Climate change disrupts the seasonal coupling of plant and soil microbial nutrient cycling in an alpine ecosystem.

The seasonal coupling of plant and soil microbial nutrient demands is crucial for efficient ecosystem nutrient cycling and plant production, especially in strongly seasonal alpine ecosystems. Yet, how these seasonal nutrient cycling processes are modified by climate change and what the consequences are for nutrient loss and retention in alpine ecosystems remain unclear. Here, we explored how two pervasive climate change factors, reduced snow cover and shrub expansion, interactively modify the seasonal coupling of plant and soil microbial nitrogen (N) cycling in alpine grasslands, which are warming at double the rate of the global average. We found that the combination of reduced snow cover and shrub expansion disrupted the seasonal coupling of plant and soil N-cycling, with pronounced effects in spring (shortly after snow melt) and autumn (at the onset of plant senescence). In combination, both climate change factors decreased plant organic N-uptake by 70% and 82%, soil microbial biomass N by 19% and 38% and increased soil denitrifier abundances by 253% and 136% in spring and autumn, respectively. Shrub expansion also individually modified the seasonality of soil microbial community composition and stoichiometry towards more N-limited conditions and slower nutrient cycling in spring and autumn. In winter, snow removal markedly reduced the fungal:bacterial biomass ratio, soil N pools and shifted bacterial community composition. Taken together, our findings suggest that interactions between climate change factors can disrupt the temporal coupling of plant and soil microbial N-cycling processes in alpine grasslands. This could diminish the capacity of these globally widespread alpine ecosystems to retain N and support plant productivity under future climate change.

High intensity perturbations induce an abrupt shift in soil microbial state.

Soil microbial communities play a pivotal role in regulating ecosystem functioning. But they are increasingly being shaped by human-induced environmental change, including intense "pulse" perturbations, such as droughts, which are predicted to increase in frequency and intensity with climate change. While it is known that soil microbial communities are sensitive to such perturbations and that effects can be long-lasting, it remains untested whether there is a threshold in the intensity and frequency of perturbations that can trigger abrupt and persistent transitions in the taxonomic and functional characteristics of soil microbial communities. Here we demonstrate experimentally that intense pulses of drought equivalent to a 30-year drought event (<15% WHC) induce a major shift in the soil microbial community characterised by significantly altered bacterial and fungal community structures of reduced complexity and functionality. Moreover, the characteristics of this transformed microbial community persisted after returning soil to its previous moisture status. As a result, we found that drought had a strong legacy effect on bacterial community function, inducing an enhanced growth rate following subsequent drought. Abrupt transitions are widely documented in aquatic and terrestrial plant communities in response to human-induced perturbations. Our findings demonstrate that such transitions also occur in soil microbial communities in response to high intensity pulse perturbations, with potentially deleterious consequences for soil health.

Defoliation and fertilisation differentially moderate root trait effects on soil abiotic and biotic properties.

Root functional traits are known to influence soil properties that underpin ecosystem functioning. Yet few studies have explored how root traits simultaneously influence physical, chemical, and biological properties of soil, or how these responses are modified by common grassland perturbations that shape roots, such as defoliation and fertilisation.Here, we explored how root traits of a wide range of grassland plant species with contrasting resource acquisition strategies (i.e. conservative vs. exploitative strategy plant species) respond to defoliation and fertilisation individually and in combination, and examined cascading impacts on a range of soil abiotic and biotic properties that underpin ecosystem functioning.We found that the amplitude of the response of root traits to defoliation and fertilisation varied among plant species, in most cases independently of plant resource acquisition strategies. However, the direction of the root trait responses (increase or decrease) to perturbations was consistent across all plant species, with defoliation and fertilisation exerting opposing effects on root traits. Specific root length increased relative to non-perturbed control in response to defoliation, while root biomass, root mass density, and root length density decreased. Fertilisation induced the opposite responses. We also found that both defoliation and fertilisation individually enhanced the role of root traits in regulating soil biotic and abiotic properties, especially soil aggregate stability. Synthesis: Our results indicate that defoliation and fertilisation, two common grassland perturbations, have contrasting impacts on root traits of grassland plant species, with direct and indirect short-term consequences for a wide range of soil abiotic and biotic properties that underpin ecosystem functioning.

