Soil fauna diversity increases CO2 but suppresses N2O emissions from soil

Soil faunal activity can be a major control of greenhouse gas (GHG) emissions from soil. Effects of single faunal species, genera or families have been investigated, but it is unknown how soil fauna diversity may influence emissions of both carbon dioxide (CO2, end product of decomposition of organic matter) and nitrous oxide (N2O, an intermediate product of N transformation processes, in particular denitrification). Here, we studied how CO2 and N2O emissions are affected by species and species mixtures of up to eight species of detritivorous/fungivorous soil fauna from four different taxonomic groups (earthworms, potworms, mites, springtails) using a microcosm set‐up. We found that higher species richness and increased functional dissimilarity of species mixtures led to increased faunal‐induced CO2 emission (up to 10%), but decreased N2O emission (up to 62%). Large ecosystem engineers such as earthworms were key drivers of both CO2 and N2O emissions. Interestingly, increased biodiversity of other soil fauna in the presence of earthworms decreased faunal‐induced N2O emission despite enhanced C cycling. We conclude that higher soil fauna functional diversity enhanced the intensity of belowground processes, leading to more complete litter decomposition and increased CO2 emission, but concurrently also resulting in more complete denitrification and reduced N2O emission. Our results suggest that increased soil fauna species diversity has the potential to mitigate emissions of N2O from soil ecosystems. Given the loss of soil biodiversity in managed soils, our findings call for adoption of management practices that enhance soil biodiversity and stimulate a functionally diverse faunal community to reduce N2O emissions from managed soils.

[1]  S. Tresch,et al.  Litter decomposition driven by soil fauna, plant diversity and soil management in urban gardens. , 2019, The Science of the total environment.

[2]  G. Velthof,et al.  The role of nitrifier denitrification in the production of nitrous oxide revisited , 2018, Soil Biology and Biochemistry.

[3]  M. Dodd,et al.  Influence of earthworm abundance and diversity on soil structure and the implications for soil services throughout the season , 2017 .

[4]  I. Bertrand,et al.  Can changes in litter quality drive soil fauna structure and functions , 2017 .

[5]  Bart R. Johnson,et al.  Quantifying global soil carbon losses in response to warming , 2016, Nature.

[6]  S. Schrader,et al.  Influence of Lumbricus terrestris and Folsomia candida on N2 O formation pathways in two different soils - with particular focus on N2 emissions. , 2016, Rapid communications in mass spectrometry : RCM.

[7]  W. Wieder,et al.  Beyond microbes: Are fauna the next frontier in soil biogeochemical models? , 2016 .

[8]  M. Loreau,et al.  Soil fauna: key to new carbon models , 2016 .

[9]  P. Kardol,et al.  A hierarchical framework for studying the role of biodiversity in soil food web processes and ecosystem services , 2016 .

[10]  M. V. D. van der Heijden,et al.  An Underground Revolution: Biodiversity and Soil Ecological Engineering for Agricultural Sustainability. , 2016, Trends in ecology & evolution.

[11]  J. W. Groenigen,et al.  Exploring the relationship between soil mesofauna, soil structure and N2O emissions , 2016 .

[12]  S. Ogle,et al.  Climate-smart soils , 2016, Nature.

[13]  Pete Smith Soil carbon sequestration and biochar as negative emission technologies , 2016, Global change biology.

[14]  J. Roy,et al.  Functional dissimilarity across trophic levels as a driver of soil processes in a Mediterranean decomposer system exposed to two moisture levels , 2015 .

[15]  L. Brussaard,et al.  Reduced greenhouse gas mitigation potential of no-tillage soils through earthworm activity , 2015, Scientific Reports.

[16]  Haitao Wu,et al.  Interactions between earthworms and mesofauna has no significant effect on emissions of CO2 and N2O from soil , 2015 .

[17]  Petr Baldrian,et al.  Biotic interactions mediate soil microbial feedbacks to climate change , 2015, Proceedings of the National Academy of Sciences.

[18]  E. Blagodatskaya,et al.  Microbial hotspots and hot moments in soil: Concept & review , 2015 .

