species composition and phenology rather than abiotic factors. Specifically, we identified vegetation phenology as the main driver of the seasonal GPPmax trajectory. Abiotic anomalies (i.e. in air temperature and water table level), however, caused species-specific divergence between the trajectories of GPPmax and plant development. Our study demonstrates that photosynthetically active biomass constrains the potential peatland photosynthesis while abiotic factors act as secondary modifiers. This further calls for a better representation of species-specific vegetation phenology in process-based peatland models to improve predictions of global change impacts on the peatland carbon cycle.

Does salt stress constrain spatial distribution of dune building grasses Ammophila arenaria and Elytrichia juncea on the beach?

Rising sea levels threaten coastal safety by increasing the risk of flooding. Coastal dunes provide a natural form of coastal protection. Understanding drivers that constrain early development of dunes is necessary to assess whether dune development may keep pace with sea-level rise. In this study, we explored to what extent salt stress experienced by dune building plant species constrains their spatial distribution at the Dutch sandy coast. We conducted a field transplantation experiment and a glasshouse experiment with two dune building grasses Ammophila arenaria and Elytrigia juncea. In the field, we measured salinity and monitored growth of transplanted grasses in four vegetation zones: (I) nonvegetated beach, (II) E. juncea occurring, (III) both species co-occurring, and (IV) A. arenaria dominant. In the glasshouse, we subjected the two species to six soil salinity treatments, with and without salt spray. We monitored biomass, photosynthesis, leaf sodium, and nutrient concentrations over a growing season. The vegetation zones were weakly associated with summer soil salinity; zone I and II were significantly more saline than zones III and IV. Ammophila arenaria performed equally (zone II) or better (zones III, IV) than E. juncea, suggesting soil salinity did not limit species performance. Both species showed severe winter mortality. In the glasshouse, A. arenaria biomass decreased linearly with soil salinity, presumably as a result of osmotic stress. Elytrigia juncea showed a nonlinear response to soil salinity with an optimum at 0.75% soil salinity. Our findings suggest that soil salinity stress either takes place in winter, or that development of vegetated dunes is less sensitive to soil salinity than hitherto expected.

Forage plants of an Arctic-nesting herbivore show larger warming response in breeding than wintering grounds, potentially disrupting migration phenology.

During spring migration, herbivorous waterfowl breeding in the Arctic depend on peaks in the supply of nitrogen-rich forage plants, following a "green wave" of grass growth along their flyway to fuel migration and reproduction. The effects of climate warming on forage plant growth are expected to be larger at the Arctic breeding grounds than in temperate wintering grounds, potentially disrupting this green wave and causing waterfowl to mistime their arrival on the breeding grounds. We studied the potential effect of climate warming on timing of food peaks along the migratory flyway of the Russian population of barnacle geese using a warming experiment with open-top chambers. We measured the effect of 1.0-1.7°C experimental warming on forage plant biomass and nitrogen concentration at three sites along the migratory flyway (temperate wintering site, temperate spring stopover site, and Arctic breeding site) during 2 months for two consecutive years. We found that experimental warming increased biomass accumulation and sped up the decline in nitrogen concentration of forage plants at the Arctic breeding site but not at temperate wintering and stop-over sites. Increasing spring temperatures in the Arctic will thus shorten the food peak of nitrogen-rich forage at the breeding grounds. Our results further suggest an advance of the local food peak in the Arctic under 1-2°C climate warming, which will likely cause migrating geese to mistime their arrival at the breeding grounds, particularly considering the Arctic warms faster than the temperate regions. The combination of a shorter food peak and mistimed arrival is likely to decrease goose reproductive success under climate warming by reducing growth and survival of goslings after hatching.

A modification of the constant-head permeameter to measure saturated hydraulic conductivity of highly permeable media.

