Publications

Publications in peer reviewed journals

22 Publications found
  • Contrasting drivers of belowground nitrogen cycling in a montane grassland exposed to a multifactorial global change experiment with elevated CO, warming, and drought

    Maxwell TL, Canarini A, Bogdanovic I, Böckle T, Martin V, Noll L, Prommer J, Séneca J, Simon E, Piepho HP, Herndl M, Pötsch EM, Kaiser C, Richter A, Bahn M, Wanek W
    2022 - Global Change Biology, 28: 2425-2441

    Abstract: 

    Depolymerization of high-molecular weight organic nitrogen (N) represents the major bottleneck of soil N cycling and yet is poorly understood compared to the subsequent inorganic N processes. Given the importance of organic N cycling and the rise of global change, we investigated the responses of soil protein depolymerization and microbial amino acid consumption to increased temperature, elevated atmospheric CO2, and drought. The study was conducted in a global change facility in a managed montane grassland in Austria, where elevated CO2 (eCO2) and elevated temperature (eT) were stimulated for 4 years, and were combined with a drought event. Gross protein depolymerization and microbial amino acid consumption rates (alongside with gross organic N mineralization and nitrification) were measured using 15N isotope pool dilution techniques. Whereas eCO2 showed no individual effect, eT had distinct effects which were modulated by season, with a negative effect of eT on soil organic N process rates in spring, neutral effects in summer, and positive effects in fall. We attribute this to a combination of changes in substrate availability and seasonal temperature changes. Drought led to a doubling of organic N process rates, which returned to rates found under ambient conditions within 3 months after rewetting. Notably, we observed a shift in the control of soil protein depolymerization, from plant substrate controls under continuous environmental change drivers (eT and eCO2) to controls via microbial turnover and soil organic N availability under the pulse disturbance (drought). To the best of our knowledge, this is the first study which analyzed the individual versus combined effects of multiple global change factors and of seasonality on soil organic N processes and thereby strongly contributes to our understanding of terrestrial N cycling in a future world.

  • Putting vascular epiphytes on the traits map

    Hietz P, Wagner K, Nunes Ramos F, Cabral J, Agudelo C, Benavides AM, Cach-Pérez MJ, Cardelús C, Chilpa Galván N, Costa L, de Paula Oliveira R, Einzmann H, Farias R, Guzmán JV, Kattge J, Kessler M, Kirby C, Kreft H, Kromer T, Males J, Monsalve Correa S, Moreno-Chacón M, Petter G, Reyes-Garcia C, Saldana A, Schellenberger Costa D, Taylor A, Velázquez Rosas N, Wanek W, Woods C, Zotz G
    2022 - Journal of Ecology, 110: 340-358

    Abstract: 

    1. Plant functional traits impact the fitness and environmental niche of plants. Major plant functional types have been characterized by their trait spectrum, and the environmental and phylogenetic imprints on traits have advanced several ecological fields. Yet, very few trait data on epiphytes, which represent almost 10% of vascular plants, are available.
    2. We collated 76,561 trait observations for 2,882 species of vascular epiphytes and compared these to non-epiphytic herbs and trees to test hypotheses related to how the epiphytic habit affects traits, and if epiphytes occupy a distinct region in the global trait space. We also compared variation in traits among major groups of epiphytes, and investigated the coordination of traits in epiphytes, ground-rooted herbs and trees.
    3. Epiphytes differ from ground-rooted plants mainly in traits related to water relations. Unexpectedly, we did not find lower leaf nutrient concentrations, except for nitrogen. Mean photosynthetic rates are much lower than in ground-rooted plants and lower than expected from the nitrogen concentrations. Trait syndromes clearly distinguish epiphytes from trees and from most non-epiphytic herbs.
    4. Among the three largest epiphytic taxa, orchids differ from bromeliads and ferns mainly by having smaller and more numerous stomata, while ferns differ from bromeliads by having thinner leaves, higher nutrient concentrations, and lower water content and water use efficiency.
    5. Trait networks differ among epiphytes, herbs and trees. While all have central nodes represented by SLA and mass-based photosynthesis, in epiphytes, traits related to plant water relations have stronger connections, and nutrients other than potassium have weaker connections to the remainder of the trait network. Whereas stem-specific density reflects mechanical support related to plant size in herbs and trees, in epiphytes it mostly reflects water storage and scales with leaf water content.
    6. Synthesis. Our findings advance our understanding of epiphyte ecology, but we note that currently mainly leaf traits are available. Important gaps are root, shoot and whole plant, demographic and gas exchange traits. We suggest how future research might use available data and fill data gaps.
    • We collated 76,561 trait observations for 2,882 species of vascular epiphytes and compared these to non-epiphytic herbs and trees to test hypotheses related to how the epiphytic habit affects traits, and if epiphytes occupy a distinct region in the global trait space. We also compared variation in traits among major groups of epiphytes, and investigated the coordination of traits in epiphytes, ground-rooted herbs and trees.
    • Epiphytes differ from ground-rooted plants mainly in traits related to water relations. Unexpectedly, we did not find lower leaf nutrient concentrations, except for nitrogen. Mean photosynthetic rates are much lower than in ground-rooted plants and lower than expected from the nitrogen concentrations. Trait syndromes clearly distinguish epiphytes from trees and from most non-epiphytic herbs.
    • Among the three largest epiphytic taxa, orchids differ from bromeliads and ferns mainly by having smaller and more numerous stomata, while ferns differ from bromeliads by having thinner leaves, higher nutrient concentrations, and lower water content and water use efficiency.
    • Trait networks differ among epiphytes, herbs and trees. While all have central nodes represented by SLA and mass-based photosynthesis, in epiphytes, traits related to plant water relations have stronger connections, and nutrients other than potassium have weaker connections to the remainder of the trait network. Whereas stem-specific density reflects mechanical support related to plant size in herbs and trees, in epiphytes it mostly reflects water storage and scales with leaf water content.
    • Synthesis. Our findings advance our understanding of epiphyte ecology, but we note that currently mainly leaf traits are available. Important gaps are root, shoot and whole plant, demographic and gas exchange traits. We suggest how future research might use available data and fill data gaps.
  • Soil greenhouse gas fluxes in floodplain forests of the Danube National Park – Effects of flooding and soil microclimate

