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Effects of epigeic earthworm (Eisenia fetida) and arbuscular mycorrhizal fungus (Glomus intraradices) on enzyme activities of a sterilized soil–sand mixture and nutrient uptake by maize

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Abstract

A pot experiment was conducted to investigate the effect of epigeic earthworm (Eisenia fetida) and arbuscular mycorrhizal (AM) fungi (Glomus intraradices) on soil enzyme activities and nutrient uptake by maize, which was grown on a mixture of sterilized soil and sand. Maize plants were grown in pots inoculated or not inoculated with AMF, treated or not treated with earthworms. Wheat straw was added as a feed source for earthworms. Mycorrhizal colonization of maize was markedly increased in AM fungi inoculated pots and further increased by addition of epigeic earthworms. AM fungi and epigeic earthworms increased maize shoot and root biomass, respectively. Soil acid phosphatase activity was increased by both earthworms and mycorrhiza, while urease and cellulase activities were only affected by earthworms. Inoculation with AM fungi significantly (p < 0.001) increased the activity of soil acid phosphatase but decreased soil available phosphorus (P) and potassium (K) concentrations at harvest. Addition of earthworms alone significantly (p < 0.05) increased soil ammonium-N content, but decreased soil available P and K contents. AM fungi increased maize shoot weight and root P content, while earthworms improved N, P, and K contents in shoots. AM fungi and earthworm interactively increased maize shoot and root biomass through their regulation of soil enzyme activities and on the content of available soil N, P, and K.

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References

  • Aira M, Monroy F, Domínguez J (2005) Ageing effects on nitrogen dynamics and enzyme activities in casts of Apprrectodea caliginosa (Lumbricidae). Pedobiologia 49:467–473

    Article  CAS  Google Scholar 

  • Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10

    Article  PubMed  CAS  Google Scholar 

  • Axmann H, Sebastianelli A, Arrillaga JL (1990) Sample preparation techniques of biological material for isotope analysis. In: Hardarson G (ed) Use of nuclear techniques in studies of soil–plant relationship. International Atomic Energy Agency, Viena, pp 41–53

    Google Scholar 

  • Azcón R, Azcon-Aguilar C, Barea JM (1978) Effect of plant hormones present in bacterial cultures on the formation and responses to VA endomycorrhiza. New Phytol 80:359–364

    Article  Google Scholar 

  • Bago B, PfefferP E, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:924–957

    Article  Google Scholar 

  • Bardgett RD (2005) The biology of soil: a community and ecosystem approach. Oxford University Press, Oxford, 69–85

  • Calvet C, Pera J, Barea JM (1993) Growth response of marigold (Tagetes erecta L.) to inoculation with Glomus mosseae, Trichoderma aureoviridae and Pythium ultimum in a peat–perlite mixture. Plant Soil 148:1–6

    Article  Google Scholar 

  • Caravaca F, Alguacil MM, Figueroa D, Barea JM, Roldan A (2003) Re-establishment of Retama sphaerocarpa as a target species for reclamation of soil physical and biological properties in a semi-arid Mediterranean area. Forest Ecol Manage 182:49–58

    Article  Google Scholar 

  • Caravaca F, Alguacil MM, Azcón R, Díaz G, Roldán A (2004) Comparing the effectiveness of mycorrhizal inoculation and amendment with sugar beet, rock phosphate and Aspergillus niger to enhance field performance of the leguminous shrub Dorycnium pentaphyllum L. Appl Soil Ecol 25:169–180

    Article  Google Scholar 

  • Cheng J-M, Yu X-Z, Wong M-H (2005) Roles of earthworm–mycorrhiza interactions on phytoremediation of Cd contaminated soil. Aata Ecologica Sinica 25:1256–1263

    CAS  Google Scholar 

  • Cheng J-M, Yu X-Z, Wong M-H (2006) Effect of earthworm–mycorrhiza interaction on available nutrients and ryegrass growth in Cd contaminated soil. J Agro-Environ Sci 25:685–689

    CAS  Google Scholar 

  • Dilly O, Irmler U (1998) Succession in the food web during the decomposition of leaf litter in a black alder (Alnus glutinosa (Gaertn.) L.) forest. Pedobioligia 42:109–123

