Skip to main content
SpringerLink
Log in

Effect of Collembola on mineralization of litter and soil organic matter

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

Although soil Collembola are known to contribute to soil carbon (C) cycling, their contribution to the mineralization of C sources that differ in bioavailability, such as soil organic C (SOC) and leaf litter, is unknown. Stable C isotopes are often used to quantify the effects of both soil C and litter C on C mineralization. Here, 13C-labeled litter was used to investigate the effects of Collembola (Folsomia candida) on the mineralization of both SOC and litter C in laboratory microcosms. The three microcosm treatments were soil alone (S); soil treated with δ13C-labeled litter (SL); and soil treated with δ13C-labeled litter and Collembola (SLC). The presence of Collembola did not significantly affect soil microbial biomass or litter mass loss and only had a small effect on CO2 release during the first week of the experiment, when most of the CO2 was derived from litter rather than from SOC. Later, during the experiment (days 21 and 63), when litter-derived labile C had been depleted and when numbers of Collembola had greatly increased, Collembola substantially increased the emission of SOC-derived CO2. These results suggest that the effect of Collembola on soil organic C mineralization is negatively related to C availability.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Addison JA, Trofymow JA, Marshall VG (2003) Functional role of Collembola in successional coastal temperate forests on Vancouver Island. Canada Appl Soil Ecol 24:247–261. doi:10.1016/S0929-1393(03)00089-1

    Article  Google Scholar 

  • Andren O, Schnurer J (1985) Barley straw decomposition with varied levels of microbial grazing by Folsomia-Fimetaria (L) (Collembola, Isotomidae). Oecologia 68:57–62. doi:10.1007/Bf00379474

    Article  CAS  PubMed  Google Scholar 

  • Aslam TJ, Benton TG, Nielsen UN, Johnson SN (2015) Impacts of eucalypt plantation management on soil faunal communities and nutrient bioavailability: trading function for dependence? Biol Fert Soils 51:637–644

    Article  Google Scholar 

  • Baath E (2003) The use of neutral lipid fatty acids to indicate the physiological conditions of soil fungi. Microbial Ecol 45:373–383. doi:10.1007/s00248-003-2002-y

    Article  CAS  Google Scholar 

  • Blair GJ, Lefroy RDB, Lise L (1995) Soil carbon fractions based on their degree of oxidation, and the development of a carbon management index for agricultural systems. Aust J Agric Res 46:1459–1466. doi:10.1071/Ar9951459

    Article  Google Scholar 

  • Blair GJ, Lefroy RDB, Singh BP, Till AR (1997) Development and use of a carbon management index to monitor changes in soil C pool size and turnover rate. In: Cadisch G, Giller KE (eds) Driven by nature: plant litter quality & decomposition. pp 273–282

  • Bossio DA, Scow KM (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microbial Ecol 35:265–278

    Article  CAS  Google Scholar 

  • Chahartaghi M, Langel R, Scheu S, Ruess L (2005) Feeding guilds in Collembola based on nitrogen stable isotope ratios. Soil Biol Biochem 37:1718–1725. doi:10.1016/j.soilbio.2005.02.006

    Article  CAS  Google Scholar 

  • Chamberlain PM, McNamara NP, Chaplow J, Stott AW, Black HIJ (2006) Translocation of surface litter carbon into soil by Collembola. Soil Biol Biochem 38:2655–2664. doi:10.1016/j.soilbio.2006.03.021

    Article  CAS  Google Scholar 

  • Chen JX, Ma ZC, Yan HJ, Zhang F (2007) Roles of springtails in soil ecosystem. Biodivers Sci 15:154–161. doi:10.1360/biodiv.060288

    Article  Google Scholar 

  • Coleman DC, Crossley DA, Hendrix PF (2004) Fundamentals of soil ecology (second edition)

  • Coulson JC, Whittaker JB (1978) Ecology of moorland animals. Springer, Berlin Heidelberg

    Book  Google Scholar 

  • Cragg RG, Bardgett RD (2001) How changes in soil faunal diversity and composition within a trophic group influence decomposition processes. Soil Biol Biochem 33:2073–2081. doi:10.1016/S0038-0717(01)00138-9

    Article  CAS  Google Scholar 

  • 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. doi:10.1016/j.soilbio.2009.02.022

    Article  CAS  Google Scholar 

  • Filser J (2002) The role of Collembola in carbon and nitrogen cycling in soil: proceedings of the Xth international colloquium on Apterygota, České Budějovice 2000: Apterygota at the beginning of the third millennium. Pedobiologia 46:234–245

    Google Scholar 

  • Fox O, Vetter S, Ekschmitt K, Wolters V (2006) Soil fauna modifies the recalcitrance-persistence relationship of soil carbon pools. Soil Biol Biochem 38:1353–1363. doi:10.1016/j.soilbio.2005.10.014

    Article  CAS  Google Scholar 

  • Frostegard A, Tunlid A, Baath E (2011) Use and misuse of PLFA measurements in soils. Soil Biol Biochem 43:1621–1625. doi:10.1016/j.soilbio.2010.11.021

