Biogeography and Genetic Diversity of Terrestrial Mites in the Ross Sea Region, Antarctica.

Free-living terrestrial mites (Acari) have persisted through numerous glacial cycles in Antarctica. Very little is known, however, of their genetic diversity and distribution, particularly within the Ross Sea region. To redress this gap, we sampled mites throughout the Ross Sea region, East Antarctica, including Victoria Land and the Queen Maud Mountains (QMM), covering a latitudinal range of 72-85 °S, as well as Lauft Island near Mt. Siple (73 °S) in West Antarctica and Macquarie Island (54oS) in the sub-Antarctic. We assessed genetic diversity using mitochondrial cytochrome c oxidase subunit I gene sequences (COI-5P DNA barcode region), and also morphologically identified voucher specimens. We obtained 130 sequences representing four genera: Nanorchestes (n = 30 sequences), Stereotydeus (n = 46), Coccorhagidia (n = 18) and Eupodes (n = 36). Tree-based analyses (maximum likelihood) revealed 13 genetic clusters, representing as many as 23 putative species indicated by barcode index numbers (BINs) from the Barcode of Life Datasystems (BOLD) database. We found evidence for geographically-isolated cryptic species, e.g., within Stereotydeus belli and S. punctatus, as well as unique genetic groups occurring in sympatry (e.g., Nanorchestes spp. in QMM). Collectively, these data confirm high genetic divergence as a consequence of geographic isolation over evolutionary timescales. From a conservation perspective, additional targeted sampling of understudied areas in the Ross Sea region should be prioritised, as further diversity is likely to be found in these short-range endemic mites.

Soil biodiversity needs policy without borders.

Soil health laws should account for global soil connections.

Strong Dispersal Limitation of Microbial Communities at Shackleton Glacier, Antarctica.

Microbial communities can be structured by both deterministic and stochastic processes, but the relative importance of these processes remains unknown. The ambiguity partly arises from an inability to disentangle soil microbial processes from confounding factors, such as aboveground plant communities or anthropogenic disturbance. In this study, we characterized the relative contributions of determinism and stochasticity to assembly processes of soil bacterial communities across a large environmental gradient of undisturbed Antarctic soils. We hypothesized that harsh soils would impose a strong environmental selection on microbial communities, whereas communities in benign soils would be structured largely by dispersal. Contrary to our expectations, dispersal was the dominant assembly mechanism across the entire soil environmental gradient, including benign environments. The microbial community composition reflects slowly changing soil conditions and dispersal limitation of isolated sites. Thus, stochastic processes, as opposed to deterministic, are primary drivers of soil ecosystem assembly across space at our study site. This is especially surprising given the strong environmental constraints on soil microorganisms in one of the harshest environments on the planet, suggesting that dispersal could be a driving force in microbial community assembly in soils worldwide. IMPORTANCE Because of their diversity and ubiquity, microbes provide an excellent means to tease apart how natural communities are structured. In general, ecologists believe that stochastic assembly processes, like random drift and dispersal, should dominate in benign environments while deterministic processes, like environmental filtering, should be prevalent in harsh environments. To help resolve this debate, we analyzed microbial community composition in pristine Antarctic soils devoid of human influence or plant communities for eons. Our results demonstrate that dispersal limitation is a surprisingly potent force of community limitation throughout all soil conditions. Thus, dispersal appears to be a driving force of microbial community assembly, even in the harshest of conditions.

Threat management priorities for conserving Antarctic biodiversity.

Antarctic terrestrial biodiversity faces multiple threats, from invasive species to climate change. Yet no large-scale assessments of threat management strategies exist. Applying a structured participatory approach, we demonstrate that existing conservation efforts are insufficient in a changing world, estimating that 65% (at best 37%, at worst 97%) of native terrestrial taxa and land-associated seabirds are likely to decline by 2100 under current trajectories. Emperor penguins are identified as the most vulnerable taxon, followed by other seabirds and dry soil nematodes. We find that implementing 10 key threat management strategies in parallel, at an estimated present-day equivalent annual cost of US$23 million, could benefit up to 84% of Antarctic taxa. Climate change is identified as the most pervasive threat to Antarctic biodiversity and influencing global policy to effectively limit climate change is the most beneficial conservation strategy. However, minimising impacts of human activities and improved planning and management of new infrastructure projects are cost-effective and will help to minimise regional threats. Simultaneous global and regional efforts are critical to secure Antarctic biodiversity for future generations.