    Schindlbacher A, Heinzle J, Gollobich G, Wanek W, Michel K, Kitzler K
    2022 - Biogeochemistry, 159: 193-213

    Abstract: 

    The relevance of soil greenhouse gas (GHG) fluxes from temperate floodplain forests has yet remained elusive. We studied the soil methane (CH4), nitrous oxide (N2O) and carbon dioxide (CO2) dynamics at three forest sites along a flooding gradient in the Danube National Park (Austria) to estimate annual GHG budgets and to assess if and how seasonal flooding affects individual GHG fluxes. Soil surface GHG fluxes were determined along with GHG concentrations in soil air and pore-water at a non-flooded (NF), an infrequently-flooded (IF), and a frequently-flooded (FF) site. Both study years were characterized by dry summers, and only the FF site was flooded during the study period. Soils at all sites were annual CH4 sinks (NF: − 4.50 ± 0.85, IF: − 2.54 ± 0.57, FF: − 0.67 ± 1.06 kg CH4-C ha−1 year−1) and the sink strength correlated positively with soil moisture. Pulse-like CH4 emissions were not observed during or after flooding. Soil N2O fluxes showed large temporal and spatial variations, without any significant differences between sites (average NF: 6.5 ± 7.1, IF: 10.4 ± 14.3, FF: 9.4 ± 10.5 µg N2O-N m−2 h−1). Pulse N2O emissions (up to ~ 80 µg N2O-N m−2 h−1) occurred during freeze/thaw events, but not during or after flooding. Mean annual soil CO2 effluxes at NF and IF were 9.4 ± 1.1 and 9.4 ± 2.1 t C ha−1 year−1, respectively. Soil CO2 efflux was significantly higher at the FF site (18.54 ± 6.21 t C ha−1 year−1). High soil air CO2 concentrations (> 10%) in aerated deeper soil layers indicated a substantial contribution of the usually waterlogged sub-soils to the summertime soil CO2 efflux at the FF site. Overall, our results suggest that the studied temperate floodplain forest soils do not absorb/emit substantially more CH4 and N2O than soils of comparable upland forests, whereas low groundwater level can lead to periodically enhanced CO2 emissions from normally waterlogged soil layers.

  • Vertical profiles of leaf photosynthesis and leaf traits and soil nutrients in two tropical rainforests in French Guiana before and after a 3-year nitrogen and phosphorus addition experiment

    Verryckt LT, Vicca S, Van Langenhove L, Stahl C, Asensio D, Urbina I, Ogaya R, Llusià J, Grau O, Peguero G, Gargallo-Garriga A, Courtois EA, Margalef O, Portillo-Estrada M, Ciais P, Obersteiner M, Fuchslueger L, Lugli LF, Fernandez-Garberi PR, Vallicrosa H, Verlinden M, Ranits C, Vermeir P, Coste S, Verbruggen E, Bréchet L, Sardans J, Chave J, Peñuelas J, Janssens IA
    2022 - Earth Syst. Sci. Data, 14: 5-8

    Abstract: 

    Terrestrial biosphere models typically use the biochemical model of Farquhar, von Caemmerer, and Berry (1980) to simulate photosynthesis, which requires accurate values of photosynthetic capacity of different biomes. However, data on tropical forests are sparse and highly variable due to the high species diversity, and it is still highly uncertain how these tropical forests respond to nutrient limitation in terms of C uptake. Tropical forests often grow on soils low in phosphorus (P) and are, in general, assumed to be P rather than nitrogen (N) limited. However, the relevance of P as a control of photosynthetic capacity is still debated. Here, we provide a comprehensive dataset of vertical profiles of photosynthetic capacity and important leaf traits, including leaf N and P concentrations, from two 3-year, large-scale nutrient addition experiments conducted in two tropical rainforests in French Guiana. These data present a unique source of information to further improve model representations of the roles of NP, and other leaf nutrients in photosynthesis in tropical forests. To further facilitate the use of our data in syntheses and model studies, we provide an elaborate list of ancillary data, including important soil properties and nutrients, along with the leaf data. As environmental drivers are key to improve our understanding of carbon (C) and nutrient cycle interactions, this comprehensive dataset will aid to further enhance our understanding of how nutrient availability interacts with C uptake in tropical forests. The data are available at https://doi.org/10.5281/zenodo.5638236 (Verryckt, 2021).

  • Nitrogen fixation by diverse diazotrophic communities can support population growth of arboreal ants

    Nepel M, Pfeifer J, Oberhauser FB, Richter A, Woebken D, Mayer VE
    2022 - BMC Biology, 20: Article 135

    Abstract: 

    Background

    Symbiotic ant-plant associations, in which ants live on plants, feed on plant-provided food, and protect host trees against threats, are ubiquitous across the tropics, with the Azteca-Cecropia associations being amongst the most widespread interactions in the Neotropics. Upon colonization of Cecropia’s hollow internodes, Azteca queens form small patches with plant parenchyma, which are then used as waste piles when the colony grows. Patches—found in many ant-plant mutualisms—are present throughout the colony life cycle and may supplement larval food. Despite their initial nitrogen (N)-poor substrate, patches in Cecropia accommodate fungi, nematodes, and bacteria. In this study, we investigated the atmospheric N2 fixation as an N source in patches of early and established ant colonies.

