OJF  Vol.4 No.1 , January 2014
The Effectiveness of Arbuscular Mycorrhizal Inoculation and Bio-Compost Addition for Enhancing Reforestation with Argania spinosa in Morocco
Abstract: A field experiment was carried out in arid area to assess the influence of mycorrhizal inoculation with a native complex and bio-compost addition on establishment of Argania spinosa. The experimental area was located in the Admine forest at Agadir (Southwestern Morocco). The results showed a positive effect of arbuscular mycorrhizal fungi (AMF) on the growth of Argania spinosa seedlings in the nursery. Six months after planting, the mycorrhizal complex revealed an increase in the growth of Argan seedlings (51%) compared to non mycorrhizal plants. In the field conditions, after one year of transplantation, this benefit was maintained. Results showed that the height of Argan seedlings treated with AMF was double that of the control group. An additional positive effect of inoculation with AMF on plant biomass was observed and it was closely related to colonization by these microorganisms. There was an estimated 169% increase in biomass compared to control plants. The use of bio-compost alone or in combination with AMF improved the production of shoot biomass of Argan plants (84% and 108% respectively compared to control plants). In addition, AMF improved the survival rate and the contents of nitrogen (N) and phosphorus (P) in the tissues of A. spinosa plants. A significant positive correlation between dry biomass and nutrient content in plant tissue was detected. The content of (P) in the leaves and roots of inoculated plants was higher than those in non-inoculated and planted seedlings in amended soils. This result reaffirms the prime necessity of mycorrhiza in arid conditions. Thus the introduction of mycorrhizal fungi in forest nurseries is a key tool to improve the quality of seedlings produced and their resistance in reforestation sites.
Cite this paper: Mrabet, S. , Ouahmane, L. , Mousadik, A. , Msanda, F. & Abbas, Y. (2014). The Effectiveness of Arbuscular Mycorrhizal Inoculation and Bio-Compost Addition for Enhancing Reforestation with Argania spinosa in Morocco. Open Journal of Forestry, 4, 14-23. doi: 10.4236/ojf.2014.41003.

[1]   Abbas, Y., Bakkali, Y. S., Prin, Y., Arahou, M., Abourouh, M., & Duponnois, R. (2013). Growth and nutrition of Tetraclinis articulata (Vahl) Mast.cultivated in different rhizosphere soils collected from Tetraclinis stand. Biotechnology, Agronomy, Society and Environment, 17, 3-11.

[2]   Alados, C. L., & El Aich, A. (2008). Stress assessment of Argan (Argania spinosa (L.) Skeels) in response to land uses across an aridity gradient: Translational asymmetry and branch fractal dimension. Journal of Arid Environment, 72, 338-349.

[3]   Albaladejo, J., Martinez-Mena, M., Roldan, A., & Castillo, V. (1998). Soil degradation and desertification induced by vegetation removal in a semiarid environment. Soil Use Manage, 14, 1-5.

[4]   Alguacil, M. M., Caravaca, F., Azcónb, R., & Roldán, A. (2008). Changes in biological activity of a degraded Mediterranean soil after using microbially-treated dry olive cake as a biosolid amendment and arbuscular mycorrhizal fungi. European Journal of Soil Biology, 44, 347-354.

[5]   Alguacil, M. M., Torrecillas, E., Kohler, J., & Roldan, A. (2011). Amolecular approach to ascertain the success of “in situ” AM fungi inoculation in the revegetation of a semiarid, degraded land. Science of the Total Environment, 409, 2874-2880.

[6]   Augé, R. M. (2001). Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza, 11, 3-42.

[7]   Azcon, R., & Barea, J. M. (1992). Nodulation, N2 fixation (5N) and N nutrition relationships in mycorrhizal or phosphate-amended alfalfa plants. Symbiosis, 12, 33-41.

[8]   Azcón-Aguilar, C., Palenzuela, E. J., Roldan, A., Bautista, S., Vallejo, R., & Barea, J. M. (2002). Analysis of the mycorrhizal potential in the rhizosphere of representative plant species from desertificationthreatened Mediterranean shrublands. Applied Soil Ecology, 21, 1-9.

[9]   Bago, B., Pfeffer, P. E., Zipfel, W., Lammers, P., & Shachar-Hill, Y. (2002). Tracking metabolism and imaging transport in arbuscular mycorrhizal fungi. Metabolism and transport in AM fungi. Plant and Soil, 244, 189-197.