Islands in the ice: Potential impacts of habitat transformation on Antarctic biodiversity.

Antarctic biodiversity faces an unknown future with a changing climate. Most terrestrial biota is restricted to limited patches of ice-free land in a sea of ice, where they are adapted to the continent's extreme cold and wind and exploit microhabitats of suitable conditions. As temperatures rise, ice-free areas are predicted to expand, more rapidly in some areas than others. There is high uncertainty as to how species' distributions, physiology, abundance, and survivorship will be affected as their habitats transform. Here we use current knowledge to propose hypotheses that ice-free area expansion (i) will increase habitat availability, though the quality of habitat will vary; (ii) will increase structural connectivity, although not necessarily increase opportunities for species establishment; (iii) combined with milder climates will increase likelihood of non-native species establishment, but may also lengthen activity windows for all species; and (iv) will benefit some species and not others, possibly resulting in increased homogeneity of biodiversity. We anticipate considerable spatial, temporal, and taxonomic variation in species responses, and a heightened need for interdisciplinary research to understand the factors associated with ecosystem resilience under future scenarios. Such research will help identify at-risk species or vulnerable localities and is crucial for informing environmental management and policymaking into the future.

Elevational Constraints on the Composition and Genomic Attributes of Microbial Communities in Antarctic Soils.

The inland soils found on the Antarctic continent represent one of the more challenging environments for microbial life on Earth. Nevertheless, Antarctic soils harbor unique bacterial and archaeal (prokaryotic) communities able to cope with extremely cold and dry conditions. These communities are not homogeneous, and the taxonomic composition and functional capabilities (genomic attributes) of these communities across environmental gradients remain largely undetermined. We analyzed the prokaryotic communities in soil samples collected from across the Shackleton Glacier region of Antarctica by coupling quantitative PCR, marker gene amplicon sequencing, and shotgun metagenomic sequencing. We found that elevation was the dominant factor explaining differences in the structures of the soil prokaryotic communities, with the drier and saltier soils found at higher elevations harboring less diverse communities and unique assemblages of cooccurring taxa. The higher-elevation soil communities also had lower maximum potential growth rates (as inferred from metagenome-based estimates of codon usage bias) and an overrepresentation of genes associated with trace gas metabolism. Together, these results highlight the utility of assessing community shifts across pronounced environmental gradients to improve our understanding of the microbial diversity found in Antarctic soils and the strategies used by soil microbes to persist at the limits of habitability. IMPORTANCE Antarctic soils represent an ideal system to study how environmental properties shape the taxonomic and functional diversity of microbial communities given the relatively low diversity of Antarctic soil microbial communities and the pronounced environmental gradients that occur across soils located in reasonable proximity to one another. Moreover, the challenging environmental conditions typical of most Antarctic soils present an opportunity to investigate the traits that allow soil microbes to persist in some of the most inhospitable habitats on Earth. We used cultivation-independent methods to study the bacterial and archaeal communities found in soil samples collected from across the Shackleton Glacier region of the Transantarctic Mountains. We show that those environmental characteristics associated with elevation have the greatest impact on the structure of these microbial communities, with the colder, drier, and saltier soils found at higher elevations sustaining less diverse communities that were distinct from those in more hospitable soils with respect to their composition, genomic attributes, and overall life-history strategies. Notably, the harsher conditions found in higher-elevation soils likely select for taxa with lower maximum potential growth rates and an increased reliance on trace gas metabolism to support growth.

Response of Antarctic soil fauna to climate-driven changes since the Last Glacial Maximum.

