Global hotspots for soil nature conservation.

Soils are the foundation of all terrestrial ecosystems1. However, unlike for plants and animals, a global assessment of hotspots for soil nature conservation is still lacking2. This hampers our ability to establish nature conservation priorities for the multiple dimensions that support the soil system: from soil biodiversity to ecosystem services. Here, to identify global hotspots for soil nature conservation, we performed a global field survey that includes observations of biodiversity (archaea, bacteria, fungi, protists and invertebrates) and functions (critical for six ecosystem services) in 615 composite samples of topsoil from a standardized survey in all continents. We found that each of the different ecological dimensions of soils-that is, species richness (alpha diversity, measured as amplicon sequence variants), community dissimilarity and ecosystem services-peaked in contrasting regions of the planet, and were associated with different environmental factors. Temperate ecosystems showed the highest species richness, whereas community dissimilarity peaked in the tropics, and colder high-latitudinal ecosystems were identified as hotspots of ecosystem services. These findings highlight the complexities that are involved in simultaneously protecting multiple ecological dimensions of soil. We further show that most of these hotspots are not adequately covered by protected areas (more than 70%), and are vulnerable in the context of several scenarios of global change. Our global estimation of priorities for soil nature conservation highlights the importance of accounting for the multidimensionality of soil biodiversity and ecosystem services to conserve soils for future generations.

Unearthing the soil-borne microbiome of land plants.

Plant-soil biodiversity interactions are fundamental for the functioning of terrestrial ecosystems. Yet, the existence of a set of globally distributed topsoil microbial and small invertebrate organisms consistently associated with land plants (i.e., their consistent soil-borne microbiome), together with the environmental preferences and functional capabilities of these organisms, remains unknown. We conducted a standardized field survey under 150 species of land plants, including 58 species of bryophytes and 92 of vascular plants, across 124 locations from all continents. We found that, despite the immense biodiversity of soil organisms, the land plants evaluated only shared a small fraction (less than 1%) of all microbial and invertebrate taxa that were present across contrasting climatic and soil conditions and vegetation types. These consistent taxa were dominated by generalist decomposers and phagotrophs and their presence was positively correlated with the abundance of functional genes linked to mineralization. Finally, we showed that crossing environmental thresholds in aridity (aridity index of 0.65, i.e., the transition from mesic to dry ecosystems), soil pH (5.5; i.e., the transition from acidic to strongly acidic soils), and carbon (less than 2%, the lower limit of fertile soils) can result in drastic disruptions in the associations between land plants and soil organisms, with potential implications for the delivery of soil ecosystem processes under ongoing global environmental change.

Genetic control underlying the flowering-drought tolerance trade-off in the Antarctic plant Colobanthus quitensis.

Plants inhabiting environments with stressful conditions often exhibit a low number of flowers, which can be attributed to the energetic cost associated with reproduction. One of the most stressful environments for plants is the Antarctic continent, characterized by limited soil water availability and low temperatures. Induction of dehydrins like those from the COR gene family and auxin transcriptional response repressor genes (IAAs), which are involved in floral repression, has been described in response to water stress. Here, we investigated the relationship between the water deficit-induced stress response and the number of flowers in Colobanthus quitensis plants collected from populations along a latitudinal gradient. The expression levels of COR47 and IAA12 genes in response to water deficit were found to be associated with the number of flowers. The relationship was observed both in the field and growth chambers. Watering the plants in the growth chambers alleviated the stress and stimualted flowering, thereby eliminating the trade-off observed in the field. Our study provides a mechanistic understanding of the ecological constraints on plant reproduction along a water availability gradient. However, further experiments are needed to elucidate the primary role of water availability in regulating resource allocation to reproduction in plants inhibiting extreme environments.

Isolation and characterization of microsatellites for the endangered endemic tree Nothofagus alessandrii (Nothofagaceae).