[10]   Barea, J. M., Salamanca, C. P., Herrera, M. A., & Roldán-Fajardo, B. E. (1990). La simbiosis microbio planta en el establecimiento de unacubiertavegetal sobre suelosdegradados. In: J. Albaladejo, M. Stocking, & E. Díaz (Eds.), Soil degradation and rehabilitation in Mediterranean environmental conditions (pp. 139-156). Murcia: Consejo Superior de Investigaciones Científicas.

[11]   Barea, J. M., Palenzuela, J., Cornejo, P., Sánchez, I., Navarro, C., Quinones, P. B., Azcón, R., Ferrol, N., & Azcón-Aguilar, C. (2007). Significado, diversidad e impacto de los hongos de las micorrizasarbusculares en ambientesmediterráneos. In: J. M. Barea-Azcón, M. Moleón, R. Travesí, E. Ballesteros, J. M. Luzón, & J. M. Tierno (Eds.), Biodiversidad y conservación de fauna y flora en ambientes Mediterráneos (pp. 155-185). Granada: Sociedad Granatense de Historia Natural.

[12]   Barea, J. M., Ferrol, N., Azcón-Aguilar, C., & Azcón, R. (2008). Mycorrhizal symbioses. Series. In: P. J. White, & J. P. Hammond (Eds.), The ecophysiology of plant-phosphorus interactions. Plant cophysiology, Vol. 7 (pp. 143-163). Dordrecht: Springer.

[13]   Benabid, A. (2000). Flore et écosystèmes du Maroc. Paris: Ed Ibis Press.

[14]   Bousselmane, F., Kenny, L., & Achouri, M. (2002). Effet des mycorhizes à vésicules et arbuscules sur la croissance et la nutrition de l’arganier (Argania spinosa L.). Revue Marocaine des Sciences Agronomiques et Vétérinaires, 22, 193-198.

[15]   Boutekrabt, A., Chevalier, G., Pargney, J. C., & Dexheimer, J. (1999). Mycorhization par Tuber melanosporumVitt de vitroplants de Quercus robur L et Quercus pubescensWilld. Agronomie, 2, 127-132.

[16]   Brundrett, M. C., Piche, Y., & Peterson, R. L. (1985). A developmental study of the early stages in vesicular-arbuscular mycorrhizal formation. Canadian Journal of Botany, 63, 184-194.

[17]   Carrillo-García, A., León de la Luz, J. L., Bashan, Y., & Bethlenfalvay, G. J. (1999). Nurse plants, mycorrhizae, and plant establishment in a disturbed area of the Sonoran desert. Restoration Ecology, 7, 321-335.

[18]   Caravaca, F., Barea, J. M., Figueroa, D., & Roldań, A. (2002). Assessing the effectiveness of mycorrhizal inoculation and soil compost addition for reafforestation with Olea europaea subsp. sylvestris through changes in soil biological and physical parameters. Applied Soil Ecology, 20, 107-118.

[19]   Caravaca, F., Alguacil, M. M., Figueroa, D., Barea, J. M., & Roldán, A. (2003a). Re-establishment of Retama sphaerocarpa as a target species for reclamation of soil physical and biological properties in a semiarid Mediterranean land. Forest Ecology and Management, 182, 49-58.

[20]   Caravaca, F., Barea, J. M., Palenzuela, J., Figueroa, D., Alguacil, M. M., & Roldán, A. (2003b). Establishment of shrub species in a degraded semiarid site after inoculation with native or allochthonous arbuscular mycorrhizal fungi. Applied Soil Ecology, 22, 103-111.

[21]   Caravaca, F., Alguacil, M. M., Azcón, R., Díiaz, 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. Applied Soil Ecology, 25, 169-180.

[22]   Dalpé, Y. (2005). Les mycorhizes: Un outil de protection des plantes mais non une panacée. Phytoprotection, 86, 53-59.

[23]   Duponnois, R., Ouahmane, L., Kane, A., Thioulouse, J., Hafidi, M., Boumezzough, A., Prin, Y., Baudoin, E., Galiana, A., & Dreyfus, B. (2011). Nurse shrubs increased the early growth of Cupressus seedlings by enhancing belowground mutualism and soil microbial activity. Soil Biology & Biochemistry, 43, 2160-2168.

[24]   Echairi, A., Nouaim, R., & Chaussod, R. (2008). Intérêt de la mycorhization controlée pour la production de plants d’arganier (Argania spinosa) en conditions de pépinière. Sécheresse, 19, 277-281.

