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• W2977791744 abstract "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. 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. During the Anthropocene, a large fraction of the natural land has been turned into human-influenced biomes, which now represent about 75% of all land on Earth [1Ellis E.C. Ramankutty N. Putting people in the map: anthropogenic biomes of the world.Front. Ecol. Environ. 2008; 6: 439-447Crossref Scopus (1163) Google Scholar]. The rapidly increasing human population and the increasing ecological footprint per capita is placing further pressure on the remaining natural land. Along with that, the Earth’s climate is changing more rapidly than ever before: extreme events including the incidence and severity of drought and heavy storms are increasing, and invasions of introduced exotic organisms that can change entire ecosystems have become more prevalent. These anthropogenic changes have profound implications for all types of species on the planet, and total species diversity is decreasing at a rate 1,000 times higher than before human presence [2Joppa L.N. Connor B. Visconti P. Smith C. Geldmann J. Hoffmann M. Watson J.E.M. Butchart S.H.M. Virah-Sawmy M. Halpern B.S. et al.Filling in biodiversity threat gaps.Science. 2016; 352: 416Crossref PubMed Scopus (149) Google Scholar]. Such biodiversity declines may be well illustrated by the fact that the global biomass of livestock has become more than ten times that of all wild mammals and birds together [3Bar-On Y.M. Phillips R. Milo R. The biomass distribution on Earth.Proc. Natl. Acad. Sci. USA. 2018; 115: 6506-6511Crossref PubMed Scopus (1196) Google Scholar]. So far, the focus on diversity declines by scientific researchers and the public has been almost entirely concerned with macroscopic plants and animals, both in water and on land [4Dirzo R. Young H.S. Galetti M. Ceballos G. Isaac N.J.B. Collen B. Defaunation in the Anthropocene.Science. 2014; 345: 401-406Crossref PubMed Scopus (2174) Google Scholar, 5Young H.S. McCauley D.J. Galetti M. Dirzo R. Patterns, causes, and consequences of Anthropocene defaunation.Annu. Rev. Ecol. Evol. Syst. 2016; 47: 333-358Crossref Scopus (258) Google Scholar]. Far less is known about anthropogenic impacts on the diversity of microscopic organisms and those animals that are living hidden in soils (Figure 1), despite the fact that these organisms — together with plants — dominate the living biomass [3Bar-On Y.M. Phillips R. Milo R. The biomass distribution on Earth.Proc. Natl. Acad. Sci. USA. 2018; 115: 6506-6511Crossref PubMed Scopus (1196) Google Scholar] on Earth. Although the exact mechanisms often remain unknown [6Wall D.H. Bardgett R.D. Kelly E. Biodiversity in the dark.Nat. Geosci. 2010; 3: 297Crossref Scopus (93) Google Scholar], soil biodiversity plays a pivotal role in providing key ecosystem functions and services [7Bardgett R.D. van der Putten W.H. Belowground biodiversity and ecosystem functioning.Nature. 2014; 515: 505-511Crossref PubMed Scopus (1670) Google Scholar]. As such, a decrease in soil biodiversity is associated with a simultaneous decrease of several soil functions [8Wagg C. Bender S.F. Widmer F. van der Heijden M.G.A. Soil biodiversity and soil community composition determine ecosystem multifunctionality.Proc. Natl. Acad. Sci. USA. 2014; 111: 5266-5270Crossref PubMed Scopus (1134) Google Scholar]. Knowledge about the composition and functions of soil biota are increasing, particularly due to new methods such as high-throughput sequencing [9Geisen S. Briones M.J.I. Gan H. Behan-Pelletier V.M. Friman V.P. De Groot G.A. Hannula S.E. Lindo Z. Philippot L. Tiunov A.V. et al.A methodological framework to embrace soil biodiversity.Soil Biol. Biochem. 