Section: Ecology
Topic: Ecology, Biology of interactions

The contrasted impacts of grasshoppers on soil microbial activities in function of primary production and herbivore diet

Ibanez, Sébastien1  ; Foulquier, Arnaud1 ; Brun, Charles1, 2; Colace, Marie-Pascale1; Piton, Gabin1 ; Bernard, Lionel1 ; Gallet, Christiane1; Clément, Jean-Christophe1, 3 
1 Univ. Grenoble Alpes, Univ. Savoie Mont Blanc, CNRS UMR 5553, LECA, Chambéry, France
2 University of Applied Sciences and Arts Western Switzerland – Land, Nature, Environment Institute, Hepia Geneva, Route de Presinge 150, CH-1254, Jussy, Switzerland
3 Univ. Savoie Mont Blanc, INRAE, CARRTEL, Thonon-Les-Bains, France

10.24072/pcjournal.229 - Peer Community Journal, Volume 3 (2023), article no. e12.

Get full text PDF Peer reviewed and recommended by PCI
article image

Herbivory can have contrasted impacts on soil microbes and nutrient cycling, which has stimulated the development of conceptual frameworks exploring the links between below- and aboveground processes. The “productivity model” predicts that herbivores stimulate microbial activities and accelerate nutrient mineralization in productive ecosystems, while they have an opposite effect in less productive ecosystems. In parallel, the “diet model” predicts that herbivores feeding on conservative plants accelerate nutrient cycling while those feeding on exploitative plants decelerate nutrient cycling, due to changes in litter inputs. Since these two frameworks can lead to conflicting predictions in some cases, experimental evidence combining herbivore diet and plant productivity is required. During two consecutive years, we conducted an experiment controlling the presence of three grasshopper species consuming either grasses, forbs or both in twelve natural and managed alpine grasslands with contrasted productivities. In order to assess the effects of herbivory on soil microbes, we measured their extracellular enzymatic activities, biomass and potential nitrogen mineralization (PNM). Soil and vegetation were also characterized to test how much they modulated the effects of herbivory on microbes. Contrary to the predictions of the diet model, the effects of herbivory on microbial characteristics did not depend on the herbivores diet, but were influenced by primary production, though in a way that differed from the productivity model. The most productive sites were constituted by exploitative plant species which depleted N resources in the soil, and by microbes producing relatively few extracellular enzymes, leading to a lower PNM. Herbivory increased microbial biomass and decreased the production of extracellular enzymes in those sites, possibly through the stimulation of root exudates produced by exploitative species. The least productive sites were characterized by conservative plants, high soil C content, and by microbes having a resource acquisition strategy (more extracellular enzymes, higher PNM). Herbivory decreased microbial biomass and increased the production of extracellular enzymes in those sites. This pattern can be explained by the loss of carbon associated with insect respiration, which increases the resource requirements of microbes and by a lower production of root exudates by conservative species. Therefore, the effects of two years of herbivory on soil microbes were at odds with the productivity model, which focuses instead on longer term effects corresponding to herbivory-induced changes in plant species composition. This highlights the multidimensional feature of the impacts of herbivory on ecosystem functioning, both in space and time.

Published online:
DOI: 10.24072/pcjournal.229
Type: Research article

Ibanez, Sébastien 1; Foulquier, Arnaud 1; Brun, Charles 1, 2; Colace, Marie-Pascale 1; Piton, Gabin 1; Bernard, Lionel 1; Gallet, Christiane 1; Clément, Jean-Christophe 1, 3