[25]   EL Yousfi, M. (1988). Dégradation du couvert forestier dans le Sud Marocain: Cas de l’arganeraie d’Admine. Rabat: Mémoire de 3ème cycle IAV Hassan II, 117p.

[26]   Fisher, R. A., & Yates, F. (1970). Statistical tables for biological agriculture and medical research (6th ed.). Davien: Hafner Publishing Company.

[27]   Fuentes, D., Valdecantos, A., Llovet, J., Cortina, J., & Vallejo, V. R., (2010). Fine-tuning of sewage sludge application to promote the establishment of Pinus halepensis seedlings. Ecological Engineering, 36, 1213-1221.

[28]   Garcia, C., Hernández, T., Albaladejo, J., Castillo, V., & Roldán, A. (1998). Revegetation in semiarid zones: Influence of terracing and organic refuse on microbial activity. Soil Science Society of America Journal, 62, 670-676.

[29]   Garcia, C., León de la Luz, J.-L., Bashan, Y., & Bethlenfalvay, G. J. (1999). Nurse plants, mycorrhizae, and plant establishment in a disturbed area of the Sonoran desert. Restoration Ecology, 7, 321-335.

[30]   Giovannetti, M., & Mosse, B. (1980). An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytologist, 84, 489-499.

[31]   Harrison, M. J. (1999). Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 361-389.

[32]   Helgason, T., Daniell, T. J., Husband, R., Fitter, A. H., & Young, J. P. Y. (1998). Ploughing up the wood-wide web? Nature, 394, 431.

[33]   Helgason, T., & Fitter, A. H. (2009). Natural selection and evolution in the arbuscular mycorrhizal fungi (Phylum Glomeromycota). Journal of Experimental Botany, 60, 2465-2480.

[34]   Herrera, M. A., Salamanca, C. P., & Barea, J. M. (1993). Inoculation of woody legumes with selected arbuscular mycorrhizal fungi and rhizobia to recover desertified Mediterranean ecosystems. Applied and Environmental Microbiology, 59, 129-133.

[35]   Hodge, A., Campbell, C. D., & Fitter, A. H. (2001). An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature, 413, 297-299.

[36]   Honrubia, M. (2009). The Mycorrhizae: A plant-fungus relation that has existed for more than 400 million years. Anales del Jardín Botánico de Madrid, 66, 133-144.

[37]   IFN (1996). Synthèse de l’Inventaire forestier national marocain. Rabat: Direction de Développement Forestier.

[38]   Jasper, D. A. (1994). Management of mycorrhiza in revegetation. In A. D. Robson, L. K. Abbot, & N. Malajczuk (Eds.), Management of mycorrhizas in agriculture, horticulture and forestry (pp. 211-219). Dordrecht: Kluwer Academic Press.

[39]   Jeffries, P., & Barea, J. M. (2001). Arbuscular mycorrhiza—A key component of sustainable plant-soil ecosystems. In: B. Hock (Ed.), The Mycota. IX Fungal Associations (pp. 95-113). Berlin: SpringerVerlag.

[40]   Jeffries, P., Gianinazzi, S., Perotto, S., Turnau, K., & Barea, J. M. (2003). The contribution of arbuscularmycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biology and Fertility of Soils, 37, 1-16.

[41]   Kennedy, A. C., & Smith, K. L. (1995). Soil microbial diversity and the sustainability of agricultural soils. Plant and Soil, 170, 75-86.

[42]   Lax, A., Roldán, A., Caravaca, F., & García-Orenes, F. (1997). Relationships between aggregate improvement, microbiological activity and organo-mineral complex formation in soils from semiarid areas. In: S. G. Pandalai (Ed.), Recent research developments in soil biology and biochemistry (pp. 77-92). Trivandrum: Research Signpost.

[43]   López-Bermúdez, F., & Albaladejo, J. (1990). Factores ambientales de la degradación delsuelo en el áreamediterránea. In: J. Albadejo, M. A. Stocking, & E. Díaz (Eds.), Soil degradation and rehabilitation in Mediterranean environmental conditions (pp. 15-45). Murcia: Consejo Superior de Investigaciones Científicas.

[44]   Martínez-García, L. B., & Pugnaire, F. I. (2009). Interacciones entre las comunidades de hongosformadores de micorrizasarbusculares y de plantas. Algunosejemplos en los ecosistemassemiáridos. Ecosistemas, 18, 44-54.

