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Mycorrhizal colonization and nitrogen uptake by maize: combined effect of tropical earthworms and velvetbean mulch

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Abstract

Earthworms and mulch can have positive or negative effects on mycorrhizae (fungus-roots) and N uptake by plants. In the present experiment, maize plants were grown under greenhouse conditions with or without tropical earthworms (Balanteodrilus pearsei) and mulch of velvetbean (Mucuna pruriens var. utilis). The formation of vesicles and hyphae of arbuscular-mycorrhizal (AM) fungi in roots and N uptake by maize plants was measured at harvest. The addition of earthworms and velvetbean reduced AM root colonization. Earthworms had no effect on plant root or shoot biomass. In the absence of velvetbean, earthworms reduced AM colonization, but when velvetbean was present, this effect disappeared. The addition of velvetbean mulch, on the other hand, had an effect on plant biomass (above- and belowground) and a positive effect on AM fungal colonization of roots in presence of worms, but a negative effect when worms were absent. When both M. pruriens and B. pearsei were added, shoot and root biomass and N concentrations increased. Vesicle formation was related to velvetbean mulch decomposition as well as the higher N concentration in maize roots. Management of mulch–earthworm interactions may be of value, particularly in low-input and organic agricultural systems, and deserves further investigation.

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References

  • Alphei J, Bonkoswski M, Scheu S (1996) Protozoa, Nematoda and Lumbricidae in the rhizosphere of Hordelymus europaeus (Poaceae): faunal interactions, response of microorganisms and effects on plant growth. Oecologia 106:111–126

    Google Scholar 

  • Anderson JM, Ingram JSI (1993) Tropical soil biology and fertility: a handbook of methods, 2nd edn. CABI, Wallingford

    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. Training course number 2. Viena, Austria, pp 41–53

  • Baker GH, Amato M, Ladd J (2003) Influences of Aporrectodea trapezoides and A. rosea (Lumbricidae) on the uptake of nitrogen and yield of oats (Avena fatua) and lupins (Lupinus angustifolius). Pedobiologia 47:857–862

    Google Scholar 

  • Blanchart E, Villenave C, Viallatoux A, Barthès B, Girardin C, Azontone A, Feller C (2006) Long-term effect of a legume cover crop (Mucuna pruriens var. utilis) on the communities of soil macrofauna and nematofauna, under maize cultivation, in southern Benin. Eur J Soil Biol 42(Suppl 1):S136–S144

    Article  Google Scholar 

  • Bonkowski M, Griffiths BS, Ritz K (2000) Food preferences of earthworms for soil fungi. Pedobiologia 44:666–676

    Article  Google Scholar 

  • Brown GG, Doube BM (2004) Functional interactions between earthworms, microorganisms, invertebrates and plants. In: Edwards CA (ed) Earthworm ecology, 2nd edn. CRC Press, Boca Raton, pp 213–240

    Google Scholar 

  • Brown GG, Hendrix PF, Beare MH (1998) Earthworms (Lumbricus rubellus) and the fate of 15N in surface-applied sorghum residue. Soil Biol Biochem 30:1701–1705

    Article  CAS  Google Scholar 

  • Brown GG, Barois I, Lavelle P (2000) Regulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains. Eur J Soil Biol 36:177–198

    Article  Google Scholar 

  • Brown GG, Edwards CA, Brussaard L (2004) How earthworms affect plant growth: burrowing into the mechanisms. In: Edwards CA (ed) Earthworm ecology. CRC Press, Boca Raton, pp 13–49

    Google Scholar 

  • Buckles D (1995) Velvetbean: a new plant with a history. Econ Bot 49:151–162

    Google Scholar 

  • Callahan MA Jr, Hendrix P (1998) Impact of earthworms (Diplocardia: Megascolecidae) on cycling and uptake of nitrogen in coastal plain forest soils from Norwest Florida, USA. Appl Soil Ecol 9:233–239

    Article  Google Scholar 

  • Curry JP, Schmidt O (2007) The feeding ecology of earthworms—a review. Pedobiologia 50:463–477

    Article  Google Scholar 

  • FAO (1988) FAO/UNESCO soil map of the world, revised legend. World soil resources. Report no. 60. FAO, Rome

  • Gange AC (1993) Translocation of mycorrhizal fungi by earthworms during early succession. Soil Biol Biochem 25:1021–1026

    Article  Google Scholar 

  • Gange AC (2000) Arbuscular mycorrhizal fungi, Collembola and plant growth. Trends Ecol Evol 15:369–372

    Article  PubMed  Google Scholar 

  • Gange AC, Ayres RL (1999) On the relation between arbuscular mycorrhizal colonization and plant ‘benefit’. Oikos 87:615–621

    Article  Google Scholar 

  • García JA, Fragoso C (2003) Influence of different food substrates on growth and reproduction of two tropical earthworms (Pontoscolex corethrurus and Amynthas corticis). Pedobiologia 47:754–763

