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Mycorrhiza

, Volume 22, Issue 3, pp 175–187 | Cite as

Response of native soil microbial functions to the controlled mycorrhization of an exotic tree legume, Acacia holosericea in a Sahelian ecosystem

  • Ablasse Bilgo
  • Sheikh K. Sangare
  • Jean Thioulouse
  • Yves Prin
  • Victor Hien
  • Antoine Galiana
  • Ezekeil Baudoin
  • Mohamed Hafidi
  • Amadou M. Bâ
  • Robin DuponnoisEmail author
Original Paper

Abstract

Fifty years of overexploitation have disturbed most forests within Sahelian areas. Exotic fast growing trees (i.e., Australian Acacia species) have subsequently been introduced for soil improvement and fuelwood production purposes. Additionally, rhizobial or mycorrhizal symbioses have sometimes been favored by means of controlled inoculations to increase the performance of these exotic trees in such arid and semiarid zones. Large-scale anthropogenic introduction of exotic plants could also threaten the native biodiversity and ecosystem resilience. We carried out an experimental reforestation in Burkina Faso in order to study the effects of Acacia holosericea mycorrhizal inoculation on the soil nutrient content, microbial soil functionalities and mycorrhizal soil potential. Treatments consisted of uninoculated A. holosericea, preplanting fertilizer application and arbuscular mycorrhizal inoculation with Glomus intraradices. Our results showed that (i) arbuscular mycorrhizal (AM) inoculation and prefertilizer application significantly improved A. holosericea growth after 4 years of plantation and (ii) the introduction of A. holosericea trees significantly modified soil microbial functions. The results clearly showed that the use of exotic tree legume species should be directly responsible for important changes in soil microbiota with great disturbances in essential functions driven by microbial communities (e.g., catabolic diversity and C cycling, phosphatase activity and P availability). They also highlighted the importance of AM symbiosis in the functioning of soils and forest plantation performances. The AM effect on soil functions was significantly correlated with the enhanced mycorrhizal soil potential recorded in the AM inoculation treatment.

Keywords

Arbuscular mycorrhizal symbiosis Functional diversity Mycorrhizal soil potential Acacia holosericea Glomus intraradices Soil microbial communities Exotic tree species 