    Results

    Via 15N2 tracer assays, N2 fixation was frequently detected in all investigated patch types formed by three Azteca ant species. Quantified fixation rates were similar in early and established ant colonies and higher than in various tropical habitats. Based on amplicon sequencing, the identified microbial functional guild—the diazotrophs—harboring and transcribing the dinitrogenase reductase (nifH) gene was highly diverse and heterogeneous across Azteca colonies. The community composition differed between early and established ant colonies and partly between the ant species.

    Conclusions

    Our data show that N2 fixation can result in reasonable amounts of N in ant colonies, which might not only enable bacterial, fungal, and nematode growth in the patch ecosystems but according to our calculations can even support the growth of ant populations. The diverse and heterogeneous diazotrophic community implies a functional redundancy, which could provide the ant-plant-patch system with a higher resilience towards changing environmental conditions. Hence, we propose that N2 fixation represents a previously unknown potential to overcome N limitations in arboreal ant colonies.

  • Stoichiometric regulation of priming effects and soil carbon balance by microbial life strategies

    Zhu Z, Fang Y, Liang Y, Li Y, Liu S, Li B, Gao W, Yuan H, Kuzyakov Y, Wu J, Richter A, Ge T
    2022 - Soil Biology and Biochemistry, 169: Article 108669

    Abstract: 

    Carbon and nutrient inputs are required to stimulate the formation and mineralization of soil organic carbon (SOC) through processes related to microbial growth and priming effects (PEs). PEs are thought to affect microbial life strategies, however, the mechanisms underlying their role in SOC formation and microbial dynamics remain largely unknown, particularly in paddy soils. Here, we examined the underlying strategies and response mechanisms of microorganisms in regulating PEs and C accumulation in flooded paddy soil. Levels and stoichiometric ratios of resources were evaluated over a 60-day incubation period. Low (equivalent to 50% soil microbial biomass C [MBC]) and high (500% MBC) doses of 13C-labeled glucose were added to the soil, along with mineral N, P, and S (NPS) fertilizers at five concentrations. Glucose mineralization increased linearly with NPS concentration under both low and high glucose inputs. However, glucose addition without nutrients induced the preferential microbial utilization of the readily available C, leading to negative PEs. Under high-glucose input, the intensity of negative PEs increased with increasing NPS addition (PE: from −460 to −710 mg C kg−1 soil). In contrast, under low-glucose inputs, the intensity of positive PEs increased with increasing NPS addition (PE: 60–100 mg C kg−1 soil). High-glucose input with NPS fertilization favored high-yield microbial strategists (Y-strategists), increasing glucose-derived SOC accumulation. This phenomenon was evidenced by the large quantities of 13C detected in microbial biomass and phospholipid fatty acids (PLFAs), increasing the soil net C balance (from 0.76 to 1.2 g C kg−1). In contrast, low levels of glucose and NPS fertilization shifted the microbial community composition toward dominance of resource-acquisition strategists (A-strategists), increasing SOC mineralization. This was evidenced by 13C incorporation into the PLFAs of gram-positive bacteria, increased activity of N- and P-hydrolases, and positive PEs for acquiring C and nutrients from soil organic matter. Consequently, the soil net C balance decreased from 0.31 to 0.01 g C kg−1 soil. In conclusion, high C input (i.e., 500% MBC), particularly alongside hig NPS addition, increases SOC content via negative priming and microbial-derived C accumulation due to the shift toward Y-strategist communities which efficiently utilize resources. This study highlights the importance of mineral fertilization management when incorporating organic supplements in paddy soils to stimulate microbial turnover and C sequestration.

  • Litter diversity accelerates labile carbon but slows recalcitrant carbon decomposition

    Wang L, Zhou Y, Chen Y, Xu Z, Zhang J, Liu Y, Joly FX
    2022 - Soil Biology and Biochemistry, 168: Article 108632

    Abstract: 

    In biodiverse ecosystems, leaf litter of different plant species decomposes in mixtures, for which decomposition rates notoriously deviate from that expected from monospecific treatments. Despite important research efforts in past decades, these litter diversity effects remain difficult to predict. We hypothesized that this is due to a focus on bulk litter decomposition, while different carbon fractions constituting the litter may respond differently to litter diversity, thereby blurring the overall response. To test this hypothesis, we determined how the decomposition of (i) soluble compounds, (ii) cellulose, and (iii) lignin responded to litter mixing in a 3.5-year field experiment in an alpine forest. We found that the decomposition of soluble compounds and cellulose in mixtures was faster than expected from monospecific treatments, while that of lignin was slower. These deviations from expected decomposition rates of each litter carbon fraction were driven by different aspects of the litter functional diversity. This suggests that different mechanisms operating on distinct litter fractions lead to synergistic and antagonistic interactions that simultaneously affect bulk litter decomposition. Furthermore, the magnitude of these fraction-specific deviations from expected decomposition rates consistently decreased throughout decomposition. Considering the response of litter fractions and their temporality, rather than focusing on bulk litter thus seems critical to evaluate the response of decomposition to plant diversity and identify underlying mechanisms.

