Plant nutrient uptake and productivity are driven by a multitude of factors that have been modified by human activities, like climate change and the activity of decomposers. However, interactive effects of climate change and key decomposer groups like earthworms have rarely been studied. In a field microcosm experiment, we investigated the effects of a mean future climate scenario with warming (+ 0.50 °C to + 0.62 °C) and altered precipitation (+ 10% in spring and autumn, - 20% in summer) and earthworms (anecic-two Lumbricus terrestris, endogeic-four Allolobophora chlorotica and both together within 10 cm diameter tubes) on plant biomass and stoichiometry in two land-use types (intensively used meadow and conventional farming). We found little evidence for earthworm effects on aboveground biomass. However, future climate increased above- (+40.9%) and belowground biomass (+44.7%) of grass communities, which was mainly driven by production of the dominant Festulolium species during non-summer drought periods, but decreased the aboveground biomass (- 36.9%) of winter wheat. Projected climate change and earthworms interactively affected the N content and C:N ratio of grasses. Earthworms enhanced the N content (+1.2%) thereby decreasing the C:N ratio (- 4.1%) in grasses, but only under ambient climate conditions. The future climate treatment generally decreased the N content of grasses (aboveground: - 1.1%, belowground: - 0.15%) and winter wheat (- 0.14%), resulting in an increase in C:N ratio of grasses (aboveground: + 4.2%, belowground: +6.3%) and wheat (+5.9%). Our results suggest that climate change diminishes the positive effects of earthworms on plant nutrient uptakes due to soil water deficit, especially during summer drought.

Biology Centre of the Czech Academy of Sciences Institute of Soil Biology and Biogeochemistry České Budějovice Czech Republic

Centre of Biodiversity and Sustainable Land Use University of Göttingen Göttingen Germany

Department of Community Ecology Helmholtz Centre for Environmental Research UFZ Halle Germany

Department of Ecosystem Biology Faculty of Science University of South Bohemia České Budějovice Czech Republic

German Centre for Integrative Biodiversity Research Halle Jena Leipzig Leipzig Germany

Institute for Biology Leipzig University Leipzig Germany

Institute of Agricultural and Nutritional Sciences Martin Luther University Halle Wittenberg Halle Germany

Johann Friedrich Blumenbach Institute of Zoology and Anthropology University of Göttingen Göttingen Germany

Zobrazit více v PubMed

Angst G, Frouz J, van Groenigen JW, Scheu S, Kogel-Knabner I, Eisenhauer N. Earthworms as catalysts in the formation and stabilization of soil microbial necromass. Glob Change Biol. 2022;28:4775–4782. doi: 10.1111/gcb.16208. PubMed DOI PMC

Ayres E, Steltzer H, Simmons BL, Simpson RT, Steinweg JM, Wallenstein MD, Mellor N, Parton WJ, Moore JC, Wall DH. Home-field advantage accelerates leaf litter decomposition in forests. Soil Biol Biochem. 2009;41:606–610. doi: 10.1016/j.soilbio.2008.12.022. DOI

Bai H, Xiao D, Wang B, Liu L, Tang J. Simulation of wheat response to future climate change based on coupled model inter-comparison project phase 6 multi-model ensemble projections in the north china plain. Front Plant Sci. 2022;13:829580. doi: 10.3389/fpls.2022.829580. PubMed DOI PMC

Bardgett RD, van der Putten WH. Belowground biodiversity and ecosystem functioning. Nature. 2014;515:505–511. doi: 10.1038/nature13855. PubMed DOI

Bassirirad H. Kinetics of nutrient uptake by roots: responses to global change. New Phytol. 2000;147:155–169. doi: 10.1046/j.1469-8137.2000.00682.x. DOI

Bates D, Machler M, Bolker BM, Walker SC. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67:1–48. doi: 10.18637/jss.v067.i01. DOI

Blouin M, Hodson ME, Delgado EA, Baker G, Brussaard L, Butt KR, Dai J, Dendooven L, Peres G, Tondoh JE, Cluzeau D, Brun JJ. A review of earthworm impact on soil function and ecosystem services. Eur J Soil Sci. 2013;64:161–182. doi: 10.1111/ejss.12025. DOI

Bothe A, Westermeier P, Wosnitza A, Willner E, Schum A, Dehmer KJ, Hartmann S. Drought tolerance in perennial ryegrass (Lolium perenne L.) as assessed by two contrasting phenotyping systems. J Agronomy Crop Sci. 2018;204:375–389. doi: 10.1111/jac.12269. DOI

Brown GG, Edwards CA, Brussaard L. How earthworms affect plant growth: burrowing into the mechanisms. Earthworm Ecol. 2004;2:13–49.

Coleman DC, Callaham M, Jr, Crossley DA. Fundamentals of Soil Ecology. 3. London: Academic press; 2017.

Craven D, Thakur MP, Cameron EK, Frelich LE, Beausejour R, Blair RB, Blossey B, Burtis J, Choi A, Davalos A, Fahey TJ, Fisichelli NA, Gibson K, Handa IT, Hopfensperger K, Loss SR, Nuzzo V, Maerz JC, Sackett T, Scharenbroch BC, Smith SM, Vellend M, Umek LG, Eisenhauer N. The unseen invaders: introduced earthworms as drivers of change in plant communities in North American forests (a meta-analysis) Glob Chang Biol. 2017;23:1065–1074. doi: 10.1111/gcb.13446. PubMed DOI PMC

Edwards CA, Bohlen PJ. Biology and ecology of earthworms. 3. London: Springer Science & Business Media; 1996.

Eisenhauer N, Eisenhauer E. The “intestines of the soil”: the taxonomic and functional diversity of earthworms – a review for young ecologists. EcoEvoRxiv. 2020 doi: 10.32942/osf.io/tfm5y. DOI

Eisenhauer N, Scheu S. Earthworms as drivers of the competition between grasses and legumes. Soil Biol Biochem. 2008;40:2650–2659. doi: 10.1016/j.soilbio.2008.07.010. DOI

Eisenhauer N, Milcu A, Sabais ACW, Bessler H, Weigelt A, Engels C, Scheu S. Plant community impacts on the structure of earthworm communities depend on season and change with time. Soil Biol Biochem. 2009;41:2430–2443. doi: 10.1016/j.soilbio.2009.09.001. DOI

Eisenhauer N, Fisichelli NA, Frelich LE, Reich PB. Interactive effects of global warming and ‘global worming’ on the initial establishment of native and exotic herbaceous plant species. Oikos. 2012;121:1121–1133. doi: 10.1111/j.1600-0706.2011.19807.x. DOI

Fierer N, Schimel JP. Effects of drying–rewetting frequency on soil carbon and nitrogen transformations. Soil Biol Biochem. 2002;34:777–787. doi: 10.1016/S0038-0717(02)00007-X. DOI

Franklin J, Serra-Diaz JM, Syphard AD, Regan HM. Global change and terrestrial plant community dynamics. Proc Natl Acad Sci USA. 2016;113:3725–3734. doi: 10.1073/pnas.1519911113. PubMed DOI PMC

Gherardi LA, Sala OE. Effect of interannual precipitation variability on dryland productivity: a global synthesis. Glob Change Biol. 2019;25:269–276. doi: 10.1111/gcb.14480. PubMed DOI

Görgen K, Beersma J, Brahmer G, Buiteveld H, Carambia M, De Keizer O, Krahe P, Nilson E, Lammersen R, Perrin C. Assessment of climate change impacts on discharge in the Rhine River Basin: results of the RheinBlick2050 project. CHR Lelystad; 2010.

Gu L, Hanson PJ, Mac Post W, Kaiser DP, Yang B, Nemani R, Pallardy SG, Meyers T. The 2007 eastern US spring freezes: Increased cold damage in a warming world? Bioscience. 2008;58:253–262. doi: 10.1641/B580311. DOI

Han WX, Fang JY, Reich PB, Woodward FI, Wang ZH. Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China. Ecol Lett. 2011;14:788–796. doi: 10.1111/j.1461-0248.2011.01641.x. PubMed DOI

Helgadóttir Á, Frankow-Lindberg B, Seppänen M, Søegaard K, Østrem L. European grasslands overview: Nordic region. Grassl Sci Eur. 2014;19:15–28.

Hodson ME, Brailey-Jones P, Burn WL, Harper AL, Hartley SE, Helgason T, Walker HF. Enhanced plant growth in the presence of earthworms correlates with changes in soil microbiota but not nutrient availability. Geoderma. 2023 doi: 10.1016/j.geoderma.2023.116426. DOI

Humphreys MW, Yadav RS, Cairns AJ, Turner LB, Humphreys J, Skot L. A changing climate for grassland research. New Phytol. 2006;169:9–26. doi: 10.1111/j.1469-8137.2005.01549.x. PubMed DOI

Humphreys MW, O'Donovan SA, Farrell MS, Gay AP, Kingston-Smith AH. The potential of novel Festulolium (2n = 4x = 28) hybrids as productive, nutrient-use-efficient fodder for ruminants. Food Energy Secur. 2014;3:98–110. doi: 10.1002/fes3.50. DOI

Jacquiod S, Puga-Freitas R, Spor A, Mounier A, Monard C, Mougel C, Philippot L, Blouin M. A core microbiota of the plant-earthworm interaction conserved across soils. Soil Biol Biochem. 2020 doi: 10.1016/j.soilbio.2020.107754. DOI

Kano-Nakata M, Inukai Y, Wade LJ, Siopongco JDLC, Yamauchi A. Root development, water uptake, and shoot dry matter production under water deficit conditions in two CSSLs of rice: functional roles of root plasticity. Plant Prod Sci. 2011;14:307–317. doi: 10.1626/pps.14.307. DOI

Kuznetsova A, Brockhoff PB, Christensen RH. lmerTest package: tests in linear mixed effects models. J Stat Softw. 2017;82:1–26. doi: 10.18637/jss.v082.i13. DOI

Lambers H, Chapin FS, Pons TL. Plant physiological ecology. Springer; 2008.

Laossi K-R, Ginot A, Noguera DC, Blouin M, Barot S. Earthworm effects on plant growth do not necessarily decrease with soil fertility. Plant Soil. 2009;328:109–118. doi: 10.1007/s11104-009-0086-y. DOI

Laossi K-R, Noguera DC, Bartolomé-Lasa A, Mathieu J, Blouin M, Barot S. Effects of an endogeic and an anecic earthworm on the competition between four annual plants and their relative fecundity. Soil Biol Biochem. 2009;41:1668–1673. doi: 10.1016/j.soilbio.2009.05.009. DOI

Lavelle P, Barois I, Blanchart E, Brown G, Brussaard L, Decaëns T, Fragoso C, Jimenez JJ, Kajondo KK, Martinez MDLA, Moreno A, Pashanasi B, Senapati B, Villenave C. Earthworms as a resource in tropical agroecosystems. Nat Resour. 1998;34:26–40.

Li XN, Pu HC, Liu FL, Zhou Q, Cai J, Dai TB, Cao WX, Jiang D. Winter wheat photosynthesis and grain yield responses to spring freeze. Agron J. 2015;107:1002–1010. doi: 10.2134/agronj14.0460. DOI

Meng B, Shi BK, Zhong SZ, Chai H, Li SX, Wang YB, Henry HAL, Ma JY, Sun W. Drought sensitivity of aboveground productivity in Leymus chinensis meadow steppe depends on drought timing. Oecologia. 2019;191:685–696. doi: 10.1007/s00442-019-04506-w. PubMed DOI

Rosenzweig C, Tubiello FN, Goldberg R, Mills E, Bloomfield J. Increased crop damage in the US from excess precipitation under climate change. Global Environ Chang. 2002;12:197–202. doi: 10.1016/S0959-3780(02)00008-0. DOI

Sala OE, Chapin FS, 3rd, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH. Global biodiversity scenarios for the year 2100. Science. 2000;287:1770–1774. doi: 10.1126/science.287.5459.1770. PubMed DOI

Sampoux JP, Baudouin P, Bayle B, Beguier V, Bourdon P, Chosson JF, de Bruijn K, Deneufbourg F, Galbrun C, Ghesquiere M, Noel D, Tharel B, Viguie A. Breeding perennial ryegrass (Lolium perenne L.) for turf usage: an assessment of genetic improvements in cultivars released in Europe, 1974–2004. Grass Forage Sci. 2013;68:33–48. doi: 10.1111/j.1365-2494.2012.00896.x. DOI

Schädler M, Buscot F, Klotz S, Reitz T, Durka W, Bumberger J, Merbach I, Michalski SG, Kirsch K, Remmler P, Schulz E, Auge H. Investigating the consequences of climate change under different land-use regimes: a novel experimental infrastructure. Ecosphere. 2019;10:e02635. doi: 10.1002/ecs2.2635. DOI

Scheu S. Effects of earthworms on plant growth: patterns and perspectives. Pedobiologia. 2003;47:846–856. doi: 10.1078/0031-4056-00270. DOI

Schimel J, Balser TC, Wallenstein M. Microbial stress-response physiology and its implications for ecosystem function. Ecology. 2007;88:1386–1394. doi: 10.1890/06-0219. PubMed DOI

Schmidt O, Curry JP. Effects of earthworms on biomass production, nitrogen allocation and nitrogen transfer in wheat-clover intercropping model systems. Plant Soil. 1999;214:187–198. doi: 10.1023/A:1004723914623. DOI

Shi L, Lin Z, Wei X, Peng C, Yao Z, Han B, Xiao Q, Zhou H, Deng Y, Liu K, Shao X. Precipitation increase counteracts warming effects on plant and soil C:N: P stoichiometry in an alpine meadow. Front Plant Sci. 2022;13:1044173. doi: 10.3389/fpls.2022.1044173. PubMed DOI PMC

Shipitalo MJ, Nuutinen V, Butt KR. Interaction of earthworm burrows and cracks in a clayey, subsurface-drained, soil. Appl Soil Ecol. 2004;26:209–217. doi: 10.1016/j.apsoil.2004.01.004. DOI

Singh J, Schadler M, Demetrio W, Brown GG, Eisenhauer N. Climate change effects on earthworms - a review. Soil Org. 2019;91:114–138. doi: 10.25674/so91iss3pp114. PubMed DOI PMC

Song J, Wan S, Piao S, Knapp AK, Classen AT, Vicca S, Ciais P, Hovenden MJ, Leuzinger S, Beier C, Kardol P, Xia J, Liu Q, Ru J, Zhou Z, Luo Y, Guo D, Adam Langley J, Zscheischler J, Dukes JS, Tang J, Chen J, Hofmockel KS, Kueppers LM, Rustad L, Liu L, Smith MD, Templer PH, Quinn Thomas R, Norby RJ, Phillips RP, Niu S, Fatichi S, Wang Y, Shao P, Han H, Wang D, Lei L, Wang J, Li X, Zhang Q, Li X, Su F, Liu B, Yang F, Ma G, Li G, Liu Y, Liu Y, Yang Z, Zhang K, Miao Y, Hu M, Yan C, Zhang A, Zhong M, Hui Y, Li Y, Zheng M. A meta-analysis of 1,119 manipulative experiments on terrestrial carbon-cycling responses to global change. Nat Ecol Evol. 2019;3:1309–1320. doi: 10.1038/s41559-019-0958-3. PubMed DOI

Tang Z, Xu W, Zhou G, Bai Y, Li J, Tang X, Chen D, Liu Q, Ma W, Xiong G, He H, He N, Guo Y, Guo Q, Zhu J, Han W, Hu H, Fang J, Xie Z. Patterns of plant carbon, nitrogen, and phosphorus concentration in relation to productivity in China's terrestrial ecosystems. Proc Natl Acad Sci USA. 2018;115:4033–4038. doi: 10.1073/pnas.1700295114. PubMed DOI PMC

Thakur MP, Risch AC, van der Putten WH. Biotic responses to climate extremes in terrestrial ecosystems. iScience. 2022;25:104559. doi: 10.1016/j.isci.2022.104559. PubMed DOI PMC

van Groenigen JW, Lubbers IM, Vos HM, Brown GG, De Deyn GB, van Groenigen KJ. Earthworms increase plant production: a meta-analysis. Sci Rep-Uk. 2014;4:6365. doi: 10.1038/srep06365. PubMed DOI PMC

Viciedo DO, Prado RD, Martinez CA, Habermann E, Piccolo MD. Short-term warming and water stress affect Panicum maximum Jacq. stoichiometric homeostasis and biomass production. Sci Total Environ. 2019;681:267–274. doi: 10.1016/j.scitotenv.2019.05.108. PubMed DOI

Wang Z-Y, Lu J-Z, Erktan A, Fu L-B, Chen H, Yin M, Cao W-D, Scheu S. Crop productivity, resource allocation and nitrogen concentration as affected by soil decomposers, mixed cropping and crop genotype. Soil Biol Biochem. 2022 doi: 10.1016/j.soilbio.2022.108855. DOI

Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Putten WHvd, Wall DH, Ecological linkages between aboveground and belowground biota. Science. 2004;304:1629–1633. doi: 10.1126/science.1094875. PubMed DOI

Wilschut RA, De Long JR, Geisen S, Hannula SE, Quist CW, Snoek B, Steinauer K, Wubs ERJ, Yang Q, Thakur MP. Combined effects of warming and drought on plant biomass depend on plant woodiness and community type: a meta-analysis. Proc Biol Sci. 2022;289:20221178. doi: 10.1098/rspb.2022.1178. PubMed DOI PMC

Wu Z, Dijkstra P, Koch GW, Penuelas J, Hungate BA. Responses of terrestrial ecosystems to temperature and precipitation change: a meta-analysis of experimental manipulation. Glob Change Biol. 2011;17:927–942. doi: 10.1111/j.1365-2486.2010.02302.x. DOI

Wurst S, Langel R, Reineking A, Bonkowski M, Scheu S. Effects of earthworms and organic litter distribution on plant performance and aphid reproduction. Oecologia. 2003;137:90–96. doi: 10.1007/s00442-003-1329-x. PubMed DOI

Wurst S, Langel R, Scheu S. Do endogeic earthworms change plant competition? A microcosm study. Plant Soil. 2005;271:123–130. doi: 10.1007/s11104-004-2201-4. DOI

Yan C, Liu Z, Yuan Z, Shi X, Lock TR, Kallenbach RL. Aridity modifies the responses of plant stoichiometry to global warming and nitrogen deposition in semi-arid steppes. Sci Total Environ. 2022;831:154807. doi: 10.1016/j.scitotenv.2022.154807. PubMed DOI

Yue K, Fornara DA, Yang WQ, Peng Y, Li ZJ, Wu FZ, Peng CH. Effects of three global change drivers on terrestrial C:N: P stoichiometry: a global synthesis. Glob Change Biol. 2017;23:2450–2463. doi: 10.1111/gcb.13569. PubMed DOI