2019; 136: 107536Crossref Scopus (50) Google Scholar]. As we advance our understanding of soil biodiversity, are we missing something relevant? The simple answer is yes: soil contains an unknown repertoire of organisms that are directly involved in biochemical nutrient cycling, such as in the global carbon cycle, as well as in other ecosystem processes and services [10Bünemann E.K. Bongiorno G. Bai Z. Creamer R.E. De Deyn G. de Goede R. Fleskens L. Geissen V. Kuyper T.W. Mäder P. et al.Soil quality – A critical review.Soil Biol. Biochem. 2018; 120: 105-125Crossref Scopus (1012) Google Scholar]. Therefore, soil biota are directly involved in climate warming-related processes, such as the control of greenhouse gas emissions [7Bardgett R.D. van der Putten W.H. Belowground biodiversity and ecosystem functioning.Nature. 2014; 515: 505-511Crossref PubMed Scopus (1670) Google Scholar, 11Singh B.K. Bardgett R.D. Smith P. Reay D.S. Microorganisms and climate change: terrestrial feedbacks and mitigation options.Nat. Rev. Microbiol. 2010; 8: 779-790Crossref PubMed Scopus (677) Google Scholar]. However, the soil biota also contains some devastating plant and animal pests [12Wall D.H. Nielsen U.N. Six J. Soil biodiversity and human health.Nature. 2015; 528: 69-76Crossref PubMed Scopus (361) Google Scholar]. Human influences on the environment may, directly or indirectly, alter the physiological activity of the soil biota, thereby enhancing their contributions to warming, pest outbreaks, and altering other soil-borne ecosystem services [7Bardgett R.D. van der Putten W.H. Belowground biodiversity and ecosystem functioning.Nature. 2014; 515: 505-511Crossref PubMed Scopus (1670) Google Scholar, 8Wagg C. Bender S.F. Widmer F. van der Heijden M.G.A. Soil biodiversity and soil community composition determine ecosystem multifunctionality.Proc. Natl. Acad. Sci. USA. 2014; 111: 5266-5270Crossref PubMed Scopus (1134) Google Scholar]. Soil biodiversity offers major and nearly infinite opportunities; it serves as a reservoir of novel antibiotics, acts as biocontrol agents and biofertilizers, and provides certain other ecosystem services. In order to use this immense biotic reservoir and mitigate negative anthropogenic changes that threaten belowground biodiversity, we must learn a great deal more about the complex communities of the soil. We argue that understanding, protecting, and using soil biodiversity will be key challenges in order to maintain a functional ecosystem and to increase ecosystem health for soil, plants, animals and humans. Most of the biotic carbon on Earth is bound in plants (450 gigatons), whereas the second largest pool consists of soil biota, equaling roughly 92 gigatons when including subsoils [3Bar-On Y.M. Phillips R. Milo R. The biomass distribution on Earth.Proc. Natl. Acad. Sci. USA. 2018; 115: 6506-6511Crossref PubMed Scopus (1196) Google Scholar]. This immense reservoir of biotic carbon bound up in the soil prevents carbon from entering the atmosphere [11Singh B.K. Bardgett R.D. Smith P. Reay D.S. Microorganisms and climate change: terrestrial feedbacks and mitigation options.Nat. Rev. Microbiol. 2010; 8: 779-790Crossref PubMed Scopus (677) Google Scholar], but also supports long food chains, as a single gram of soil hosts millions of microbes and dozens of tiny invertebrate animals [7Bardgett R.D. van der Putten W.H. Belowground biodiversity and ecosystem functioning.Nature. 