Lowland plant arrival in alpine ecosystems facilitates a decrease in soil carbon content under experimental climate warming.

Climate warming is releasing carbon from soils around the world, constituting a positive climate feedback. Warming is also causing species to expand their ranges into new ecosystems. Yet, in most ecosystems, whether range expanding species will amplify or buffer expected soil carbon loss is unknown. Here, we used two whole-community transplant experiments and a follow-up glasshouse experiment to determine whether the establishment of herbaceous lowland plants in alpine ecosystems influences soil carbon content under warming. We found that warming (transplantation to low elevation) led to a negligible decrease in alpine soil carbon content, but its effects became significant and 52% ± 31% (mean ± 95% confidence intervals) larger after lowland plants were introduced at low density into the ecosystem. We present evidence that decreases in soil carbon content likely occurred via lowland plants increasing rates of root exudation, soil microbial respiration, and CO2 release under warming. Our findings suggest that warming-induced range expansions of herbaceous plants have the potential to alter climate feedbacks from this system, and that plant range expansions among herbaceous communities may be an overlooked mediator of warming effects on carbon dynamics.

In a terrestrial ecosystem, the carbon cycle primarily represents the balance between plants consuming carbon dioxide from the atmosphere and soil microbes releasing carbon stored in the soil into the atmosphere (mostly as carbon dioxide). Given that carbon dioxide traps heat in the atmosphere, the balance of carbon inputs and outputs from an ecosystem can have important consequences for climate change. Rising temperatures caused by climate warming have led plants from lowland ecosystems to migrate uphill and start growing in alpine ecosystems, where temperatures are lower and most carbon is stored in the soil. Soil microbes use carbon stored in the soil and exuded from plants to grow, and they release this carbon ­ in the form of carbon dioxide ­ into the atmosphere through respiration. Walker et al. wanted to know how the arrival of lowland plants in alpine ecosystems under climate warming would affect carbon stores in the soil. To answer this question, Walker et al. simulated warmer temperatures by moving turfs (plants and soil) from alpine ecosystems to a warmer downhill site and planting lowland plants into the turfs. They compared the concentration of soil carbon in these turfs to that of soil in alpine turfs that had not been moved downhill and had no lowland plants. Their results showed that the warmed turfs containing lowland plants had a lower concentration of soil carbon. This suggests that climate warming will lead to more soil carbon being released into the atmosphere if lowland plants also migrate into alpine ecosystems. Walker et al. also wanted to know the mechanism through which lowland plants were decreasing soil carbon concentration under warming. They find that lowland plants probably release more small molecules into the soil than alpine plants. Soil microbes use the carbon and nutrients in these molecules to break down more complex molecules in the soil, thereby releasing nutrients and carbon that can then be used in respiration. This finding suggests that soil microbes breakdown and respire native soil carbon faster in the presence of lowland plants, releasing more carbon dioxide into the atmosphere and reducing carbon stores in the soil. Walker et al.'s results reveal a new mechanism through which uphill migration of lowland plants could increase the effects of climate change, in a feedback loop. Further research as to whether this mechanism occurs in different regions and ecosystems could help to quantify the magnitude of this feedback and allow scientists to make more accurate predictions about climate change.

Cropping systems alter hydraulic traits of barley but not pea grown in mixture.

Extreme events such as drought and heatwaves are among the biggest challenges to agricultural production and food security. However, the effects of cropping systems on drought resistance of arable crops via their hydraulic behaviour remain unclear. We investigated how hydraulic traits of a field-grown pea-barley (Pisum sativum L. and Hordeum vulgare L.) mixture were affected by different cropping systems, that is, organic and conventional farming with intensive or conservation tillage. Xylem vulnerability to cavitation of both species was estimated by measuring the pressure inducing 50% loss of hydraulic conductivity (P50 ), while the water stress plants experienced in the field were assessed using native percentage loss of hydraulic conductivity (nPLC). Pea and barley showed contrasting hydraulic behaviours: pea was less vulnerable to xylem cavitation and less stressed than barley; cropping systems affected the xylem vulnerability of barley, but not of pea. Barley grown under conventional farming with no tillage was more vulnerable and stressed than under organic farming with intensive tillage. nPLC proved to be a valuable indicator for plant water stress. Our results highlight the impact of cropping systems on crop xylem vulnerability and drought resistance, thus plant hydraulic traits, for protecting food security under future climate.