Nothofagus alessandrii (Nothofagaceae) is one of the most endangered trees from Chile due to high rates of habitat disturbance caused by human activities. Despite its conservation status, few molecular markers are available to study its population genetic, connectivity and to assist reproduction programs. Thus, the species needs urgent actions to restore its original distribution. Novel polymorphic microsatellites from the genome of N. alessandrii were isolated and characterized using high-through sequencing. A total of 30 primer pairs were synthesized and 18 microsatellites were amplified correctly. Polymorphism and genetic diversity was evaluated in 58 individuals from three populations of N. alessandrii. Sixteen of them were polymorphic and the number of alleles in the pooled sample ranged from 2 to 14, the mean number of alleles was 4.81. The mean values of observed heterozigosity (HO) and excepted heterozygosity (HE) are similar in all studied populations. Linkage disequilibrium was found between a few pairs of loci (five out of 263 tests) suggesting that most of the markers can be considered as independent. Significant deviations from Hardy-Weinberg equilibrium (P < 0.05) were found in four loci probably due to low sampling size. Transferability to the congeneric N. pumilio was successful in only four out of the sixteen polymorphic markers. The microsatellite markers developed in this study will be useful to study the genetic diversity and structure and to develop integrated management plans for the conservation of this endangered species.

Functional roles of microbial symbionts in plant cold tolerance.

In this review, we examine the functional roles of microbial symbionts in plant tolerance to cold and freezing stresses. The impacts of symbionts on antioxidant activity, hormonal signaling and host osmotic balance are described, including the effects of the bacterial endosymbionts Burkholderia, Pseudomonas and Azospirillum on photosynthesis and the accumulation of carbohydrates such as trehalose and raffinose that improve cell osmotic regulation and plasma membrane integrity. The influence of root fungal endophytes and arbuscular mycorrhizal fungi on plant physiology at low temperatures, for example their effects on nutrient acquisition and the accumulation of indole-3-acetic acid and antioxidants in tissues, are also reviewed. Meta-analyses are presented showing that aspects of plant performance (shoot biomass, relative water content, sugar and proline concentrations and Fv /Fm ) are enhanced in symbiotic plants at low (-1 to 15 °C), but not at high (20-26 °C), temperatures. We discuss the implications of microbial symbionts for plant performance at low and sub-zero temperatures in the natural environment and propose future directions for research into the effects of symbionts on the cold and freezing tolerances of plants, concluding that further studies should routinely incorporate symbiotic microbes in their experimental designs.

Root endophytic Penicillium promotes growth of Antarctic vascular plants by enhancing nitrogen mineralization.

Fungal endophyte associations have been suggested as a possible strategy of Antarctic vascular plants for surviving the extreme environmental conditions of Antarctica. However, the mechanisms by which this occurs are still poorly understood. The role of root fungal endophytes in nitrogen mineralization and nutrient uptake, as well as their impact on the performance of Antarctic plants, were studied. We tested root endophytes, isolated from Colobanthus quitensis and Deschampsia antarctica, for lignocellulolytic enzyme production, nitrogen mineralization, and growth enhancement of their host plants. Penicillium chrysogenum and Penicillium brevicompactum were identified using a molecular approach as the main root endophytes inhabiting C. quitensis and D. antarctica, respectively. Both root endophytes were characterized as psychrophilic fungi displaying amylase, esterase, protease, cellulase, hemicellulase, phosphatase and urease enzymatic activities, mainly at 4 °C. Moreover, the rates and percentages of nitrogen mineralization, as well as the final total biomass, were significantly higher in symbiotic C. quitensis and D. antarctica individuals. Our findings suggest that root endophytes exert a pivotal ecological role based not only to breakdown different nutrient sources but also on accelerating nitrogen mineralization, improving nutrient acquisition, and therefore promoting plant growth in Antarctic terrestrial ecosystems.

Morphological and molecular identification of the invasive freshwater snail Physa acuta (Gastropoda: Physidae) into Llanquihue Lake, Chilean Patagonia.

The sewage snail Physa acuta, native to North America, is an effective invasive species around the world. In Chile, it was first reported in 2014 in the north central area of the country. So far, the species has not been recorded in southern Chile. Sampling performed in 2015 in three localities from Llanquihue Lake, Chilean Patagonia, only provided native freshwater snails. However, new collections performed in February 2018 in the same three sites were successful for physid specimens suggesting a biological invasion entailing a large southward range expansion of these snails. Here we performed morphological, microstructural and phylogenetic analyses to investigate whether the new samples belong to Physa acuta. The shell morphology, male copulatory complex and radula microstructure of the new material agree with those of the sewage snail. The molecular phylogenetic analyses using the cytochrome c oxidase subunit 1 (COI) gene confirmed morphological identification. We suggest to take prompt measures to prevent the expansion of Physa acuta in Llanquihue Lake or nearby aquatic ecosystems.

