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Ecological Importance of Soil Bacterivores for Ecosystem Functions Jean Trap, Michael Bonkowski, Claude Plassard, Cécile Villenave, Eric Blanchart

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Ecological Importance of Soil Bacterivores for Ecosystem Functions Jean Trap, Michael Bonkowski, Claude Plassard, Cécile Villenave, Eric Blanchart Ecological importance of soil bacterivores for ecosystem functions Jean Trap, Michael Bonkowski, Claude Plassard, Cécile Villenave, Eric Blanchart To cite this version: Jean Trap, Michael Bonkowski, Claude Plassard, Cécile Villenave, Eric Blanchart. Ecological impor- tance of soil bacterivores for ecosystem functions. Plant and Soil, Springer Verlag, 2015, 398 (1-2), pp.1-24. 10.1007/s11104-015-2671-6. hal-01214705 HAL Id: hal-01214705 https://hal.archives-ouvertes.fr/hal-01214705 Submitted on 12 Oct 2015 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Manuscript Click here to download Manuscript: manuscrit.doc Click here to view linked References 1 Number of words (main text): 8583 2 Number of words (abstract): 157 3 Number of figures: 7 4 Number of tables: 1 5 Number of appendix: 1 6 7 Title 8 Ecological importance of soil bacterivores on ecosystem functions 9 10 Authors 11 Jean Trap1, Michael Bonkowski2, Claude Plassard3, Cécile Villenave4, Eric Blanchart1 12 13 Affiliations 14 15 1Institut de Recherche pour le Développement – UMR Eco&Sols, 2 Place Viala, 34060, Version postprint 16 Montpellier, France 17 2Dept. of Terrestrial Ecology, Institut of Zoology, University of Cologne, D-50674 Köln, 18 Germany 19 3Institut National de Recherche Agronomique – UMR Eco&Sols, 2 Place Viala, 34060, 20 Montpellier, France 21 4ELISOL environnement, 10 avenue du Midi, 30111 Congenies, France 22 23 1 Comment citer ce document : Trap, J., Bonkowski, M., Plassard, C., Villenave, C., Blanchart, E. (2015). Ecological importance of soil bacterivores for ecosystem functions. Plant and Soil, 1-24. DOI : 10.1007/s11104-015-2671-6 24 Abstract 25 Background 26 Bacterivores, mostly represented by protists and nematodes, are a key component of soil 27 biodiversity involved in soil fertility and plant productivity. In the current context of global 28 change and soil biodiversity erosion, it becomes urgent to suitably recognize and quantify 29 their ecological importance in the maintenance of ecosystem functions. 30 Scope 31 Using meta-analysis tools, we aimed at providing a quantitative synthesis of the ecological 32 importance of soil bacterivores on ecosystem functions. We also intended to produce an 33 overview of the ecological factors that are expected to drive the magnitude of bacterivore 34 effects on ecosystem functions. 35 Conclusions Version postprint 36 Bacterivores in soil contributed significantly to numerous key ecosystem functions. We 37 propose a new theoretical framework based on ecological stoichiometry stressing the role of 38 C:N:P ratios in soil, microbial and plant biomass as important parameters driving bacterivore- 39 effects on soil N and P availability for plants, immobilization of N and P in the bacterial 40 biomass, and plant responses in nutrition and growth. 41 42 Keywords 43 Bacterivores; Protists, Nematodes; Microbial loop; Plant growth; Plant nutrition ; Ecological 44 stoichiometry; Meta-analysis 45 2 Comment citer ce document : Trap, J., Bonkowski, M., Plassard, C., Villenave, C., Blanchart, E. (2015). Ecological importance of soil bacterivores for ecosystem functions. Plant and Soil, 1-24. DOI : 10.1007/s11104-015-2671-6 46 1. Introduction 47 48 Soils are some of the most biologically diverse environments, encompassing about 25% of 49 global biodiversity in terms of species (Coleman and Wall 2015; Decaëns 2010). One gram of 50 soil can host 6000 different bacterial genomes, several hundred meters of fungal hyphae and a 51 wide range of protists, nematodes, enchytraeids or mites (Jones et al. 2009; Lavelle and Spain 52 2001; Wall et al. 2010). Through their activities, soil organisms ensure key soil functions 53 (Barrios 2007; Brussaard et al. 2007; Wagg et al. 2014) and contribute to many ecosystem 54 services (de Vries et al. 2013; Kibblewhite et al. 2008). 55 Unfortunately, soils are also among the most threatened environments in terms of biodiversity 56 loss (Kibblewhite 2012). Many pressures (soil erosion, land use change, overexploitation, 57 pollution, biological invasion, etc.) have been identified as directly disturbing soil organism 58 abundance, distribution and activity (Bossio et al. 2005; Dupouey et al. 2002; Foley et al. 59 2005; Gardi et al. 2013; Pimentel 2006; Schlaghamersky et al. 2014). A thorough 60 understanding of the many roles of soil biodiversity is required in order to predict how these Version postprint 61 threats could damage ecosystem services accomplished by soil organisms. 