[19]  M. Scheffer,et al.  Causal feedbacks in climate change , 2015 .

[20]  J. Frouz,et al.  Intensive agriculture reduces soil biodiversity across Europe , 2015, Global change biology.

[21]  Richard D. Bardgett,et al.  Belowground biodiversity and ecosystem functioning , 2014, Nature.

[22]  G. Brown,et al.  Earthworms increase plant production: a meta-analysis , 2014, Scientific Reports.

[23]  K. Cassman,et al.  Limited potential of no-till agriculture for climate change mitigation , 2014 .

[24]  A. Brauman,et al.  Contribution of white grubs (Scarabaeidae: Coleoptera) to N2O emissions from tropical soils , 2014 .

[25]  R. Aerts,et al.  Consequences of biodiversity loss for litter decomposition across biomes , 2014, Nature.

[26]  J. W. Groenigen,et al.  Interactions between microbial-feeding and predatory soil fauna trigger N2O emissions , 2014 .

[27]  F. Bello,et al.  Disentangling community functional components in a litter-macrodetritivore model system reveals the predominance of the mass ratio hypothesis , 2014, Ecology and evolution.

[28]  J. Cortet,et al.  The impact of agricultural practices on soil biota: A regional study , 2013 .

[29]  Madhav P. Thakur,et al.  Soil invertebrate fauna affect N2O emissions from soil , 2013, Global change biology.

[30]  J. Frouz,et al.  Soil food web properties explain ecosystem services across European land use systems , 2013, Proceedings of the National Academy of Sciences.

[31]  J. W. Groenigen,et al.  Earthworms can increase nitrous oxide emissions from managed grassland: a field study , 2013 .

[32]  J. Six,et al.  Greenhouse-gas emissions from soils increased by earthworms , 2013 .

[33]  F. Bello,et al.  An experimental framework to identify community functional components driving ecosystem processes and services delivery , 2013 .

[34]  O. Oenema,et al.  A Novel Method for Quantifying Nitrous Oxide Reduction in Soil , 2012 .

[35]  D. Six,et al.  Soil Ecology and Ecosystem Services , 2012 .

[36]  L. Brussaard,et al.  Agricultural intensification and de-intensification differentially affect taxonomic diversity of predatory mites, earthworms, enchytraeids, nematodes and bacteria , 2012 .

[37]  Chris D. Evans,et al.  Methane emissions from soils: synthesis and analysis of a large UK data set , 2012 .

[38]  Pete Smith,et al.  Soil physics meets soil biology: Towards better mechanistic prediction of greenhouse gas emissions from soil , 2012 .

[39]  J. V. van Groenigen,et al.  Association of Earthworm-Denitrifier Interactions with Increased Emission of Nitrous Oxide from Soil Mesocosms Amended with Crop Residue , 2011, Applied and Environmental Microbiology.

[40]  Y. Capowiez,et al.  Using X-ray tomography to quantify earthworm bioturbation non-destructively in repacked soil cores , 2011 .

[41]  L. Brussaard,et al.  Earthworm‐induced N mineralization in fertilized grassland increases both N2O emission and crop‐N uptake , 2011 .

[42]  D. Powlson,et al.  Soil carbon sequestration to mitigate climate change: a critical re‐examination to identify the true and the false , 2011 .

[43]  D. Wall,et al.  Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity–function relationships , 2011 .

[44]  R. Gutiérrez,et al.  A holistic view of nitrogen acquisition in plants. , 2011, Journal of experimental botany.

[45]  N. Kaneko,et al.  Influence of Collembola on nitrogen mineralization varies with soil moisture content , 2011 .

[46]  W. Landman Climate change 2007: the physical science basis , 2010 .

[47]  N. Ostrom,et al.  Evidence for the predominance of denitrification as a source of N2O in temperate agricultural soils based on isotopologue measurements , 2009 .

[48]  Davey L. Jones,et al.  Carbon flow in the rhizosphere: carbon trading at the soil–root interface , 2009, Plant and Soil.