1 Univ. Grenoble Alpes, Univ. Savoie Mont Blanc, CNRS UMR 5553, LECA, Chambéry, France
2 University of Applied Sciences and Arts Western Switzerland – Land, Nature, Environment Institute, Hepia Geneva, Route de Presinge 150, CH-1254, Jussy, Switzerland
3 Univ. Savoie Mont Blanc, INRAE, CARRTEL, Thonon-Les-Bains, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
@article{10_24072_pcjournal_229,
     author = {Ibanez, S\'ebastien and Foulquier, Arnaud and Brun, Charles and Colace, Marie-Pascale and Piton, Gabin and Bernard, Lionel and Gallet, Christiane and Cl\'ement, Jean-Christophe},
     title = {The contrasted impacts of grasshoppers on soil microbial activities in function of primary production and herbivore diet},
     journal = {Peer Community Journal},
     eid = {e12},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.229},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.229/}
}
TY  - JOUR
AU  - Ibanez, Sébastien
AU  - Foulquier, Arnaud
AU  - Brun, Charles
AU  - Colace, Marie-Pascale
AU  - Piton, Gabin
AU  - Bernard, Lionel
AU  - Gallet, Christiane
AU  - Clément, Jean-Christophe
TI  - The contrasted impacts of grasshoppers on soil microbial activities in function of primary production and herbivore diet
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.229/
DO  - 10.24072/pcjournal.229
ID  - 10_24072_pcjournal_229
ER  - 
%0 Journal Article
%A Ibanez, Sébastien
%A Foulquier, Arnaud
%A Brun, Charles
%A Colace, Marie-Pascale
%A Piton, Gabin
%A Bernard, Lionel
%A Gallet, Christiane
%A Clément, Jean-Christophe
%T The contrasted impacts of grasshoppers on soil microbial activities in function of primary production and herbivore diet
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.229/
%R 10.24072/pcjournal.229
%F 10_24072_pcjournal_229
Ibanez, Sébastien; Foulquier, Arnaud; Brun, Charles; Colace, Marie-Pascale; Piton, Gabin; Bernard, Lionel; Gallet, Christiane; Clément, Jean-Christophe. The contrasted impacts of grasshoppers on soil microbial activities in function of primary production and herbivore diet. Peer Community Journal, Volume 3 (2023), article  no. e12. doi : 10.24072/pcjournal.229. https://peercommunityjournal.org/articles/10.24072/pcjournal.229/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.ecology.100105

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Agrawal, A. A. Induced responses to herbivory in wild radish: effects on several herbivores and plant fitness, Ecology, Volume 80 (1999) no. 5, pp. 1713-1723 | DOI

[2] Bakker, E. S.; Olff, H.; Boekhoff, M.; Gleichman, J. M.; Berendse, F. Impact of herbivores on nitrogen cycling: contrasting effects of small and large species, Oecologia, Volume 138 (2004) no. 1, pp. 91-101 | DOI

[3] Bardgett, R. The biology of soil: a community and ecosystem approach, Oxford university press, 2005

[4] Bardgett, R.; Wardle, D. Aboveground-belowground linkages: biotic interactions, ecosystem processes, and global change , Oxford University Press, Oxford, 2010

[5] Bardgett, R. D.; Wardle, D. A. Herbivore-mediated linkages between aboveground and belowground communities, Ecology, Volume 84 (2003) no. 9, pp. 2258-2268 | DOI

[6] Bell, C. W.; Fricks, B. E.; Rocca, J. D.; Steinweg, J. M.; McMahon, S. K.; Wallenstein, M. D. High-throughput Fluorometric Measurement of Potential Soil Extracellular Enzyme Activities, Journal of Visualized Experiments (2013) no. 81 | DOI

[7] Belovsky, G. E.; Slade, J. B. Insect herbivory accelerates nutrient cycling and increases plant production, Proceedings of the National Academy of Sciences, Volume 97 (2000) no. 26, pp. 14412-14417 | DOI

[8] Belovsky, G. E.; Slade, J. B. Grasshoppers affect grassland ecosystem functioning: Spatial and temporal variation, Basic and Applied Ecology, Volume 26 (2018), pp. 24-34 | DOI

[9] Borcard, D.; Legendre, P.; Drapeau, P. Partialling out the Spatial Component of Ecological Variation, Ecology, Volume 73 (1992) no. 3, pp. 1045-1055 | DOI