References

  1. Anderson TH, Domsch KH (1989) Ratios of microbial biomass carbon to total organic carbon in arable soils. Soil Biol Biochem 21:471–479CrossRefGoogle Scholar
  2. Austin MP (1987) Models for analyses of species’ response to environmental gradients. Vegetatio 69:35–45CrossRefGoogle Scholar
  3. Bardgett RD (2005) The biology of soil. Oxford University Press, Oxford, p 242CrossRefGoogle Scholar
  4. Bardgett RD, McAlister E (1999) The measurement of soil fungal: bacterial biomass ratios as an indicator of ecosystem self-regulation in temperate meadow grasslands. Biol Fertil Soils 29:282–290CrossRefGoogle Scholar
  5. Bargali SS, Singh RP, Joshi M (1993) Changes in soil characteristics in eucalypt plantations replacing natural broadleaved forests. J Veg Sci 4:25–28CrossRefGoogle Scholar
  6. Boesch DF (2006) Scientific requirements for ecosystem-based management in the restoration of Chesapeak Bay and coastal Louisiana. Ecol Eng 26:6–26CrossRefGoogle Scholar
  7. Bossio D, Scow K, Gunapala N (1998) Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microbiol Ecol 36:1–12CrossRefGoogle Scholar
  8. Brundrett MC (1991) Mycorrhizas in natural ecosystems. In: Macfayden A, Begon M, Fitter AH (eds) Advances in ecological research, vol 21. Academic, London, pp 171–313Google Scholar
  9. Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443CrossRefGoogle Scholar
  10. Caravaca F, Alguacil MM, Azcon R, Diaz G, Roldan G (2004) Comparing the effectiveness of mycorrhizal inoculum and amendment with sugar beet, rock phosphate and Aspergillus niger to enhance field performance of the leguminous shrub Dorycnium pentaphyllum L. Appl Soil Ecol 25:169–180CrossRefGoogle Scholar
  11. Carpenter AT, Allen MF (1988) Responses of Hedysarum borelae Nutt. to mycorrhizas and Rhizobium: plant and soil nutrient changes in a disturbed shrub-steppe. New Phytol 109:125–132CrossRefGoogle Scholar
  12. Cornet F, Diem HG, Dommergues YR (1982) Effet de l’inoculation avec Glomus mosseae sur la croissance d’Acacia holosericea en pépinière et après transplantation sur le terrain, In: Les Mycorhizes: biologie et utilisation. INRA, Dijon, pp 287–293Google Scholar
  13. Cossalter C (1986) Introducing Australian acacias in dry, tropical Africa, Australian acacias in developing countries. In: Turnbull JW (ed) Proceedings of an international workshop at the Forestry Training Center. Gympie, Australia. ACIAR, Canberra, pp 118–122Google Scholar
  14. Cossalter C (1987) Introduction of Australian acacias into dry, tropical West Africa. For Ecol Manag 16:367–389CrossRefGoogle Scholar
  15. Culhane AC, Perriere G, Considine EC, Cotter TG, Higgins DG (2002) Between-group analysis of microarray data. Bioinformatics 18:1600–1608PubMedCrossRefGoogle Scholar
  16. D’Odorico P, Laio F, Ridolfi L (2005) Noise-induced stability in dryland plant ecosystems. PNAS 102:10819–10822PubMedCrossRefGoogle Scholar
  17. Dabire AP, Hien V, Kisa M, Bilgo A, Sangare KS, Plenchette C, Galiana A, Prin Y, Duponnois R (2007) Responses of soil microbial catabolic diversity to arbuscular mycorrhizal inoculation and soil disinfection. Mycorrhiza 17:537–545PubMedCrossRefGoogle Scholar
  18. de la Cruz RE, Garcia MU (1991) Nitrogen fixation and mycorrhizae in acacias on degraded grasslands. In: Awang K, Taylor DA (eds) Tropical acacias in East Asia and the Pacific. Winrock International, Bangkok, pp 59–71Google Scholar
  19. Degens BP, Harris JA (1997) Development of a physiological approach to measuring the metabolic diversity of soil microbial communities. Soil Biol Biochem 29:1309–1320CrossRefGoogle Scholar
  20. Degens BP, Vojvodic-Vukovic M (1999) A sampling strategy to assess the effects of land use on microbial functional diversity in soils. Aust J Soil Res 37:593–601Google Scholar
  21. Degens BP, Shipper LA, Sparling GP, Duncan LC (2001) Is the microbial community in a soil with reduced catabolic diversity less resistant to stress or disturbance? Soil Biol Biochem 33:1143–153CrossRefGoogle Scholar
  22. del Moral R, Muller CH (1970) The allelopathic effects of Eucalyptus camaldulensis. Am Midl Nat 83:254–282CrossRefGoogle Scholar