Decoupling of soil nutrient cycles as a function of aridity in global drylands.

The biogeochemical cycles of carbon (C), nitrogen (N) and phosphorus (P) are interlinked by primary production, respiration and decomposition in terrestrial ecosystems. It has been suggested that the C, N and P cycles could become uncoupled under rapid climate change because of the different degrees of control exerted on the supply of these elements by biological and geochemical processes. Climatic controls on biogeochemical cycles are particularly relevant in arid, semi-arid and dry sub-humid ecosystems (drylands) because their biological activity is mainly driven by water availability. The increase in aridity predicted for the twenty-first century in many drylands worldwide may therefore threaten the balance between these cycles, differentially affecting the availability of essential nutrients. Here we evaluate how aridity affects the balance between C, N and P in soils collected from 224 dryland sites from all continents except Antarctica. We find a negative effect of aridity on the concentration of soil organic C and total N, but a positive effect on the concentration of inorganic P. Aridity is negatively related to plant cover, which may favour the dominance of physical processes such as rock weathering, a major source of P to ecosystems, over biological processes that provide more C and N, such as litter decomposition. Our findings suggest that any predicted increase in aridity with climate change will probably reduce the concentrations of N and C in global drylands, but increase that of P. These changes would uncouple the C, N and P cycles in drylands and could negatively affect the provision of key services provided by these ecosystems.

Disturbance and density-dependent processes (competition and facilitation) influence the fine-scale genetic structure of a tree species' population.

BACKGROUND AND AIMS: Disturbances, dispersal and biotic interactions are three major drivers of the spatial distribution of genotypes within populations, the last of which has been less studied than the other two. This study aimed to determine the role of competition and facilitation in the degree of conspecific genetic relatedness of nearby individuals of tree populations. It was expected that competition among conspecifics will lead to low relatedness, while facilitation will lead to high relatedness (selection for high relatedness within clusters). METHODS: The stand structure and spatial genetic structure (SGS) of trees were examined within old-growth and second-growth forests (including multi-stemmed trees at the edge of forests) of Nothofagus pumilio following large-scale fires in Patagonia, Chile. Genetic spatial autocorrelations were computed on a spatially explicit sampling of the forests using five microsatellite loci. As biotic plant interactions occur among immediate neighbours, mean nearest neighbour distance (MNND) among trees was computed as a threshold for distinguishing the effects of disturbances and biotic interactions. KEY RESULTS: All forests exhibited a significant SGS for distances greater than the MNND. The old-growth forest genetic and stand structure indicated gap recolonization from nearby trees (significantly related trees at distances between 4 and 10 m). At distances smaller than the MNND, trees of the second-growth interior forest showed significantly lower relatedness, suggesting a fading of the recolonization structure by competition, whereas the second-growth edge forest showed a positive and highly significant relatedness among trees (higher among stems of a cluster than among stems of different clusters), resulting from facilitation. CONCLUSIONS: Biotic interactions are shown to influence the genetic composition of a tree population. However, facilitation can only persist if individuals are related. Thus, the genetic composition in turn influences what type of biotic interactions will take place among immediate neighbours in post-disturbance forests.

Anthropogenic fire drives the evolution of seed traits.

Fire is a major disturbance affecting ecosystems worldwide. Phylogenetic studies have shown that the evolution of seed persistence (fire resistance) is associated with fire frequency or severity. However, the existence of specific seed traits resulting from natural selection mediated by fire remains a key question in plant evolution. We evaluated the role of fire in the evolution of seed traits from a microevolutionary perspective, using as a study system a native forb from the Chilean matorral, where fire is a novel, anthropogenic disturbance. We show that anthropogenic fires are shaping the evolution of seed traits such as pubescence and shape. Among-population variation in seed pubescence, shape, and pericarp thickness was strongly associated with fire frequency, and within a population, fire selected those plants with more pubescent seeds, thicker pericarps, and less rounded seeds. Seed pubescence and shape were shown to be heritable traits. Our findings provide insights into the understanding of the evolution of seed traits in fire-prone environments and demonstrate that human-made fires can be driving evolutionary changes in plant species from ecosystems where fires do not occur naturally.

Identifying Strategies for Effective Biodiversity Preservation and Species Status of Chilean Amphibians.

Resources are limited in global biodiversity conservation efforts, which emphasizes the significance of setting conservation priorities. Using standardized criteria, we evaluated 58 amphibian species in Chile to determine their conservation priority (CP). Species with insufficient historical data had their values marked as missing. With a median value of p = 1.67, the results demonstrated CP values ranging from p = 0.48 to p = 3.0, classifying species into priority and non-priority groups. Four levels were established for the priority categories: no priority, low priority, medium priority, and high priority. Additionally, the Telmatobiidae and Alsodidae families were identified as two more priority families. Notably, the species with the highest priority were found to be T. halli, T. fronteriensis, T. philippii, T. chusmisensis, A. pehuenche, and Alsodes tumultuosus, where T. philippii and T. fronteriensis have equal priority for conservation at the national level according to the conservation priority analysis. Eight priority families-the Alsodidae, Batrachylidae, Bufonidae, Ceratophryidae, Leptodactylidae, Rhinodermatidae, and Telmatobiidae-were determined, and 14 species-or 24% of the species examined-need further study. Based on the conservation priority analysis, the species T. fronteriensis and T. philippii share the highest priority for conservation at the national level (p = 2.50). With 70% of the amphibians under study being threatened mainly by habitat loss, pollution, and emerging diseases, the creation of conservation categories made the threat assessment process easier. Due to a lack of information on geographic distribution and abundance, quantitatively classifying amphibians in Chile remains difficult. The analysis of conservation priorities and potential extinction threats informs appropriate management strategies.

Seabirds modify El Niño effects on tree growth in a southern Pacific island.

Oceanic island ecosystems are particularly sensitive to El Niño effects due to their dependence on energy and nutrient inputs from marine systems. Seabirds play a key role in transporting resources of marine origin to insular ecosystems. We report tree-growth patterns showing how the effects of El Niño rainy events on tree species in a southern Pacific island depend on the presence of local seabird colonies. We performed manipulative experiments in order to assess the mechanisms underlying these patterns. Tree ring data showed that, in normal years, the growth of all tree species (Aextoxicon punctatum, Cryptocarya alba, and Pinus radiata) was significantly lower in seabird sites compared to adjacent patches without seabirds (control sites). In contrast, in El Niño years, trees formerly hosting seabird colonies grew more than those in control sites. Experiments showed that (1) pine plants on soil from seabird sites grew more than those on soil from control sites, (2) pine individuals with seabird feces on their leaves grew less than those sprayed with an aqueous solution, and (3) soil moisture had little effect on plant growth. The stress produced by massive cormorant nesting on trees, which impairs tree growth and physiological performance, is relieved during El Niño events because of seabird migration due to decreased prey availability and pouring rains that flood nests. Soils enriched by the seabird guano, together with the increased water availability associated with El Niño, foster the growth of trees from seabird sites. We suggest that El Niño may be a key determinant of tree performance in forest communities from island and coastal ecosystems of the Pacific Ocean.

Genetic Diversity, Morphometric Characterization, and Conservation Reassessment of the Critically Endangered Freshwater Snail, Heleobia atacamensis, in the Atacama Saltpan, Northern Chile.

Evaporitic ecosystems of the Atacama Desert contain a rich endemic fauna, including mollusk species. A recent study performed in the freshwater snail Heleobia atacamensis, endemic to the Atacama Saltpan, revealed a strong interdependence of genetic patterns with climatic fluctuations and landscape physiography. The species is currently listed as Critically Endangered at regional scale and as Data Deficient on the International Union for Conservation of Nature (IUCN) Red List. Here, we studied genetic diversity and demographic history of several populations of the species occurring on a connectivity gradient, including snails from new peripherical localities (Peine and Tilomonte), which were compared with topotype specimens. In addition, we reassessed the conservation status using the IUCN Red List categories and criteria considering species-specific idiosyncrasy. Phylogenetic and phylogeographical analyses indicated that snails from Peine and Tilomonte belong to H. atacamensis. We discovered significant differentiation in shell morphology, which was generally greater in geographically isolated populations. We also inferred six genetic clusters and a demographic expansion congruent with the wet periods that occurred at the end of the Pleistocene. Considering the highest risk category obtained, H. atacamensis was reassessed as Endangered at regional scale. Future conservation plans should consider the genetic assemblages as conservation units.

Distribution, conservation status and proposed measures for preservation of Radiodiscus microgastropods in Chile.

The genus Radiodiscus includes minute terrestrial snails occurring throughout the American continent. We assessed the conservation status of eight poorly known Chilean Radiodiscus species using the International Union for Conservation of Nature (IUCN) and NatureServe categories and criteria. Under the IUCN guidelines the species were assessed using the Criterion B of geographic range, which considers the extent of occurrence (EOO) and area of occupancy (AOO) as subcriteria. For NatureServe we used these two parameters plus the number of occurrences, ecological viability, and threats. Considering species rarity and possible sampling bias, we also used ecological niche modeling to determine climate and environmental tolerances and predict potential species distributions analyzing bioclimatic and geographical layers. Radiodiscus australis, R. coarctatus and R. quillajicola were listed as Critically Endangered by IUCN and NatureServe standards; R. coppingeri, R. flammulatus, R. magellanicus and R. villarricensis as Endangered by both methods; while R. riochicoensis as Endangered by IUCN standards and Vulnerable by NatureServe standards. Niche modeling results indicated that Radiodiscus species respond to different environmental conditions and that the predicted distribution areas contain suitable habitats beyond the current ranges, which may be helpful for future management plans. Nature-based sport tourism, forestry activities, urbanization, roads, pollution, mining, forest fires, livestock, volcanism, tsunamis, soil erosion and introduced species are among the major threats affecting these snails. Based on the low number of occurrences and the threats identified, the most at-risk species are R. coarctatus and R. quillajicola (one record), R. australis (two records) and R. villarricensis (three records); the latter two lacking occurrences within protected areas. Compiling our findings, we propose a list of actions to preserve Chilean Radiodiscus species.

Electromagnetic fields disrupt the pollination service by honeybees.

We assessed the effect that electromagnetic field (EMF) exerts on honeybees' pollination efficiency using field and laboratory experiments. First, we measured levels of gene and protein expression in metabolic pathways involved in stress and behavioral responses elicited by EMF. Second, we assessed the effect of EMF on honeybee behavior and seed production by the honeybee-pollinated California poppy and, lastly, by measuring the consequences of pollination failure on plants' community richness and abundance. EMF exposure exerted strong physiological stress on honeybees as shown by the enhanced expression of heat-shock proteins and genes involved in antioxidant activity and affected the expression levels of behavior-related genes. Moreover, California poppy individuals growing near EMF received fewer honeybee visits and produced fewer seeds than plants growing far from EMF. Last, we found a hump-shaped relationship between EMF and plant species richness and plant abundance. Our study provides conclusive evidence of detrimental impacts of EMF on honeybee's pollination behavior, leading to negative effects on plant community.

Soil contamination in nearby natural areas mirrors that in urban greenspaces worldwide.

Soil contamination is one of the main threats to ecosystem health and sustainability. Yet little is known about the extent to which soil contaminants differ between urban greenspaces and natural ecosystems. Here we show that urban greenspaces and adjacent natural areas (i.e., natural/semi-natural ecosystems) shared similar levels of multiple soil contaminants (metal(loid)s, pesticides, microplastics, and antibiotic resistance genes) across the globe. We reveal that human influence explained many forms of soil contamination worldwide. Socio-economic factors were integral to explaining the occurrence of soil contaminants worldwide. We further show that increased levels of multiple soil contaminants were linked with changes in microbial traits including genes associated with environmental stress resistance, nutrient cycling, and pathogenesis. Taken together, our work demonstrates that human-driven soil contamination in nearby natural areas mirrors that in urban greenspaces globally, and highlights that soil contaminants have the potential to cause dire consequences for ecosystem sustainability and human wellbeing.

The global distribution and environmental drivers of the soil antibiotic resistome.

BACKGROUND: Little is known about the global distribution and environmental drivers of key microbial functional traits such as antibiotic resistance genes (ARGs). Soils are one of Earth's largest reservoirs of ARGs, which are integral for soil microbial competition, and have potential implications for plant and human health. Yet, their diversity and global patterns remain poorly described. Here, we analyzed 285 ARGs in soils from 1012 sites across all continents and created the first global atlas with the distributions of topsoil ARGs. RESULTS: We show that ARGs peaked in high latitude cold and boreal forests. Climatic seasonality and mobile genetic elements, associated with the transmission of antibiotic resistance, were also key drivers of their global distribution. Dominant ARGs were mainly related to multidrug resistance genes and efflux pump machineries. We further pinpointed the global hotspots of the diversity and proportions of soil ARGs. CONCLUSIONS: Together, our work provides the foundation for a better understanding of the ecology and global distribution of the environmental soil antibiotic resistome. Video Abstract.

Phylogeography and molecular species delimitation reveal cryptic diversity in Potamolithus (Caenogastropoda: Tateidae) of the southwest basin of the Andes.

The species of the genus Potamolithus inhabiting the southwestern basin of the Andes are difficult to distinguish due to small size and similar shell morphology. Only Potamolithus australis and Potamolithus santiagensis have been traditionally recognized in this region, but the occurrence of several morphologically similar undescribed populations could increase the regional richness. Here we delimit described and potentially undescribed cryptic species of the genus using partial sequences of the mitochondrial cytochrome c oxidase subunit I (COI) gene. Network analysis and diversity indices inferred six highly differentiated haplogroups, many of them sympatric and widespread in the study area. Phylogeographic analyses suggest a scenario of recent diversification and the occurrence of multiple refuges during the successive Pleistocene glaciations. Phylogenetic analysis also recovered six major clades that showed no relationship with physiography. Species delimitation analyses consistently recognized three or four candidate species apart from P. australis and P. santiagensis. Divergence times indicate that speciation of Chilean Potamolithus began at the end of the Pliocene, probably driven by climatic rather than geographic events. Considering the high inter- and intra-basin genetic diversity, conservation efforts should be focused on protecting sympatric taxa in the basins with the highest species richness.

Species and genera in Aleurodiscus sensu lato as viewed from the Southern Hemisphere.

Phylogenetic relationships of 12 species in Aleurodiscus sensu lato (Stereaceae, Russulales) described from the Patagonian forests of Chile and Argentina were investigated based on sequences of nuc rDNA internal transcribed spacer region ITS1-5.8S-ITS2 (ITS) and the D1-D2 domains of nuc 28S rDNA (28S). A new genus and a new species are presented, and 10 new combinations proposed. The genus Gloeosoma is shown to be phylogenetically well supported and morphologically circumscribed; it includes G. vitellinum (type species), G. mirabile, comb. nov., G. zealandicum, comb. nov., and Gloeosoma decorticans, sp. nov., which is newly described from Chile. The new genus Stereodiscus is proposed to accommodate a group of taxa characterized by an austral distribution and morphologically by smooth, thin-walled, amyloid basidiospores and a lack of gloeocystidia and acanthocystidia; three species develop Stereum-like basidiomata and two species present discoid ones. The new genus includes the species formerly known as Aleurodiscus antarcticus, A. limonisporus, A. parmuliformis, A. patagonicus, and A. triviale. Specimens of Stereodiscus parmuliformis (A. parmuliformis) from New Zealand (where it was originally described) and southern Chile are shown to be phylogenetically conspecific, which confirms its presence in Patagonia. Gloeosoma and Stereodiscus are shown to be distantly related to Aleurodiscus s. str. and other genera in Stereaceae. The new combinations Aleurocystidiellum bernicchiae, Aleurocystidiellum hallenbergii, and Acanthobasidium quilae are proposed based on morphology and phylogenetic analyses, and Aleurodiscus cerussatus is shown to be a cryptic species complex.