    Google Scholar 

  • Don A, Steinberg B, Schöning I, Pritsch K, Joschko M, Gleixner G, Schulze E-D (2008) Organic carbon sequestration in earthworm burrows. Soil Biol Biochem 40:1803–1812

    Article  CAS  Google Scholar 

  • Edwards CA (2004) Earthworm ecology. CRC, Boca Raton, p 441

    Book  Google Scholar 

  • Edwards CA, Fletcher KE (1988) Interactions between earthworms and micro-organisms in organic-matter breakdown. Agr Ecosyst Environ 24:235–247

    Article  Google Scholar 

  • Eisenhauer N, Scheu S (2008) Earthworms as drivers of the competition between grasses and legumes. Soil Biol Biochem 40:2650–2659

    Article  CAS  Google Scholar 

  • Eisenhauer N, Stephan K, Alexander CWS, Renker C, Buscot F, Scheu S (2009) Impacts of earthworms and arbuscular mycorrhizal fungi (Glomus intraradices) on plant performance are not interrelated. Soil Biol Biochem 3:561–567

    Article  Google Scholar 

  • Gormsen D, Olsson PA, Hedlund K (2004) The influence of collembolans and earthworms on AM fungal. Appl Soil Ecol 27:211–220

    Article  Google Scholar 

  • Gryndler M, Hrselova H, Cajthaml T, Havrankova M, Rezacova V, Gryndlerova H, Larsen J (2009) Influence of soil organic matter decomposition on arbuscular mycorrhizal fungi in terms of asymbiotic hyphal growth and root colonization. Mycorrhiza 19:255–266

    Article  PubMed  Google Scholar 

  • Hayman DS, Tavares M (1985) Plant growth responses to vesicular-arbuscular mycorrhiza. XV. Influence of soil pH on the symbiotic efficiency of different endophytes. New Phytol 100:367–377

    Article  Google Scholar 

  • He X-L, Li Y-P, Zhao L-L (2010) Dynamics of arbuscular mycorrhizal fungi and glomalin in the rhizosphere of Artemisia ordosica Krasch. in Mu Us Sandland, China. Soil Biol Biochem 42:1313–1319

    Article  CAS  Google Scholar 

  • Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots. New Phytol 120:371–380

    Article  CAS  Google Scholar 

  • Jeffries P, Gianinazz S, Perotto S, Turnau K, Barea JM (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fert Soils 37:1–16

    Google Scholar 

  • Jones JJ, Case VW (1990) Sampling, handling, and analyzing plant tissue samples. Samples. In: Westerman R (ed) Soil testing and plant analysis, vol 3, SSSA Book Series. Soil Science Society of America, Madison, pp 389–427

    Google Scholar 

  • Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils 6:68–72

    Article  CAS  Google Scholar 

  • Keeney DR, Nelson DW (1982) Nitrogen-inorganic forms. In: Page AL (ed) Methods of soil analysis. Part 1, vol 9, 2nd edn, Agron. Monogr. ASA and SSSA, Madison, pp 643–698

    Google Scholar 

  • Laossi KR, Ginot A, Noguera DC, Blouin M, Barot S (2010) Earthworm effects on plant growth do not necessarily decrease with soil fertility. Plant Soil 328:109–118

    Article  CAS  Google Scholar 

  • Lavelle PI (1988) Earthworm activities and the soil system. Biol Fertil Soils 6:237–251

    Article  Google Scholar 

  • Li H, Li X-L, Dou Z-X, Zhang J-L, Wang C (2012) Earthworm (Aporrectodea trapezoides)–mycorrhiza (Glomus intraradices) interaction and nitrogen and phosphorus uptake by maize. Biol Fertil Soils 48:75–85

    Google Scholar 

  • Ma Y, Dickinson NM, Wong M-H (2006) Beneficial effect of earthworms and arbuscular mycorrhizal fungi on establishment of leguminous trees on Pb/Zn mine tailings. Soil Biol Biochem 38:1403–1412

    Article  CAS  Google Scholar 

  • Mandels M, Andreotti R, Roche C (1976) Measurement of saccharifying cellulase. Biotechnol Bioeng 6:21–34