Shrub expansion modulates belowground impacts of changing snow conditions in alpine grasslands.

Climate change is disproportionately impacting mountain ecosystems, leading to large reductions in winter snow cover, earlier spring snowmelt and widespread shrub expansion into alpine grasslands. Yet, the combined effects of shrub expansion and changing snow conditions on abiotic and biotic soil properties remains poorly understood. We used complementary field experiments to show that reduced snow cover and earlier snowmelt have effects on soil microbial communities and functioning that persist into summer. However, ericaceous shrub expansion modulates a number of these impacts and has stronger belowground effects than changing snow conditions. Ericaceous shrub expansion did not alter snow depth or snowmelt timing but did increase the abundance of ericoid mycorrhizal fungi and oligotrophic bacteria, which was linked to decreased soil respiration and nitrogen availability. Our findings suggest that changing winter snow conditions have cross-seasonal impacts on soil properties, but shifts in vegetation can modulate belowground effects of future alpine climate change.

Climate change alters temporal dynamics of alpine soil microbial functioning and biogeochemical cycling via earlier snowmelt.

Soil microbial communities regulate global biogeochemical cycles and respond rapidly to changing environmental conditions. However, understanding how soil microbial communities respond to climate change, and how this influences biogeochemical cycles, remains a major challenge. This is especially pertinent in alpine regions where climate change is taking place at double the rate of the global average, with large reductions in snow cover and earlier spring snowmelt expected as a consequence. Here, we show that spring snowmelt triggers an abrupt transition in the composition of soil microbial communities of alpine grassland that is closely linked to shifts in soil microbial functioning and biogeochemical pools and fluxes. Further, by experimentally manipulating snow cover we show that this abrupt seasonal transition in wide-ranging microbial and biogeochemical soil properties is advanced by earlier snowmelt. Preceding winter conditions did not change the processes that take place during snowmelt. Our findings emphasise the importance of seasonal dynamics for soil microbial communities and the biogeochemical cycles that they regulate. Moreover, our findings suggest that earlier spring snowmelt due to climate change will have far reaching consequences for microbial communities and nutrient cycling in these globally widespread alpine ecosystems.

Local adaptation optimizes photoprotection strategies in a Neotropical legume tree under drought stress.

Photoprotection is a plant functional mechanism to prevent photooxidative damage by excess light. This is most important when carbon assimilation is limited by drought, and as such, it entails a trade-off between carbon assimilation vs stress avoidance. The ecological adaptation of plants to local water availability can lead to different photoprotective strategies. To test this, we used different provenances of Caesalpinia spinosa (Mol.) Kuntze (commonly known as 'tara') along a precipitation gradient. Tara is a Neotropical legume tree with high ecological and commercial value, found in dry tropical forests, which are increasingly threatened by climate change. Morphological and physiological responses of tara provenances were analysed under three different treatments of drought and leaflet immobilization, i.e., light stress, in a common garden greenhouse experiment. Tara quickly responded to drought by reducing stomatal conductance, evapotranspiration, photochemical efficiency, carbon assimilation and growth, while increasing structural and chemical photoprotection (leaflet angle and pigments for thermal dissipation). Leaflet closure was an efficient photoprotection strategy with overall physiological benefits for seedlings as it diminished the evaporative demand and avoided photodamage, but also entailed costs by reducing net carbon assimilation opportunities. These responses depended on seed origin, with seedlings from the most xeric locations showing the highest dehydration tolerance, suggesting local adaptation and highlighting the value of different strategies under distinct environments. This plasticity in its response to environmental stress allows tara to thrive in locations with contrasting water availability. Our findings increase the understanding of the factors controlling the functional ecology of tara in response to drought, which can be leveraged to improve forecasts of changes in its distribution range, and for planning restoration projects with this keystone tree species.

Drought soil legacy overrides maternal effects on plant growth.