[45]   Martínez-García, L. B. (2010). Micorrizas arbusculares en ecosistemassemiáridos. Respuesta a factoresde estrésambiental. Tesis Doctorales, Almería: Universidad de Almería.

[46]   Meddad-Hamza, A., Beddiar, A., Gollotte, A., Lemoine, M. C., Kuszala, C., & Gianinazzi, S. (2010). Arbuscular mycorrhizal fungi improve the growth of olive trees and their resistance to transplantation stress. African Journal of Biotechnology, 9, 1159-1167.

[47]   Msanda, F. (2004). Végétation de l’Anti Atlass occidental et de sa retombée saharienne (Maroc). Essai de Synthèse, Thèse de Doctorat ès Sciences, Agadir: Université Ibn Zohr.

[48]   Murphy, J., & Riley, J. P. (1962). A modified single solution method for determination of phosphate in natural waters. Analytica Chimica Acta, 27, 31-36.

[49]   Nelson, C. E., & Safir, G. R. (1982). Increased drought tolerance of mycorrhizal onion plants caused by improved phosphorus nutrition. Planta, 154, 407-413.

[50]   Nouaim, R. (1994). écologie microbienne des sols d’arganeraies. Activités microbiologiques des sols et role des endomycorhizes dans la croissance et la nutrition de l’Arganier. Thèse d’état, Agadir: Université Ibn Zohr.

[51]   Olsen, S. R., Cole, C. V., Watanabe, F. S., & Dean, L. A. (1954). Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Circular, Vol 939 (p. 19). Washington, DC: US Department of Agriculture.

[52]   Ohtomo, R., & Saito, M. (2005). Polyphosphate dynamics in mycorrhizal roots during colonization of an arbuscular mycorrhizal fungus. New Phytologist, 167, 571-578.

[53]   Ouahmane, L. (2007). Roles des plantes associées (Lavandula et Thymus) dans la régénération du cypres de l’atlas—Effets sur la diversité rhizosphérique. Thèse de Doctorat National, Marrakech: Université cadi Ayyad.

[54]   Ouahmane, L., Hafidi, M., Thioulouse, J., Ducousso, M., Kisa, M., Prin, Y., Galiana, A., Boumezzough, A., & Duponnois, R. (2007). Improvement of Cupressus atlantica Gaussen growth by inoculation with native arbuscular mycorrhizal fungi. Journal of Applied Microbiology, 103, 683-690.

[55]   Ouahmane, L., Ndoye, I., Morino, A., Ferradous, A., Sfairi, Y., Al Faddy, M. N., & Abourouh, M. (2012). Inoculation of Ceratonia siliqua L. with native arbuscular mycorrhizal fungi mixture improves seedling establishment under greenhouse conditions. African Journal of Biotechnology, 11, 16422-16426.

[56]   Page, A. L., Miller, R. H., & Keeny, O. R. (1982). Methods of soil analysis. Madison: American Society of Agronomy.

[57]   Palenzuela, J., Azcoń-Aguilar, C., Figueroa, D., Caravaca, F., Roldań, A., & Barea, J. M. (2002). Effects of mycorrhizal inoculation of shrubs from Mediterranean ecosystems and composted residue application on transplant performance and mycorrhizal developments in a desertified soil. Biology and Fertility of Soils, 26, 170-175.

[58]   Phillips, J. M., & Hayman, D. S. (1970). Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society, 55, 158-161.

[59]   Plenchette, C., Fortin, J. A., & Furlan, V. (1983). Growth responses of several plant species to mycorrhizae in a soil of moderate P fertility. I. Mycorrhizal dependency under field conditions. Plant and Soil, 70, 199-209.

[60]   Pozo, M. J., Azcón-Aguilar, C., Dumas-Gaudot, E., & Barea, J. M. (1999). β-1,3-glucanase activities in tomato roots inoculated with arbuscular mycorrhizal fungi and/or Phytophthora parasitica: Time course analysis and possible involvement in bioprotection. Plant Science, 141, 149-157.

[61]   Requena, N., Perez-Solis, E., Azcon-Aguilar, C., Jeffries, P., & Barea J. M. (2001). Management of indigenous plant-microbe symbioses aids restoration of desertified ecosystems. Applied and Environmental Microbiology, 67, 495-498.

[62]   Rillig, M., & Mummey, D. L. (2006). Mycorrhizas and soil structure. New Phytologist, 171, 41-53.

[63]   Roldán, A., García-Orenes, F., & Lax, A. (1994). An incubation experiment to determine factors involving aggregation changes in an arid soil receiving urban refuse. Soil Biology and Biochemistry, 26, 16991707.

