Skip to main content
SpringerLink
Log in

Depth distribution of soil organic matter and burrowing activity of earthworms—mesocosm study using X-ray tomography and luminophores

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

Abstract

Earthworms feed on organic matter present at the soil surface or within the soil. Thus, its distribution in the soil profile is likely to greatly influence earthworm behavior and, in turn, their burrow system. To test this idea, two anecic and two endogeic earthworm species were introduced into repacked soil cores (depth = 30 cm) upper half filled with a top soil containing 4% organic matter (0–15 cm) and lower half filled with a deep soil at 2% organic matter (15–30 cm). Earthworm behavior was studied using X-ray tomography combined with luminophores (colored particulate tracers of 63–125 μm size) placed at 0, 3, and 12 cm depth, a method widely used in sediment ecology. We observed that anecic and endogeic earthworms had contrasting reactions to the conditions with only endogeic species burrowing more intensively in the upper part. From a quantitative point of view, only a few percent of luminophores were displaced. However, luminophore displacements also provided qualitative information to complement the tomography: (i) endogeic species and especially Aporrectodea caliginosa bioturbated the most soil close to the surface (3 cm depth) and (ii) the two anecic species influenced the luminophore distribution differentially with Lumbricus terrestris displacing significantly more luminophores, whatever their initial depth, than Aporrectodea nocturna due to intense surface cast activity. Beyond methodological developments, our study found that endogeic earthworms burrow more in zones with higher organic matter contents and this explains why they are mainly found close to the soil surface in non-tilled soils.

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

Similar content being viewed by others

References

  • Anschutz P, Ciutat A, Lecroart P, Gérino M, Boudou A (2012) Bioturbation effects by tubificids worms on freshwater sediment biogeochemistry. Aquatic Geochemistry 18:475–497

    Article  CAS  Google Scholar 

  • Auclerc A, Capowiez Y, Guérold F, Nahmani J (2013) Application of X-ray tomography to evaluate liming impact on earthworm burrowing activity in an acidic forest soil under laboratory conditions. Geoderma 202-203:45–50

  • Bastardie F, Capowiez Y, Renault P, Cluzeau D (2005a) A radio-labelled study of earthworm behaviour in artificial soil cores in term of ecological types. Biol Fertil Soils 41:320–327

    Article  Google Scholar 

  • Bastardie F, Capowiez Y, Cluzeau D (2005b) 3D characterization of earthworm burrow systems in natural soil cores collected in a 12-year-old pasture. Appl Soil Ecol 30:34–46

    Article  Google Scholar 

  • Bernier N (1998) Earthworm feeding activity and the development of the humus profile. Biol Fertil Soils 26:215–223

    Article  Google Scholar 

  • Black KS, Athey S, Wilson P, Evans D (2007) The use of particle tracking in sediment transport studies: a review. J Geol Soc 274:73–91

    Google Scholar 

  • Bottinelli N, Zhou H, Capowiez Y, Zhang ZB, Qiu J, Jouquet P, Peng XH (2017) Earthworm burrowing activity of two non-Lumbricidae earthworm species incubated in soils with contrasting carbon content (Vertisol vs. Ultisol) Biol Fertil Soils 53:951-955

  • Bottinelli N, Hedde M, Jouquet P, Capowiez Y (2020) An explicit definition of earthworm ecological categories - Marcel Bouché’s triangle revisited. Geoderma 372:114361

    Article  Google Scholar 

  • Bouché MB (1972) Lombriciens de France. Ecologie et systématique, INRA, Paris

    Google Scholar 

  • Bouché MB (1977) Stratégies lombriciennes. Ecol Bull 22:122–132

    Google Scholar 

  • Boudreau BP (1986) Mathematics of tracer mixing in sediments 1. Spatially dependent, diffusive mixing. Am J Sci 286:1161–1198

    Article  Google Scholar 

  • Capowiez Y, Monestiez P, Belzunces L (2001) Burrow systems made by Aporrectodea nocturna and Allolobophora chlorotica in artificial cores: morphological differences and effects of interspecific interactions. Appl Soil Ecol 16:109–120