Genetically Different Isolates of the Arbuscular Mycorrhizal Fungus Rhizophagus irregularis Induce Differential Responses to Stress in Cassava.

Water scarcity negatively impacts global crop yields and climate change is expected to greatly increase the severity of future droughts. The use of arbuscular mycorrhizal fungi (AMF) can potentially mitigate the effects of water stress in plants. Cassava is a crop that feeds approximately 800 million people daily. Genetically different isolates of the AMF R. irregularis as well as their clonal progeny have both been shown to greatly alter cassava growth in field conditions. Given that cassava experiences seasonal drought in many of the regions in which it is cultivated, we evaluated whether intraspecific variation in R. irregularis differentially alters physiological responses of cassava to water stress. In a first experiment, conducted in field conditions in Western Kenya, cassava was inoculated with two genetically different R. irregularis isolates and their clonal progeny. All cassava plants exhibited physiological signs of stress during the dry period, but the largest differences occurred among plants inoculated with clonal progeny of each of the two parental fungal isolates. Because drought had not been experimentally manipulated in the field, we conducted a second experiment in the greenhouse where cassava was inoculated with two genetically different R. irregularis isolates and subjected to drought, followed by re-watering, to allow recovery. Physiological stress responses of cassava to drought differed significantly between plants inoculated with the two different fungi. However, plants that experienced higher drought stress also recovered at a faster rate following re-watering. We conclude that intraspecific genetic variability in AMF significantly influences cassava physiological responses during water stress. This highlights the potential of using naturally existing variation in AMF to improve cassava tolerance undergoing water stress. However, the fact that clonal progeny of an AMF isolate can differentially affect how cassava copes with natural drought stress in field conditions, highlights the necessity to understand additional factors, beyond genetic variation, which can account for such large differences in cassava responses to drought.

Effects of Sphagnum Leachate on Competitive Sphagnum Microbiome Depend on Species and Time.

Plant specialized metabolites play an important role in soil carbon (C) and nutrient fluxes. Through anti-microbial effects, they can modulate microbial assemblages and associated microbial-driven processes, such as nutrient cycling, so to positively or negatively cascade on plant fitness. As such, plant specialized metabolites can be used as a tool to supplant competitors. These compounds are little studied in bryophytes. This is especially notable in peatlands where Sphagnum mosses can dominate the vegetation and show strong interspecific competition. Sphagnum mosses form carpets where diverse microbial communities live and play a crucial role in Sphagnum fitness by regulating C and nutrient cycling. Here, by means of a microcosm experiment, we assessed to what extent moss metabolites of two Sphagnum species (S. fallax and S. divinum) modulate the competitive Sphagnum microbiome, with particular focus on microbial respiration. Using a reciprocal leachate experiment, we found that interactions between Sphagnum leachates and microbiome are species-specific. We show that both Sphagnum leachates differed in compound richness and compound relative abundance, especially sphagnum acid derivates, and that they include microbial-related metabolites. The addition of S. divinum leachate on the S. fallax microbiome immediately reduced microbial respiration (-95%). Prolonged exposition of S. fallax microbiome to S. divinum leachate destabilized the food web structure due to a modulation of microbial abundance. In particular, leachate addition decreased the biomass of testate amoebae and rotifers but increased that of ciliates. These changes did not influence microbial CO2 respiration, suggesting that the structural plasticity of the food web leads to its functional resistance through the replacement of species that are functionally redundant. In contrast, S. fallax leachate neither affected S. divinum microbial respiration, nor microbial biomass. We, however, found that S. fallax leachate addition stabilized the food web structure associated to S. divinum by changing trophic interactions among species. The differences in allelopathic effects between both Sphagnum leachates might impact their competitiveness and affect species distribution at local scale. Our study further paves the way to better understand the role of moss and microbial specialized metabolites in peatland C dynamics.

Effects of climate warming on Sphagnum photosynthesis in peatlands depend on peat moisture and species-specific anatomical traits.