  • Crop rotational complexity affects plant-soil nitrogen cycling during water deficit

    Bowles TM, Jilling A, Morán-Rivera K, Schnecker J, Grandy AS
    2022 - Soil Biology and Biochemistry, 166: Article 108552

    Abstract: 

    One of the biggest environmental challenges facing agriculture is how to both supply and retain nitrogen (N), especially as precipitation becomes more variable with climate change. We used a greenhouse experiment to assess how contrasting histories of crop rotational complexity affect plant-soil-microbe interactions that govern N processes, including during water stress. With higher levels of carbon and N cycling hydrolytic enzymes, higher mineral-associated organic matter N concentrations, and an altered microbial community, soils from the most complex rotation enabled 80% more corn N uptake under two moisture regimes, compared to soil from monoculture corn. Higher levels of plant N likely drove the changes in corn leaf gas exchange, particularly increasing intrinsic water use efficiency by 9% in the most complex rotation. The water deficit increased the standing pool of nitrate 44-fold in soils with a history of complex crop rotations, compared to an 11-fold increase in soils from the corn monoculture. The implications of this difference must be considered in a whole cropping systems and field context. Cycling of 15N-labeled fresh clover residue into soil N pools did not depend on the water regime or rotation history, with 2-fold higher recovery in the mineral vs. particulate organic N pool. In contrast, the water deficit reduced recovery of clover 15N in corn shoots by 37%, showing greater impacts of water deficit on plant N uptake compared to organic N cycling in soil. This study provides direct experimental evidence that long-term crop rotational complexity influences microbial N cycling and availability with feedbacks to plant physiology. Collectively, these results could help explain general observations of higher yields in more complex crop rotations, including specifically during dry conditions.

  • Isotopically characterised N2O reference materials for use as community standards

    Mohn J, Biasi C, Bodé S, Boeckx P, Brewer PJ, Eggleston S, Geilmann H, Guillevic M, Kaiser J, Kantnerová K, Moossen H, Müller J, Nakagawa M, Pearce R, von Rein I, Steger D, Toyoda S, Wanek W, Wexler SK, Yoshida N, Yu L
    2022 - Rapid Communications in Mass Spectrometry, 36: Article e9296

    Abstract: 

    Rationale

    Information on the isotopic composition of nitrous oxide (N2O) at natural abundance supports the identification of its source and sink processes. In recent years, a number of mass spectrometric and laser spectroscopic techniques have been developed and are increasingly used by the research community. Advances in this active research area, however, critically depend on the availability of suitable N2O isotope Reference Materials (RMs).

    Methods

    Within the project Metrology for Stable Isotope Reference Standards (SIRS), seven pure N2O isotope RMs have been developed and their 15N/14N, 18O/16O, 17O/16O ratios and 15N site preference (SP) have been analysed by specialised laboratories against isotope reference materials. A particular focus was on the 15N site-specific isotopic composition, as this measurand is both highly diagnostic for source appointment and challenging to analyse and link to existing scales.

    Results

    The established N2O isotope RMs offer a wide spread in delta (δ) values: δ15N: 0 to +104‰, δ18O: +39 to +155‰, and δ15NSP: −4 to +20‰. Conversion and uncertainty propagation of δ15N and δ18O to the Air-N2 and VSMOW scales, respectively, provides robust estimates for δ15N(N2O) and δ18O(N2O), with overall uncertainties of about 0.05‰ and 0.15‰, respectively. For δ15NSP, an offset of >1.5‰ compared with earlier calibration approaches was detected, which should be revisited in the future.

    Conclusions

    A set of seven N2O isotope RMs anchored to the international isotope-ratio scales was developed that will promote the implementation of the recommended two-point calibration approach. Particularly, the availability of δ17O data for N2O RMs is expected to improve data quality/correction algorithms with respect to δ15NSP and δ15N analysis by mass spectrometry. We anticipate that the N2O isotope RMs will enhance compatibility between laboratories and accelerate research progress in this emerging field.

  • Plant-microbial linkages underpin carbon sequestration in contrasting mountain tundra vegetation types

    Gavazov K, Canarini A, Jassey VEJ, Mills R, Richter A, Sundqvist MK, Väisänen M, Walker TWN, Wardle DA, Dorrepaal E
    2022 - Soil Biology and Biochemistry, Article 108530

    Abstract: 

    Tundra ecosystems hold large stocks of soil organic matter (SOM), likely due to low temperatures limiting rates of microbial SOM decomposition more than those of SOM accumulation from plant primary productivity and microbial necromass inputs. Here we test the hypotheses that distinct tundra vegetation types and their carbon supply to characteristic rhizosphere microbes determine SOM cycling independent of temperature. In the subarctic Scandes, we used a three-way factorial design with paired heath and meadow vegetation at each of two elevations, and with each combination of vegetation type and elevation subjected during one growing season to either ambient light (i.e., ambient plant productivity), or 95% shading (i.e., reduced plant productivity). We assessed potential above- and belowground ecosystem linkages by uni- and multivariate analyses of variance, and structural equation modelling. We observed direct coupling between tundra vegetation type and microbial community composition and function, which underpinned the ecosystem's potential for SOM storage. Greater primary productivity at low elevation and ambient light supported higher microbial biomass and nitrogen immobilisation, with lower microbial mass-specific enzymatic activity and SOM humification. Congruently, larger SOM at lower elevation and in heath sustained fungal-dominated microbial communities, which were less substrate-limited, and invested less into enzymatic SOM mineralisation, owing to a greater carbon-use efficiency (CUE). Our results highlight the importance of tundra plant community characteristics (i.e., productivity and vegetation type), via their effects on soil microbial community size, structure and physiology, as essential drivers of SOM turnover. The here documented concerted patterns in above- and belowground ecosystem functioning is strongly supportive of using plant community characteristics as surrogates for assessing tundra carbon storage potential and its evolution under climate and vegetation changes.

