Reductions in home-range size and social interactions among dehorned black rhinoceroses (Diceros bicornis).

Poaching for horns and tusks is driving declines of megaherbivores worldwide, including the critically endangered African black rhinoceros (Diceros bicornis). By proactively dehorning entire rhinoceros populations, conservationists aim to deter poaching and prevent species loss. However, such conservation interventions may have hidden and underestimated effects on animals' behavior and ecology. Here, we combine >15 y of black rhino-monitoring data across 10 South African game reserves, comprising >24,000 sightings of 368 individuals, to determine the consequences of dehorning for black rhino space use and social interactions. While preventative dehorning at these reserves coincided with a nationwide decrease in black rhino mortality from poaching and did not infer increased natural mortality, dehorned black rhinos decreased their home range area by, on average, 11.7 km2 (45.5%) and were 37% less likely to engage in social encounters. We conclude that dehorning black rhinos as an antipoaching measure alters their behavioral ecology, although the potential population-level effects of these changes remain to be determined.

Spatial and evolutionary predictability of phytochemical diversity.

To cope with environmental challenges, plants produce a wide diversity of phytochemicals, which are also the source of numerous medicines. Despite decades of research in chemical ecology, we still lack an understanding of the organization of plant chemical diversity across species and ecosystems. To address this challenge, we hypothesized that molecular diversity is not only related to species diversity, but also constrained by trophic, climatic, and topographical factors. We screened the metabolome of 416 vascular plant species encompassing the entire alpine elevation range and four alpine bioclimatic regions in order to characterize their phytochemical diversity. We show that by coupling phylogenetic information, topographic, edaphic, and climatic variables, we predict phytochemical diversity, and its inherent composition, of plant communities throughout landscape. Spatial mapping of phytochemical diversity further revealed that plant assemblages found in low to midelevation habitats, with more alkaline soils, possessed greater phytochemical diversity, whereas alpine habitats possessed higher phytochemical endemism. Altogether, we present a general tool that can be used for predicting hotspots of phytochemical diversity in the landscape, independently of plant species taxonomic identity. Such an approach offers promising perspectives in both drug discovery programs and conservation efforts worldwide.

Biotic Interactions in Soil are Underestimated Drivers of Microbial Carbon Use Efficiency.

Microbial carbon use efficiency (CUE)-the balance between microbial growth and respiration-strongly impacts microbial mediated soil carbon storage and is sensitive to many well-studied abiotic environmental factors. However, surprisingly, little work has examined how biotic interactions in soil may impact CUE. Here, we review the theoretical and empirical lines of evidence exploring how biotic interactions affect CUE through the lens of life history strategies. Fundamentally, the CUE of a microbial population is constrained by population density and carrying capacity, which, when reached, causes species to grow more quickly and less efficiently. When microbes engage in interspecific competition, they accelerate growth rates to acquire limited resources and release secondary chemicals toxic to competitors. Such processes are not anabolic and thus constrain CUE. In turn, antagonists may activate one of a number of stress responses that also do not involve biomass production, potentially further reducing CUE. In contrast, facilitation can increase CUE by expanding species realized niches, mitigating environmental stress and reducing production costs of extracellular enzymes. Microbial interactions at higher trophic levels also influence CUE. For instance, predation on microbes can positively or negatively impact CUE by changing microbial density and the outcomes of interspecific competition. Finally, we discuss how plants select for more or less efficient microbes under different contexts. In short, this review demonstrates the potential for biotic interactions to be a strong regulator of microbial CUE and additionally provides a blueprint for future research to address key knowledge gaps of ecological and applied importance for carbon sequestration.

Increased microbial growth, biomass, and turnover drive soil organic carbon accumulation at higher plant diversity.

Species-rich plant communities have been shown to be more productive and to exhibit increased long-term soil organic carbon (SOC) storage. Soil microorganisms are central to the conversion of plant organic matter into SOC, yet the relationship between plant diversity, soil microbial growth, turnover as well as carbon use efficiency (CUE) and SOC accumulation is unknown. As heterotrophic soil microbes are primarily carbon limited, it is important to understand how they respond to increased plant-derived carbon inputs at higher plant species richness (PSR). We used the long-term grassland biodiversity experiment in Jena, Germany, to examine how microbial physiology responds to changes in plant diversity and how this affects SOC content. The Jena Experiment considers different numbers of species (1-60), functional groups (1-4) as well as functional identity (small herbs, tall herbs, grasses, and legumes). We found that PSR accelerated microbial growth and turnover and increased microbial biomass and necromass. PSR also accelerated microbial respiration, but this effect was less strong than for microbial growth. In contrast, PSR did not affect microbial CUE or biomass-specific respiration. Structural equation models revealed that PSR had direct positive effects on root biomass, and thereby on microbial growth and microbial biomass carbon. Finally, PSR increased SOC content via its positive influence on microbial biomass carbon. We suggest that PSR favors faster rates of microbial growth and turnover, likely due to greater plant productivity, resulting in higher amounts of microbial biomass and necromass that translate into the observed increase in SOC. We thus identify the microbial mechanism linking species-rich plant communities to a carbon cycle process of importance to Earth's climate system.