Climate change will influence plant photosynthesis by altering patterns of temperature and precipitation, including their variability and seasonality. Both effects may be important for peatlands as the carbon (C) sink potential of these ecosystems depends on the balance between plant C uptake through photosynthesis and microbial decomposition. Here, we show that the effect of climate warming on Sphagnum community photosynthesis toggles from positive to negative as the peatland goes from rainy to dry periods during summer. More particularly, we show that mechanisms of compensation among the dominant Sphagnum species (Sphagnum fallax and Sphagnum medium) stabilize the average photosynthesis and productivity of the Sphagnum community during summer despite rising temperatures and frequent droughts. While warming had a negligible effect on S. medium photosynthetic capacity (Amax ) during rainy periods, Amax of S. fallax increased by 40%. On the opposite, warming exacerbated the negative effects of droughts on S. fallax with an even sharper decrease of its Amax while S. medium Amax remained unchanged. S. medium showed a remarkable resistance to droughts due to anatomical traits favouring its water holding capacity. Our results show that different phenotypic plasticity among dominant Sphagnum species allow the community to cope with rising temperatures and repeated droughts, maintaining similar photosynthesis and productivity over summer in warmed and control conditions. These results are important because they provide information on how soil water content may modulate the effects of climate warming on Sphagnum productivity in boreal peatlands. It further confirms the transitory nature of warming-induced photosynthesis benefits in boreal systems and highlights the vulnerability of the ecosystem to excess warming and drying.

Responses of plant leaf economic and hydraulic traits mediate the effects of early- and late-season drought on grassland productivity.

Drought can occur at different times during the grassland growing season, likely having contrasting effects on forage production when happening early or later in the season. However, knowledge about the interacting effects of the timing of drought and the development stage of the vegetation during the growing season is still scarce, thus limiting our ability to accurately predict forage quantity losses. To investigate plant community responses to drought seasonality (early- vs. late-season), we established a drought experiment in two permanent grasslands of the Swiss Jura Mountains that are used for forage production. We measured three plant functional traits, including two leaf traits related to plant economics (specific leaf area, SLA; leaf dry matter content, LDMC) and one hydraulic trait related to physiological function (predicted percentage loss of hydraulic conductance, PLCp), of the most abundant species, and plant above-ground biomass production. Plant species composition was also determined to calculate community-weighted mean (CWM) traits. First, we observed that CWM trait values strongly varied during the growing season. Second, we found that late-season drought had stronger effects on CWM trait values than early-season drought and that the plant hydraulic trait was the most variable functional trait. Using a structural equation model, we also showed that reduction in soil moisture had no direct impacts on above-ground biomass production. Instead, we observed that the drought-induced decrease in above-ground biomass production was mediated by a higher CWM PLCp (i.e. higher risk of hydraulic failure) and lower CWM SLA under drought. Change in CWM SLA in response to drought was the best predictor of community above-ground biomass production. Our findings reveal the importance of drought timing together with the plant trait responses to assess drought impacts on grassland biomass production and suggest that incorporating these factors into mechanistic models could considerably improve predictions of climate change impacts.

Plastic and genetic responses of a common sedge to warming have contrasting effects on carbon cycle processes.

Climate warming affects plant physiology through genetic adaptation and phenotypic plasticity, but little is known about how these mechanisms influence ecosystem processes. We used three elevation gradients and a reciprocal transplant experiment to show that temperature causes genetic change in the sedge Eriophorum vaginatum. We demonstrate that plants originating from warmer climate produce fewer secondary compounds, grow faster and accelerate carbon dioxide (CO2 ) release to the atmosphere. However, warmer climate also caused plasticity in E. vaginatum, inhibiting nitrogen metabolism, photosynthesis and growth and slowing CO2 release into the atmosphere. Genetic differentiation and plasticity in E. vaginatum thus had opposing effects on CO2 fluxes, suggesting that warming over many generations may buffer, or reverse, the short-term influence of this species over carbon cycle processes. Our findings demonstrate the capacity for plant evolution to impact ecosystem processes, and reveal a further mechanism through which plants will shape ecosystem responses to climate change.

Fagopyrum esculentum Alters Its Root Exudation after Amaranthus retroflexus Recognition and Suppresses Weed Growth.