The saturated hydraulic conductivity (Ks ) is a key characteristic of porous media, describing the rate of water flow through saturated porous media. It is an indispensable parameter in a broad range of simulation models that quantify saturated and/or unsaturated water flow. The constant-head permeameter test is a common laboratory method to determine Ks on undisturbed soil samples collected from the field. In this paper we show that the application of this conventional method may result in a biased Ks in the case of highly permeable media, such as the top layer of Sphagnum peat and gravel. Tubes in the conventional permeameter, that collect water under the sample, introduce a hydraulic head-dependent resistance for highly permeable media and result in an underestimation of Ks . We present a simple and low-budget alternative of the constant-head permeameter test that overcomes the disadvantages of conventional permeameters. The new method was successfully tested on intact highly permeable peatmoss collected from a northern peatland. •Conventional constant-head permeameters underestimate Ks of highly permeable media due to flow resistance in tubing systems•We developed the low-resistance permeameter to overcome this disadvantage.•Testing of the low-resistance permeameter demonstrated no systematic bias and successful application for highly permeable media.

Including hydrological self-regulating processes in peatland models: Effects on peatmoss drought projections.

The water content of the topsoil is one of the key factors controlling biogeochemical processes, greenhouse gas emissions and biosphere - atmosphere interactions in many ecosystems, particularly in northern peatlands. In these wetland ecosystems, the water content of the photosynthetic active peatmoss layer is crucial for ecosystem functioning and carbon sequestration, and is sensitive to future shifts in rainfall and drought characteristics. Current peatland models differ in the degree in which hydrological feedbacks are included, but how this affects peatmoss drought projections is unknown. The aim of this paper was to systematically test whether the level of hydrological detail in models could bias projections of water content and drought stress for peatmoss in northern peatlands using downscaled projections for rainfall and potential evapotranspiration in the current (1991-2020) and future climate (2061-2090). We considered four model variants that either include or exclude moss (rain)water storage and peat volume change, as these are two central processes in the hydrological self-regulation of peatmoss carpets. Model performance was validated using field data of a peatland in northern Sweden. Including moss water storage as well as peat volume change resulted in a significant improvement of model performance, despite the extra parameters added. The best performance was achieved if both processes were included. Including moss water storage and peat volume change consistently reduced projected peatmoss drought frequency with >50%, relative to the model excluding both processes. Projected peatmoss drought frequency in the growing season was 17% smaller under future climate than current climate, but was unaffected by including the hydrological self-regulating processes. Our results suggest that ignoring these two fine-scale processes important in hydrological self-regulation of northern peatlands will have large consequences for projected climate change impact on ecosystem processes related to topsoil water content, such as greenhouse gas emissions.

N deposition affects N availability in interstitial water, growth of Sphagnum and invasion of vascular plants in bog vegetation.

• We studied the effects of N deposition on shrub-moss competition and the establishment and growth of invasive Betula pubescens and Molinia caerulea in intact bog vegetation removed from a site subject to 40 kg N ha -1 yr -1 . • Mesocosms with and without introduced Betula seedlings and Molinia sprouts were kept under a roof and received an equivalent of 0, 40 and 80 kg N ha -1 yr -1 for two growing seasons. • N concentration in both interstitial water and Sphagnum decreased when N input ceased and increased when N input was doubled. Molinia biomass was positively related to the inorganic N concentration in the interstitial water. Adding N increased production of Molinia and prolonged survival of Betula seedlings in the first year. Sphagnum height increment showed a hump-shaped relationship with light interception by vascular plants. • N deposition encouraged vascular plants to grow by enhancing N availability in the rhizosphere. Water table level and the availability of P were found to be important in explaining species-specific responses to N deposition. The underlying mechanisms and the reversibility of N effects are discussed.

Nutritional constraints in ombrotrophic Sphagnum plants under increasing atmospheric nitrogen deposition in Europe.