62 A key component of soil biodiversity involved in soil fertility and plant productivity are 63 bacterivores (Bardgett et al. 1999; Bonkowski 2004; Bonkowski et al. 2009; Brussaard 1997). 64 These bacterivores are mostly represented by protists and nematodes (Ronn et al. 2012). 65 Bacterivorous soil protists are generally unicellular heterotrophic eukaryotes, that were 66 traditionally grouped into ciliates, flagellates, naked amoebae and testate amoebae 67 (Darbyshire 1994). However, molecular studies reveal an enormous taxonomic diversity in 68 soils (Geisen et al. 2014; Geisen et al. 2015), and only the ciliated protists are monophyletic, 69 while flagellated, and naked, and testate amoeboid morphotypes repeatedly originated during 70 protist evolution (Adl et al. 2005; Adl et al. 2012). 3 Comment citer ce document : Trap, J., Bonkowski, M., Plassard, C., Villenave, C., Blanchart, E. (2015). Ecological importance of soil bacterivores for ecosystem functions. Plant and Soil, 1-24. DOI : 10.1007/s11104-015-2671-6 71 Despite their small size (average size 2-50 µm), protists can largely contribute to total soil 72 faunal biomass (Bonkowski 2004). Nematodes are small multicellular eukaryotes (0.03-1 mm 73 size range) and form a highly diverse monophyletic group including about one million of 74 species (Lambshead 1993), making this phylum one of the most diverse animal taxa on Earth 75 (Lambshead et al. 2004). Both bacterial-feeding protists and nematodes are widely distributed 76 in terrestrial ecosystems and successful colonizers of soil niches (Cowling 1994; Geisen et al. 77 2014). It has been estimated than tens of millions of protists and hundreds of thousands of 78 nematode individuals co-exist in only one forest square meter (Cowling 1994; Foissner 1999; 79 Yeates 2007; Yeates 2003). Still, they remain poorly studied in comparison to other soil taxa 80 (Coleman and Wall 2015; Couteaux and Darbyshire 1998). Only a fraction of protist and 81 nematode species have been described yet, and their biology and ecology remain poorly 82 known (Brussaard et al. 2007). It thus becomes urgent, in the current context of global change 83 that is expected to alter soil bacterivore communities, to suitably recognize the species and to 84 quantify their ecological importance in the maintenance of ecosystems. 85 Here, as a complement to detailed reviews published in the past (Bonkowski 2004; Version postprint 86 Bonkowski and Clarholm 2012; Bonkowski et al. 2009; Chen et al. 2007), we aimed at 87 providing a quantitative synthesis of the ecological importance of bacterivores in soil on 88 ecosystem functions using meta-analysis tools. We also intended to produce an overview of 89 the ecological (biotic and abiotic) factors that are expected to drive the magnitude of their 90 effects on ecosystem functions. 91 92 2. Meta-analysis - Data sources, extraction and analysis 93 94 We investigated the literature published in peer-reviewed journals before December 2014 95 through computer searches in available databases (Google Scholar and ISI Web of 4 Comment citer ce document : Trap, J., Bonkowski, M., Plassard, C., Villenave, C., Blanchart, E. (2015). Ecological importance of soil bacterivores for ecosystem functions. Plant and Soil, 1-24. DOI : 10.1007/s11104-015-2671-6 96 Knowledge), with no restriction on the year of publication, that investigate bacterivore- 97 induced effects. We used the following key-words (alone or in combination): soil, 98 biodiversity, bacteria, bacterivore, bacterial-feeders/grazers, protozoa, protists, nematodes, 99 predators, mycorrhiza, earthworms, nodules, nutrient, nitrogen, phosphorus, microbial loop. 100 We also searched studies in the reference lists of relevant articles and reviews. We selected 101 studies that (i) tested the effects of bacterivores on ecosystem functions by successfully 102 manipulating soil bacterivores in controlled experimental conditions, (ii) measured at least 103 one function of interest, and (iii) reported means of treatment and control. We excluded field 104 studies that monitored soil bacterivore population changes after perturbation or during 105 seasonal cycles, or eliminated soil bacterivores by adding biocides in the soil, freezing or 106 sieving the soil without measuring the success of the elimination. We also excluded studies 107 comparing low versus high soil bacterivore densities and modelling studies. 108 We analyzed the effects of bacterivores on 18 microbial and plant functions: soil microbial 109 biomass (measured by fumigation or substrate-induced respiration), soil
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