[10] Brown, V. K.; Gange, A. C. Secondary plant succession: how is it modified by insect herbivory?, Vegetatio, Volume 101 (1992) no. 1, pp. 3-13 | DOI

[11] Buckland, S. M.; Grime, J. P. The effects of trophic structure and soil fertility on the assembly of plant communities: a microcosm experiment, Oikos, Volume 91 (2000) no. 2, pp. 336-352 | DOI

[12] Calderón-Sanou, I.; Münkemüller, T.; Zinger, L.; Schimann, H.; Yoccoz, N. G.; Gielly, L.; Foulquier, A.; Hedde, M.; Ohlmann, M.; Roy, M.; Si-Moussi, S.; Thuiller, W. Cascading effects of moth outbreaks on subarctic soil food webs, Scientific Reports, Volume 11 (2021) no. 1 | DOI

[13] Cease, A. J.; Elser, J. J.; Ford, C. F.; Hao, S.; Kang, L.; Harrison, J. F. Heavy Livestock Grazing Promotes Locust Outbreaks by Lowering Plant Nitrogen Content, Science, Volume 335 (2012) no. 6067, pp. 467-469 | DOI

[14] Chu, H.; Grogan, P. Soil microbial biomass, nutrient availability and nitrogen mineralization potential among vegetation-types in a low arctic tundra landscape, Plant and Soil, Volume 329 (2009) no. 1-2, pp. 411-420 | DOI

[15] Clauss, M.; Lechner-Doll, M.; Streich, W. J. Ruminant diversification as an adaptation to the physicomechanical characteristics of forage, Oikos, Volume 102 (2003) no. 2, pp. 253-262 | DOI

[16] Denton, C. S.; Bardgett, R. D.; Cook, R.; Hobbs, P. J. Low amounts of root herbivory positively influence the rhizosphere microbial community in a temperate grassland soil, Soil Biology and Biochemistry, Volume 31 (1998) no. 1, pp. 155-165 | DOI

[17] Deraison, H.; Badenhausser, I.; Loeuille, N.; Scherber, C.; Gross, N. Functional trait diversity across trophic levels determines herbivore impact on plant community biomass, Ecology Letters, Volume 18 (2015) no. 12, pp. 1346-1355 | DOI

[18] Dray, S.; Chessel, D.; Thioulouse, J. Co-inertia analysis and the linking of ecological data tables, Ecology, Volume 84 (2003) no. 11, pp. 3078-3089 | DOI

[19] Dray, S.; Dufour, A.-B. The ade4 Package: Implementing the Duality Diagram for Ecologists, Journal of Statistical Software, Volume 22 (2007) no. 4 | DOI

[20] Farrell, M.; Hill, P. W.; Farrar, J.; Bardgett, R. D.; Jones, D. L. Seasonal variation in soluble soil carbon and nitrogen across a grassland productivity gradient, Soil Biology and Biochemistry, Volume 43 (2011) no. 4, pp. 835-844 | DOI

[21] Fielding, D. J.; Trainor, E.; Zhang, M. Diet influences rates of carbon and nitrogen mineralization from decomposing grasshopper frass and cadavers, Biology and Fertility of Soils, Volume 49 (2012) no. 5, pp. 537-544 | DOI

[22] Findlay, S.; Carreiro, M.; Krischik, V.; Jones, C. G. Effects of Damage to Living Plants on Leaf Litter Quality, Ecological Applications, Volume 6 (1996) no. 1, pp. 269-275 | DOI

[23] Frank, D. A.; Groffman, P. M.; Evans, R. D.; Tracy, B. F. Ungulate stimulation of nitrogen cycling and retention in Yellowstone Park grasslands, Oecologia, Volume 123 (2000) no. 1, pp. 116-121 | DOI

