Soil Oligochaeta communities after 9 decades of continuous fertilization in a bare fallow experiment
DOI:
https://doi.org/10.25674/so92iss2pp129Keywords:
Potworms, fertilizers, physico-chemical soil properties, long-term field experimentsAbstract
Mineral and organic fertilizers and amendments modify soil characteristics and impact beneficial soil organisms. However, conventional fertilizer experiments cannot separate impacts mediated through changes in crop productivity and through changes in soil chemical properties. We assessed populations of earthworms and enchytraeids (Oligochaeta, Annelida) in the surface horizons of a loess Luvisol of a world-unique long-term bare fallow experiment of INRAE (Versailles, France) to test the trophic and edaphic limits of existence for these soil taxa. Continuous annual applications since 1928 of 16 different treatments including nitrogen, phosphorus, potassium fertilizers but also basic (alkaline) and organic amendments, led to strongly diverging physical and chemical properties in the soil’s surface layer. The feeding activity of soil organisms was also assessed using the bait lamina method, assuming that lower bait consumption rates would be observed in treatments where fewer terrestrial Oligochaeta persist. We showed that compared to conventionally managed cultivated soils, both taxa were much less abundant in these extreme soil treatments, but enchytraeids were relatively more abundant than earthworms, ascribed to the enchytraeids’ higher tolerance to low pH soil conditions and a different feeding ecology. Most of the enchytraeid and earthworm individuals were found under horse manure inputs and basic amendments, suggesting that organic matter contents and/or pH would drive most of the Oligochaeta communities. Moreover, the bait-lamina feeding activity was significantly positively correlated with enchytraeid abundance. This study underlines the usefulness of historic long-term trials to improve knowledge on the ecology of soil organisms, and it presents an example of long-term soil biological resilience in highly degraded soils.
References
AFNOR (2004): Evaluation de la qualité des sols. 1. Méthodes d’analyse chimique. – AFNOR, Saint-Denis La Plaine, France.
Arrouays, D., J. Balesdent, J. C. Germon, P. A.Jayet, J.F. Soussana & P. Stengel (2002): Contribution à la lutte contre l’effet de serre, Stocker du carbone dans les sols agricoles de France? – Rapport d’expertise scientifique de l’INRA à la demande du Ministère de l’Ecologie et du Développement Durable, Editeurs scientifiques, 334p.
Barré, P., T. Eglin, B. T. Christensen, P. Ciais, S. Houot, T. Kätterer, F. van Oort, P. Peylin, P. R. Poulton, V. Romanenkov & C. Chenu (2010): Quantifying and isolating stable soil organic carbon using long-term bare fallow experiments. – Biogeosciences 7: 3839–3850.
Bart, S., C. Laurent, A. R. R. Péry, C. Mougin & C. Pelosi (2017): Differences in sensitivity between earthworms and enchytraeids exposed to two commercial fungicides. – Ecotoxicology and Environmental Safety 140: 177–184.
Briones M. J. I. & P. Ineson (2002): Use of C-14 carbon dating to determine feeding behaviour of enchytraeids. – Soil Biology & Biochemistry 34: 881–884.
Briones M. J. I., M. H. Garnett & T. G. Piearce (2005): Earthworm ecological groupings based on C-14 analysis. – Soil Biology & Biochemistry 37: 2145–2149.
Burgevin H. & S. Hénin (1939): Dix années d’expériences sur l’action des engrais sur la composition et les propriétés d’un sol de limon. – Annales Agronomiques 9: 771–799.
Čoja, T., K. Zehetner, A. Bruckner, A. Watzinger & E. Meyer (2008): Efficacy and side effects of five sampling methods for soil earthworms (Annelida, Lumbricidae). – Ecotoxicology and Environmental Safety 71: 552–565.
Curry, J. P. & O. Schmidt (2007): The feeding ecology of earthworms: A review. – Pedobiologia 50: 463–477.
Didden W.A.M. (1993): Ecology of terrestrial Enchytraeidae. – Pedobiologia 37: 2–29.
Didden, W. A. M., J. C. Y. Marinissen, M. J. Vreeken-Buijs, S. L. G. E. Burgers, R. de Fluiter, M. Geurs & L. Brussaard (1994): Soil meso- and macrofauna in two agricultural systems: factors affecting population dynamics and evaluation of their role in carbon and nitrogen dynamics. – Agriculture, Ecosystems & Environment 51: 171–186.
Doran, J. W. & T. B. Parkin (1996): Quantitative indicators of soil quality: a minimum data set. – In: Doran, J. W. & A. J. Jones (eds) Methods for Assessing Soil Quality. – SSSA, Inc., Madison, WI: 25–37.