  • Long-term soil warming alters fine root dynamics and morphology, and their ectomycorrhizal fungal community in a temperate forest soil

    Kwatcho Kengdo S, Peršoh D, Schindlbacher A, Heinzle J, Tian Y, Wanek W, Borken W
    2022 - Global Change Biology, in press

    Abstract: 

    Climate warming is predicted to affect temperate forests severely, but the response of fine roots, key to plant nutrition, water uptake, soil carbon, and nutrient cycling is unclear. Understanding how fine roots will respond to increasing temperature is a prerequisite for predicting the functioning of forests in a warmer climate. We studied the response of fine roots and their ectomycorrhizal (EcM) fungal and root-associated bacterial communities to soil warming by 4°C in a mixed spruce-beech forest in the Austrian Limestone Alps after 8 and 14 years of soil warming, respectively. Fine root biomass (FRB) and fine root production were 17% and 128% higher in the warmed plots, respectively, after 14 years. The increase in FRB (13%) was not significant after 8 years of treatment, whereas specific root length, specific root area, and root tip density were significantly higher in warmed plots at both sampling occasions. Soil warming did not affect EcM exploration types and diversity, but changed their community composition, with an increase in the relative abundance of Cenoccocum at 0–10 cm soil depth, a drought-stress-tolerant genus, and an increase in short- and long-distance exploration types like Sebacina and Boletus at 10–20 cm soil depth. Warming increased the root-associated bacterial diversity but did not affect their community composition. Soil warming did not affect nutrient concentrations of fine roots, though we found indications of limited soil phosphorus (P) and potassium (K) availability. Our findings suggest that, in the studied ecosystem, global warming could persistently increase soil carbon inputs due to accelerated fine root growth and turnover, and could simultaneously alter fine root morphology and EcM fungal community composition toward improved nutrient foraging.

  • Growth of soil microbes is not limited by the availability of nitrogen and phosphorus in a Mediterranean oak-savanna

    Morris KA, Richter A, Migliavacca M, Schrumpf M
    2022 - Soil Biology and Biochemistry, 169: Article 108680

    Abstract: 

    The environmental conditions under which the availability of inorganic nutrients such as nitrogen (N) and phosphorus (P) influence soil microbial growth are poorly understood, especially with regards to how fertilization changes specific aspects of microbial growth such as carbon-use efficiency (CUE). Microbial CUE is the fraction of C converted into biomass out of all C taken in and plays a critical role in global C budgets. Using the 18O labeled water method we tested short vs. long-term effects of N and/or P fertilization on microbial growth, CUE, and C, N, and P-acquiring enzyme activities in two soils from an oak-savanna, which differ in their soil organic matter (SOM) content. We hypothesized that soils with more SOM (from under tree canopies) would have higher microbial growth rates than soils with less SOM (from open grassland), and that microbial growth and CUE would increase with fertilization. We further hypothesized that these increases would be associated with a decrease in enzyme activity and a shift towards older SOM substrates in the short-term, in contrast to substrates from recently fixed C resulting from increased plant productivity in the long-term. We found that nutrient additions did not affect microbial growth or CUE in the relatively high SOM habitat on either time scale. In contrast, the low SOM habitat had lower growth and CUE when single nutrients were added, with significantly reduced growth when P alone was added, but was unchanged when N and P were added together. Our results show that short-term, stoichiometric imbalances can reduce microbial growth and that microbial growth at this site is limited not by nutrients but by the amount of C available to soil microbes.

  • Long-term warming reduced microbial biomass but increased recent plant-derived C in microbes of a subarctic grassland

    Verbrigghe N, Meeran K, Bahn M, Canarini A, Fransen E, Fuchslueger L, Ingrisch J, Janssens IA, Richter A, Sigurdsson BD, Soong JL, Vicca S
    2022 - Soil Biology and Biochemistry, 167: Article 108590

    Abstract: 

    Long-term soil warming and nitrogen (N) availability have been shown to affect microbial biomass and community composition. Altered assimilation patterns of recent plant-derived C and changes in soil C stocks following warming as well as increased N availability are critical in mediating the direction and magnitude of these community shifts. A 13C pulse labelling experiment was done on a warming gradient in an Icelandic grassland (Sigurdsson et al., 2016), to investigate the role of recent plant-derived C and warming on the microbial community structure and size. We observed an overall increase of microbial 13C (e.g., root-exudate) uptake, while warming led to significant microbial biomass loss in all microbial groups. The increase of microbial 13C uptake with warming differed between microbial groups: an increase was only observed in the general and Gram-positive bacterial phospholipid fatty acid (PLFA) markers and in the PLFA and neutral lipid fatty acid (NLFA) markers of arbuscular mycorrhizal fungi (AMF). Nitrogen addition of 50 kg ha−1 y−1 for two years had no effect on the microbial uptake, microbial biomass or community composition, indicating that microbes were not N limited, and no plant-mediated N addition effects occurred. Additionally, we show that both warming and soil C depletion were responsible for the microbial biomass loss. Soil warming caused stronger loss in microbial groups with higher 13C uptake. In our experiment, warming caused a general reduction of microbial biomass, despite a relative increase in microbial 13C uptake, and altered microbial community composition. The warming effects on microbial biomass and community composition were partly mediated through soil C depletion with warming and changes in recent plant-derived C uptake patterns of the microbial community.