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.

Full 15N tracer accounting to revisit major assumptions of 15N isotope pool dilution approaches for gross nitrogen mineralization.

The 15N isotope pool dilution (IPD) technique is the only available method for measuring gross ammonium (NH4 +) production and consumption rates. Rapid consumption of the added 15N-NH4 + tracer is commonly observed, but the processes responsible for this consumption are not well understood. The primary objectives of this study were to determine the relative roles of biotic and abiotic processes in 15N-NH4 + sconsumption and to investigate the validity of one of the main assumptions of IPD experiments, i.e., that no reflux of the consumed 15N tracer occurs during the course of the experiments. We added a 15N-NH4 + tracer to live and sterile (autoclaved) soil using mineral topsoil from a beech forest and a grassland in Austria that differed in NH4 + concentrations and NH4 + consumption kinetics. We quantified both biotic tracer consumption (i.e. changes in the concentrations and 15N enrichments of NH4 +, dissolved organic N (DON), NO3 - and the microbial N pool) and abiotic tracer consumption (i.e., fixation by clay and/or humic substances). We achieved full recovery of the 15N tracer in both soils over the course of the 48 h incubation. For the forest soil, we found no rapid consumption of the 15N tracer, and the majority of tracer (78%) remained unconsumed at the end of the incubation period. In contrast, the grassland soil showed rapid 15N-NH4 + consumption immediately after tracer addition, which was largely due to both abiotic fixation (24%) and biotic processes, largely uptake by soil microbes (10%) and nitrification (13%). We found no evidence for reflux of 15N-NH4 + over the 48 h incubation period in either soil. Our study therefore shows that 15N tracer reflux during IPD experiments is negligible for incubation times of up to 48 h, even when rapid NH4 + consumption occurs. Such experiments are thus robust to the assumption that immobilized labeled N is not re-mobilized during the experimental period and does not impact calculations of gross N mineralization.

plantMASST - Community-driven chemotaxonomic digitization of plants.

Understanding the distribution of hundreds of thousands of plant metabolites across the plant kingdom presents a challenge. To address this, we curated publicly available LC-MS/MS data from 19,075 plant extracts and developed the plantMASST reference database encompassing 246 botanical families, 1,469 genera, and 2,793 species. This taxonomically focused database facilitates the exploration of plant-derived molecules using tandem mass spectrometry (MS/MS) spectra. This tool will aid in drug discovery, biosynthesis, (chemo)taxonomy, and the evolutionary ecology of herbivore interactions.

Leaf metabolic traits reveal hidden dimensions of plant form and function.

The metabolome is the biochemical basis of plant form and function, but we know little about its macroecological variation across the plant kingdom. Here, we used the plant functional trait concept to interpret leaf metabolome variation among 457 tropical and 339 temperate plant species. Distilling metabolite chemistry into five metabolic functional traits reveals that plants vary on two major axes of leaf metabolic specialization-a leaf chemical defense spectrum and an expression of leaf longevity. Axes are similar for tropical and temperate species, with many trait combinations being viable. However, metabolic traits vary orthogonally to life-history strategies described by widely used functional traits. The metabolome thus expands the functional trait concept by providing additional axes of metabolic specialization for examining plant form and function.

Open and reusable annotated mass spectrometry dataset of a chemodiverse collection of 1,600 plant extracts.