Filzek, P. D., D. J. Spurgeon, G. Broll, C. Svendsen, P. K. Hankard, N. R. Parekh, H. E. Stubberud & J. M. Weeks (2004): Metal effects on soil invertebrate feeding: measurements using the bait lamina method. – Ecotoxicology 13: 807–816.
Frampton, G. K., S. Jänsch, J. J. Scott-Fordsmand, J. Römbke & P. J. Van den Brink (2006): Effects of pesticides on soil invertebrates in laboratory studies: A review and analysis using species sensitivity distributions. – Environmental Toxicology and Chemistry 25: 2480–2489.
Gajda, Ł., S. Gorgoń & A. Z. Urbisz (2017): Food preferences of enchytraeids. – Pedobiologia 63: 19–36.
Graefe, U. & R. M. Schmelz (1999): Indicator values, strategy types and life forms of terrestrial Enchytraeidae and other microannelids. – In: Schmelz, R. K. S. (ed.), Newsletter on Enchytraeidae 6. Universitätsverlag Rasch, Osnabrück:59–67.
Healy, B. (1980): Distribution of terrestrial Enchytraeidae in Ireland. – Pedobiologia 20: 159–175.
Helling, B., G. Pfeiff & O. Larink (1998): A comparison of feeding activity of collembolan and enchytraeid in laboratory studies using the bait-lamina test. – Applied Soil Ecology 7: 207–212.
Henneron, L., L. Bernard, M. Hedde, C. Pelosi, C. Villenave, C. Chenu, M. Bertrand, C. Girardin & E. Blanchart (2015): Fourteen years of evidence for positive effects of conservation agriculture and organic farming on soil life. – Agronomy for Sustainable Development 35: 169–181.
ISO (2014): ISO 18311 Soil quality: method for testing effects of soil contaminants on the feeding activity of soil dwelling organisms – Bait-lamina test. – International Organization for Standardization (ISO), Geneva.
ISO (2007): ISO 23611-3 Soil quality: sampling of soil invertebrates – Part 3: Sampling and soil extraction of enchytraeids. – International Organization for Standardization (ISO), Geneva.
Jänsch, S., J. Römbke & W. Didden (2005): The use of enchytraeids in ecological soil classification and assessment concepts. – Ecotoxicology and Environmental Safety 62: 266–277.
Jastrzebska, M., M. K. Kostrzewska & K. Treder (2020): Phosphorus fertilizers from sewage sludge ash and animal blood have no effect on earthworms. – Agronomy 10: 525 [https://doi.org/10.3390/agronomy10040525].
Jensen, J., P. H. Krogh & L. E. Sverdrup (2003): Effects of the antibacterial agents tiamulin, olanquindox and metronidazole and the anthelmintic ivermectin on the soil invertebrate species Folsomia fimetaria (Collembola) and Enchytraeus crypticus (Enchytraeidae). – Chemosphere 50: 437–443.
Kuperman, R. G., R. T. Checkai, M. V. B. Garcia, J. Römbke, G. L. Stephenson & J. P. Sousa (2009): State of the science and the way forward for the ecotoxicological assessment of contaminated land. – Pesquisa Agropecuária Brasileira 44: 811–824.
Lagerlöf, J., O. Andrén & K. Paustian (1989): Dynamics and contribution to carbon flows of Enchytraeidae (Oligochaeta) under four cropping systems. – Journal of Applied Ecology 26: 183–199.
Lal, R. (2015): Restoring soil quality to mitigate soil degradation. – Sustainability 7: 5875–5895 [https://doi.org/10.3390/su7055875].
Lalthanzara, H. & S. N. Ramanujam (2010): Effect of fertilizer (NPK) on earthworm population in the agro-forestry system of Mizoram India. – Science Vision 10: 159–167.
Larink, O. (1993): Bait lamina as a tool for testing feeding activity of animals in contaminated soils. – In: Donker, M. H., H. Eijsackers & F. Heimbach (eds): Ecotoxicology of Soil Organisms. – Lewis Publishers Inc, Boca Raton: 339–345.
Larsen, T., M. M. Pollierer, M. Holmstrup, A. D’Annibale, K. Maraldo, N. Andersen & J. Eriksen (2016): Substantial nutritional contribution of bacterial amino acids to earthworms and enchytraeids: A case study from organic grasslands. – Soil Biology & Biochemistry 99: 21–27.
Lee, K. E. (1985): Earthworms: Their ecology and relationships with soils and land use. – Academic Press, London: 411pp.