    CAS  Google Scholar 

  • Mar Vázquez M, César S, Azcón R, Barea JM (2000) Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Appl Soil Ecol 15:261–272

    Article  Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective-measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • McLatchey GP, Reddy KR (1998) Regulation of organic matter decomposition and nutrient release in a wetland soil. J Environ Qual 27:1268–1274

    Article  CAS  Google Scholar 

  • Metson AJ (1956) Methods of chemical analysis for soil survey samples. NZ Soil Bureau Bull. No. 12

  • Miller GL (1969) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428

    Article  Google Scholar 

  • Milleret R, Renée-Claire LB, Jean-Michel G (2009) Root, mycorrhiza and earthworm interactions: their effects on soil structuring processes, plant and soil nutrient concentrations and plant biomass. Plant Soil 316:1–12

    Article  CAS  Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for determination of phosphate in natural waters. Anal Chim Acta 27:31–36

    Article  CAS  Google Scholar 

  • Nannipieri P, Kandeler E, Ruggiero P (2002) Enzyme activities and microbiological and biochemical processes in soil. In: Burns RG, Dick RP (eds) Enzymes in the environment. Activity, ecology and applications. Marcel Dekker, New York, pp 1–33

    Google Scholar 

  • Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670

    Article  Google Scholar 

  • Newman EI (1966) A method of estimating total length of root in a sample. J Appl Ecol 3:139–145

    Article  Google Scholar 

  • Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorous in soils by extraction with sodium bicarbonate. USDA Circular 939:1–8

    Google Scholar 

  • Ortiz-Ceballos AI, Pena-Cabriales JJ, Fragoso C, Brown GG (2007) Mycorrhizal colonization and nitrogen uptake by maize: combined effect of tropical earthworms and velvetbean mulch. Biol Fert Soils 44:181–186

    Article  Google Scholar 

  • Parthasarathi K, Ranganathan LS (2000) Aging effect on enzyme activities in pressmud vermicasts of Lampito mauritii (Kinberg) and Eudrilus eugeniae (Kinberg). Biol Fertil Soils 30:347–350

    Article  CAS  Google Scholar 

  • Partsch S, Milcu A, Scheu S (2006) Decomposers (Lumbricidae, Collembola) affect plant performance in model grasslands of different diversity. Ecology 87:2548–2558

    Article  PubMed  Google Scholar 

  • Pattinson GS, Smith SE, Doube BM (1997) Earthworm Aporrectodea trapezoides had no effect on the dispersal of a vesicular-arbuscular mycorrhizal fungi, Glomus intraradices. Soil Biol Biochem 29:1079–1088

    Article  CAS  Google Scholar 

  • Römbke J, Jänsch S, Didden W (2005) The use of earthworms in ecological soil classification and assessment concepts. Ecotoxicol Environ Saf 62:266–277

    Article  PubMed  Google Scholar 

  • Scheu S (1987) The role of substrate feeding earthworms (Lumbricidae) for bioturbation in a beechwood soil. Oecologia 72:192–196

    Article  Google Scholar 

  • Scheu S (2003) Effects of earthworms on plant growth: patterns and perspectives. Pedobiologia 47:846–856

    Google Scholar 

  • Six J, Feller C, Denef K, Ogle SM, Sa JCD, Albrecht A (2002) Soil organic matter, biota and aggregation in temperate and tropical soils-effects of no-tillage. Agronomie 22:755–775

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, San Diego, 1–20

  • Tabatabai MA (1982) Soil enzymes. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, part 2. American Society of Agronomy, Madison, pp 903–947

    Google Scholar 

  • Tao J, Griffiths B, Zhang S, Chen X, Liu M, Hu F, Li H-X (2009) Effects of earthworms on soil enzyme activity in an organic residue amended rice–wheat rotation agro-ecosystem. Appl Soil Ecol 42:221–226

    Article  Google Scholar 

  • Tiwari SC, Tiwari BK, Mishra RR (1989) Microbial populations, enzyme activities and nitrogen–phosphorus–potassium enrichment in earthworm casts and in the surrounding soil of a pineapple plantation. Biol Fertil Soils 8:178–182