    Article  Google Scholar 

  • Capowiez Y, Sammartino S, Michel E (2011) Using X-ray tomography to quantify earthworm bioturbation non-destructively in repacked soil cores. Geoderma 162:124–131

    Article  Google Scholar 

  • Capowiez Y, Bottinelli N, Sammartino S, Michel E, Jouquet P (2015) Morphological and functional characterization of the burrow system of sin earthworm species (Lumbricidae). Biol Fertil Soils 51:869–877

    Article  Google Scholar 

  • Cook SMF, Linden DR (1996) Effect of food type and placement on earthworm (Aporrectodea tuberculata) burrowing and soil turnover. Biol Fertil Soils 21:201–206

    Article  Google Scholar 

  • Duport E, Stora G, Tremblay P, Gilbert F (2006) Effects of population density on the sediment mixing induced by the gallery-diffusor Hediste (Nereis) diversicolor O.F. Müller, 1776. J Exp Mar Biol Ecol 336:33–41

    Article  Google Scholar 

  • Foulquier A, Simon L, Gilbert F, Fourel F, Malard F, Mermillod-Blondin F (2010) Relative influences of DOC flux and subterranean fauna on microbial abundance and activity in aquifer sediments: new insights from 13C-tracer experiments? Freshwater Biol 55:1560–1576

    Article  CAS  Google Scholar 

  • Francis GS, Fraser PM (1998) The effects of three earthworm species on soil microporosity and hydraulic conductivity. Appl Soil Ecol 10:11–19

    Article  Google Scholar 

  • François F, Gérino M, Stora G, Durbec J-P, Poggiale J-C (2002) Functional approach to sediment reworking by gallery-forming macrobenthic organisms: modelling and application with the polychaete Nereis diversicolor. Mar Ecol Prog Ser 229:127–136

    Article  Google Scholar 

  • Frazao J, de Goede RGM, Capowiez Y, Pulleman MM (2019) Soil structure formation and organic matter distribution as affected by earthworm species interaction and crop residues placement. Geoderma 338:453–463

    Article  Google Scholar 

  • Gerard BM (1967) Factors affecting earthworms in pasture. Animal Ecology 36:235–252

    Article  Google Scholar 

  • Gérino M, Aller RC, Lee C, Cochran JK, Aller JY, Green MA, Hirschberg D (1998) Comparison of different tracers and methods used to quantify bioturbation during a spring bloom: 234-Thorium, luminophores and chlorophylla. Estuar Coast Shelf Sci 46:531–547

    Article  Google Scholar 

  • Gérino M, Frignani M, Mugnai C, Bellucci LG, Prevedelli P, Valentini A, Castelli A, Delmotte S, Sauvage S (2007) Bioturbation quantification and related organisms in the Venice Lagoon. Acta Oecologica-Intern J Ecol 32:14–25

    Article  Google Scholar 

  • Gilbert F, Hulth S, Strömberg N, Ringdahl K, Poggiale JC (2003) 2-D optical quantification of particle reworking activities in surface marine sediments. J Exp Mar Biol Ecol 285(286):251–263

    Article  Google Scholar 

  • Gilbert F, Hulth S, Grossi V, Poggiale JC, Desrosiers G et al (2007) Sediment reworking by marine benthic species from the Gullmar Fjord (Western Sweden): importance of faunal biovolume. J Exp Mar Biol Ecol 348:133–144

    Article  Google Scholar 

  • Gutiérrez Y, Ott D, Töpperwien M, Salditt T, Sherber C (2018) X-ray computed tomography and its potential in ecological research: a review of studies and optimization of specimen. Ecol Evol 8:7717–7732

    Article  PubMed  PubMed Central  Google Scholar 

  • Hedman JE, Gunnarsson JS, Samuelsson G, Gilbert F (2011) Particle reworking and solute transport by the sediment-living polychaetes Marenzelleria neglecta and Hediste diversicolor. J Exp Mar Biol Ecol 407:294–301