  23. Diallo MD, Duponnois R, Guisse A, Sall S, Chotte J-L, Thioulouse J (2006) Biological effects of native and exotic plant residues on plant growth, microbial biomass and N availability under controlled conditions. Eur J Soil Biol 42:238–246CrossRefGoogle Scholar
  24. Dolédec S, Chessel D (1989) Rythmes saisonniers et composantes stationnelles en milieu aquatique II- Prise en compte et élimination d’effets dans un tableau faunistique. Acta Oecol 10:207–232Google Scholar
  25. Drobner U, Bibby J, Smith B, Wilson JB (1998) The relation between community biomass and evenness: what does community theory predict and can these prediction be tested? Oikos 82:295–302CrossRefGoogle Scholar
  26. Duponnois R, Plenchette C (2003) A mycorrhiza helper bacterium (MHB) enhances ectomycorrhizal and endomycorrhizal symbiosis of Australian Acacia species. Mycorrhiza 13:85–91PubMedCrossRefGoogle Scholar
  27. Duponnois R, Plenchette C, Thioulouse J, Cadet P (2001) The mycorrhizal soil infectivity and arbuscular mycorrhizal fungal spore communities in soils of different aged fallows in Senegal. Appl Soil Ecol 17:239–251CrossRefGoogle Scholar
  28. Duponnois R, Founoune H, Masse D, Pontanier R (2005) Inoculation of Acacia holosericea with ectomycorrhizal fungi in a semiarid site in Senegal: growth response and influences on the mycorrhizal soil infectivity after 2 years plantation. For Ecol Manag 207:351–362CrossRefGoogle Scholar
  29. Duponnois R, Plenchette C, Prin Y, Ducousso M, Kisa M, Bâ AM, Galiana A (2007) Use of mycorrhizal inoculation to improve reafforestation process with Australian Acacia in Sahelian ecozones. Ecol Eng 29:105–112CrossRefGoogle Scholar
  30. Frey B, Schüepp H (1993) Acquisition of nitrogen by external hyphae of arbuscular mycorrhizal fungi associated with Zea mays L. New Phytol 124:221–230CrossRefGoogle Scholar
  31. Galiana A, Prin Y, Mallet B, Ghahona GM, Poitel M, Diem HG (1994) Inoculation of Acacia mangium with alginate beads containing Bradyrhizobium strains under field conditions: long-term effect on plant growth and persistence of the introduced strain in soil. Appl Environ Microbiol 60:3974–3980PubMedGoogle Scholar
  32. Garcia C, Hernandez T (1996) Influence of salinity on the biological and biochemical activity of a calciorthid soil. Plant Soil 178:225–263CrossRefGoogle Scholar
  33. Garcia C, Roldan A, Hernandez T (1997) Changes in microbial activity after abandonment of cultivation in a semiarid Mediterranean environment. J Environ Qual 26:285–291CrossRefGoogle Scholar
  34. Garcia C, Roldan A, Hernandez T (2005) Ability of different plant species to promote microbiological processes in semiarid soil. Geoderma 124:193–202CrossRefGoogle Scholar
  35. Grayston SJ, Vaughan D, Jones D (1996) Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl Soil Ecol 5:29–56CrossRefGoogle Scholar
  36. Heinemeyer O, Insam H, Kaiser EA, Walenzik G (1989) Soil microbial biomass and respiration measurements: an automated technique based on infrared gas analysis. Plant Soil 116:77–81CrossRefGoogle Scholar
  37. Huberty CJ (1994) Applied discriminant analysis. Wiley, New YorkGoogle Scholar
  38. Insam H (1990) Are the soil microbial biomass and basal respiration governed by the climatic regime? Soil Biol Biochem 22:525–532CrossRefGoogle Scholar
  39. Insam H, Domsch KH (1988) Relationship between soil organic carbon and microbial biomass on chronosequences of reclamation sites. Microbiol Ecol 15:177–188CrossRefGoogle Scholar
  40. Insam H, Merschak P (1997) Nitrogen leaching from forest soil cores after amending organic recycling products and fertilizers. Waste Manage Res 15:277–292Google Scholar
  41. Jakobsen I, Rosendahl L (1990) Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol 115:77–83CrossRefGoogle Scholar
  42. Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48:1–13PubMedCrossRefGoogle Scholar
  43. John MK (1970) Colorimetric determination in soil and plant material with ascorbic acid. Soil Sci 68:171–177Google Scholar
  44. Joner EJ, Johansen A (2000) Phosphatase activity of external hyphae of two arbuscular mycorrhizal fungi. Mycol Res 104:81–86CrossRefGoogle Scholar