Maternal effects (i.e. trans-generational plasticity) and soil legacies generated by drought and plant diversity can affect plant performance and alter nutrient cycling and plant community dynamics. However, the relative importance and combined effects of these factors on plant growth dynamics remain poorly understood.We used soil and seeds from an existing plant diversity and drought manipulation field experiment in temperate grassland to test maternal, soil drought and diversity legacy effects, and their interactions, on offspring plant performance of two grassland species (Alopecurus pratensis and Holcus lanatus) under contrasting glasshouse conditions.Our results showed that drought soil legacy effects eclipsed maternal effects on plant biomass. Drought soil legacy effects were attributed to changes in both abiotic (i.e. nutrient availability) and biotic soil properties (i.e. microbial carbon and enzyme activity), as well as plant root and shoot atom 15N excess. Further, plant tissue nutrient concentrations and soil microbial C:N responses to drought legacies varied between the two plant species and soils from high and low plant diversity treatments. However, these diversity effects did not affect plant root or shoot biomass.These findings demonstrate that while maternal effects resulting from drought occur in grasslands, their impacts on plant performance are likely minor relative to drought legacy effects on soil abiotic and biotic properties. This suggests that soil drought legacy effects could become increasingly important drivers of plant community dynamics and ecosystem functioning as extreme weather events become more frequent and intense with climate change. A plain language summary is available for this article.

High throughput method for measuring urease activity in soil.

Extracellular enzymes break down soil organic matter into smaller compounds and their measurement has proved to be a powerful tool to evaluate the functionality of soils. Urease is the enzyme that degrades urea and is widely considered to be a good proxy of nitrogen (N) mineralisation. But the methods available to measure this enzyme are time consuming; as such, urease is not commonly included in standard enzyme profiling of soils. We developed a fast, high throughput and reproducible colorimetric microplate technique to evaluate urease activity in soil. The method involves the incubation of soil slurries in 96-deepwell blocks with urea solutions and the measurement, by colorimetric reaction, of ammonium produced. We compared the new method with existing methods, yielding comparable results, and evaluated optimal conditions for urease analysis (soil slurry concentration, substrate concentration, incubation times and extractant salt concentration) in different grassland soils. The method proved to be a faster, higher throughput, and more precise alternative to existing methods for evaluating this important N-related enzyme.

Forest restoration in a fog oasis: evidence indicates need for cultural awareness in constructing the reference.

BACKGROUND: In the Peruvian Coastal Desert, an archipelago of fog oases, locally called lomas, are centers of biodiversity and of past human activity. Fog interception by a tree canopy, dominated by the legume tree tara (Caesalpinia spinosa), enables the occurrence in the Atiquipa lomas (southern Peru) of an environmental island with a diverse flora and high productivity. Although this forest provides essential services to the local population, it has suffered 90% anthropogenic reduction in area. Restoration efforts are now getting under way, including discussion as to the most appropriate reference ecosystem to use. METHODOLOGY/PRINCIPAL FINDINGS: Genetic diversity of tara was studied in the Atiquipa population and over a wide geographical and ecological range. Neither exclusive plastid haplotypes to loma formations nor clear geographical structuring of the genetic diversity was found. Photosynthetic performance and growth of seedlings naturally recruited in remnant patches of loma forest were compared with those of seedlings recruited or planted in the adjacent deforested area. Despite the greater water and nitrogen availability under tree canopy, growth of forest seedlings did not differ from that of those recruited into the deforested area, and was lower than that of planted seedlings. Tara seedlings exhibited tight stomatal control of photosynthesis, and a structural photoprotection by leaflet closure. These drought-avoiding mechanisms did not optimize seedling performance under the conditions produced by forest interception of fog moisture. CONCLUSIONS/SIGNIFICANCE: Both weak geographic partitioning of genetic variation and lack of physiological specialization of seedlings to the forest water regime strongly suggest that tara was introduced to lomas by humans. Therefore, the most diverse fragment of lomas is the result of landscape management and resource use by pre-Columbian cultures. We argue that an appropriate reference ecosystem for ecological restoration of lomas should include sustainable agroforestry practices that emulate the outcomes of ancient uses.