2014; 515: 505-511Crossref PubMed Scopus (1670) Google Scholar]. This diversity includes bacteria, fungi and their protist predators, and a wide range of animals (Figure 1) that span in size from tens of micrometers in the case of nematodes to meters in the case of earthworms or mammals, such as foxes and badgers that spend part of their life in soils. Even the largest organism on earth, an Armillaria fungus, is purely soilborne: its size equals that of more than 1,000 football (both American football and soccer) fields [13Ferguson B. Dreisbach T. Parks C. Filip G. Schmitt C. Coarse-scale population structure of pathogenic Armillaria species in a mixed-conifer forest in the Blue Mountains of northeast Oregon.Can. J. For. Res. 2003; 33: 612-623Crossref Scopus (155) Google Scholar]! In terms of functioning, the soil community contains major decomposers, playing key roles in carbon and nutrient cycling. Pathogens, parasites, and mutualists in the soil can directly control the performance of plants, which in turn change the performance of aboveground biota [7Bardgett R.D. van der Putten W.H. Belowground biodiversity and ecosystem functioning.Nature. 2014; 515: 505-511Crossref PubMed Scopus (1670) Google Scholar]. Although our understanding of soil biodiversity is increasing, the taxonomic diversity of the soil biota remains undescribed, and ecological functioning at high taxonomic resolution, such as at the species level, remains unknown for most soil organisms, particularly microorganisms (viruses, bacteria, fungi and protists) [6Wall D.H. Bardgett R.D. Kelly E. Biodiversity in the dark.Nat. Geosci. 2010; 3: 297Crossref Scopus (93) Google Scholar, 7Bardgett R.D. van der Putten W.H. Belowground biodiversity and ecosystem functioning.Nature. 2014; 515: 505-511Crossref PubMed Scopus (1670) Google Scholar]. Despite the functional importance of soil biodiversity for major soil functions and ecosystem services [8Wagg C. Bender S.F. Widmer F. van der Heijden M.G.A. Soil biodiversity and soil community composition determine ecosystem multifunctionality.Proc. Natl. Acad. Sci. USA. 2014; 111: 5266-5270Crossref PubMed Scopus (1134) Google Scholar] — such as provisioning of clean drinking water, prevention of greenhouse gas production, and control of diseases — soil organisms are not typically included in assessments of soil quality or biodiversity declines, nor are they incorporated in Earth-system models [10Bünemann E.K. Bongiorno G. Bai Z. Creamer R.E. De Deyn G. de Goede R. Fleskens L. Geissen V. Kuyper T.W. Mäder P. et al.Soil quality – A critical review.Soil Biol. Biochem. 2018; 120: 105-125Crossref Scopus (1012) Google Scholar, 14Wieder W.R. Allison S.D. Davidson E.A. Georgiou K. Hararuk O. He Y. Hopkins F. Luo Y. Smith M.J. Sulman B. et al.Explicitly representing soil microbial processes in Earth system models.Global Biogeochem. Cycles. 2015; 29: 1782-1800Crossref Scopus (199) Google Scholar]. Considering and integrating soil biodiversity into large-scale analyses and models will help us to better understand the importance of soil biodiversity at a global scale. Soil biodiversity is structured by physical and chemical soil properties, as well as by interactions with other soil and aboveground biota, including plants [7Bardgett R.D. van der Putten W.H. Belowground biodiversity and ecosystem functioning.Nature. 2014; 515: 505-511Crossref PubMed Scopus (1670) Google Scholar, 15Fierer N. Embracing the unknown: disentangling the complexities of the soil microbiome.Nat. Rev. Microbiol. 2017; 15: 579-590Crossref PubMed Scopus (1318) Google Scholar]. Soil type, pH, carbon and nutrient contents, and soil moisture predominantly determine the structure of soil biodiversity on local, regional, and global scales [16Delgado-Baquerizo M. Oliverio A.M. Brewer T.E. Benavent-González A. Eldridge D.J. Bardgett R.D. Maestre F.T. Singh B.K. Fierer N. A global atlas of the dominant bacteria found in soil.Science. 2018; 359: 320-325Crossref PubMed Scopus (925) Google Scholar, 17Tedersoo L. Bahram M. Põlme S. Kõljalg U. Yorou N.S. Wijesundera R. Ruiz L.V. Vasco-Palacios A.M. Thu P.Q. Suija A. et al.Global diversity and geography of soil fungi.Science. 2014; 346: 1256688Crossref PubMed Scopus (1929) Google Scholar, 18van den Hoogen J. Geisen S. Routh D. Ferris H. Traunspurger W. Wardle D.A. de Goede R.G.M. Adams B.J. Ahmad W. Andriuzzi W.S. et al.Soil nematode abundance and functional group composition at a global scale.Nature. 2019; 572: 194-198Crossref PubMed Scopus (420) Google Scholar]. However, plants also shape soil biodiversity, often in a plant species-specific manner [19Berg G. Smalla K. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere.FEMS Microbiol. Ecol. 2009; 68: 1-13Crossref PubMed Scopus (1471) Google Scholar], and trophic, competitive, facilitative, and other types of interactions between soil organisms further influence the structure of soil biodiversity as a whole [20Bahram M. Hildebrand F. Forslund S.K. Anderson J.L. Soudzilovskaia N.A. Bodegom P.M. Bengtsson-Palme J. Anslan S. Coelho L.P. Harend H. et al.Structure and function of the global topsoil microbiome.Nature. 2018; 560: 233-237Crossref PubMed Scopus (830) Google Scholar, 21Thakur M.P. Geisen S. Trophic regulations of the soil microbiome.Trends Microbiol. 2019; 27: 771-780Abstract Full Text Full Text PDF PubMed Scopus (139) Google Scholar]. The tight dependency of the soil biota on the surrounding abiotic and biotic environment makes it highly susceptible to anthropogenic changes [22de Vries F.T. Liiri M.E. Bjørnlund L. Bowker M.A. Christensen S. Setala H.M. Bardgett R.D. Land use alters the resistance and resilience of soil food webs to drought.Nat. Clim. Chang. 2012; 2: 276-280Crossref Scopus (377) Google Scholar, 23Griffiths B.S. Philippot L. Insights into the resistance and resilience of the soil microbial community.FEMS Microbiol. Rev. 2013; 37: 112-129Crossref PubMed Scopus (623) Google Scholar]. These changes are linked to the rapid growth of the human population and an increasing proportion of the land surface is sealed to expand cities and other infrastructure: every year in the European Union alone an amount of open soil with a surface as large as the city of Berlin is sealed [24Scalenghe R. Marsan F.A. The anthropogenic sealing of soils in urban areas. Landsc.Urban Plan. 2009; 90: 1-10Crossref Scopus (326) Google Scholar]. In addition, land is being taken for mining activities to support us with energy and for agriculture to produce food, feed, and bioenergy (Figure 2). For food production alone, about one billion hectares of land could be turned into agriculturally managed land by 2050 [25Tilman D. Balzer C. Hill J. Befort B.L. Global food demand and the sustainable intensification of agriculture.Proc. Natl. Acad. Sci. USA. 2011; 108: 20260Crossref PubMed Scopus (4161) Google Scholar]. Furthermore, agricultural practices are being intensified to support the growing human population [25Tilman D. Balzer C. Hill J. Befort B.L. Global food demand and the sustainable intensification of agriculture.Proc. Natl. Acad. Sci. USA. 2011; 108: 20260Crossref PubMed Scopus (4161) Google Scholar]. Intensified agriculture heavily depends on irrigation, the use of heavy machines and increased application of chemical fertilizers and pesticides. These practices cause habitat modifications that immediately change soil structure and physicochemical properties, which, together with changes in plant biodiversity, affect and commonly reduce soil biodiversity [26Wardle D.A. Bonner K.I. Barker G.M. Yeates G.W. Nicholson K.S. Bardgett R.D. Watson R.N. Ghani A. Plant removals in perennial grassland: Vegetation dynamics, decomposers, soil biodiversity, and ecosystem properties.Ecol. Monogr. 