  45. Joner EJ, Magid J, Gahoonia TS, Jakobsen I (1995) P depletion and activity of phosphatases in the rhizosphere of mycorrhizal and non mycorrhizal cucumber (Cucumis sativus L.). Soil Biol Biochem 27:1145–1151CrossRefGoogle Scholar
  46. Jones DL, Dennis PG, Owen AG, van Hees PAW (2003) Organic acid behavior in soils — misconceptions and knowledge gaps. Plant Soil 248:31–41CrossRefGoogle Scholar
  47. Kisa M, Sanon A, Thioulouse J, Assigbetse K, Sylla S, Spichiger R, Dieng L, Berthelin J, Prin Y, Galiana A, Lepage M, Duponnois R (2007) Arbuscular mycorrhizal symbiosis can counterbalance the negative influence of the exotic tree species Eucalyptus camaldulensis on the structure and functioning of soil microbial communities in a sahelian soil. FEMS Microbiol Ecol 62:32–44PubMedCrossRefGoogle Scholar
  48. Kourtev PS, Ehrenfeld JG, Haggblom M (2003) Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol Biochem 35:895–905CrossRefGoogle Scholar
  49. Lavorel S (1999) Ecological diversity and resilience of Mediterranean vegetation to disturbance. Divers Distrib 5:3–13CrossRefGoogle Scholar
  50. Linderman RG (1988) Mycorrhizal interactions with the rhizosphere microflora: the mycorrhizosphere effect. Phytopathology 78:366–371Google Scholar
  51. Lundström US, Van Breemen N, Jongmans AG (1995) Evidence for microbial decomposition of organic acids during podzolization. Eur J Soil Sci 46:489–496CrossRefGoogle Scholar
  52. Ma Z, Miyasaka SC (1998) Oxalate exudation by taro in response to Al. Plant Physiol 118:861–865PubMedCrossRefGoogle Scholar
  53. Magurran AE (1988) Ecological diversity and its measurement. Croom Helm, LondonGoogle Scholar
  54. Marilley L, Aragno M (1999) Phylogenetic diversity of bacterial communities differing in degree of proximity of Lolium perenne and Trifolium repens roots. Appl Soil Ecol 13:127–136CrossRefGoogle Scholar
  55. Marschner H (1995) Mineral nutrition of higher plants. Academic, LondonGoogle Scholar
  56. Micales JA (1997) Localization and induction of oxalate decarboxylase in the brown-rot wood decay fungus Postia placenta. Int J Biodet Biodegr 39:125–132CrossRefGoogle Scholar
  57. Odum EP (1959) Fundamentals of ecology. Saunders, Philadelphia, p 546Google Scholar
  58. Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. U.S. Department of Agriculture circular, vol 546. U.S. Department of Agriculture, Washington, DC, p 19Google Scholar
  59. Ouahmane L, Thioulouse J, Hafidi M, Prin Y, Ducousso M, Galiana A, Plenchette C, Kisa M, Duponnois R (2007) Soil functional diversity and P solubilization from rock phosphate after inoculation with native or allochtonous arbuscular mycorrhizal fungi. For Ecol Manag 241:190–199CrossRefGoogle Scholar
  60. Peterson G, Allen CR, Holling CS (1998) Ecological resilience, biodiversity, and scale. Ecosystems 1:6–18CrossRefGoogle Scholar
  61. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161CrossRefGoogle Scholar
  62. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org
  63. Rejmanek M (2000) Invasive plants: approaches and predictions. Austral Ecol 25:497–506CrossRefGoogle Scholar
  64. Remigi P, Faye A, Kane A, Deruaz M, Thioulouse J, Cissoko M, Prin Y, Galiana A, Dreyfus B, Duponnois R (2008) The exotic legume tree species Acacia holosericea alters microbial soil functionalities and the structure of the arbuscular mycorrhizal community. Appl Environ Microbiol 74:1485–1493PubMedCrossRefGoogle Scholar
  65. Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmanek M (2000) Plant invasion — the role of mutualisms. Biol Rev Camb Phil Soc 75:65–93CrossRefGoogle Scholar
  66. Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Mol Biol 52:527–560CrossRefGoogle Scholar
  67. Sanon A, Martin P, Thioulouse J, Plenchette C, Spichiger R, Lepage M, Duponnois R (2006) Displacement of an herbaceous plant species community by mycorrhizal and non-mycorrhizal Gmelina arborea, an exotic tree, grown in a microcosm experiment. Mycorrhiza 16:125–132PubMedCrossRefGoogle Scholar