Weed control by crops through growth suppressive root exudates is a promising alternative to herbicides. Buckwheat (Fagopyrum esculentum) is known for its weed suppression and redroot pigweed (Amaranthus retroflexus) control is probably partly due to allelopathic root exudates. This work studies whether other weeds are also suppressed by buckwheat and if the presence of weeds is necessary to induce growth repression. Buckwheat and different weeds were co-cultivated in soil, separating roots by a mesh allowing to study effects due to diffusion. Buckwheat suppressed growth of pigweed, goosefoot and barnyard grass by 53, 42, and 77% respectively without physical root interactions, probably through allelopathic compounds. Root exudates were obtained from sand cultures of buckwheat (BK), pigweed (P), and a buckwheat/pigweed mixed culture (BK-P). BK-P root exudates inhibited pigweed root growth by 49%. Characterization of root exudates by UHPLC-HRMS and principal component analysis revealed that BK and BK-P had a different metabolic profile suggesting that buckwheat changes its root exudation in the presence of pigweed indicating heterospecific recognition. Among the 15 different markers, which were more abundant in BK-P, tryptophan was identified and four others were tentatively identified. Our findings might contribute to the selection of crops with weed suppressive effects.

Vapor-pressure deficit and extreme climatic variables limit tree growth.

Assessing the effect of global warming on forest growth requires a better understanding of species-specific responses to climate change conditions. Norway spruce and European beech are among the dominant tree species in Europe and are largely used by the timber industry. Their sensitivity to changes in climate and extreme climatic events, however, endangers their future sustainability. Identifying the key climatic factors limiting their growth and survival is therefore crucial for assessing the responses of these two species to ongoing climate change. We studied the vulnerability of beech and spruce to warmer and drier conditions by transplanting saplings from the top to the bottom of an elevational gradient in the Jura Mountains in Switzerland. We (1) demonstrated that a longer growing season due to warming could not fully account for the positive growth responses, and the positive effect on sapling productivity was species-dependent, (2) demonstrated that the contrasting growth responses of beech and spruce were mainly due to different sensitivities to elevated vapor-pressure deficits (VPD), (3) determined the species-specific limits to VPD above which growth rate began to decline, and (4) demonstrated that models incorporating extreme climatic events could account for the response of growth to warming better than models using only average values. These results support that the sustainability of forest trees in the coming decades will depend on how extreme climatic events will change, irrespective of the overall warming trend.

Global warming leads to more uniform spring phenology across elevations.

One hundred years ago, Andrew D. Hopkins estimated the progressive delay in tree leaf-out with increasing latitude, longitude, and elevation, referred to as "Hopkins' bioclimatic law." What if global warming is altering this well-known law? Here, based on ∼20,000 observations of the leaf-out date of four common temperate tree species located in 128 sites at various elevations in the European Alps, we found that the elevation-induced phenological shift (EPS) has significantly declined from 34 d⋅1,000 m-1 conforming to Hopkins' bioclimatic law in 1960, to 22 d⋅1,000 m-1 in 2016, i.e., -35%. The stronger phenological advance at higher elevations, responsible for the reduction in EPS, is most likely to be connected to stronger warming during late spring as well as to warmer winter temperatures. Indeed, under similar spring temperatures, we found that the EPS was substantially reduced in years when the previous winter was warmer. Our results provide empirical evidence for a declining EPS over the last six decades. Future climate warming may further reduce the EPS with consequences for the structure and function of mountain forest ecosystems, in particular through changes in plant-animal interactions, but the actual impact of such ongoing change is today largely unknown.

Asymmetric effects of cooler and warmer winters on beech phenology last beyond spring.

In temperate trees, the timings of plant growth onset and cessation affect biogeochemical cycles, water, and energy balance. Currently, phenological studies largely focus on specific phenophases and on their responses to warming. How differently spring phenology responds to the warming and cooling, and affects the subsequent phases, has not been yet investigated in trees. Here, we exposed saplings of Fagus sylvatica L. to warmer and cooler climate during the winter 2013-2014 by conducting a reciprocal transplant experiment between two elevations (1,340 vs. 371 m a.s.l., ca. 6°C difference) in the Swiss Jura mountains. To test the legacy effects of earlier or later budburst on the budset timing, saplings were moved back to their original elevation shortly after the occurrence of budburst in spring 2014. One degree decrease in air temperature in winter/spring resulted in a delay of 10.9 days in budburst dates, whereas one degree of warming advanced the date by 8.8 days. Interestingly, we also found an asymmetric effect of the warmer winter vs. cooler winter on the budset timing in late summer. Budset of saplings that experienced a cooler winter was delayed by 31 days compared to the control, whereas it was delayed by only 10 days in saplings that experienced a warmer winter. Budburst timing in 2015 was not significantly impacted by the artificial advance or delay of the budburst timing in 2014, indicating that the legacy effects of the different phenophases might be reset during each winter. Adapting phenological models to the whole annual phenological cycle, and considering the different response to cooling and warming, would improve predictions of tree phenology under future climate warming conditions.