    Article  Google Scholar 

  • Tuffen F, Eason WR, Scullion J (2002) The effect of earthworms and arbuscular mycorrhizal fungi on growth of and 32P transfer between Allium porrum plants. Soil Biol Biochem 34:1027–1036

    Article  CAS  Google Scholar 

  • Walkley A (1947) A critical examination of a rapid method for determining organic carbon in soils: effect of variations in digestion conditions and of inorganic soil constituents. Soil Sci 63:251–264

    Article  CAS  Google Scholar 

  • Wang F-Y, Lin X-G, Yi R, Wu L-H (2006) Effects of arbuscular mycorrhizal inoculation on the growth of Elsholtzia splendens and Zea mays and the activities of phosphatase and urease in a multi-metal-contaminated soil under unsterilized conditions. Appl Soil Ecol 31:110–119

    Article  Google Scholar 

  • Wang M-Y, Xia R-X, Wu Q-S, Liu J-H, Hu L-M (2007) Influence of arbuscular mycorrhizal fungi on microbes and enzymes of soils from different cultivated densities of red clover. Ann Microbiol 57:1–7

    Article  CAS  Google Scholar 

  • Welke SE, Parkinson D (2003) Effect of Aporrectodea trapezoides activity on seedling growth of Pseudotsuga menziesii, nutrient dynamics and microbial activity in different soils. Forest Ecol Manag 173:169–186

    Article  Google Scholar 

  • Wurst S, Dugassa-Gobena D, Langel R, Bonkoski M, Scheu S (2004) Combined effects of earthworms and vesicular–arbuscular mycorrhizas on plant and aphid performance. New Phytol 163:169–176

    Article  Google Scholar 

  • Wurst S, Gebhardt K, Rillig MC (2010) Independent effects of arbuscular mycorrhiza and earthworms on plant diversity and newcomer plant establishment. J Veg Sci 22:1021–1030

    Article  Google Scholar 

  • Zarea MJ, Ghalavand A, Goltapeh EM (2009) Effects of mixed cropping, earthworms (Pheretima sp.), and arbuscular mycorrhizal fungi (Glomus mosseae) on plant yield, mycorrhizal colonization rate, soil microbial biomass, and nitrogenase activity of free-living rhizosphere bacteria. Pedobiologia 4:223–235

    Article  Google Scholar 

  • Zhang B-G, Li G-T, Shen T-S, Wang J-K, Sun Z (2000) Changes in microbial biomass C, N, and P and enzyme activities in soil incubated with the earthworms Metaphire guillelmi or Eisenia fetida. Soil Biol Biochem 32:2055–2062

    Article  CAS  Google Scholar 

  • Zhang L, Zhang J, Christie P, Li X (2008) Pre-inoculation with arbuscular mycorrhizal fungi suppresses root knot nematode (Meloidogyne incognita) on cucumber (Cucumis sativus). Biol Fertil Soils 45:205–211

    Article  CAS  Google Scholar 

  • Zhang H, Wu X, Li G, Qin P (2011) Interactions between arbuscular mycorrhizal fungi and phosphate-solubilizing fungus (Mortierella sp.) and their effects on Kostelelzkya virginica growth and enzyme activities of rhizosphere and bulk soils at different salinities. Biol Fertil Soils 47:543–554

    Article  CAS  Google Scholar 

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Acknowledgments

We are grateful to Dr. Zhiguo Wu from University of Pennsylvania for comments on the manuscript. This work was funded by the Special Scientific Fund for Non-profit Public Industry (MOA, 201103003), National Natural Science Foundation of China (Project 31172037), Innovative Group Grant of NSFC (31121062), and Scientific Research Foundation at China Agricultural University (Project 2010JS112).

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Correspondence to Chong Wang.

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Dan Xiang contributed equally.

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Li, H., Xiang, D., Wang, C. et al. Effects of epigeic earthworm (Eisenia fetida) and arbuscular mycorrhizal fungus (Glomus intraradices) on enzyme activities of a sterilized soil–sand mixture and nutrient uptake by maize. Biol Fertil Soils 48, 879–887 (2012). https://doi.org/10.1007/s00374-012-0679-0

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