  • Lignin Preservation and Microbial Carbohydrate Metabolism in Permafrost Soils

    Dao TT, Mikutta R, Sauheitl L, Gentsch N, Shibistova O, Wild B, Schnecker J, Barta J, Capek P, Gittel A, Lashchinskiy N, Urich T, Santruckova H, Richter A, Guggenberger G
    2022 - JGR Biogeosciences, 127: Article e2020JG00618

    Abstract: 

    Permafrost-affected soils in the northern circumpolar region store more than 1,000 Pg soil organic carbon (OC), and are strongly vulnerable to climatic warming. However, the extent to which changing soil environmental conditions with permafrost thaw affects different compounds of soil organic matter (OM) is poorly understood. Here, we assessed the fate of lignin and non-cellulosic carbohydrates in density fractionated soils (light fraction, LF vs. heavy fraction, HF) from three permafrost regions with decreasing continentality, expanding from east to west of northern Siberia (Cherskiy, Logata, Tazovskiy, respectively). In soils at the Tazovskiy site with thicker active layers, the LF showed smaller OC-normalized contents of lignin-derived phenols and plant-derived sugars and a decrease of these compounds with soil depth, while a constant or even increasing trend was observed in soils with shallower active layers (Cherskiy and Logata). Also in the HF, soils at the Tazovskiy site had smaller contents of OC-normalized lignin-derived phenols and plant-derived sugars along with more pronounced indicators of oxidative lignin decomposition and production of microbial-derived sugars. Active layer deepening, thus, likely favors the decomposition of lignin and plant-derived sugars, that is, lignocelluloses, by increasing water drainage and aeration. Our study suggests that climate-induced degradation of permafrost soils may promote carbon losses from lignin and associated polysaccharides by abolishing context-specific preservation mechanisms. However, relations of OC-based lignin-derived phenols and sugars in the HF with mineralogical properties suggest that future OM transformation and carbon losses will be modulated in addition by reactive soil minerals.

  • Decay of similarity across tropical forest communities: integrating spatial distance with soil nutrients

    Peguero G, Ferrín M, Sardans J, Verbruggen E, Ramírez-Rojas I, Van Langenhove L, Verryckt LT, Murienne J, Iribar A, Zinger L, Grau O, Orivel J, Stahl C, Courtois EA, Asensio D, Gargallo-Garriga A, Llusià J, Margalef O, Ogaya R, Richter A, Janssens IA, Peñuelas J
    2022 - Ecology, 103: Article e03599

    Abstract: 

    Understanding the mechanisms that drive the change of biotic assemblages over space and time is the main quest of community ecology. Assessing the relative importance of dispersal and environmental species selection in a range of organismic sizes and motilities has been a fruitful strategy. A consensus for whether spatial and environmental distances operate similarly across spatial scales and taxa, however, has yet to emerge. We used censuses of four major groups of organisms (soil bacteria, fungi, ground insects, and trees) at two observation scales (1-m2 sampling point vs. 2,500-m2 plots) in a topographically standardized sampling design replicated in two tropical rainforests with contrasting relationships between spatial distance and nutrient availability. We modeled the decay of assemblage similarity for each taxon set and site to assess the relative contributions of spatial distance and nutrient availability distance. Then, we evaluated the potentially structuring effect of tree composition over all other taxa. The similarity of nutrient content in the litter and topsoil had a stronger and more consistent selective effect than did dispersal limitation, particularly for bacteria, fungi, and trees at the plot level. Ground insects, the only group assessed with the capacity of active dispersal, had the highest species turnover and the flattest nonsignificant distance−decay relationship, suggesting that neither dispersal limitation nor nutrient availability were fundamental drivers of their community assembly at this scale of analysis. Only the fungal communities at one of our study sites were clearly coordinated with tree composition. The spatial distance at the smallest scale was more important than nutrient selection for the bacteria, fungi, and insects. The lower initial similarity and the moderate variation in composition identified by these distance-decay models, however, suggested that the effects of stochastic sampling were important at this smaller spatial scale. Our results highlight the importance of nutrients as one of the main environmental drivers of rainforest communities irrespective of organismic or propagule size and how the overriding effect of the analytical scale influences the interpretation, leading to the perception of greater importance of dispersal limitation and ecological drift over selection associated with environmental niches at decreasing observation scales.

  • Broad- and small-scale environmental gradients drive variation in chemical, but not morphological, leaf traits of vascular epiphytes

    Guzmán-Jacob V, Guerrero-Ramírez NR, Craven D, Brant PAterno G, Taylor A, Kromer T, Wanek W, Zotz G, Kreft H
    2022 - Functional Ecology, in press

    Abstract: 

    1. Variation in leaf functional traits along environmental gradients can reveal how vascular epiphytes respond to broad- and small-scale environmental gradients. Along elevational gradients, both temperature and precipitation likely play an important role as drivers of leaf trait variation, but these traits may also respond to small-scale changes in light, temperature and humidity along the vertical environmental gradient within forest canopies. However, the relative importance of broad- and small-scale environmental gradients as drivers of variation in leaf functional traits of vascular epiphytes is poorly understood.
    2. Here, we examined variation in morphological and chemical leaf traits of 102 vascular epiphyte species spanning two environmental gradients along Cofre de Perote mountain in Mexico: (i) a broad-scale environmental gradient approximated by elevation as well as by species' lower and upper elevational limits, and (ii) small-scale environmental gradients using the relative height of attachment of an epiphyte on a host tree as a proxy for variation in environmental conditions within the forest canopy. We also assessed whether variation in morphological and chemical leaf traits along these gradients was consistent across photosynthetic pathways (CAM and C3).
    3. Broad- and small-scale environmental gradients explained more variation in chemical traits (marginal R2: 11%–89%) than in morphological traits (marginal R2: 2%–31%). For example, leaf carbon isotope signatures (δ13C), which reflects water-use efficiency, varied systematically across both environmental gradients, suggesting a decrease in water-use efficiency with increasing lower and upper elevational limits and an increase in water-use efficiency with relative height of attachment. The influence of lower and upper elevational limits on trait variation differed between photosynthetic pathways, except for leaf dry matter content and leaf nitrogen-to-phosphorus ratio. Contrary to our expectations, broad- and small-scale environmental gradients explained minimal variation in morphological leaf traits, suggesting that environmental conditions do not constrain morphological leaf trait values of vascular epiphytes.
    4. Our findings suggest that assessing multiple drivers of leaf trait variation among photosynthetic pathways is key for disentangling the mechanisms underlying responses of vascular epiphytes to environmental conditions.