Herbaceous Angiosperms Are Not More Vulnerable to Drought-Induced Embolism Than Angiosperm Trees.

The water transport pipeline in herbs is assumed to be more vulnerable to drought than in trees due to the formation of frequent embolisms (gas bubbles), which could be removed by the occurrence of root pressure, especially in grasses. Here, we studied hydraulic failure in herbaceous angiosperms by measuring the pressure inducing 50% loss of hydraulic conductance (P50) in stems of 26 species, mainly European grasses (Poaceae). Our measurements show a large range in P50 from -0.5 to -7.5 MPa, which overlaps with 94% of the woody angiosperm species in a worldwide, published data set and which strongly correlates with an aridity index. Moreover, the P50 values obtained were substantially more negative than the midday water potentials for five grass species monitored throughout the entire growing season, suggesting that embolism formation and repair are not routine and mainly occur under water deficits. These results show that both herbs and trees share the ability to withstand very negative water potentials without considerable embolism formation in their xylem conduits during drought stress. In addition, structure-function trade-offs in grass stems reveal that more resistant species are more lignified, which was confirmed for herbaceous and closely related woody species of the daisy group (Asteraceae). Our findings could imply that herbs with more lignified stems will become more abundant in future grasslands under more frequent and severe droughts, potentially resulting in lower forage digestibility.

Loss of testate amoeba functional diversity with increasing frost intensity across a continental gradient reduces microbial activity in peatlands.

Soil microbial communities significantly contribute to global fluxes of nutrients and carbon. Their response to climate change, including winter warming, is expected to modify these processes through direct effects on microbial functions due to osmotic stress, and changing temperature regimes. Using four European peatlands reflecting different frequencies of frost events, we show that peatland testate amoeba communities diverge among sites with different winter climates, and that this is reflected through contrasting functions. We found that exposure to harder soil frost promoted species ß-diversity (species turnover) thus shifting the community composition of testate amoebae. In particular, we found that harder soil frost, and lower water-soluble phenolic compounds, induced functional turnover through the decrease of large species (-68%, >80µm) and the increase of small-bodied mixotrophic species (i.e. Archerella flavum; +79%). These results suggest that increased exposure to soil frost could be highly limiting for large species while smaller species are more resistant. Furthermore, we found that ß-glucosidase enzymatic activity, in addition to soil temperature, strongly depended of the functional diversity of testate amoebae (R2=0.95, ANOVA). Changing winter conditions can therefore strongly impact peatland decomposition process, though it remains unclear if these changes are carried-over to the growing season.

Persistent high temperature and low precipitation reduce peat carbon accumulation.

Extreme climate events are predicted to become more frequent and intense. Their ecological impacts, particularly on carbon cycling, can differ in relation to ecosystem sensitivity. Peatlands, being characterized by peat accumulation under waterlogged conditions, can be particularly sensitive to climate extremes if the climate event increases soil oxygenation. However, a mechanistic understanding of peatland responses to persistent climate extremes is still lacking, particularly in terms of aboveground-belowground feedback. Here, we present the results of a transplantation experiment of peat mesocosms from high to low altitude in order to simulate, during 3 years, a mean annual temperature c. 5 °C higher and a mean annual precipitation c. 60% lower. Specifically, we aim at understanding the intensity of changes for a set of biogeochemical processes and their feedback on carbon accumulation. In the transplanted mesocosms, plant productivity showed a species-specific response depending on plant growth forms, with a significant decrease (c. 60%) in peat moss productivity. Soil respiration almost doubled and Q10 halved in the transplanted mesocosms in combination with an increase in activity of soil enzymes. Spectroscopic characterization of peat chemistry in the transplanted mesocosms confirmed the deepening of soil oxygenation which, in turn, stimulated microbial decomposition. After 3 years, soil carbon stock increased only in the control mesocosms whereas a reduction in mean annual carbon accumulation of c. 30% was observed in the transplanted mesocosms. Based on the above information, a structural equation model was built to provide a mechanistic understanding of the causal connections between peat moisture, vegetation response, soil respiration and carbon accumulation. This study identifies, in the feedback between plant and microbial responses, the primary pathways explaining the reduction in carbon accumulation in response to recurring climate extremes in peat soils.