    Article  CAS  Google Scholar 

  • Grogan DW, Cronan JE Jr (1997) Cyclopropane ring formation in membrane lipids of bacteria. Microbiol Mol Biol Rev 61:429–441

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gusewell S, Verhoeven JTA (2006) Litter N: P ratios indicate whether N or P limits the decomposability of graminoid leaf litter. Plant Soil 287:131–143. doi:10.1007/s11104-006-9050-2

    Article  Google Scholar 

  • Haubert D, Haggblom MM, Langel R, Scheu S, Ruess L (2006) Trophic shift of stable isotopes and fatty acids in Collembola on bacterial diets. Soil Biol Biochem 38:2004–2007. doi:10.1016/j.soilbio.2005.11.031

    Article  CAS  Google Scholar 

  • Huang WJ, Liu JX, Wang YP, Zhou GY, Han TF, Li Y (2013) Increasing phosphorus limitation along three successional forests in southern China. Plant Soil 364:181–191. doi:10.1007/s11104-012-1355-8

    Article  CAS  Google Scholar 

  • Huang JH, Zhang WX, Liu MY, Briones MJI, Eisenhauer N, Shao YH, Cai X, Fu SL, Xia HP (2015) Different impacts of native and exotic earthworms on rhizodeposit carbon sequestration in a subtropical soil. Soil Biol Biochem 90:152–160. doi:10.1016/j.soilbio.2015.08.011

    Article  CAS  Google Scholar 

  • Hunter MD, Adl S, Pringle CM, Coleman DC (2003) Relative effects of macroinvertebrates and habitat on the chemistry of litter during decomposition. Pedobiologia 47:101–115

    Article  CAS  Google Scholar 

  • Johnson D, Krsek M, Wellington EMH, Stott AW, Cole L, Bardgett RD, Read DJ, Leake JR (2005) Soil invertebrates disrupt carbon flow through fungal networks. Science 309:1047–1047. doi:10.1126/science.1114769

    Article  CAS  PubMed  Google Scholar 

  • Kaneda S, Kaneko N (2008) Collembolans feeding on soil affect carbon and nitrogen mineralization by their influence on microbial and nematode activities. Biol Fert Soils 44:435–442. doi:10.1007/s00374-007-0222-x

    Article  CAS  Google Scholar 

  • Kaneko N, McLean MA, Parkinson D (1998) Do mites and Collembola affect pine litter fungal biomass and microbial respiration? Appl Soil Ecol 9:209–213

    Article  Google Scholar 

  • Ke X, Winter K, Filser J (2005) Effects of soil mesofauna and farming management on decomposition of clover litter: a microcosm experiment. Soil Biol Biochem 37:731–738. doi:10.1016/j.soilbio.2004.10.005

    Article  CAS  Google Scholar 

  • Kuzyakov Y (2011) How to link soil C pools with CO2 fluxes? Biogeosciences 8:1523–1537

    Article  CAS  Google Scholar 

  • Lagerlöf J, Andrén O (1985) Succession and activity of microarthropods and enchytraeids during barley straw decomposition. Pedobiologia 28:343–357

    Google Scholar 

  • Lavelle P (1997) Faunal activities and soil processes: adaptive strategies that determine ecosystem function. Adv Ecol Res 27:93–132. doi:10.1016/S0065-2504(08)60007-0

    Article  Google Scholar 

  • Liu P, Sun OJ, Huang JH, Li LH, Han XG (2007) Nonadditive effects of litter mixtures on decomposition and correlation with initial litter N and P concentrations in grassland plant species of northern China. Biol Fert Soils 44:211–216. doi:10.1007/s00374-007-0195-9

    Article  Google Scholar 

  • Løkke H (1998) Handbook of soil invertebrate toxicity tests. John Wiley & Sons, Chichester

    Google Scholar 

  • Lussenhop J, BassiriRad H (2005) Collembola effects on plant mass and nitrogen acquisition by ash seedlings (Fraxinus pennsylvanica). Soil Biol Biochem 37:645–650. doi:10.1016/j.soilbio.2004.08.021

    Article  CAS  Google Scholar 

  • Marhan S, Langel R, Kandeler E, Scheu S (2007) Use of stable isotopes (13C) for studying the mobilisation of old soil organic carbon by endogeic earthworms (Lumbricidae). Eur J Soil Biol 43:S201–S208

    Article  CAS  Google Scholar 

  • Neher DA, Weicht TR, Barbercheck ME (2012) Linking invertebrate communities to decomposition rate and nitrogen availability in pine forest soils. Appl Soil Ecol 54:14–23. doi:10.1016/j.apsoil.2011.12.001

    Article  Google Scholar 

  • Pausch J, Kuzyakov Y (2012) Soil organic carbon decomposition from recently added and older sources estimated by δ13C values of CO2 and organic matter. Soil Biol Biochem 55:40–47

    Article  CAS  Google Scholar 

  • Persson T, Bååth E, Clarholm M, Lundkvist H, Söderström BE, Sohlenius B (1980) Trophic structure, biomass dynamic and carbon metabolism of soil organisms in a scots pine forest. Ecol Bull 32:419–459