[64]   Roldán, A., Albaladejo, J., & Thornes, J. B. (1996a). Aggregate stability changes in a semiarid soil after treatment with different organic amendments. Arid Soil Research and Rehabilitation, 10, 139-148.

[65]   Roldán, A., Querejeta, J. I., Albaladejo, J., & Castillo, V. (1996b). Growth response of Pinus halepensis to inoculation with Pisolithus arhizus in a terraced rangeland amended with urban refuse. Plant and Soil, 179, 35-43.

[66]   Roldán, A., García, C., & Albaladejo, J. (1997). AM fungal abundance and activity in a chronosequence of abandoned fields in a semiarid Mediterranean site. Arid Soil Research and Rehabilitation, 11, 211-220.

[67]   Schmid, T., Meyer, J., & Oehl, F. (2008). Integration of mycorrhizal inoculum in high alpine revegetation. Mycorrhiza works. In: F. Feldmann, Y. Kapulnik, & J. Baar (Eds.), Proceedings of the International Symposium “Mycorrhiza for Plant Vitality” and the Joint Meeting of Working Groups 1 4 of COST Action 870 (pp. 278-288). Braunschweig: Deutsche Phytomedizinische Gesellschaft.

[68]   Schollemberger, C. J., & Simon, R. H. (1954). Determination of exchange capacity and exchangeable bases in soils. Soil Science, 59, 13-24.

[69]   Sieverding, E. (1991). Vesicular-arbuscular mycorrhiza management in tropical agrosystems. Eschborn: GTZ.

[70]   Skujins, J., & Allen, M. F. (1986). Use of mycorrhizae for land rehabilitation. MIRCEN Journal of Applied Microbiology and Biotechnology, 2, 161-176.

[71]   Smith, S. E., & Read, D. J. (1997). Mycorrhizal symbiosis (2nd ed.). Academic Press, London.

[72]   Smith, S. E., Smith, F. A., & Jakobsen, I. (2004). Functional diversity in arbuscular mycorrhizal (AM) symbioses: The contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytologist, 162, 511-524.

[73]   Smith, S. E., & Read, D. J., (2008). Mycorrhizal symbiosis (3rd ed.). London: Academic Press.

[74]   Smith, F. A., Grace, E. J., & Smith, S. E. (2009). More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytologist, 182, 347-358.

[75]   Sylvia, D. M. (1990). Inoculation of native woody plants with vesiculararbuscular mycorrhizal fungi for phosphate mine land reclamation. Agriculture, Ecosystems & Environment, 31, 253-261.

[76]   Tahat, M. M., Kamaruzaman, S., & Radziah, O. (2012). The potential of endomycorrhizal fungi in controlling tomato bacterial wilt Ralstonia solanacearum under glasshouse conditions. African Journal of Biotechnology, 11, 13085-13094.

[77]   Toro, M., Azcón, R., & Barea, J. M. (1997). Improvement of arbuscular mycorrhiza development by inoculaltion of soil phosphate solubilizing rhizobacteria to improve rock phosphate bioavailability (32P) and nutrient cycling. Applied and Environmental Microbiology, 63, 4408-4412.

[78]   Van der Hejden, M. G. A., Klironomos, J. N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., Wiemken, A., & Sanders, I. R. (1998). Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature, 396, 69-72.

[79]   Yanai, R. D., Fahey, T. J., & Miller, S. L. (1995). Efficiency of nutrient acquisition by fine roots and mycorrhizae. In: W. K. Smith, & T. M. Hinckley (Eds.), Resource physiology of conifers: Acquisition, allocation and utilization (pp. 75-103). London: Academic Press.

[80]   Yeomans, J. C., & Bremner, J. M. (1989). A rapid and precise method for routine determination of organic carbon in soil. Communications in Soil Science and Plant Analysis, 19, 1467-1476.

[81]   Zebarth, L. B. J., Neilsen, G. H., Hogue, E., & Neilsen, D. (1999). Influence of organic waste amendments on selected soil physical and chemical properties. Canadian Journal of Soil Science, 79, 501-504.

[82]   Zendejas, L. H. S., Solís, O. M., López, W. W., Vera, R. A., & González, P. J. M. (2011). Effects of compost made with sludge and organic residues on bean (Phaseolus vulgaris L.) crop and arbuscular mycorrhizal fungi density. African Journal of Agricultural Research, 6, 1580-1585.