An unexpected role for mixotrophs in the response of peatland carbon cycling to climate warming.

Mixotrophic protists are increasingly recognized for their significant contribution to carbon (C) cycling. As phototrophs they contribute to photosynthetic C fixation, whilst as predators of decomposers, they indirectly influence organic matter decomposition. Despite these direct and indirect effects on the C cycle, little is known about the responses of peatland mixotrophs to climate change and the potential consequences for the peatland C cycle. With a combination of field and microcosm experiments, we show that mixotrophs in the Sphagnum bryosphere play an important role in modulating peatland C cycle responses to experimental warming. We found that five years of consecutive summer warming with peaks of +2 to +8°C led to a 50% reduction in the biomass of the dominant mixotrophs, the mixotrophic testate amoebae (MTA). The biomass of other microbial groups (including decomposers) did not change, suggesting MTA to be particularly sensitive to temperature. In a microcosm experiment under controlled conditions, we then manipulated the abundance of MTA, and showed that the reported 50% reduction of MTA biomass in the field was linked to a significant reduction of net C uptake (-13%) of the entire Sphagnum bryosphere. Our findings suggest that reduced abundance of MTA with climate warming could lead to reduced peatland C fixation.

Effects of an extended drought period on physiological properties of grassland species in the field.

A very high percentage (around 70%) of the agronomic area in Switzerland is covered by grasslands at various altitudes where environmental conditions, management, community structure and productivity vary widely. As heat waves and drought are predicted to increase in future climate, survival of plant species in grasslands is a major issue of concern in Central Europe. The effect of summer drought on representative grasslands in Switzerland was studied through drought experiments (using rain-out shelters avoiding natural precipitation) to understand the response of predominant species to changed climatic conditions. The physiological performance (gas exchange, leaf water potential) of selected species was investigated at three locations in Switzerland. The pre-dawn leaf water potential of all species was lower (more negative) under the dryer conditions at the three sites. Net photosynthesis and stomatal conductance of forb and legume species did not show major changes under drought, while grass species showed large decreases at the lowland site. These differences between forb-legume and grass species were not observed at the pre-alpine and alpine site. The apparent drought tolerance of the forb-legume species seems to be due-at least partially-to increased water use efficiency under drought conditions.

Genotypic variation in drought stress response and subsequent recovery of wheat (Triticum aestivum L.).

Three wheat (Triticum aestivum L.) genotypes, Sadovo, Katya and Prelom, with different tolerance to drought were comparatively evaluated in terms of leaf respiratory responses to progressing dehydration and consecutive rewatering. Under drought stress, the respiration of all varieties gradually decreased, as the drought-tolerant Katya showed the most pronounced decline at earlier stages of dehydration. When water stress intensified, this genotype gave relatively stable respiration rates compared with the drought-sensitive varieties. Additionally, dehydrated Katya leaves displayed lower stomatal conductance and higher photosynthesis values, which resulted in greater water use efficiency during the dehydration period. Combination of drought stress and short-term changes in leaf temperature also induced genotype-specific response that differed from the response to drought only. Over the whole temperature range, the leaves of Katya exposed to dehydration for 14 days, showed higher respiration rates compared to the drought-sensitive varieties. The sensitive varieties maintained higher respiration rates under control conditions and mild dehydration, and very low rates under severe drought. In Katya, respiration and photosynthesis were fully restored from the stress within the first day of rewatering. The drought-sensitive genotypes displayed a considerably slower recovering capacity. The results are discussed in terms of possible physiological mechanisms underlying plant tolerance to drought.