As privileged structures, natural products often display potent biological activities. However, the discovery of novel bioactive scaffolds is often hampered by the chemical complexity of the biological matrices they are found in. Large natural extract collections are thus extremely valuable for their chemical novelty potential but also complicated to exploit in the frame of drug-discovery projects. In the end, it is the pure chemical substances that are desired for structural determination purposes and bioactivity evaluation. Researchers interested in the exploration of large and chemodiverse extract collections should thus establish strategies aiming to efficiently tackle such chemical complexity and access these structures. Establishing carefully crafted digital layers documenting the spectral and chemical complexity as well as bioactivity results of natural extracts collections can help prioritize time-consuming but mandatory isolation efforts. In this note, we report the results of our initial exploration of a collection of 1,600 plant extracts in the frame of a drug-discovery effort. After describing the taxonomic coverage of this collection, we present the results of its liquid chromatography high-resolution mass spectrometric profiling and the exploitation of these profiles using computational solutions. The resulting annotated mass spectral dataset and associated chemical and taxonomic metadata are made available to the community, and data reuse cases are proposed. We are currently continuing our exploration of this plant extract collection for drug-discovery purposes (notably looking for novel antitrypanosomatids, anti-infective and prometabolic compounds) and ecometabolomics insights. We believe that such a dataset can be exploited and reused by researchers interested in computational natural products exploration.

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.

Ecometabolomics for a Better Understanding of Plant Responses and Acclimation to Abiotic Factors Linked to Global Change.

The number of ecometabolomic studies, which use metabolomic analyses to disentangle organisms' metabolic responses and acclimation to a changing environment, has grown exponentially in recent years. Here, we review the results and conclusions of ecometabolomic studies on the impacts of four main drivers of global change (increasing frequencies of drought episodes, heat stress, increasing atmospheric carbon dioxide (CO2) concentrations and increasing nitrogen (N) loads) on plant metabolism. Ecometabolomic studies of drought effects confirmed findings of previous target studies, in which most changes in metabolism are characterized by increased concentrations of soluble sugars and carbohydrate derivatives and frequently also by elevated concentrations of free amino acids. Secondary metabolites, especially flavonoids and terpenes, also commonly exhibited increased concentrations when drought intensified. Under heat and increasing N loads, soluble amino acids derived from glutamate and glutamine were the most responsive metabolites. Foliar metabolic responses to elevated atmospheric CO2 concentrations were dominated by greater production of monosaccharides and associated synthesis of secondary metabolites, such as terpenes, rather than secondary metabolites synthesized along longer sugar pathways involving N-rich precursor molecules, such as those formed from cyclic amino acids and along the shikimate pathway. We suggest that breeding for crop genotypes tolerant to drought and heat stress should be based on their capacity to increase the concentrations of C-rich compounds more than the concentrations of smaller N-rich molecules, such as amino acids. This could facilitate rapid and efficient stress response by reducing protein catabolism without compromising enzymatic capacity or increasing the requirement for re-transcription and de novo biosynthesis of proteins.

A systemic overreaction to years versus decades of warming in a subarctic grassland ecosystem.

Temperature governs most biotic processes, yet we know little about how warming affects whole ecosystems. Here we examined the responses of 128 components of a subarctic grassland to either 5-8 or >50 years of soil warming. Warming of >50 years drove the ecosystem to a new steady state possessing a distinct biotic composition and reduced species richness, biomass and soil organic matter. However, the warmed state was preceded by an overreaction to warming, which was related to organism physiology and was evident after 5-8 years. Ignoring this overreaction yielded errors of >100% for 83 variables when predicting their responses to a realistic warming scenario of 1 °C over 50 years, although some, including soil carbon content, remained stable after 5-8 years. This study challenges long-term ecosystem predictions made from short-term observations, and provides a framework for characterization of ecosystem responses to sustained climate change.

Microbial temperature sensitivity and biomass change explain soil carbon loss with warming.

Soil microorganisms control carbon losses from soils to the atmosphere1-3, yet their responses to climate warming are often short-lived and unpredictable4-7. Two mechanisms, microbial acclimation and substrate depletion, have been proposed to explain temporary warming effects on soil microbial activity8-10. However, empirical support for either mechanism is unconvincing. Here we used geothermal temperature gradients (> 50 years of field warming)11 and a short-term experiment to show that microbial activity (gross rates of growth, turnover, respiration and carbon uptake) is intrinsically temperature sensitive and does not acclimate to warming (+ 6 ºC) over weeks or decades. Permanently accelerated microbial activity caused carbon loss from soil. However, soil carbon loss was temporary because substrate depletion reduced microbial biomass and constrained the influence of microbes over the ecosystem. A microbial biogeochemical model12-14 showed that these observations are reproducible through a modest, but permanent, acceleration in microbial physiology. These findings reveal a mechanism by which intrinsic microbial temperature sensitivity and substrate depletion together dictate warming effects on soil carbon loss via their control over microbial biomass. We thus provide a framework for interpreting the links between temperature, microbial activity and soil carbon loss on timescales relevant to Earth's climate system.