Leroy, B. L. M., O. Schmidt, A. Van den Bossche, D. Reheul & M. Moens (2008): Earthworm population dynamics as influenced by the quality of exogenous organic matter. – Pedobiologia 52: 139–150.
Liu, T., X. Chen, X. Gong, I. M. Lubbers, Y. Jiang, W. Feng, X. Li, J. K. Whalen, M. Bonkowski, B. S. Griffiths, F. Hu & M. Liu (2019): Earthworms coordinate soil biota to improve multiple ecosystem functions. – Current Biology 29: 3420–3429.
MacLean Jr, S. F. (1980): The detritus-based trophic system. – In: Brown, J., P. C. Miller, L. L. Tieszen & F. L. Bunnell (eds): An Arctic Ecosystem: the Coastal Tundra at Barrow, Alaska. Stroudsburg: US/IBP Synthesis Series 12. – Hutchinson and Ross, Dowden: 411–457.
Marhan, S. & S. Scheu (2005): The influence of mineral and organic fertilisers on the growth of the endogeic earthworm Octolasion tyrtaeum (Savigny). – Pedobiologia 49: 239–249.
Mazzei, P. & A. Piccolo (2015): Interactions between natural organic matter and organic pollutants as revealed by NMR spectroscopy. – Magnetic Resonance in Chemistry 53: 667–678.
Nowak, E. (2004): Enchytraeids (Oligochaeta) in the agricultural landscape. – Polish Journal of Ecology 52: 115–122.
O’Connor, F. B. (1962): The extraction of Enchytraeidae from soil. – In: Murphy, P.W. (ed.): Progress in Soil Zoology. Butterworths, London: 279–285.
Owojori, O.J., A.J. Reinecke, P. Voua-Otomo & S.A. Reinecke (2009): Comparative study of the effects of salinity on life-cycle parameters of four soil-dwelling species (Folsomia candida, Enchytraeus doerjesi, Eisenia fetida and Aporrectodea caliginosa). – Pedobiologia 52: 351–360.
Paoletti, M. G. (1999): The role of earthworms for assessment of sustainability and as bioindicators. – Agriculture, Ecosystems and Environment 74: 137–155.
Paradelo R., F. van Oort & C. Chenu (2013): Water dispersible clay in bare fallow soils after 80 years of continuous fertilizers addition. – Geoderma, 200/201: 40–44.
Parmelee, R. W., M. H. Beare, W. Cheng, E. F. Hendrix, S. J. Rider, Jr. D. A. Crossley & D. C. Coleman (1990): Earthworms and enchytraeids in conventional and no-tillage agroecosystems: A biocide approach to assess their role in organic matter breakdown. – Biology and Fertility of Soils 10: 1–10.
Paulus, R., J. Römbke, A. Ruf & L. Beck (1999): A comparison of the litterbag-, minicontainer- and bait-lamina-methods in an ecotoxicological field experiment with diflubenzuron and btk. – Pedobiologia 43: 120–133.
Pernes-Debuyser, A. & D. Tessier (2002): Influence de matières fertilisantes sur les propriétés des sols: cas des 42 parcelles de l’INRA à Versailles. – Etude et Gestion des Sols 9: 177–186.
R Development Core Team (2018): R: A Language and Environment for Statistical Computing. – Vienna, Austria: the R Foundation for Statistical Computing. ISBN: 3-900051-07-0. Available online at http://www.R-project.org/.
Ricci, F., L. Bentze, D. Montagne, S. Houot, M. Bertrand & C. Pelosi (2015): Positive effects of alternative cropping systems on terrestrial Oligochaeta (Clitellata, Annelida). – Soil Organisms 87: 71–83.
Riley, H., R. Pommeresche, R. Eltun, S. Hansen & A. Korsaeth (2008): Soil structure, organic matter and earthworm activity in a comparison of cropping systems with contrasting tillage, rotations, fertilizer levels and manure use. – Agriculture, Ecosystems & Environment 124: 275–284.
Römbke, J., S. Jänsch, H. Höfer, F. Horak, M. Roß-Nickoll, D. Russell, U. Burkhardt & A. Toschki (2013) State of knowledge of enchytraeid communities in German soils as a basis for biological soil quality assessment. – Soil Organisms 85: 123–146.
Schmelz, R. M. & R. Collado (2010): A guide to European terrestrial and freshwater species of Enchytraeida (Oligochaeta). – Soil Organisms 82: 1–176.
Schmidt O., J. P. Curry, J. Dyckmans, E. Rota & C. M. Scrimgeour (2004): Dual stable isotope analysis (δ13C and δ15N) of soil invertebrates and their food sources. – Pedobiologia 48: 171–180.