    Article  CAS  Google Scholar 

  • Hughes MS, Bull CM, Doube BM (1996) Microcosm investigations into the influence of sheep manure on the behaviour of the geophagous earthworms Aporrectodea trapezoides and Microscolex dubius. Biol Fertil Soils 22:71–75

    Article  Google Scholar 

  • Jégou D, Cluzeau D, Wolf HJ, Gandon Y, Tréhen P (1998) Assessment of the burrow system of Lumbricus terrestris, Aporrectodea giardi and Aporrectodea caliginosa using X-ray computed tomography. Biol Fertil Soils 26:116–121

    Google Scholar 

  • Joschko M, Muller PC, Kotzke K, Dohring W, Larink O (1993) Earthworm burrow system-development assessed by means of X-ray computed tomography. Geoderma 56:209–221

  • Joyner JW, Harmon NP (1961) Burrows and oscillative behavior therein of Lumbricus terrestris. Proceedings of Indiana Academy of Science 71:378–384

    Google Scholar 

  • Kobel-Lamparski A, Lamparski F (1987) Burrow construction during the development of Lumbricus badensis individuals. Biol Fert Soils 3:125–129

    Google Scholar 

  • Kristensen E, Penha-Lopes G, Delefosse M, Valdemarsen T, Quintana CO, Banta G (2012) What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Mar Ecol Prog Ser 446:285–303

    Article  Google Scholar 

  • Lagauzère S, Coppin F, Gérino M, Delmotte S, Stora G, Bonzom JM (2011) An alternative method of particulate fluorescent tracer analysis in sediments using a microplate fluorimeter. Environ Technol 32:551–560

    Article  PubMed  Google Scholar 

  • Le Couteulx A, Wolf C, Hallaire V, Péres G (2015) Burrowing and casting activities of three endogeic earthworm species affected by organic matter location. Pedobiologia 58:97–103

    Article  Google Scholar 

  • Lee KE (1985) Earthworms. Their ecology and relationships with soil and land use. Academic Press, Sydney

    Google Scholar 

  • Leroy BLM, Schmidt O, Van den Bossche A, Reheul D, Moens M (2008) Earthworm population dynamics as influenced by the quality of exogenous organic matter. Pedobiologia 52:139–150

    Article  CAS  Google Scholar 

  • Ligthart TN, Peek GJCW (1997) Evolution of earthworm burrow systems after inoculation of lumbricid earthworms in a pasture in the Netherlands. Soil Biol Biochem 29:453–462

    Article  CAS  Google Scholar 

  • Lindqvist S, Gilbert F, Eriksson SP, Hulth S (2013) Activities by Hediste diversicolor during light and dark conditions: experimental quantification of particle reworking using time-resolved imaging. J Exp Mar Biol Ecol 448:240–249

    Article  Google Scholar 

  • Mahaut ML, Graf G (1987) A luminophore tracer technique for bioturbation studies. Oceanol Acta 10:323–328

    Google Scholar 

  • Maire O, Lecroart P, Meysman FJR, Rosenberg R, Duchene JC, Gremare A (2008) Methods of sediment reworking assessment in bioturbation research: a review. Aquatic Biology 2:219–238

    Article  Google Scholar 

  • McTavish MJ, Gorgolewski A, Murphy SD, Basiliko N (2019) Anecic earthworm (Lumbricus terrestris) facilitate the burial of surface-applied wood ash. Biol Fertil Soils 56:195–203

    Article  Google Scholar 

  • Mombo S, Laplanche C, Besson P, Sammartino S, Schreck E, Dumat C, Capowiez Y (2018) Metal soil pollution differentially affects both the behavior and exposure of A. caliginosa and L. terrestris: a mesocom. Biol Fertil Soils 54:319–328

    Article  CAS  Google Scholar 

  • Moreau-Valencogne P, Bertrand M, Holmstrup M, Roger-Estrade J (2013) Integration of thermal and hydrotime models to describe the development and growth of temperate earthworms. Soil Biol Biochem 63:50–60

    Article  Google Scholar 

  • Pelosi C, Grandeau G, Capowiez Y (2017) Temporal dynamics of earthworm-related microporosity in tilled and non-tilled cropping systems. Geoderma 289:169–177