[24] Garibaldi, L. A.; Semmartin, M.; Chaneton, E. J. Grazing-induced changes in plant composition affect litter quality and nutrient cycling in flooding Pampa grasslands, Oecologia, Volume 151 (2007) no. 4, pp. 650-662 | DOI

[25] Grigulis, K.; Lavorel, S.; Krainer, U.; Legay, N.; Baxendale, C.; Dumont, M.; Kastl, E.; Arnoldi, C.; Bardgett, R. D.; Poly, F.; Pommier, T.; Schloter, M.; Tappeiner, U.; Bahn, M.; Clément, J.-C. Relative contributions of plant traits and soil microbial properties to mountain grassland ecosystem services, Journal of Ecology, Volume 101 (2012) no. 1, pp. 47-57 | DOI

[26] Hamilton, E. W.; Frank, D. A. Can plants stimulate soil microbes and their own nutrient supply? Evidence from a grazing tolerant grass, Ecology, Volume 82 (2001), pp. 2397-2402 | DOI

[27] Hamilton, E. W.; Frank, D. A.; Hinchey, P. M.; Murray, T. R. Defoliation induces root exudation and triggers positive rhizospheric feedbacks in a temperate grassland, Soil Biology and Biochemistry, Volume 40 (2008) no. 11, pp. 2865-2873 | DOI

[28] Harrison, K. Browsing by red deer negatively impacts on soil nitrogen availability in regenerating native forest, Soil Biology and Biochemistry, Volume 36 (2004) no. 1, pp. 115-126 | DOI

[29] Hättenschwiler, S.; Vitousek, P. M. The role of polyphenols in terrestrial ecosystem nutrient cycling, Trends in Ecology & Evolution, Volume 15 (2000) no. 6, pp. 238-243 | DOI

[30] Hofmann, R. R. Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system, Oecologia, Volume 78 (1989) no. 4, pp. 443-457 | DOI

[31] Holland, J. N. Effects of above-ground herbivory on soil microbial biomass in conventional and no-tillage agroecosystems, Applied Soil Ecology, Volume 2 (1995) no. 4, pp. 275-279 | DOI

[32] Holland, J. N.; Cheng, W.; Crossley, D. A. Herbivore-induced changes in plant carbon allocation: assessment of below-ground C fluxes using carbon-14, Oecologia, Volume 107 (1996) no. 1, pp. 87-94 | DOI

[33] Hunter, M. D. Insect population dynamics meets ecosystem ecology: effects of herbivory on soil nutrient dynamics, Agricultural and Forest Entomology, Volume 3 (2001) no. 2, pp. 77-84 | DOI

[34] Hunter, M. D.; Reynolds, B. C.; Hall, M. C.; Frost, C. J. Effects of herbivores on terrestrial ecosystem processes, Trait-Mediated Indirect Interactions, Cambridge University Press, 2012, pp. 339-370 | DOI

[35] Ibanez, S. R script for: The contrasted impacts of grasshoppers on soil microbial activities in function of ecosystem productivity and herbivore diet, Zenodo, 2022 no. 6831330 | DOI

[36] Ibanez, S. Data collected for: The contrasted impacts of grasshoppers on soil microbial activities in function of ecosystem productivity and herbivore diet, Dryad, 2022 | DOI

[37] Ibanez, S.; Brun, C.; Millery, A.; Piton, G.; Bernard, L.; Avrillier, J.-N.; Gallet, C.; Foulquier, A.; Clément, J.-C. Litter and soil characteristics mediate the buffering effect of snow cover on litter decomposition, Plant and Soil, Volume 460 (2021) no. 1-2, pp. 511-525 | DOI

[38] Ibanez, S.; Lavorel, S.; Puijalon, S.; Moretti, M. Herbivory mediated by coupling between biomechanical traits of plants and grasshoppers, Functional Ecology, Volume 27 (2013) no. 2, pp. 479-489 | DOI

[39] Jenkinson, D. Measuring soil microbial biomass, Soil Biology and Biochemistry, Volume 36 (2004) no. 1, pp. 5-7 | DOI