• We studied the effects of increasing levels of atmospheric nitrogen (N) deposition on nutrient limitation of ombrotrophic Sphagnum plants. • Fifteen mires in 11 European countries were selected across a natural gradient of bulk atmospheric N deposition from 0.1 to 2 g/m2  year-1 . Nutritional constraints were assessed based on nutrient ratios of N, phosphorus (P), and potassium (K) in Sphagnum plants collected in hummocks (i.e. relatively drier microhabitats) and in lawns (i.e. relatively wetter microhabitats). • Nutrient ratios in Sphagnum plants increased steeply at low atmospheric N input, but above a threshold of N deposition of c. 1 g/m2  year-1 the N : P and N : K ratios tended to saturation. Increasing atmospheric N deposition was also accompanied by a reduced retention of Ca and Mg in Sphagnum plants and a decreased stem volumetric density in hummock Sphagnum plants. • We suggest a critical load of N deposition in Europe of 1 g/m2  year-1 above which Sphagnum plants change from being N-limited to be K + P colimited, at N : P > 30 and N : K > 3.

Spatio-temporal trends of nitrogen deposition and climate effects on Sphagnum productivity in European peatlands.

To quantify potential nitrogen (N) deposition impacts on peatland carbon (C) uptake, we explored temporal and spatial trends in N deposition and climate impacts on the production of the key peat forming functional group (Sphagnum mosses) across European peatlands for the period 1900-2050. Using a modelling approach we estimated that between 1900 and 1950 N deposition impacts remained limited irrespective of geographical position. Between 1950 and 2000 N deposition depressed production between 0 and 25% relative to 1900, particularly in temperate regions. Future scenarios indicate this trend will continue and become more pronounced with climate warming. At the European scale, the consequences for Sphagnum net C-uptake remained small relative to 1900 due to the low peatland cover in high-N areas. The predicted impacts of likely changes in N deposition on Sphagnum productivity appeared to be less than those of climate. Nevertheless, current critical loads for peatlands are likely to hold under a future climate.

How does tree density affect water loss of peatlands? A mesocosm experiment.

Raised bogs have accumulated more atmospheric carbon than any other terrestrial ecosystem on Earth. Climate-induced expansion of trees and shrubs may turn these ecosystems from net carbon sinks into sources when associated with reduced water tables. Increasing water loss through tree evapotranspiration could potentially deepen water tables, thus stimulating peat decomposition and carbon release. Bridging the gap between modelling and field studies, we conducted a three-year mesocosm experiment subjecting natural bog vegetation to three birch tree densities, and studied the changes in subsurface temperature, water balance components, leaf area index and vegetation composition. We found the deepest water table in mesocosms with low tree density. Mesocosms with high tree density remained wettest (i.e. highest water tables) whereas the control treatment without trees had intermediate water tables. These differences are attributed mostly to differences in evapotranspiration. Although our mesocosm results cannot be directly scaled up to ecosystem level, the systematic effect of tree density suggests that as bogs become colonized by trees, the effect of trees on ecosystem water loss changes with time, with tree transpiration effects of drying becoming increasingly offset by shading effects during the later phases of tree encroachment. These density-dependent effects of trees on water loss have important implications for the structure and functioning of peatbogs.

Persistent versus transient tree encroachment of temperate peat bogs: effects of climate warming and drought events.

Peatlands store approximately 30% of global soil carbon, most in moss-dominated bogs. Future climatic changes, such as changes in precipitation patterns and warming, are expected to affect peat bog vegetation composition and thereby its long-term carbon sequestration capacity. Theoretical work suggests that an episode of rapid environmental change is more likely to trigger transitions to alternative ecosystem states than a gradual, but equally large, change in conditions. We used a dynamic vegetation model to explore the impacts of drought events and increased temperature on vegetation composition of temperate peat bogs. We analyzed the consequences of six patterns of summer drought events combined with five temperature scenarios to test whether an open peat bog dominated by moss (Sphagnum) could shift to a tree-dominated state. Unexpectedly, neither a gradual decrease in the amount of summer precipitation nor the occurrence of a number of extremely dry summers in a row could shift the moss-dominated peat bog permanently into a tree-dominated peat bog. The increase in tree biomass during drought events was unable to trigger positive feedbacks that keep the ecosystem in a tree-dominated state after a return to previous 'normal' rainfall conditions. In contrast, temperature increases from 1 °C onward already shifted peat bogs into tree-dominated ecosystems. In our simulations, drought events facilitated tree establishment, but temperature determined how much tree biomass could develop. Our results suggest that under current climatic conditions, peat bog vegetation is rather resilient to drought events, but very sensitive to temperature increases, indicating that future warming is likely to trigger persistent vegetation shifts.