    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 

  • Graham JH, Eissenstat DM (1998) Field evidence for the carbon cost of citrus mycorrhizas. New Phytol 140:103–110

    Article  Google Scholar 

  • Haimi JH, Huhta V, Boucelham M (1992) Growth increase of birch seedlings under the influence of earthworms—a laboratory study. Soil Biol Biochem 12:1525–1528

    Article  Google Scholar 

  • Hodge A, Robinson D, Fitter AH (2000) An arbuscular mycorrhizal inoculum enhances root proliferation in, but not nitrogen capture from, nutrient-rich patches in soil. New Phytol 145:575–584

    Article  CAS  Google Scholar 

  • Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299

    Article  PubMed  CAS  Google Scholar 

  • Huerta E, Fragoso C, Barois I, Lavelle P (2005) Enhancement of growth and reproduction of the tropical earthworm Polypheretima elongata (Megascolecidae) by addition of Zea mayz and Mucuna pruriens var. utilis litter to the soil. Eur J Soil Biol 41:45–53

    Article  Google Scholar 

  • Huerta E, De la Cruz-Mondragon M (2006) Response of earthworm (Dichogaster saliens) to different feeding substrates. Compost Sci Util 14:211–214

    Google Scholar 

  • Insightful (2001) S-PLUS 6 for Windows guide to statistics, vol 1. Insightful, Seattle, WA, USA

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

    Google Scholar 

  • Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135:575–585

    Article  Google Scholar 

  • Johnson D, Leake JR, Ostle N, Ineson P, Read DJ (2002) In situ 13CO2 pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. New Phytol 153:327–334

    Article  CAS  Google Scholar 

  • Lavelle P, Spain AV (2001) Soil ecology. Kluwer, Dordrecht, The Netherlands

    Google Scholar 

  • Lawrence B, Fisk MC, Fahey J, Suaréz ER (2003) Influence of nonnative earthworms on mycorrhizal colonization of sugar maple (Acer saccharum). New Phytol 157:145–153

    Article  Google Scholar 

  • Mäder P, Vierhailig H, Streitwolf-Engel R, Boller T, Frey B, Christie P, Wiemken A (2000) Transport of 15N from soil compartment separated by a polytetrafluoroethylene membrane to plant roots via the hyphae of arbuscular mycorrhizal fungi. New Phytol 146:155–161

    Article  Google Scholar 

  • Ortiz-Ceballos AI, Fragoso C (2004) Earthworm populations under tropical maize cultivation: the effect of mulching with velvetbean. Biol Fertil Soils 39:438–445

    Article  Google Scholar 

  • Ortiz-Ceballos AI, Fragoso C, Equihua M, Brown GG (2005) Influence of food quality, soil moisture and the earthworm Pontoscolex corethrurus on the growth, reproduction and activity of a tropical earthworm Balanteodrilus pearsei. Pedobiologia 49:89–98

    Article  Google Scholar 

  • Ortiz-Ceballos AI, Fragoso C, Brown G (2007) Synergistic effect of a tropical earthworm Balanteodrilus pearsei and velvetbean Mucuna pruriens var. utilis on maize growth and crop production. Appl Soil Ecol 35:356–362

    Article  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 

  • Phyllips JM, Hayman OS (1970) Improved procedures for clearing roots and staining parasitic and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. T Brit Mycol So 55:158–161

    Google Scholar 

  • Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytol 157:475–492

    Article  Google Scholar 

  • Reddel P, Spain AV (1991) Earthworms as vectors of viable propagules of mycorrhizal fungi. Soil Biol Biochem 23:767–774

    Article  Google Scholar 

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

    Google Scholar 

  • Schmidt O, Curry JP (1999) Effects of earthworms on biomass production, nitrogen allocation and nitrogen transfer in wheat–clover intercropping model systems. Plant Soil 214:187–198

    Article  CAS  Google Scholar 

  • Tiunov AV, Dobrovolskaya TG (2002) Fungal and bacterial communities in Lumbricus terrestris burrow walls: a laboratory experiment. Pedobiologia 46:595–605

    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 

  • 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 

Download references

Acknowledgments

The authors are grateful to Prof. P. Nannipieri and anonymous reviewers for insightful comments and careful revision of the manuscript. We thank José A. García for helpful discussions; Antonio Vera for efficient analysis of AM hyphae and vesicle formation and total N concentration; and Antonio Angeles for technical assistance. This research work was partially supported by the International Atomic Energy Agency through contracts MEX 10959/R0-R4 of the Tropical Acid Soils Coordinated Research Project.

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Correspondence to Angel I. Ortiz-Ceballos.

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Ortiz-Ceballos, A.I., Peña-Cabriales, J.J., Fragoso, C. et al. Mycorrhizal colonization and nitrogen uptake by maize: combined effect of tropical earthworms and velvetbean mulch. Biol Fertil Soils 44, 181–186 (2007). https://doi.org/10.1007/s00374-007-0193-y

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  • DOI: https://doi.org/10.1007/s00374-007-0193-y

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