[40] Jones, D.; Willett, V. Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil, Soil Biology and Biochemistry, Volume 38 (2006) no. 5, pp. 991-999 | DOI

[41] Kristensen, J. Å.; Rousk, J.; Metcalfe, D. B. Below‐ground responses to insect herbivory in ecosystems with woody plant canopies: A meta‐analysis, Journal of Ecology, Volume 108 (2019) no. 3, pp. 917-930 | DOI

[42] Kuznetsova, A.; Brockhoff, P. B.; Christensen, R. H. B. lmerTest Package: Tests in Linear Mixed Effects Models, Journal of Statistical Software, Volume 82 (2017) no. 13 | DOI

[43] Lavorel, S.; Grigulis, K.; McIntyre, S.; Williams, N. S. G.; Garden, D.; Dorrough, J.; Berman, S.; Quétier, F.; Thébault, A.; Bonis, A. Assessing functional diversity in the field – methodology matters!, Functional Ecology, Volume 0 (2007) no. 0 | DOI

[44] Legay, N.; Grassein, F.; Robson, T. M.; Personeni, E.; Bataillé, M.-P.; Lavorel, S.; Clément, J.-C. Comparison of inorganic nitrogen uptake dynamics following snowmelt and at peak biomass in subalpine grasslands, Biogeosciences, Volume 10 (2013) no. 11, pp. 7631-7645 | DOI

[45] Levy, E. G.; Madden, E. A. The point method of vegetation analysis, New Zealand Journal of Agriculture, Volume 46 (1933), pp. 267-279

[46] Lovett, G. M.; Ruesink, A. E. Carbon and nitrogen mineralization from decomposing gypsy moth frass, Oecologia, Volume 104 (1995) no. 2, pp. 133-138 | DOI

[47] Malik, A. A.; Martiny, J. B. H.; Brodie, E. L.; Martiny, A. C.; Treseder, K. K.; Allison, S. D. Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change, The ISME Journal, Volume 14 (2019) no. 1, pp. 1-9 | DOI

[48] Malik, A. A.; Puissant, J.; Goodall, T.; Allison, S. D.; Griffiths, R. I. Soil microbial communities with greater investment in resource acquisition have lower growth yield, Soil Biology and Biochemistry, Volume 132 (2019), pp. 36-39 | DOI

[49] McNaughton, S. J. Compensatory Plant Growth as a Response to Herbivory, Oikos, Volume 40 (1983) no. 3 | DOI

[50] McNaughton, S. J.; Banyikwa, F. F.; McNaughton, M. M. Promotion of the Cycling of Diet-Enhancing Nutrients by African Grazers, Science, Volume 278 (1997) no. 5344, pp. 1798-1800 | DOI

[51] McNaughton, S. J.; Ruess, R. W.; Seagle, S. W. Large Mammals and Process Dynamics in African Ecosystems, BioScience, Volume 38 (1988) no. 11, pp. 794-800 | DOI

[52] Nitschke, N.; Wiesner, K.; Hilke, I.; Eisenhauer, N.; Oelmann, Y.; Weisser, W. W. Increase of fast nutrient cycling in grassland microcosms through insect herbivory depends on plant functional composition and species diversity, Oikos, Volume 124 (2014) no. 2, pp. 161-173 | DOI

[53] Parker, T. C.; Sadowsky, J.; Dunleavy, H.; Subke, J.-A.; Frey, S. D.; Wookey, P. A. Slowed Biogeochemical Cycling in Sub-arctic Birch Forest Linked to Reduced Mycorrhizal Growth and Community Change after a Defoliation Event, Ecosystems, Volume 20 (2016) no. 2, pp. 316-330 | DOI

[54] Pastor, J.; Dewey, B.; Naiman, R. J.; McInnes, P. F.; Cohen, Y. Moose Browsing and Soil Fertility in the Boreal Forests of Isle Royale National Park, Ecology, Volume 74 (1993) no. 2, pp. 467-480 | DOI