     

    Read the free Plain Language Summary for this article on the Journal blog.

     

    1. Variation in leaf functional traits along environmental gradients can reveal how vascular epiphytes respond to broad- and small-scale environmental gradients. Along elevational gradients, both temperature and precipitation likely play an important role as drivers of leaf trait variation, but these traits may also respond to small-scale changes in light, temperature and humidity along the vertical environmental gradient within forest canopies. However, the relative importance of broad- and small-scale environmental gradients as drivers of variation in leaf functional traits of vascular epiphytes is poorly understood.
    2. Here, we examined variation in morphological and chemical leaf traits of 102 vascular epiphyte species spanning two environmental gradients along Cofre de Perote mountain in Mexico: (i) a broad-scale environmental gradient approximated by elevation as well as by species' lower and upper elevational limits, and (ii) small-scale environmental gradients using the relative height of attachment of an epiphyte on a host tree as a proxy for variation in environmental conditions within the forest canopy. We also assessed whether variation in morphological and chemical leaf traits along these gradients was consistent across photosynthetic pathways (CAM and C3).
    3. Broad- and small-scale environmental gradients explained more variation in chemical traits (marginal R2: 11%–89%) than in morphological traits (marginal R2: 2%–31%). For example, leaf carbon isotope signatures (δ13C), which reflects water-use efficiency, varied systematically across both environmental gradients, suggesting a decrease in water-use efficiency with increasing lower and upper elevational limits and an increase in water-use efficiency with relative height of attachment. The influence of lower and upper elevational limits on trait variation differed between photosynthetic pathways, except for leaf dry matter content and leaf nitrogen-to-phosphorus ratio. Contrary to our expectations, broad- and small-scale environmental gradients explained minimal variation in morphological leaf traits, suggesting that environmental conditions do not constrain morphological leaf trait values of vascular epiphytes.
    4. Our findings suggest that assessing multiple drivers of leaf trait variation among photosynthetic pathways is key for disentangling the mechanisms underlying responses of vascular epiphytes to environmental conditions.

     

    Read the free Plain Language Summary for this article on the Journal blog.

  • Negative priming of soil organic matter following long-term in situ warming of sub-arctic soils

    Verbrigghe N, Meeran K, Bahn M, Fuchslueger L, Janssens IA, Richter A, Sigurdsson BD, Soong JL, Vicca A
    2022 - Geoderma, 410: Article 115652

    Abstract: 

    Priming is the change of microbial soil organic matter (SOM) decomposition induced by a labile carbon (C) source. It is recognised as an important mechanism influencing soil C dynamics and C storage in terrestrial ecosystems. Microbial nitrogen (N) mining in SOM and preferential substrate utilisation, i.e., a shift in microbial carbon use from SOM to more labile energy sources, are possible, counteracting, mechanisms driving the priming effect. Climate warming and increased N availability might affect these mechanisms, and thus determine the direction and magnitude of the priming effect. Hence, these abiotic factors can indirectly affect soil C stocks, which makes their understanding crucial for predicting the soil C feedback in a warming world. We conducted a short-term incubation experiment (6 days) with soils from a subarctic grassland that had been subjected to long-term geothermal warming (>55 years) by 2-4°C above unwarmed soil. Soil samples were amended with 13C-labelled glucose and 15N-labelled NH4NO3. We found a significantly negative relationship between in situ warming and cumulative primed C, with negative priming in the warmed soils. The negative priming suggests that preferential substrate utilisation was a key mechanism in our experiment. Our results indicate that changes in SOM characteristics associated with the in situ warming gradient can play a major role in determining the rate and direction of the priming effect. Additionally, we found that neither microbial N limitation nor N addition affected the priming effect, providing evidence that in our experiment, N mining did not lead to positive priming.

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

    Walker TWN, Gavazov K, Guillaume T, Lambert T, Mariotte P, Routh D, Signarbieux C, Block S, Münkemüller T, Nomoto H, Crowther TW, Richter A, Buttler A, Alexander JM
    2022 - eLife, 11: Article e78555

    Abstract: 

    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.

  • From diversity to complexity: Microbial networks in soils

    Guseva K, Darcy S, Simon E, Alteio LV, Montesinos-Navarro A, Kaiser C
    2022 - Soil Biology and Biochemistry, 169: Article 108604

    Abstract: 