  68. Schnürer T, Rosswall T (1982) Fluorescein diacetate hydrolysis as a measure of total microbial activity in soil and litter. Appl Environ Microbiol 43:1256–1261PubMedGoogle Scholar
  69. Shachar-Hill Y, Pfeffer PE, Douds D, Osman SF, Doner LW, Ratcliffe RG (1995) Partitioning of intermediary carbon metabolism in vesicular-arbuscular mycorrhizal leeks. Plant Physiol 108:7–15PubMedGoogle Scholar
  70. Sicardi M, Garcia-Préchac F, Frioni L (2004) Soil microbial indicators sensitive to land use conversion from pastures to commercial Eucalyptus grandis (Hill ex Maiden) plantations in Uruguay. Appl Soil Ecol 27:125–133CrossRefGoogle Scholar
  71. Skujins J (1976) Extracellular enzymes in soil. Crit Rev Microbiol 4:383–421CrossRefGoogle Scholar
  72. Sparling GP (1995) The substrate induced respiration method. In: Alef K, Nannipieri P (eds) Methods in applied soil microbiology and biochemistry. Academic, London, pp 397–404Google Scholar
  73. Stevenson BA, Sparling GP, Schipper LA, Degens BP, Duncan LC (2004) Pasture and forest soil microbial communities show distinct patterns in their catabolic respiration responses at a landscape scale. Soil Biol Biochem 36:49–55CrossRefGoogle Scholar
  74. Sylvia DM, Jarstfer AG (1992) Sheared-root inocula of vesicular–arbuscular mycorrhizal fungi. Appl Environ Microbiol 58:229–232PubMedGoogle Scholar
  75. Tabatabai MA, Bremner JM (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem 1:301–307CrossRefGoogle Scholar
  76. Thébaud C, Simberloff D (2001) Are plants really larger in their introduced ranges? Am Nat 157:231–236PubMedCrossRefGoogle Scholar
  77. Thioulouse J, Dray S (2007) Interactive multivariate data analysis in R with the ade4 and ade4TkGUI packages. J Stat Soft 22:1–14Google Scholar
  78. van der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998a) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79:2082–2091CrossRefGoogle Scholar
  79. van der Heijden MGA, Klironomos JN, Ursic M, Poutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998b) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72CrossRefGoogle Scholar
  80. Venables WN, Ripley BD (2002) Modern applied statistics. Springer, New YorkGoogle Scholar
  81. Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components. Monographs in population biology, vol 34. Princeton University Press, Princeton, p 392Google Scholar
  82. West AW, Sparling GP (1986) Modifications to the substrate-induced respiration method to permit measurements of microbial biomass in soils of different water contents. J Microbiol Meth 5:177–189CrossRefGoogle Scholar
  83. Zerbo L, Koné N, Morant P, Thiombiano L (1995) Rapport sur la caractérisation des sols des stations de recherches agricoles de l’INERA: Kambouinsé. Farako-ba, Saria, Niangoloko, p 109Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Ablasse Bilgo
    • 1
  • Sheikh K. Sangare
    • 1
  • Jean Thioulouse
    • 2
  • Yves Prin
    • 3
  • Victor Hien
    • 1
  • Antoine Galiana
    • 3
  • Ezekeil Baudoin
    • 4
  • Mohamed Hafidi
    • 5
  • Amadou M. Bâ
    • 6
    • 4
  • Robin Duponnois
    • 4
    • 5
    Email author
  1. 1.Laboratoire Sol-Eau-Plante (SEP)Institut de l’Environnement et de Recherches Agricoles (INERA)OuagadougouBurkina Faso
  2. 2.UMR5558, Laboratoire de Biométrie et Biologie EvolutiveCentre National de la Recherche Scientifique (CNRS)VilleurbanneFrance
  3. 3.UMR 113 CIRAD/INRA/IRD/AGRO-M/UM2, Laboratoire des Symbioses Tropicales et méditerranéennes (LSTM), Campus International de BaillarguetCentre de Coopération Internationale en recherche agronomique pour le Développement (CIRAD)MontpellierFrance
  4. 4.UMR 113 CIRAD/INRA/IRD/AGRO-M/UM2, Laboratoire des Symbioses Tropicales et méditerranéennes (LSTM), Campus International de BaillarguetInstitut de Recherche pour le Développement (IRD)MontpellierFrance
  5. 5.Faculté des Sciences Semlalia, Laboratoire Ecologie & Environnement, Unité associée au CNRST, URAC 32Université Cadi AyyadMarrakechMaroc
  6. 6.Laboratoire Commun de Microbiologie IRD/ISRA/UCADInstitut de Recherche pour le Développement (IRD), Centre de Recherche de Bel AirDakarSenegal

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