    CAS  Google Scholar 

  • Petersen H (2002) General aspects of collembolan ecology at the turn of the millennium: proceedings of the Xth international colloquium on Apterygota, České Budějovice 2000: Apterygota at the beginning of the third millennium. Pedobiologia 46:246–260

    Google Scholar 

  • Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261–269. doi:10.1007/s00442-003-1218-3

    Article  PubMed  Google Scholar 

  • Pieper S, Weigmann G (2008) Interactions between isopods and collembolans modulate the mobilization and transport of nutrients from urban soils. Appl Soil Ecol 39:109–126. doi:10.1016/j.apsoil.2007.11.012

    Article  Google Scholar 

  • Ponge JF (2015) The soil as an ecosystem. Biol Fert Soils 51:645–648. doi:10.1007/s00374-015-1016-1

    Article  CAS  Google Scholar 

  • Rusek J (1998) Biodiversity of Collembola and their functional role in the ecosystem. Biodivers Conserv 7:1207–1219. doi:10.1023/A:1008887817883

    Article  Google Scholar 

  • Scheu S, Simmerling F (2004) Growth and reproduction of fungal feeding Collembola as affected by fungal species, melanin and mixed diets. Oecologia 139:347–353. doi:10.1007/s00442-004-1513-7

    Article  PubMed  Google Scholar 

  • Schlesinger WH, Lichter J (2001) Limited carbon storage in soil and litter of experimental forest plots under increased atmospheric CO2. Nature 411:466–469. doi:10.1038/35078060

    Article  CAS  PubMed  Google Scholar 

  • Seastedt TR (1984) The role of Microarthropods in decomposition and mineralization processes. Annu Rev Entomol 29:25–46. doi:10.1146/annurev.en.29.010184.000325

    Article  Google Scholar 

  • Seeber J, Scheu S, Meyer E (2006) Effects of macro-decomposers on litter decomposition and soil properties in alpine pastureland: a mesocosm experiment. Appl Soil Ecol 34:168–175. doi:10.1016/j.apsoil.2006.02.004

    Article  Google Scholar 

  • Teuben A (1991) Nutrient availability and interactions between soil arthropods and microorganisms during decomposition of coniferous litter—a Mesocosm study. Biol Fert Soils 10:256–266. doi:10.1007/Bf00337376

    Article  CAS  Google Scholar 

  • Vidal A, Remusat L, Watteau F, Derenne S, Quenea K (2016) Incorporation of 13C labelled shoot residues in Lumbricus terrestris casts: a combination of transmission electron microscopy and nanoscale secondary ion mass spectrometry. Soil Biol Biochem 93:8–16

    Article  CAS  Google Scholar 

  • Vidal A, Quenea K, Alexis M, Tu TTN, Mathieu J, Vaury V, Derenne S (2017) Fate of 13C labelled root and shoot residues in soil and anecic earthworm casts: a mesocosm experiment. Geoderma 285:9–18

    Article  CAS  Google Scholar 

  • Yang XD, Chen J (2009) Plant litter quality influences the contribution of soil fauna to litter decomposition in humid tropical forests, southwestern China. Soil Biol Biochem 41:910–918. doi:10.1016/j.soilbio.2008.12.028

    Article  CAS  Google Scholar 

  • Yang XD, Yang Z, Warren MW, Chen J (2012) Mechanical fragmentation enhances the contribution of Collembola to leaf litter decomposition. Eur J Soil Biol 53:23–31. doi:10.1016/j.ejsobi.2012.07.006

    Article  CAS  Google Scholar 

  • Zhang W, Hendrix PF, Dame LE, Burke RA, Wu J, Neher DA, Li J, Shao Y, Fu S (2013) Earthworms facilitate carbon sequestration through unequal amplification of carbon stabilization compared with mineralization. Nat Commun 4:324–327

    Article  Google Scholar 

Download references

Acknowledgements

The present study was supported by the National Natural Sciences Foundation of China (31270560, 41571247) and High Level University Construction Project of Guangdong Province (Regional Water Environment Safety and Water Ecological Protection).

Author information

Authors and Affiliations

  1. South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, 510650, China

    Min Wang & Hanping Xia

  2. Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, 430074, China

    Min Wang

  3. University of Chinese Academy of Sciences, Beijing, 100049, China

    Min Wang

  4. College of Environment and Planning, Henan University, Kaifeng, 475001, China

    Weixin Zhang

  5. Postdoctoral Scientific Research Stations, Chinese Academy of Agricultural Engineering, Beijing, 100125, China

    Jinhua Huang

  6. School of Geographical Sciences, Guangzhou University, Guangzhou, 510006, China

    Zhifeng Wu & Guoliang Xu

Authors
  1. Min Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Weixin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hanping Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jinhua Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhifeng Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Guoliang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Guoliang Xu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, M., Zhang, W., Xia, H. et al. Effect of Collembola on mineralization of litter and soil organic matter. Biol Fertil Soils 53, 563–571 (2017). https://doi.org/10.1007/s00374-017-1200-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-017-1200-6

Keywords

Search

Navigation