    Network analysis has been used for many years in ecological research to analyze organismal associations, for example in food webs, plant-plant or plant-animal interactions. Although network analysis is widely applied in microbial ecology, only recently has it entered the realms of soil microbial ecology, shown by a rapid rise in studies applying co-occurrence analysis to soil microbial communities. While this application offers great potential for deeper insights into the ecological structure of soil microbial ecosystems, it also brings new challenges related to the specific characteristics of soil datasets and the type of ecological questions that can be addressed. In this Perspectives Paper we assess the challenges of applying network analysis to soil microbial ecology due to the small-scale heterogeneity of the soil environment and the nature of soil microbial datasets. We review the different approaches of network construction that are commonly applied to soil microbial datasets and discuss their features and limitations. Using a test dataset of microbial communities from two depths of a forest soil, we demonstrate how different experimental designs and network constructing algorithms affect the structure of the resulting networks, and how this in turn may influence ecological conclusions. We will also reveal how assumptions of the construction method, methods of preparing the dataset, and definitions of thresholds affect the network structure. Finally, we discuss the particular questions in soil microbial ecology that can be approached by analyzing and interpreting specific network properties. Targeting these network properties in a meaningful way will allow applying this technique not in merely descriptive, but in hypothesis-driven research. Analysing microbial networks in soils opens a window to a better understanding of the complexity of microbial communities. However, this approach is unfortunately often used to draw conclusions which are far beyond the scientific evidence it can provide, which has damaged its reputation for soil microbial analysis. In this Perspectives Paper, we would like to sharpen the view for the real potential of microbial co-occurrence analysis in soils, and at the same time raise awareness regarding its limitations and the many ways how it can be misused or misinterpreted.

  • Down-regulation of the bacterial protein biosynthesis machinery in response to weeks, years, and decades of soil warming

    Söllinger A, Séneca J, Dahl MB, Motleleng LL, Prommer J, Verbruggen E, Sigurdsson BD, Janssens I, Peñuelas J, Urich T, Richter A, Tveit AT
    2022 - Science Advances, 12: eabm3230

    Abstract: 

    How soil microorganisms respond to global warming is key to infer future soil-climate feedbacks, yet poorly understood. Here, we applied metatranscriptomics to investigate microbial physiological responses to medium-term (8 years) and long-term (>50 years) subarctic grassland soil warming of +6°C. Besides indications for a community-wide up-regulation of centralmetabolic pathways and cell replication, we observed a down-regulation of the bacterial protein biosynthesis machinery in the warmed soils, coinciding with a lower microbial biomass, RNA, and soil substrate content. We conclude that permanently accelerated reaction rates at higher temperatures and reduced substrate concentrations result in cellular reduction of ribosomes, the macromolecular complexes carrying out protein biosynthesis. Later efforts to test this, including a short-term warming experiment (6 weeks, +6°C), further supported our conclusion. Down-regulating the protein biosynthesis machinery liberates energy and matter, allowing soil bacteria to maintain high metabolic activities and cell division rates even after decades of warming.

  • Plant phosphorus-use and -acquisition strategies in Amazonia

    Reichert T, Rammig A, Fuchslueger L, Lugli LF, Quesada CA, Fleischer K
    2022 - New Phytologist, 234: 1126-1143

    Abstract: 

    In the tropical rainforest of Amazonia, phosphorus (P) is one of the main nutrients controlling forest dynamics, but its effects on the future of the forest biomass carbon (C) storage under elevated atmospheric CO2 concentrations remain uncertain. Soils in vast areas of Amazonia are P-impoverished, and little is known about the variation or plasticity in plant P-use and -acquisition strategies across space and time, hampering the accuracy of projections in vegetation models. Here, we synthesize current knowledge of leaf P resorption, fine-root P foraging, arbuscular mycorrhizal symbioses, and root acid phosphatase and organic acid exudation and discuss how these strategies vary with soil P concentrations and in response to elevated atmospheric CO2. We identify knowledge gaps and suggest ways forward to fill those gaps. Additionally, we propose a conceptual framework for the variations in plant P-use and -acquisition strategies along soil P gradients of Amazonia. We suggest that in soils with intermediate to high P concentrations, at the plant community level, investments are primarily directed to P foraging strategies via roots and arbuscular mycorrhizas, whereas in soils with intermediate to low P concentrations, investments shift to prioritize leaf P resorption and mining strategies via phosphatases and organic acids.

  • The role of coupled DNRA-Anammox during nitrate removal in a highly saline lake

    Valiente N, Jirsa F, Hein T, Wanek W, Prommer J, Bonin P, Gómez-Alday JJ
    2022 - Science of The Total Environment, 806: Article 150726

    Abstract: 

    Nitrate (NO3) removal from aquatic ecosystems involves several microbially mediated processes, including denitrification, dissimilatory nitrate reduction to ammonium (DNRA), and anaerobic ammonium oxidation (anammox), controlled by slight changes in environmental gradients. In addition, some of these processes (i.e. denitrification) may involve the production of undesirable compounds such as nitrous oxide (N2O), an important greenhouse gas. Saline lakes are prone to the accumulation of anthropogenic contaminants, making them highly vulnerable environments to NO3 pollution. The aim of this paper was to investigate the effect of light and oxygen on the different NO3 removal pathways under highly saline conditions. For this purpose, mesocosm experiments were performed using lacustrine, undisturbed, organic-rich sediments from the Pétrola Lake (Spain), a highly saline waterbody subject to anthropogenic NO3 pollution. The revised 15N-isotope pairing technique (15N-IPT) was used to determine NO3 sink processes. Our results demonstrate for the first time the coexistence of denitrification, DNRA, and anammox processes in a highly saline lake, and how their contribution was determined by environmental conditions (oxygen and light). DNRA, and especially denitrification to N2O, were the dominant nitrogen (N) removal pathways when oxygen and/or light were present (up to 82%). In contrast, anoxia and darkness promoted NO3 reduction by DNRA (52%), combined with N loss by anammox (28%). Our results highlight the role of coupled DNRA-anammox, which has not yet been investigated in lacustrine sediments. We conclude that anoxia and darkness favored DNRA and anammox processes over denitrification and therefore to restrict N2O emissions to the atmosphere.

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