    Article  Google Scholar 

  • Pierret A, Capowiez Y, Belzunces L, Moran CJ (2002) 3D reconstruction and quantification of micropores using X-ray computed tomography and image analysis. Geoderma 106:247–271

    Article  Google Scholar 

  • Rogasik H, Schrader S, Onasch I, Kiesel J, Gerke HH (2014) Micro-scale dry bulk density variation around earthworm (Lumbricus terrestris) burrows based on X-ray computed tomography. Geoderma 213:471–477

    Article  Google Scholar 

  • Rushton SP (1986) The effects of soil compaction on Lumbricus terrestris and its possible implications for populations on land reclaimed from open-cast coal mining. Pedobiologia 29:85–90

    Google Scholar 

  • Schmidt S, Jouanneau J-M, Weber O, Lecroart P, Radakovitch O, Gilbert F, Jezequel D (2007) Sediment dynamic at the water-sediment interface of the Thau Lagoon (South France): from seasonal to century time scales using radiogenic and cosmogenic nuclides. Estuar Coast Shelf Sci 72:534–542

    Article  Google Scholar 

  • Shipitalo MJ, Butt KR (1999) Occupancy and geometrical properties of Lumbricus terrestris burrows affecting infiltration. Pedobiologia 43:782–794

    Google Scholar 

  • Solan M, Wigham BD, Hudson IR, Kennedy R, Coulon CH et al (2004) In situ quantification of bioturbation using time-lapse fluorescent sediment profile imaging (f-SPI), luminophore tracers and model simulation. Mar Ecol Prog Ser 271:1–12

    Article  Google Scholar 

  • Springett J, Gray R (1997) The interaction between plant roots and earthworm burrows in pasture. Soil Biol Biochem 29:621–625

    Article  CAS  Google Scholar 

  • Taina IA, Heck RJ, Elliot TR (2013) Application of X-ray computed tomography to soil science: a literature review. Can J Soil Sci 88:1–20

    Article  Google Scholar 

  • Uvarov AV (2017) Density-mediated earthworm effects on soil respiration. Polish J Ecol 64:534–546

    Article  Google Scholar 

  • van Schaik L, Palm J, Klaus J, Zehe E, Schröder B (2014) Linking spatial earthworm distribution to macropore numbers and hydrological effectiveness Ecohydrology 7:401–408

    Google Scholar 

Download references

Acknowledgments

The authors thank Georges Stora who provided relevant ideas in the earlier preparation of the work.

Funding

This study was financially supported by the Institute of Radioprotection and Nuclear Safety (IRSN, France). This is Nereis Park contribution number 42.

Author information

Authors and Affiliations

  1. INRAE, UMR1114, Environment Méditerranéen et Modélisation des Agro-Hydrosystèmes, Site Agroparc, Avignon cedex 09, 84914, Paris, France

    Yvan Capowiez

  2. EcoLab, Université de Toulouse, CNRS, Toulouse, France

    Franck Gilbert

  3. Institut de Radioprotection et de Sûreté Nucléaire (IRSN), PSE-ENV/SRTE, Laboratoire de recherche sur les effets des radionuclide sur les écosystèmes (LECO), Cadarache, Bât. 183, BP 3, 13115, St Paul-lez-Durance, France

    Audrey Vallat & Jean-Marc Bonzom

  4. Aix-Marseille Université, Université de Toulon, CNRS, IRD, MIO UM 110, 13288, Marseille, France

    Jean-Christophe Poggiale

Authors
  1. Yvan Capowiez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Franck Gilbert
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Audrey Vallat
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jean-Christophe Poggiale
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jean-Marc Bonzom
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yvan Capowiez.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 1109 kb)

ESM 2

(PPTX 37 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Capowiez, Y., Gilbert, F., Vallat, A. et al. Depth distribution of soil organic matter and burrowing activity of earthworms—mesocosm study using X-ray tomography and luminophores. Biol Fertil Soils 57, 337–346 (2021). https://doi.org/10.1007/s00374-020-01536-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-020-01536-y

Keywords

Search

Navigation