[55] Paterson, E.; Thornton, B.; Sim, A.; Pratt, S. Effects of defoliation and atmospheric CO 2 depletion on nitrate acquisition, and exudation of organic compounds by roots of Festuca rubra, Plant and Soil, Volume 250 (2003) no. 2, pp. 293-305 | DOI

[56] Piton, G.; Foulquier, A.; Martínez-García, L. B.; Legay, N.; Hedlund, K.; Martins da Silva, P.; Nascimento, E.; Reis, F.; Sousa, J. P.; De Deyn, G. B.; Clement, J. C. Disentangling drivers of soil microbial potential enzyme activity across rain regimes: An approach based on the functional trait framework, Soil Biology and Biochemistry, Volume 148 (2020) | DOI

[57] Piton, G.; Legay, N.; Arnoldi, C.; Lavorel, S.; Clément, J.-C.; Foulquier, A. Using proxies of microbial community‐weighted means traits to explain the cascading effect of management intensity, soil and plant traits on ecosystem resilience in mountain grasslands, Journal of Ecology, Volume 108 (2020) no. 3, pp. 876-893 | DOI

[58] Potthast, K.; Meyer, S.; Tischer, A.; Gleixner, G.; Sieburg, A.; Frosch, T.; Michalzik, B. Grasshopper herbivory immediately affects element cycling but not export rates in an N‐limited grassland system, Ecosphere, Volume 12 (2021) no. 3 | DOI

[59] R Core Team R: A language and environment for statistical computing, R Foundation for Statistical Computing, 2019 (http://www.r-project.org/)

[60] Reich, P. B. The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto, Journal of Ecology, Volume 102 (2014) no. 2, pp. 275-301 | DOI

[61] Rhoades, D. F. Offensive-Defensive Interactions between Herbivores and Plants: Their Relevance in Herbivore Population Dynamics and Ecological Theory, The American Naturalist, Volume 125 (1985) no. 2, pp. 205-238 | DOI

[62] Ritchie, M. E.; Tilman, D.; Knops, J. M. H. Herbivore effects on plant and nitrogen dynamics in oak savanna, Ecology, Volume 79 (1998) no. 1, pp. 165-177 | DOI

[63] Robson, T.; Lavorel, S.; Clement, J.; Roux, X. Neglect of mowing and manuring leads to slower nitrogen cycling in subalpine grasslands, Soil Biology and Biochemistry, Volume 39 (2007) no. 4, pp. 930-941 | DOI

[64] Sandén, H.; Mayer, M.; Stark, S.; Sandén, T.; Nilsson, L. O.; Jepsen, J. U.; Wäli, P. R.; Rewald, B. Moth Outbreaks Reduce Decomposition in Subarctic Forest Soils, Ecosystems, Volume 23 (2019) no. 1, pp. 151-163 | DOI

[65] Sankaran, M.; Augustine, D. J. Large herbivores suppress decomposer abundance in a semiarid grazing ecosystem, Ecology, Volume 85 (2004) no. 4, pp. 1052-1061 | DOI

[66] Satterthwaite, F. E. An Approximate Distribution of Estimates of Variance Components, Biometrics Bulletin, Volume 2 (1946) no. 6 | DOI

[67] Schimel, J. P.; Bennett, J. Nitrogen mineralization: challenges of a changing paradigm, Ecology, Volume 85 (2004) no. 3, pp. 591-602 | DOI

[68] Schmitz, O. J. Effects of Predator Hunting Mode on Grassland Ecosystem Function, Science, Volume 319 (2008) no. 5865, pp. 952-954 | DOI

[69] Schultz, J. C.; Baldwin, I. T. Oak Leaf Quality Declines in Response to Defoliation by Gypsy Moth Larvae, Science, Volume 217 (1982) no. 4555, pp. 149-151 | DOI