Schmidt O., J. Dyckmans & S. Schrader (2016): Photoautotrophic microorganisms as a carbon source for temperate soil invertebrates. – Biology Letters 12: 20150646 [https://doi.org/10.1098/rsbl.2015.0646].
Shtina E. A., L. S. Kozlovskaya & K. A. Nekrasova (1981): Relations of soil oligochaetes and algae. – Soviet Journal of Ecology 12: 44–48.
Simpson, J. E., E. Slade, T. Riutta & M. E. Taylor (2012): Factors affecting soil fauna feeding activity in a fragmented lowland temperate deciduous woodland. – PLoS ONE 7: e29616 [https://doi.org/10.1371/journal.pone.0029616].
Sims, R. W. & B. M. Gerard (1999): Earthworms. – FSC Publications, London.
Tisdall, J. M. & J. M. Oades (1982): Organic matter and water-stable aggregates in soils. – Journal of Soil Science 33: 141–163.
van der Wal, A., R. H. E. M. Geerts, H. Korevaar, A. J. Schouten, G. A. J. M. J. op Akkerhuis, M. Rutgers & C. Mulder (2009): Dissimilar response of plant and soil biota communities to long-term nutrient addition in grasslands. – Biology and Fertility of Soils 45: 663–667.
van Oort, F., R. Paradelo, N. Proix, G. Delarue, D. Baize & F. Monna (2018): Centennial fertilization-induced soil processes control trace metal dynamics. Lessons from a long-term bare fallow experiment. – Soil Systems 2: 23 [https://doi.org/10.3390/soilsystems2020023].
van Oort, F., R. Paradelo, F. Monna, C. Chenu, D. Baize, A. Guérin, S. Breuil, G. Delarue, J. C. Thoisy & N. Proix (2020): La collection historique d’échantillons de l’essai patrimonial des ‘42 parcelles’ (INRAE, Versailles): une machine à remonter le temps... – Etude et Gestion des Sols 27: 321–350.
van Vliet, P. C. J., L. T. West, P. F. Hendrix & D. C. Coleman (1993): The influence of Enchytraeidae (Oligochaeta) on the soil porosity of small microcosms. – In: Brussaard, L. & M. J. Kooistra (eds): Soil Structure/Soil Biota Interrelationships. – Elsevier, Amsterdam: 287–299.
von Törne, E. (1990): Assessing feeding activities of soil-living animals. 1. Bait-lamina-tests. – Pedobiologia 34: 89–101.
Wall, D. H. & R. A. Virginia (1999) Controls on soil biodiversity: insights from extreme environments. – Applied Soil Ecology 13: 137–150.
Wardle, D. A., R. D. Bardgett, J. N. Klironomos, H. Setala, W.H. van der Putten & D. H. Wall (2004): Ecological linkages between aboveground and belowground biota. – Science 304: 1629–1633.
Wood, S. A., D. Tirfessa & F. Baudron (2018): Soil organic matter underlies crop nutritional quality and productivity in smallholder agriculture. – Agriculture, Ecosystems & Environment 266: 100–108.
Zhang, H. & S. Schrader (1993): Earthworm effects on selected physical and chemical properties of soil aggregates. – Biology and Fertility of Soils 15: 229–234.
Downloads
Published
How to Cite
Issue
Section
License
All articles from Senckenberg’s SOIL ORGANISMS Open Access scientific journal that are made available on the Senckenberg website (www.senckenberg.de) and also www.soil-organisms.org may be read, copied, distributed, and (in limited quantity) printed for non-commercial, private, scientific purposes.
In accordance with the German Science Foundation’s „Rules for the Safeguarding of Good Scientific Practice“, references to cited articles are to be complete and correct and furnished with a link to the website of the Senckenberg journal in question.
The Senckenberg Society for Nature Research (Senckenberg Gesellschaft für Naturforschung, SGN) is a member of the Leibniz Association (Leibniz-Gemeinschaft) and is therefore committed to the idea of Open Access as explained in the Berlin Declaration (Berlin Declaration on Open Access to Scientific Knowledge, Berliner Erklärung über den offenen Zugang zu wissenschaftlichem Wissen).
Open Access is understood to mean the charge-exempt public access to scientific results via the internet. The users should be able to read, copy, print, search within, and reference the full text without limitation and to use it in any conceivable lawful manner without financial, legal or technical hindrance.
This applies also to the SGN, which publishes various scientific series. Some scientific journals are made available to the public via Open Acess in addition to printed copies.