1999; 69: 535-568Crossref Scopus (409) Google Scholar, 27Gardi C. Jeffery S. Saltelli A. An estimate of potential threats levels to soil biodiversity in EU.Glob. Chang. Biol. 2013; 19: 1538-1548Crossref PubMed Scopus (62) Google Scholar, 28Tsiafouli M.A. Thébault E. Sgardelis S.P. de Ruiter P.C. van der Putten W.H. Birkhofer K. Hemerik L. de Vries F.T. Bardgett R.D. Brady M.V. et al.Intensive agriculture reduces soil biodiversity across Europe.Glob. Chang. Biol. 2015; 21: 973-985Crossref PubMed Scopus (498) Google Scholar]. As such, microbial communities are becoming bacteria-dominated, whereas earthworms are killed, and mycorrhizal fungi disrupted by soil tillage and other agricultural practices [29Chan K.Y. An overview of some tillage impacts on earthworm population abundance and diversity — implications for functioning in soils.Soil Till. Res. 2001; 57: 179-191Crossref Scopus (309) Google Scholar, 30Giller K.E. Beare M.H. Lavelle P. Izac A.M.N. Swift M.J. Agricultural intensification, soil biodiversity and agroecosystem function.Appl. Soil Ecol. 1997; 6: 3-16Crossref Scopus (454) Google Scholar, 31Song D. Pan K. Tariq A. Sun F. Li Z. Sun X. Zhang L. Olusanya O.A. Wu X. Large-scale patterns of distribution and diversity of terrestrial nematodes.Appl. Soil Ecol. 2017; 114: 161-169Crossref Scopus (63) Google Scholar]. Land-use intensification of agricultural soil, pesticide use, such as neonicotinoids, and herbicides like glyphosate, which can remain in soils for years and impact non-target organisms, all may affect soil biodiversity [32Bünemann E.K. Schwenke G.D. Van Zwieten L. Impact of agricultural inputs on soil organisms – a review.Soil Res. 2006; 44: 379-406Crossref Scopus (317) Google Scholar]. Common non-target effects are evident for neonicotinoids, as they are assumed to be causative agents of aboveground insect declines, but also can kill soil invertebrates including insects and earthworms [33Goulson D. An overview of the environmental risks posed by neonicotinoid insecticides.J. Appl. Ecol. 2013; 50: 977-987Crossref Scopus (1084) Google Scholar, 34Pisa L.W. Amaral-Rogers V. Belzunces L.P. Bonmatin J.M. Downs C.A. Goulson D. Kreutzweiser D.P. Krupke C. Liess M. McField M. et al.Effects of neonicotinoids and fipronil on non-target invertebrates.Environ. Sci. Pollut. 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Land use alters the resistance and resilience of soil food webs to drought.Nat. Clim. Chang. 2012; 2: 276-280Crossref Scopus (377) Google Scholar, 36Thakur M.P. Del Real I.M. Cesarz S. Steinauer K. Reich P.B. Hobbie S. Ciobanu M. Rich R. Worm K. Eisenhauer N. Soil microbial, nematode, and enzymatic responses to elevated CO2, N fertilization, warming, and reduced precipitation.Soil Biol. Biochem. 2019; 135: 184-193Crossref Scopus (51) Google Scholar, 37Eisenhauer N. Cesarz S. Koller R. Worm K. Reich P.B. Global change belowground: impacts of elevated CO2, nitrogen, and summer drought on soil food webs and biodiversity.Glob. Chang. Biol. 2012; 18: 435-447Crossref Scopus (208) Google Scholar]. Extended periods of drought negatively impact most groups of soil life, for example by reducing the abundance and diversity of protists [38Geisen S. Bandow C. Römbke J. Bonkowski M. Soil water availability strongly alters the community composition of soil protists.Pedobiologia. 