[49]  W. Parton,et al.  Global decomposition experiment shows soil animal impacts on decomposition are climate-dependent , 2008, Global Change Biology.

[50]  R. Dalal,et al.  TURNER REVIEW No. 18. Greenhouse gas fluxes from natural ecosystems , 2008 .

[51]  Li Huixin,et al.  Influence of nematodes and earthworms on the emissions of soil trace gases (CO2, N2O) , 2008 .

[52]  Bradley J. Cardinale,et al.  Effects of biodiversity on the functioning of trophic groups and ecosystems , 2006, Nature.

[53]  J. W. Groenigen,et al.  Earthworm species composition affects the soil bacterial community and net nitrogen mineralization , 2006 .

[54]  H. Drake,et al.  Earthworms as a Transient Heaven for Terrestrial Denitrifying Microbes: a Review , 2006 .

[55]  M. Loreau,et al.  Biodiversity Effects on Soil Processes Explained by Interspecific Functional Dissimilarity , 2004, Science.

[56]  R. Lal,et al.  Soil Carbon Sequestration Impacts on Global Climate Change and Food Security , 2004, Science.

[57]  D. Coleman,et al.  Effects of enchytraeids (Annelida: Oligochaeta) on soil carbon and nitrogen dynamics in laboratory incubations , 2004 .

[58]  P. D. Ruiter,et al.  C and N mineralisation in the decomposer food webs of a European forest transect , 2003 .

[59]  Oene Oenema,et al.  Nitrous oxide emission from soils amended with crop residues , 2002, Nutrient Cycling in Agroecosystems.

[60]  T. Chevallier Standard soil methods for long-term ecological research , 2001 .

[61]  Michel Loreau,et al.  Partitioning selection and complementarity in biodiversity experiments , 2001, Nature.

[62]  E. Temminghoff,et al.  Soil analysis procedures using 0.01 M calcium chloride as extraction reagent , 2000 .

[63]  A. Kinzig,et al.  Original Articles: Plant Attribute Diversity, Resilience, and Ecosystem Function: The Nature and Significance of Dominant and Minor Species , 1999, Ecosystems.

[64]  J. P. Grime,et al.  Benefits of plant diversity to ecosystems: immediate, filter and founder effects , 1998 .

[65]  Keith Paustian,et al.  CO2 Mitigation by Agriculture: An Overview , 1998 .

[66]  P. Dalby,et al.  "Filter paper method" to remove soil from earthworm intestines and to standardise the water content of earthworm tissue , 1996 .

[67]  H. W. Hunt,et al.  Calculation of nitrogen mineralization in soil food webs , 1993, Plant and Soil.

[68]  H. Petersen,et al.  A comparative analysis of soil fauna populations and their role in decomposition processes , 1982 .

[69]  M. Ha-Duong,et al.  Climate change 2014 - Mitigation of climate change , 2015 .

[70]  Rattan Lal,et al.  The knowns, known unknowns and unknowns of sequestration of soil organic carbon , 2013 .

[71]  J. Whalen,et al.  Nitrous oxide production and potential denitrification in soils from riparian buffer strips: Influence of earthworms and plant litter , 2011 .

[72]  H. Setälä,et al.  Relationship between soil microarthropod species diversity and plant growth does not change when the system is disturbed , 2002 .

[73]  H. Pathak,et al.  Emission of carbon dioxide from soil , 2002 .

[74]  P. Roger,et al.  Production, oxidation, emission and consumption of methane by soils: A review , 2001 .

[75]  G. Robertson,et al.  Standard soil methods for long-term ecological research , 1999 .

[76]  T. Granli,et al.  Nitrous oxide from agriculture , 1994 .

[77]  P. D. Ruiter,et al.  Simulation of nitrogen mineralization in the belowground food webs of two winter wheat fields. , 1993 .

[78]  K. E. Lee,et al.  Soil fauna and soil structure , 1991 .

[79]  P. Brookes,et al.  Chloroform fumigation and the release of soil nitrogen: A rapid direct extraction method to measure microbial biomass nitrogen in soil , 1985 .