Ecosystem responses to reduced and oxidised nitrogen inputs in European terrestrial habitats.

While it is well established that ecosystems display strong responses to elevated nitrogen deposition, the importance of the ratio between the dominant forms of deposited nitrogen (NH(x) and NO(y)) in determining ecosystem response is poorly understood. As large changes in the ratio of oxidised and reduced nitrogen inputs are occurring, this oversight requires attention. One reason for this knowledge gap is that plants experience a different NH(x):NO(y) ratio in soil to that seen in atmospheric deposits because atmospheric inputs are modified by soil transformations, mediated by soil pH. Consequently species of neutral and alkaline habitats are less likely to encounter high NH(4)(+) concentrations than species from acid soils. We suggest that the response of vascular plant species to changing ratios of NH(x):NO(y) deposits will be driven primarily by a combination of soil pH and nitrification rates. Testing this hypothesis requires a combination of experimental and survey work in a range of systems.

Swift recovery of Sphagnum nutrient concentrations after excess supply.

Although numerous studies have addressed the effects of increased N deposition on nutrient-poor environments such as raised bogs, few studies have dealt with to what extent, and on what time-scale, reductions in atmospheric N supply would lead to recovery of the ecosystems in question. Since a considerable part of the negative effects of elevated N deposition on raised bogs can be related to an imbalance in tissue nutrient concentrations of the dominant peat-former Sphagnum, changes in Sphagnum nutrient concentration after excess N supply may be used as an early indicator of ecosystem response. This study focuses on the N and P concentrations of Sphagnum magellanicum and Sphagnum fallax before, during and after a factorial fertilization experiment with N and P in two small peatlands subject to a background bulk deposition of 2 g N m(-2) year(-1). Three years of adding N (4.0 g N m(-2) year(-1)) increased the N concentration, and adding P (0.3 g P m(-2) year(-1)) increased the P concentration in Sphagnum relative to the control treatment at both sites. Fifteen months after the nutrient additions had ceased, N concentrations were similar to the control whereas P concentrations, although strongly reduced, were still slightly elevated. The changes in the N and P concentrations were accompanied by changes in the distribution of nutrients over the capitulum and the stem and were congruent with changes in translocation. Adding N reduced the stem P concentration, whereas adding P reduced the stem N concentration in favor of the capitulum. Sphagnum nutrient concentrations quickly respond to reductions in excess nutrient supply, indicating that a management policy aimed at reducing atmospheric nutrient input to bogs can yield results within a few years.

Atmospheric nitrogen deposition promotes carbon loss from peat bogs.

Peat bogs have historically represented exceptional carbon (C) sinks because of their extremely low decomposition rates and consequent accumulation of plant remnants as peat. Among the factors favoring that peat accumulation, a major role is played by the chemical quality of plant litter itself, which is poor in nutrients and characterized by polyphenols with a strong inhibitory effect on microbial breakdown. Because bogs receive their nutrient supply solely from atmospheric deposition, the global increase of atmospheric nitrogen (N) inputs as a consequence of human activities could potentially alter the litter chemistry with important, but still unknown, effects on their C balance. Here we present data showing the decomposition rates of recently formed litter peat samples collected in nine European countries under a natural gradient of atmospheric N deposition from approximately 0.2 to 2 g.m(-2).yr(-1). We found that enhanced decomposition rates for material accumulated under higher atmospheric N supplies resulted in higher carbon dioxide (CO2) emissions and dissolved organic carbon release. The increased N availability favored microbial decomposition (i) by removing N constraints on microbial metabolism and (ii) through a chemical amelioration of litter peat quality with a positive feedback on microbial enzymatic activity. Although some uncertainty remains about whether decay-resistant Sphagnum will continue to dominate litter peat, our data indicate that, even without such changes, increased N deposition poses a serious risk to our valuable peatland C sinks.