2014; 57: 205-213Crossref Scopus (95) Google Scholar] and larger soil animals [39Lindberg N. Engtsson J.B. Persson T. Effects of experimental irrigation and drought on the composition and diversity of soil fauna in a coniferous stand.J. Appl. Ecol. 2002; 39: 924-936Crossref Scopus (175) Google Scholar]. Heavy rain events are occurring increasingly. Although these events can promote the abundance and diversity of soil biota through increasing moisture levels [40Clarholm M. Protozoan grazing of bacteria in soil—impact and importance.Microb. Ecol. 1981; 7: 343-350Crossref PubMed Scopus (248) Google Scholar], the associated waterlogging and increased soil erosion serve to reduce soil biodiversity [38Geisen S. Bandow C. Römbke J. Bonkowski M. 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Govindarajan S. Ganesh O.K. Palaeotemperature trend for Precambrian life inferred from resurrected proteins.Nature. 2008; 451: 704Crossref PubMed Scopus (265) Google Scholar]. Certain phenomena belowground are comparable to those known for aboveground biota: for example, larger soil organisms face higher extinction risks over shorter periods of time and at local scales than smaller bodied organisms [52Veresoglou S.D. Halley J.M. Rillig M.C. Extinction risk of soil biota.Nat. Commun. 2015; 6: 8862Crossref PubMed Scopus (117) Google Scholar]. Likewise, larger organisms (for example, top predators and earthworms) are impacted more strongly by changes in the soil environment than smaller-sized microbial taxa [53Kladivko E.J. Tillage systems and soil ecology.Soil Till. Res. 2001; 61: 61-76Crossref Scopus (477) Google Scholar]. The negative effects on these ecosystem engineers and controllers of entire food web structures may cause feedback loops that affect the entire soil biota and, consequently, soil functioning. For example, a loss of soil biodiversity may lead to a reduction of soil multifunctionality [8Wagg C. Bender S.F. Widmer F. van der Heijden M.G.A. Soil biodiversity and soil community composition determine ecosystem multifunctionality.Proc. Natl. Acad. Sci. USA. 2014; 111: 5266-5270Crossref PubMed Scopus (1134) Google Scholar]. One of the most obvious examples of biodiversity loss leading to reduced soil functioning is the reduction of earthworms through intensive agriculture that results in reduced water infiltration, thereby enhancing the risk of increased water erosion [28Tsiafouli M.A. Thébault E. Sgardelis S.P. de Ruiter P.C. van der Putten W.H. Birkhofer K. Hemerik L. de Vries F.T. Bardgett R.D. Brady M.V. et al.Intensive agriculture reduces soil biodiversity across Europe.Glob. Chang. Biol. 2015; 21: 973-985Crossref PubMed Scopus (498) Google Scholar, 29Chan K.Y. An overview of some tillage impacts on earthworm population abundance and diversity — implications for functioning in soils.Soil Till. Res. 2001; 57: 179-191Crossref Scopus (309) Google Scholar]. However, it should be noted that the factor causing soil biodiversity loss also has a direct impact on soil functioning. In practice, these causes and consequences of soil biodiversity loss are so far difficult to translate to changes in soil and ecosystem functioning. Newly emerging threats to soil biodiversity constantly appear (see also Box 1). Among those are diverse pharmaceuticals that spread into the environment, eventually being taken up and concentrated in soil organisms [54Kinney C.A. Furlong E.T. Kolpin D.W. Burkhardt M.R. Zaugg S.D. Werner S.L. Bossio J.P. Benotti M.J. 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• W2977791744 created "2019-10-10" @default.
• W2977791744 creator A5040233192 @default.
• W2977791744 creator A5040240993 @default.
• W2977791744 creator A5043104764 @default.
• W2977791744 date "2019-10-01" @default.
• W2977791744 modified "2023-10-14" @default.
• W2977791744 title "Challenges and Opportunities for Soil Biodiversity in the Anthropocene" @default.
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