[70] Singer, F. J.; Schoenecker, K. A. Do ungulates accelerate or decelerate nitrogen cycling?, Forest Ecology and Management, Volume 181 (2003) no. 1-2, pp. 189-204 | DOI

[71] Sinsabaugh, R. L.; Hill, B. H.; Follstad Shah, J. J. Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment, Nature, Volume 462 (2009) no. 7274, pp. 795-798 | DOI

[72] Stark, S.; Grellmann, D. Soil microbial responses to herbivory in an arctic tundra heath at two levels of nutrient availability, Ecology, Volume 83 (2002) no. 10, pp. 2736-2744 | DOI

[73] Talal, S.; Cease, A. J.; Youngblood, J. P.; Farington, R.; Trumper, E. V.; Medina, H. E.; Rojas, J. E.; Fernando Copa, A.; Harrison, J. F. Plant carbohydrate content limits performance and lipid accumulation of an outbreaking herbivore, Proceedings of the Royal Society B: Biological Sciences, Volume 287 (2020) no. 1940 | DOI

[74] Thébault, A.; Clément, J.-C.; Ibanez, S.; Roy, J.; Geremia, R. A.; Pérez, C. A.; Buttler, A.; Estienne, Y.; Lavorel, S. Nitrogen limitation and microbial diversity at the treeline, Oikos, Volume 123 (2014) no. 6, pp. 729-740 | DOI

[75] Tuomi, M.; Stark, S.; Hoset, K. S.; Väisänen, M.; Oksanen, L.; Murguzur, F. J. A.; Tuomisto, H.; Dahlgren, J.; Bråthen, K. A. Herbivore Effects on Ecosystem Process Rates in a Low-Productive System, Ecosystems, Volume 22 (2018) no. 4, pp. 827-843 | DOI

[76] van der Wal, R.; Bardgett, R. D.; Harrison, K. A.; Stien, A. Vertebrate herbivores and ecosystem control: cascading effects of faeces on tundra ecosystems, Ecography, Volume 27 (2004) no. 2, pp. 242-252 | DOI

[77] van Wijnen, H. J.; van der Wal, R.; Bakker, J. P. The impact of herbivores on nitrogen mineralization rate: consequences for salt-marsh succession, Oecologia, Volume 118 (1999) no. 2, pp. 225-231 | DOI

[78] Vance, E.; Brookes, P.; Jenkinson, D. An extraction method for measuring soil microbial biomass C, Soil Biology and Biochemistry, Volume 19 (1987) no. 6, pp. 703-707 | DOI

[79] Vittoz, P.; Guisan, A. How reliable is the monitoring of permanent vegetation plots? A test with multiple observers, Journal of Vegetation Science, Volume 18 (2007) no. 3, pp. 413-422 | DOI

[80] Wardle, D. A.; Bardgett, R. D.; Klironomos, J. N.; Setälä, H.; van der Putten, W. H.; Wall, D. H. Ecological Linkages Between Aboveground and Belowground Biota, Science, Volume 304 (2004) no. 5677, pp. 1629-1633 | DOI

[81] Wienhold, B. J. Comparison of Laboratory Methods and an In Situ Method for Estimating Nitrogen Mineralization in an Irrigated Silt‐Loam Soil, Communications in Soil Science and Plant Analysis, Volume 38 (2007) no. 13-14, pp. 1721-1732 | DOI

[82] Williams, A.; Langridge, H.; Straathof, A. L.; Muhamadali, H.; Hollywood, K. A.; Goodacre, R.; Vries, F. T. Root functional traits explain root exudation rate and composition across a range of grassland species, Journal of Ecology, Volume 110 (2021) no. 1, pp. 21-33 | DOI

[83] Wood, J. L.; Tang, C.; Franks, A. E. Competitive Traits Are More Important than Stress-Tolerance Traits in a Cadmium-Contaminated Rhizosphere: A Role for Trait Theory in Microbial Ecology, Frontiers in Microbiology, Volume 9 (2018) | DOI

Cited by Sources: