Abstract
Background
Soil microarthropods influence many soil processes that support plant growth and development.
Scope
In this paper we review the current understanding of direct microarthropod-plant interactions, how microarthropod-microbe interactions indirectly impact plant growth, and key areas for future study.
Conclusion
Microarthropod impacts on plants are primarily routed through their interactions with microbial communities, mediating organic matter decomposition, nutrient cycling and allocation, and plant-pathogen dynamics in soils. The research investigating how microarthropod-saprotrophic microbe interactions affect plants through decomposition and nutrient cycling indicates a generally positive relationship, though this relationship is influenced by the overall diversity or species richness observed in the microarthropod communities. The effects of microarthropod-plant symbionts interactions on plants are varied and there is no clear benefit or detriment to plants via this mechanism. The effects of microarthropod-plant pathogen interactions on plants suggest that, in most cases, microarthropods will reduce disease incidence and severity. The limited diversity of the study taxa in this area of research is a major limitation to our understanding of how microarthropods impact plant health. Our review revealed that while much is known about microarthropod impacts on the intermediate processes that influence plants, only a subset of studies have quantified plant responses to microarthropod activity. Overall, existing evidence indicates that the overall effects of microarthropods on plants is positive. Future research should aim to incorporate more plant metrics and consider both microarthropod and microbial community dynamics in designed and observational studies.
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References
Anderson RV, Coleman DC, Cole CV (1981) Effects of saprotrophic grazing on net mineralization. Ecol Bull 201–216. http://www.jstor.org/stable/45128662
Bardgett RD, Chan KF (1999) Experimental evidence that soil fauna enhance nutrient mineralization and plant nutrient uptake in montane grassland ecosystems. Soil Biol Biochem 31:1007–1014. https://doi.org/10.1016/S0038-0717(99)00014-0
Barrios E (2007) Soil biota, ecosystem services and land productivity. Ecol Econ 64:269–285. https://doi.org/10.1016/J.ECOLECON.2007.03.004
Beretta GM, Deere JA, Messelink GJ et al (2022) Review: predatory soil mites as biocontrol agents of above- and below-ground plant pests. Exp Appl Acarol. https://doi.org/10.1007/S10493-022-00723-W
Blouin M (2018) Chemical communication: An evidence for co-evolution between plants and soil organisms. Appl Soil Ecol 123:409–415. https://doi.org/10.1016/J.APSOIL.2017.10.028
Boerner REJ, Harris KK (1991) Effects of collembola (arthropoda) and relative germination date on competition between mycorrhizalPanicum virgatum (Poaceae) and non-mycorrhizalBrassica nigra (Brassicaceae). Plant Soil 1991 1361 136:121–129. https://doi.org/10.1007/BF02465227
Bollen GJ, Middelkoop J, Hofman TW (1991) Effects of soil fauna on infection of potato sprouts by Rhizoctonia Solani. Elsevier, Amsterdam, pp 27–34
Briones MJI (2014) Soil fauna and soil functions: a jigsaw puzzle. Front Environ Sci 2:7. https://doi.org/10.3389/fenvs.2014.00007
Briones MJI (2018) The serendipitous value of soil fauna in ecosystem functioning: The unexplained explained. Front Environ Sci 6:149
Buse T, Filser J (2014) Mucilaginous seeds and algal diets attract soil Collembola in preference tests. Eur J Soil Biol 65:1–6. https://doi.org/10.1016/j.ejsobi.2014.08.005
Cambui CA, Svennerstam H, Gruffman L, Nordin A, Ganeteg U, Näsholm T (2011) Patterns of plant biomass partitioning depend on nitrogen source. PLoS One 6(4):e19211. https://doi.org/10.1371/journal.pone.0019211
Canellas LP, Olivares FL, Okorokova-Façanha AL, Façanha AR (2002) Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H+-ATPase activity in maize roots. Plant Physiol 130:1951–1957. https://doi.org/10.1104/PP.007088
Centenaro G, Hudek C, Zanella A, Crivellaro A (2018) Root-soil physical and biotic interactions with a focus on tree root systems: A review. Appl Soil Ecol 123:318–327. https://doi.org/10.1016/J.APSOIL.2017.09.017
Chamberlain PM, McNamara NP, Chaplow J, Stott AW, Black HIJ (2006) Translocation of surface litter carbon into soil by Collembola. Soil Biol Biochem 38(9):2655–2664. https://doi.org/10.1016/J.SOILBIO.2006.03.021
Chauvat M, Forey E (2021) Temperature modifies the magnitude of a plant response to Collembola presence. Appl Soil Ecol 158:103814. https://doi.org/10.1016/j.apsoil.2020.103814
Cole L, Dromph KM, Boaglio V, Bardgett RD (2004a) Effect of density and species richness of soil mesofauna on nutrient mineralisation and plant growth. Biol Fertil Soils 39:337–343. https://doi.org/10.1007/s00374-003-0702-6
Cole L, Staddon PL, Sleep D, Bardgett RD (2004b) Soil animals influence microbial abundance, but not plant-microbial competition for soil organic nitrogen. Funct Ecol 18:631–640. https://doi.org/10.1111/j.0269-8463.2004.00894.x
Coleman DC, Callaham MA, Crossley DA (2018) Fundamentals of soil ecology, 3rd edn. Elsevier, Amsterdam
Doblas-Miranda E, Paquette A, Work TT (2014) Intercropping trees’ effect on soil oribatid diversity in agro-ecosystems. Agrofor Syst 88:671–678. https://doi.org/10.1007/s10457-014-9680-y
Dodd JC (2000) The role of arbuscular mycorrhizal fungi in agro- and natural ecosystems. Outlook Agric 29:55–62. https://doi.org/10.5367/000000000101293059
Eerpina R, Boiteau G, Lynch DH (2017) Collembola diet switching in the presence of maize roots varies with species. Can J Soil Sci 97:171–177. https://doi.org/10.1139/cjss-2016-0057
Eichmann R, Richards L, Schäfer P (2021) Hormones as go-betweens in plant microbiome assembly. Plant J 105:518–541. https://doi.org/10.1111/TPJ.15135
Eisenhauer N, Schielzeth H, Barnes AD et al (2019) A multitrophic perspective on biodiversity–ecosystemfunctioning research. Adv Ecol Res 61:1. https://doi.org/10.1016/BS.AECR.2019.06.001
Eisenhauer N, Vogel A, Jensen B, Scheu S (2018) Decomposer diversity increases biomass production and shifts aboveground-belowground biomass allocation of common wheat. Sci Rep 8(1). https://doi.org/10.1038/s41598-018-36294-3
Endlweber K, Krome K, Welzl G et al (2011) Decomposer animals induce differential expression of defence and auxin-responsive genes in plants. Soil Biol Biochem 43:1130–1138
Endlweber K, Ruess L, Scheu S (2009) Collembola switch diet in presence of plant roots thereby functioning as herbivores. Soil Biol Biochem 41:1151–1154. https://doi.org/10.1016/j.soilbio.2009.02.022
Endlweber K, Scheu S (2007) Interactions between mycorrhizal fungi and Collembola: Effects on root structure of competing plant species. Biol Fertil Soils 43:741–749. https://doi.org/10.1007/s00374-006-0157-7
Eo J (2010) Responses of weed community and soil biota to cessation of fertilization. J Ecol F Biol 33:317–323. https://doi.org/10.5141/JEFB.2010.33.4.317
Filser J, Faber JH, Tiunov AV et al (2016) Soil fauna: key to new carbon models. SOIL 2:565–582. https://doi.org/10.5194/soil-2-565-2016
Forey E, Coulibaly SFM, Chauvat M (2015) Flowering phenology of a herbaceous species (Poa annua) is regulated by soil Collembola. Soil Biol Biochem 90:30–33.https://doi.org/10.1016/j.soilbio.2015.07.024
Frey SD (2003) Arbuscular mycorrhizae: interactions in plants, rhizosphere and soils. Appl Soil Ecol 24:273. https://doi.org/10.1016/j.apsoil.2003.08.001
Friberg H, Lagerlöf J, Rämert B (2005) Influence of soil fauna on fungal plant pathogens in agricultural and horticultural systems. Biocontrol Sci Technol 15:641–658. https://doi.org/10.1080/09583150500086979
Gange A (2000) Arbuscular mycorrhizal fungi, Collembola and plant growth. Trends Ecol Evol 15:369–372. https://doi.org/10.1016/S0169-5347(00)01940-6
Ganugi P, Masoni A, Pietramellara G, Benedettelli S (2019) A review of studies from the last twenty years on plant–Arbuscular mycorrhizal fungi associations and their uses for wheat crops. Agronomy 9:840. https://doi.org/10.3390/agronomy9120840
Gergócs V, Flórián N, Tóth Z et al (2022) Detangling ecosystem services: Open-field manipulation of soil-dwelling microarthropods provides new opportunities to investigate their effects on nitrogen cycling. Ecol Evol 12. https://doi.org/10.1002/ECE3.9134
Getzin LW (1985) Chemical control of the springtail Onychiurus pseudarmatus (Collembola: Onychiuridae). J Econ Entomol 78:1337–1340. https://doi.org/10.1093/JEE/78.6.1337
Glimskar A, Ericsson T (1999) Relative nitrogen limitation at steady-state nutrition as a determinant of plasticity in five grassland plant species. Ann Bot 84(4):413–420. https://doi.org/10.1006/anbo.1999.0929
González G (2002) Soil organisms and litter decomposition. Mod Trends Appl Terr Ecol 315–329. https://doi.org/10.1007/978-1-4615-0223-4_16
Graf M, Bönn M, Feldhahn L et al (2019) Collembola interact with mycorrhizal fungi in modifying oak morphology, C and N incorporation and transcriptomics. R Soc Open Sci 6. https://doi.org/10.1098/RSOS.181869
Grandy AS, Wieder WR, Wickings K, Kyker-Snowman E (2016) Beyond microbes: Are fauna the next frontier in soil biogeochemical models? Soil Biol Biochem 102:40–44. https://doi.org/10.1016/j.soilbio.2016.08.008
Guzmán, M del PR (2021) Soil biodiversity and root pathogens in agroecosystems. In: Hufnagel L (ed) Biodiversity of Ecosystems. IntechOpen
Hansen AA, Chatterjee A, Gramig G, Prischmann-Voldseth DA (2018) Weed and insect management alter soil arthropod densities, soil nutrient availability, plant productivity, and aphid densities in an annual legume cropping system. Appl Soil Ecol 130:120–133. https://doi.org/10.1016/j.apsoil.2018.06.006
Harris KK, Boerner REJ (1990) Effects of belowground grazing by collembola on growth, mycorrhizal infection, and P uptake of Geranium robertianum. Plant Soil 1990 1292 129:203–210. https://doi.org/10.1007/BF00032414
Hedlund K, Bengtsson G, Rundgren S (1995) Fungal odour discrimination in two sympatric species of fungivorous collembolans. Funct Ecol 9:869. https://doi.org/10.2307/2389984
Heneghan L, Coleman DC, Zou X et al (1998) Soil microarthropod community structure and litter decomposition dynamics: A study of tropical and temperate sites. Appl Soil Ecol 9:33–38. https://doi.org/10.1016/S0929-1393(98)00050-X
Herrmann S, Grams TEE, Tarkka MT et al (2016) Endogenous rhythmic growth, a trait suitable for the study of interplays between multitrophic interactions and tree development. Perspect Plant Ecol Evol Syst 19:40–48. https://doi.org/10.1016/J.PPEES.2016.02.003
Huck MG, Taylor HM (1982) The rhizotron as a tool for root research. Adv Agron 35:1–35. https://doi.org/10.1016/S0065-2113(08)60320-X
Innocenti G, Sabatini MA (2018) Collembola and plant pathogenic, antagonistic and arbuscular mycorrhizal fungi: a review. Bull Insectology 71:71–76
Jana U, Barot S, Blouin M et al (2010) Earthworms influence the production of above- and belowground biomass and the expression of genes involved in cell proliferation and stress responses in Arabidopsis thaliana. Soil Biol Biochem 42:244–252. https://doi.org/10.1016/J.SOILBIO.2009.10.022
Joseph SV (2017) Effects of insecticides on Protaphorura fimata (Collembola: Poduromorpha: Onychiuridae) Feeding on Germinating Lettuce. J Entomol Sci 52:68–81. https://doi.org/10.18474/JES16-23.1
Joseph SV, Bettiga C, Ramirez C, Soto-Adames FN (2015) Evidence of Protaphorura fimata (Collembola: Poduromorpha: Onychiuridae) feeding on germinating lettuce in the Salinas Valley of California. J Econ Entomol 108:228–236. https://doi.org/10.1093/JEE/TOU021
Kaiser PA, Lussenhop J (1991) Collembolan effects on establishment of vesicular-arbuscular mycorrhizae in soybean (Glycine max). Soil Biol Biochem 23:307–308. https://doi.org/10.1016/0038-0717(91)90069-V
Kampichler C, Bruckner A (2009) The role of microarthropods in terrestrial decomposition: a meta-analysis of 40 years of litterbag studies. Biol Rev 84(3), 375–389. https://doi.org/10.1111/j.1469-185X.2009.00078.x
Kaneda S, Miura S, Yamashita N, Ohigashi K, Yamasaki S, Murakami T, Urashima Y (2012) Significance of litter layer in enhancing mesofaunal abundance and microbial biomass nitrogen in sweet corn-white clover living mulch systems. Soil Sci Plant Nutr 58(4):424–434. https://doi.org/10.1080/00380768.2012.699881
Klironomos JN, Bednarczuk EM, Neville J (1999) Reproductive significance of feeding on saprobic and arbuscular mycorrhizal fungi by the collembolan, Folsomia candida. Funct Ecol 13:756–761. https://doi.org/10.1046/J.1365-2435.1999.00379.X
Klironomos JN, Kendrick B (1995) Relationships among microarthropods, fungi, and their environment. Plant Soil 170:183–197. https://doi.org/10.1007/BF02183066
Koleva L, Ulber B, Wolf G (2009) The influence of collembola on the dissemination and antagonistic effect of pseudomonas fluorescens against pythium ultimum in soil. Soil Biotechnol &Biotechnological Equip 23:293–296. https://doi.org/10.1080/13102818.2009.10818422
Kuťáková E, Cesarz S, Münzbergová Z, Eisenhauer N (2018) Soil microarthropods alter the outcome of plant-soil feedback experiments. Sci Rep 8. https://doi.org/10.1038/s41598-018-30340-w
Lal R (2020) Soil organic matter and water retention. Agron J 112(5):3265–3277. https://doi.org/10.1002/agj2.20282
Larsen J, Jakobsen I (1996) Effects of a mycophagous Collembola on the symbioses between Trifolium subterraneum and three arbuscular mycorrhizal fungi. New Phytol 133:295–302. https://doi.org/10.1111/J.1469-8137.1996.TB01897.X
Lartey RT, Curl EA, Peterson CM (1994) Interactions of mycophagous collembola and biological control fungi in the suppression of Rhizoctonia solani. Soil Biol Biochem 26(1):81–88. https://doi.org/10.1016/0038-0717(94)90198-8
Lavelle P, Decaens T, Aubert M et al (2006) Soil invertebrates and ecosystem services. Eur J Soil Biol 42:S3–S15
Liiri M, Setälä H, Haimi J, Pennanen T, Fritze H (2002) Relationship between soil microarthropod species diversity and plant growth does not change when the system is disturbed. Oikos 96(1):137–149. https://doi.org/10.1034/j.1600-0706.2002.960115.x
Lootsma M, Scholte K (1997a) Effects of the springtail Folsomia fimetaria and the nematode Aphelenchus avenae on Rhizoctonia solani stem infection of potato at temperatures of 10 and 15°C. Plant Pathol 46:203–208. https://doi.org/10.1046/j.1365-3059.1997.d01-228.x
Lootsma M, Scholte K (1997b) Effect of soil moisture content on the suppression of Rhizoctonia stem canker on potato by the nematode Aphelenchus avenae and the springtail Folsomia fimetaria. Plant Pathol 46:209–215. https://doi.org/10.1046/j.1365-3059.1997.d01-229.x
Lootsma M, Scholte K (1998) Effect of soil pH and amendments with dried fodder rape on mycophagous soil animals and Rhizoctonia stem canker of potato. Pedobiologia (Jena) 42:215–222
Lundgren MR, Des Marais DL (2020) Life history variation as a model for understanding trade-offs in plant–environment interactions. Curr Biol 30:R180–R189. https://doi.org/10.1016/J.CUB.2020.01.003
Lussenhop J (1992) Mechanisms of microarthropod-microbial interactions in soil. Adv Ecol Res 23:1–33. https://doi.org/10.1016/S0065-2504(08)60145-2
Lussenhop J (1996) Collembola as mediators of microbial symbiont effects upon soybean. Soil Biol Biochem 28:363–369. https://doi.org/10.1016/0038-0717(95)00145-X
Lussenhop J, Treonis A, Curtis PS et al (1998) Response of soil biota to elevated atmospheric CO2 in poplar model systems. Oecologia 113:247–251. https://doi.org/10.1007/s004420050375
McGonigle TP, Fitter AH (1988) Ecological consequences of arthropod grazing on VA mycorrhizal fungi. Proc R Soc Edinburgh Sect B Biol Sci 94:25–32. https://doi.org/10.1017/S0269727000007077
Minasny B, McBratney AB (2018) Limited effect of organic matter on soil available water capacity. Eur J Soil Sci 69(1):39–47. https://doi.org/10.1111/ejss.12475
Mitschunas N, Wagner M, Filser J (2006) Evidence for a positive influence of fungivorous soil invertebrates on the seed bank persistence of grassland species. J Ecol 94:791–800. https://doi.org/10.1111/j.1365-2745.2006.01146.x
Mitschunas N, Wagner M, Filser J (2008) Increased field emergence of seedlings at high densities of fungivorous soil mesofauna. J Torrey Bot Soc 135:272–280. https://doi.org/10.3159/08-ra-022.1
Müller I, Schmid B, Weiner J (2000) The effect of nutrient availability on biomass allocation patterns in 27 species of herbaceous plants. Perspect Plant Ecol Evol Syst 3(2):115–127.https://doi.org/10.1078/1433-8319-00007
Nadeem SM, Ahmad M, Zahir ZA et al (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv 32:429–448
Nakamura Y, Matsuzaki I, Itakura J (1992) Effect of grazing by Sinella curviseta (Collembola) on Fusarium oxysporum f. sp. cucumerinum causing cucumber disease. Pedobiologia (Jena) 36:168–171
Neher DA, Barbercheck ME (2019) Soil microarthropods and soil health: intersection of decomposition and pest suppression in agroecosystems. Insects 10(12):414. https://doi.org/10.3390/insects10120414
Neumann E, George E (2010) Nutrient uptake: The arbuscular mycorrhiza fungal symbiosis as a plant nutrient acquisition strategy. In: Arbuscular Mycorrhizas: Physiology and Function. Springer Netherlands, Dordrecht, pp 137–167
Ngosong C, Gabriel E, Ruess L (2014) Collembola grazing on arbuscular mycorrhiza fungi modulates nutrient allocation in plants. Pedobiologia (Jena) 57:171–179. https://doi.org/10.1016/j.pedobi.2014.03.002
Nielsen UN, Ayres E, Wall DH, Bardgett RD (2011) Soil biodiversity and carbon cycling: a review and synthesis of studies examining diversity–function relationships. Eur J Soil Sci 62:105–116. https://doi.org/10.1111/J.1365-2389.2010.01314.X
Nietschke L, Seupt A, Burfeindt I, Filser J (2011) Collembola and seed germination: relevance of substrate quality and evidence of seed attack. Soil Org 83:451–462
NRCS Soil Health (n.d.) https://www.nrcs.usda.gov/wps/portal/nrcs/main/national/soils/health/. Accessed 5 Jan 2022
Onemli F (2004) The effects of soil organic matter on seedling emergence in sunflower (Helianthus annuus L.). Plant Soil Environ 50:494–499. https://doi.org/10.17221/4064-PSE
Partsch S, Milcu A, Scheu S (2006) Decomposers (Lumbricidae, Collembola) affect plant performance in model grasslands of different diversity. Ecology 87:2548–2558
Pollierer MM, Dyckmans J, Scheu S, Haubert D (2012) Carbon flux through fungi and bacteria into the forest soil animal food web as indicated by compound-specific 13 C fatty acid analysis. Funct Ecol 26:978–990. https://doi.org/10.1111/j.1365-2435.2012.02005.x
Pollierer MM, Langel R, Körner C et al (2007) The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol Lett 10:729–736. https://doi.org/10.1111/j.1461-0248.2007.01064.x
Porazinska DL, Seastedt TR, Gendron EMS, Schmidt SK (2022) Invasive annual cheatgrass enhances the abundance of native microbial and microinvertebrate eukaryotes but reduces invasive earthworms. Plant Soil 473:591–604. https://doi.org/10.1007/S11104-022-05312-9/FIGURES/6
Potapov AM (2022) Multifunctionality of belowground food webs: resource, size and spatial energy channels. Biol Rev 97:1691–1711. https://doi.org/10.1111/BRV.12857
Potapov AM, Goncharov AA, Semenina EE et al (2017) Arthropods in the subsoil: Abundance and vertical distribution as related to soil organic matter, microbial biomass and plant roots. Eur J Soil Biol 82:88–97. https://doi.org/10.1016/j.ejsobi.2017.09.001
Potapov AM, Goncharov AA, Tsurikov SM et al (2016) Assimilation of plant-derived freshly fixed carbon by soil collembolans: Not only via roots? Pedobiologia (Jena) 59:189–193. https://doi.org/10.1016/j.pedobi.2016.07.002
Puga-Freitas R, Barot S, Taconnat L et al (2012) Signal molecules mediate the impact of the earthworm Aporrectodea caliginosa on growth, development and defence of the plant Arabidopsis thaliana. PLoS ONE 7:e49504. https://doi.org/10.1371/JOURNAL.PONE.0049504
Puga-Freitas R, Blouin M (2015) A review of the effects of soil organisms on plant hormone signalling pathways. Environ Exp Bot 114:104–116. https://doi.org/10.1016/J.ENVEXPBOT.2014.07.006
Rickerl DH, Curl EA, Touchton J (1989) Tillage and rotation effects on collembola populations and rhizoctonia infestation. Soil Tillage Res 15:41–49
Sabatini MA, Innocenti G (2001) Effects of collembola on plant-pathogenic fungus interactions in simple experimental systems. Biol Fertil Soils 33:62–66. https://doi.org/10.1007/s003740000290
Sabatini MA, Innocenti G (2000) Soil-borne plant pathogenic fungi in relation to some collembolan species under laboratory conditions. Mycol Res 104:1197–1201. https://doi.org/10.1017/S0953756200003026
Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071–1078. https://doi.org/10.1038/NATURE08122
Scheu S, Theenhaus A, Jones TH (1999) Links between the detritivore and the herbivore system: effects of earthworms and Collembola on plant growth and aphid development. Oecologia 1999 1194 119:541–551. https://doi.org/10.1007/S004420050817
Scheunemann N, Digel C, Scheu S, Butenschoen O (2015) Roots rather than shoot residues drive soil arthropod communities of arable fields. Oecologia 179:1135–1145. https://doi.org/10.1007/S00442-015-3415-2
Schütz K, Bonkowski M, Scheu S (2008) Effects of Collembola and fertilizers on plant performance (Triticum aestivum) and aphid reproduction (Rhopalosiphum padi). Basic Appl Ecol 9:182–188. https://doi.org/10.1016/J.BAAE.2006.07.003
Seastedt TR (1984) The role of microarthropods in decomposition and mineralization processes. Annu Rev Entomol 25–46
Soong JL, Nielsen UN (2016) The role of microarthropods in emerging models of soil organic matter. Soil Biol Biochem 102:37–39. https://doi.org/10.1016/j.soilbio.2016.06.020
Soong JL, Vandegehuchte ML, Horton AJ, Nielsen UN, Denef K, Shaw EA, de Tomasel CM, Parton W, Wall DH, Cotrufo MF (2016) Soil microarthropods support ecosystem productivity and soil Caccrual: evidence from a litter decomposition study in the tallgrass prairie. Soil Biol Biochem 92:230–238. https://doi.org/10.1016/j.soilbio.2015.10.014
Stoeckeler JH, Kluender WA (1938) The hydraulic method of excavating the root systems of plants. Ecology 19:355–369. https://doi.org/10.2307/1930591
Tebbe CC, Czarnetzki AB, Thimm T (2006) Collembola as habitat for microorganisms. Soil Biology, 6th edn. Springer-Verlag, Berlin/Heidelberg, pp 133–149
Thakur MP, Eisenhauer N (2015) Plant community composition determines the strength of top-down control in a soil food web motif. Sci Rep 5. https://doi.org/10.1038/srep09134
Treseder KK (2013) The extent of mycorrhizal colonization of roots and its influence on plant growth and phosphorus content. Plant Soil 371:1–13. https://doi.org/10.1007/S11104-013-1681-5/FIGURES/4
Ulber B (1978) Zur Frage der Schädlichkeit subterraner Collembolen in Zuckerrübenbeständen / On the noxiousness of subterranean Collembola in sugar beet. J Plant Dis Prot 85(10):594–606. https://www.jstor.org/stable/43214444?seq=2#metadata_info_tab_contents
Ulber B (1980) Untersuchungen zur Nahrungswahl von Onychiurus fimatus Gisin (Onychiuridae, Collembola), einem Aufgangsschädling der Zuckerrübe. Z für Angew Entomol 90:333–346. https://doi.org/10.1111/J.1439-0418.1980.TB03536.X
Verhoef HA, Brussaard L (1990) Decomposition and nitrogen mineralization in natural and agroecosystems: the contribution of soil animals. Biogeochemistry 11:175–211. https://doi.org/10.1007/BF00004496
Visser S, Parkinson D, Hassall M (1987) Fungi associated with Onychiurus subtenuis (Collembola) in an aspen woodland. Can J Bot 65:635–642. https://doi.org/10.1139/b87-083
Wagg C, Bender SF, Widmer F, Van Der Heijden MGA (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci U S A 5266–5270. https://doi.org/10.1073/pnas.1320054111
Wall DH, Behan-Pelletier V, Jones TH et al (2012) Soil ecology and ecosystem services. OUP Oxford, Oxford
Wardle DA, Bardgett RD, Klironomos JN et al (2004) Ecological linkages between aboveground and belowground biota on JSTOR. Sci (80-) 304:1629–1633
Warnock AJ, Fitter AH, Usher MB (1982) The influence of a springtail Folsomia candida (Insecta, Collembola) on the mycorrhizal association of leek Allium porrum and the vesicular-arbuscular mycorrhizal endophyte Glomus fasciculatus. New Phytol 90:285–292. https://doi.org/10.1111/J.1469-8137.1982.TB03260.X
Weaver J (1919) The ecological relations of roots. Carnegie Institution of Washington, Washington DC
Weih M, Asplund L, Bergkvist G (2011) Assessment of nutrient use in annual and perennial crops: A functional concept for analyzing nitrogen use efficiency. Plant Soil 339:513–520. https://doi.org/10.1007/S11104-010-0599-4/TABLES/2
Wickings K, Grandy AS (2011) The oribatid mite Scheloribates moestus (Acari: Oribatida) alters litter chemistry and nutrient cycling during decomposition. Soil Biol Biochem 43:351–358. https://doi.org/10.1016/j.soilbio.2010.10.023
Winck BR, Chauvat M, Coulibaly SFM, Santonja M, Saccol de Sá EL, Forey E (2020) Functional collembolan assemblages induce different plant responses in Lolium perenne. Plant Soil 452(1–2):347–358. https://doi.org/10.1007/s11104-020-04579-0
Wu T, Su F, Han H et al (2014) Responses of soil microarthropods to warming and increased precipitation in a semiarid temperate steppe. Appl Soil Ecol 84:200–207. https://doi.org/10.1016/j.apsoil.2014.07.003
Wurst S (2013) Plant-mediated links between detritivores and aboveground herbivores. Front Plant Sci. https://doi.org/10.3389/fpls.2013.00380
Zhang P, Zhang W, Hu S(2022) Fungivorous nematode Aphelenchus avenae and collembola Hypogastrura perplexa alleviate damping-off disease caused by Pythium ultimum in tomato. Plant Soil 1–15. https://doi.org/10.1007/S11104-022-05680-2/FIGURES/6
Zhang Y, Lavallee JM, Robertson AD et al (2021) Simulating measurable ecosystem carbon and nitrogen dynamics with the mechanistically defined MEMS 2.0 model. Biogeosciences 18:3147–3171. https://doi.org/10.5194/BG-18-3147-2021
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The authors would like to thank Dr. Thomas Björkman for his review of this manuscript prior to submission.
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Ashley Jernigan conducted the literature search and wrote the first draft of the manuscript. Kyle Wickings critically revised the work. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Jernigan, A., Kao-Kniffin, J., Pethybridge, S. et al. Soil microarthropod effects on plant growth and development. Plant Soil 483, 27–45 (2023). https://doi.org/10.1007/s11104-022-05766-x
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DOI: https://doi.org/10.1007/s11104-022-05766-x