Understanding how terrestrial biotic communities have responded to glacial recession since the Last Glacial Maximum (LGM) can inform present and future responses of biota to climate change. In Antarctica, the Transantarctic Mountains (TAM) have experienced massive environmental changes associated with glacial retreat since the LGM, yet we have few clues as to how its soil invertebrate-dominated animal communities have responded. Here, we surveyed soil invertebrate fauna from above and below proposed LGM elevations along transects located at 12 features across the Shackleton Glacier region. Our transects captured gradients of surface ages possibly up to 4.5 million years and the soils have been free from human disturbance for their entire history. Our data support the hypothesis that soils exposed during the LGM are now less suitable habitats for invertebrates than those that have been exposed by deglaciation following the LGM. Our results show that faunal abundance, community composition, and diversity were all strongly affected by climate-driven changes since the LGM. Soils more recently exposed by the glacial recession (as indicated by distances from present ice surfaces) had higher faunal abundances and species richness than older exposed soils. Higher abundances of the dominant nematode Scottnema were found in older exposed soils, while Eudorylaimus, Plectus, tardigrades, and rotifers preferentially occurred in more recently exposed soils. Approximately 30% of the soils from which invertebrates could be extracted had only Scottnema, and these single-taxon communities occurred more frequently in soils exposed for longer periods of time. Our structural equation modeling of abiotic drivers highlighted soil salinity as a key mediator of Scottnema responses to soil exposure age. These changes in soil habitat suitability and biotic communities since the LGM indicate that Antarctic terrestrial biodiversity throughout the TAM will be highly altered by climate warming.

Precipitation effects on nematode diversity and carbon footprint across grasslands.

Free-living nematodes are one of the most diverse metazoan taxa in terrestrial ecosystems and are critical to the global soil carbon (C) cycling through their role in organic matter decomposition. They are highly dependent on water availability for movement, feeding, and reproduction. Projected changes in precipitation across temporal and spatial scales will affect free-living nematodes and their contribution to C cycling with unforeseen consequences. We experimentally reduced and increased growing season precipitation for 2 years in 120 field plots at arid, semiarid, and mesic grasslands and assessed precipitation controls on nematode genus diversity, community structure, and C footprint. Increasing annual precipitation reduced nematode diversity and evenness over time at all sites, but the mechanism behind these temporal responses differed for dry and moist grasslands. In arid and semiarid sites, there was a loss of drought-adapted rare taxa with increasing precipitation, whereas in mesic conditions increases in the population of predaceous taxa with increasing precipitation may have caused the observed reductions in dominant colonizer taxa and yielded the negative precipitation-diversity relationship. The effects of temporal changes in precipitation on all aspects of the nematode C footprint (respiration, production, and biomass C) were all dependent on the site (significant spatial × temporal precipitation interaction) and consistent with diversity responses at mesic, but not at arid and semiarid, grasslands. These results suggest that free-living nematode biodiversity and their C footprint will respond to climate change-driven shifts in water availability and that more frequent extreme wet years may accelerate decomposition and C turnover in semiarid and arid grasslands.

Local stability properties of complex, species-rich soil food webs with functional block structure.

Ecologists have long debated the properties that confer stability to complex, species-rich ecological networks. Species-level soil food webs are large and structured networks of central importance to ecosystem functioning. Here, we conducted an analysis of the stability properties of an up-to-date set of theoretical soil food web models that account both for realistic levels of species richness and the most recent views on the topological structure (who is connected to whom) of these food webs. The stability of the network was best explained by two factors: strong correlations between interaction strengths and the blocked, nonrandom trophic structure of the web. These two factors could stabilize our model food webs even at the high levels of species richness that are typically found in soil, and that would make random systems very unstable. Also, the stability of our soil food webs is well-approximated by the cascade model. This result suggests that stability could emerge from the hierarchical structure of the functional organization of the web. Our study shows that under the assumption of equilibrium and small perturbations, theoretical soil food webs possess a topological structure that allows them to be complex yet more locally stable than their random counterpart. In particular, results strongly support the general hypothesis that the stability of rich and complex soil food webs is mostly driven by correlations in interaction strength and the organization of the soil food web into functional groups. The implication is that in real-world food web, any force disrupting the functional structure and distribution pattern of interaction strengths (i.e., energy fluxes) of the soil food webs will destabilize the dynamics of the system, leading to species extinction and major changes in the relative abundances of species.

Global data on earthworm abundance, biomass, diversity and corresponding environmental properties.

Earthworms are an important soil taxon as ecosystem engineers, providing a variety of crucial ecosystem functions and services. Little is known about their diversity and distribution at large spatial scales, despite the availability of considerable amounts of local-scale data. Earthworm diversity data, obtained from the primary literature or provided directly by authors, were collated with information on site locations, including coordinates, habitat cover, and soil properties. Datasets were required, at a minimum, to include abundance or biomass of earthworms at a site. Where possible, site-level species lists were included, as well as the abundance and biomass of individual species and ecological groups. This global dataset contains 10,840 sites, with 184 species, from 60 countries and all continents except Antarctica. The data were obtained from 182 published articles, published between 1973 and 2017, and 17 unpublished datasets. Amalgamating data into a single global database will assist researchers in investigating and answering a wide variety of pressing questions, for example, jointly assessing aboveground and belowground biodiversity distributions and drivers of biodiversity change.

Antarctic ecosystems in transition - life between stresses and opportunities.

Important findings from the second decade of the 21st century on the impact of environmental change on biological processes in the Antarctic were synthesised by 26 international experts. Ten key messages emerged that have stakeholder-relevance and/or a high impact for the scientific community. They address (i) altered biogeochemical cycles, (ii) ocean acidification, (iii) climate change hotspots, (iv) unexpected dynamism in seabed-dwelling populations, (v) spatial range shifts, (vi) adaptation and thermal resilience, (vii) sea ice related biological fluctuations, (viii) pollution, (ix) endangered terrestrial endemism and (x) the discovery of unknown habitats. Most Antarctic biotas are exposed to multiple stresses and considered vulnerable to environmental change due to narrow tolerance ranges, rapid change, projected circumpolar impacts, low potential for timely genetic adaptation, and migration barriers. Important ecosystem functions, such as primary production and energy transfer between trophic levels, have already changed, and biodiversity patterns have shifted. A confidence assessment of the degree of 'scientific understanding' revealed an intermediate level for most of the more detailed sub-messages, indicating that process-oriented research has been successful in the past decade. Additional efforts are necessary, however, to achieve the level of robustness in scientific knowledge that is required to inform protection measures of the unique Antarctic terrestrial and marine ecosystems, and their contributions to global biodiversity and ecosystem services.

Genetic diversity of soil invertebrates corroborates timing estimates for past collapses of the West Antarctic Ice Sheet.

During austral summer field seasons between 1999 and 2018, we sampled at 91 locations throughout southern Victoria Land and along the Transantarctic Mountains for six species of endemic microarthropods (Collembola), covering a latitudinal range from 76.0°S to 87.3°S. We assembled individual mitochondrial cytochrome c oxidase subunit 1 (COI) sequences (n = 866) and found high levels of sequence divergence at both small (<10 km) and large (>600 km) spatial scales for four of the six Collembola species. We applied molecular clock estimates and assessed genetic divergences relative to the timing of past glacial cycles, including collapses of the West Antarctic Ice Sheet (WAIS). We found that genetically distinct lineages within three species have likely been isolated for at least 5.54 My to 3.52 My, while the other three species diverged more recently (<2 My). We suggest that Collembola had greater dispersal opportunities under past warmer climates, via flotation along coastal margins. Similarly increased opportunities for dispersal may occur under contemporary climate warming scenarios, which could influence the genetic structure of extant populations. As Collembola are a living record of past landscape evolution within Antarctica, these findings provide biological evidence to support geological and glaciological estimates of historical WAIS dynamics over the last ca 5 My.

Blind spots in global soil biodiversity and ecosystem function research.

Soils harbor a substantial fraction of the world's biodiversity, contributing to many crucial ecosystem functions. It is thus essential to identify general macroecological patterns related to the distribution and functioning of soil organisms to support their conservation and consideration by governance. These macroecological analyses need to represent the diversity of environmental conditions that can be found worldwide. Here we identify and characterize existing environmental gaps in soil taxa and ecosystem functioning data across soil macroecological studies and 17,186 sampling sites across the globe. These data gaps include important spatial, environmental, taxonomic, and functional gaps, and an almost complete absence of temporally explicit data. We also identify the limitations of soil macroecological studies to explore general patterns in soil biodiversity-ecosystem functioning relationships, with only 0.3% of all sampling sites having both information about biodiversity and function, although with different taxonomic groups and functions at each site. Based on this information, we provide clear priorities to support and expand soil macroecological research.

Ecto- and endoparasitic nematodes respond differently across sites to changes in precipitation.

Plant parasitic nematodes are among the greatest consumers of primary production in terrestrial ecosystems. Their feeding strategies can be divided into endoparasites and ectoparasites that differ substantially, not only in their damage potential to host tissue and primary production, but also in their susceptibility to environmental changes. Climate change is predicted to increase variability of precipitation in many systems, yet the effects on belowground biodiversity and associated impacts on primary productivity remain poorly understood. To examine the impact of altered precipitation on endo- and ectoparasitic soil nematodes, we conducted a 2-year precipitation manipulation study across an arid, a semiarid, and a mesic grassland. Plant parasite feeding type abundance, functional guilds, and herbivory index in response to precipitation were evaluated. Responses of endo- and ectoparasites to increased precipitation varied by grassland type. There was little response of ectoparasites to increased precipitation although their population declined at the mesic site with increased precipitation. The abundance of endoparasites remained unchanged with increasing precipitation at the arid site, increased at the semiarid, and decreased at the mesic site. The herbivory index followed closely the trends seen in the endoparasites response by stagnating at the arid site, increasing at the semiarid, and decreasing at the mesic site. Our findings suggest that altered precipitation has differing effects on plant parasite feeding strategies as well as functional guilds. This may have important implications for grassland productivity, as plant parasite pressure may exacerbate the effects of climate change on host plants.

A global database of soil nematode abundance and functional group composition.

As the most abundant animals on earth, nematodes are a dominant component of the soil community. They play critical roles in regulating biogeochemical cycles and vegetation dynamics within and across landscapes and are an indicator of soil biological activity. Here, we present a comprehensive global dataset of soil nematode abundance and functional group composition. This dataset includes 6,825 georeferenced soil samples from all continents and biomes. For geospatial mapping purposes these samples are aggregated into 1,933 unique 1-km pixels, each of which is linked to 73 global environmental covariate data layers. Altogether, this dataset can help to gain insight into the spatial distribution patterns of soil nematode abundance and community composition, and the environmental drivers shaping these patterns.

Towards an integrative understanding of soil biodiversity.

Soil is one of the most biodiverse terrestrial habitats. Yet, we lack an integrative conceptual framework for understanding the patterns and mechanisms driving soil biodiversity. One of the underlying reasons for our poor understanding of soil biodiversity patterns relates to whether key biodiversity theories (historically developed for aboveground and aquatic organisms) are applicable to patterns of soil biodiversity. Here, we present a systematic literature review to investigate whether and how key biodiversity theories (species-energy relationship, theory of island biogeography, metacommunity theory, niche theory and neutral theory) can explain observed patterns of soil biodiversity. We then discuss two spatial compartments nested within soil at which biodiversity theories can be applied to acknowledge the scale-dependent nature of soil biodiversity.

Global distribution of earthworm diversity.

Soil organisms, including earthworms, are a key component of terrestrial ecosystems. However, little is known about their diversity, their distribution, and the threats affecting them. We compiled a global dataset of sampled earthworm communities from 6928 sites in 57 countries as a basis for predicting patterns in earthworm diversity, abundance, and biomass. We found that local species richness and abundance typically peaked at higher latitudes, displaying patterns opposite to those observed in aboveground organisms. However, high species dissimilarity across tropical locations may cause diversity across the entirety of the tropics to be higher than elsewhere. Climate variables were found to be more important in shaping earthworm communities than soil properties or habitat cover. These findings suggest that climate change may have serious implications for earthworm communities and for the functions they provide.

Challenges and Opportunities for Soil Biodiversity in the Anthropocene.

Biodiversity on Earth is strongly affected by human alterations to the environment. The majority of studies have considered aboveground biodiversity, yet little is known about whether biodiversity changes belowground follow the same patterns as those observed aboveground. It is now established that communities of soil biota have been substantially altered by direct human activities such as soil sealing, agricultural land-use intensification, and biological invasions resulting from the introduction of non-native species. In addition, altered abiotic conditions resulting from climate change have also impacted soil biodiversity. These changes in soil biodiversity can alter ecosystem functions performed by the soil biota, and therefore, human-induced global changes have a feedback effect on ecosystem services via altered soil biodiversity. Here, we highlight the major phenomena that threaten soil biodiversity, and we propose options to reverse the decline in soil biodiversity. We argue that it is essential to protect soil biodiversity as a rich reservoir that provides insurance against the changes wrought by the Anthropocene. Overall, we need to better understand the determinants of soil biodiversity and how they function, plan to avoid further losses, and restore soil biodiversity where possible. Safeguarding this rich biotic reservoir is essential for soil sustainability and, ultimately, the sustainability of human society.