Sains Malaysiana 44(5)(2015): 671–680

 

Effects of Soil Chemical Properties and Seasonality on Mycorrhizal Status of Prickly Pear (Opuntia ficus-indica) Planted in Hot Arid Steppe Rangelands

(Kesan daripada Sifat Kimia Tanah dan Keberkitaran Status Mikoriza Pir Deduri

(Opuntia ficus-indica) yang Ditanam di Tanah Banjaran Panas Gersang Steppe)

 

S. NEFFAR1*, A. BEDDIAR2 & H. CHENCHOUNI1

1Department of Natural and Life Sciences, Faculty of Exact Sciences and Natural and Life Sciences

University of Tebessa, 12002 Tebessa, Algeria

 

2Department of Biology, Faculty of Natural and Life Science, University of Badji Mokhtar

23000 Annaba, Algeria

 

Received: 5 September 2014/Accepted: 13 January 2015

 

ABSTRACT

Mycorrhizal fungi are an essential component to consider for better management of soil fertility, particularly in degraded rangelands of drylands. The present article presents a field survey of colonization and intensity of arbuscular mycorrhizal fungi (AMF) on prickly pear (Opuntia ficus-indica) roots from young (5 years old) and old (more than 20 years) plantations. The results observed were explained by seasonality and edaphic factors. Prickly pear roots showed a mycorrhizal frequency (F%) up to 100% of colonization and a mycorrhizal intensity (M%) that may exceed 70%. According to ANOVAs, both F% and M% varied significantly between Prickly pear plantation ages, but only M% between seasons. The Generalized linear model showed that edaphic factors have no effect on the variation of F%. However the statistical model showed that M% were significantly influenced by active CaCO3, organic matter, carbon, nitrogen, phosphorus contents and C/N. Our findings highlight the importance of mycorrhization in rehabilitation programs of degraded rangelands by prickly pear plantations in semiarid and arid lands, particularly during early plant ages and under environmental abiotic stresses such as climate and soil type.

 

Keywords: Arbuscular mycorrhizal fungi; arid land reclamation; mycorrhization; Opuntia ficus-indica; soil factors; steppe degradation

 

ABSTRAK

Kulat Mikoriza adalah komponen penting untuk dipertimbangkan dalam pengurusan kesuburan tanah yang lebih baik, terutamanya di tanah banjaran usang daripada tanah kering. Artikel ini membentangkan kaji selidik lapangan tentang penanaman daripada pengkolonian dan kemantapan kulat arbuskel mikoriza (AMF) akar pir deduri (Opuntia ficus-indica) akar daripada kecil (5 tahun) dan tua (lebih 20 tahun). Keputusan ditunjukkan melalui keberkitaran dan faktor edafik. Akar pir deduri menunjukkan kekerapan mikoriza (F%) sehingga 100% pengkolonian dan keamatan mikoriza (M%) yang boleh melebihi 70%. Menurut ANOVAs, F% dan M% berubah dengan ketara antara usia ladang pir deduri, tetapi M% hanya antara musim. Model linear menyeluruh menunjukkan bahawa faktor edafik tidak mempunyai kesan ke atas perubahan F%. Walau bagaimanapun model statistik menunjukkan bahawa M% dipengaruhi secara signifikan oleh CaCO3, sebatian organik, karbon, nitrogen, kandungan fosforus dan C/N. Penemuan kami menekankan betapa pentingnya pemikorizaan dalam program pemulihan tanah banjaran usang di ladang pir deduri dalam tanah separa gersang dan gersang, terutamanya semasa awal musim penanaman dan di bawah tekanan persekitaran abiotik seperti iklim dan jenis tanah.

 

Kata kunci: Faktor tanah; kulat mikoriza arbuskula; Opuntia ficus-indica; pemikorizaan; steppe usang; tebus guna tanah gersang


REFERENCES

Abdel Latef, A.A.H. & Chaoxing, H. 2011. Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci. Hortic. 127(3): 228-233.

Aïdoud, A., Le Floc’h, E. & Le Houérou, H.N. 2006. Les steppes arides du nord de l’Afrique. Sécheresse 17(1): 19-30.

Barea, J.M., Azcon-Aguilar, C. & Azcon, R. 1997. Interactions between mycorrhizal fungi and rhizosphere micro-organisms within the context of sustainable soil–plant systems. In Multitrophic Interactions in Terrestrial Systems, edited by Gange, A.C. & Brown, V.K. Cambridge: Blackwell Science. pp. 65-77.

Beddiar, A. 2003. Les symbioses racinaires chez les principales essences forestières spontanées ou introduites dans le Nord- Est algérien (Etude particulière de la symbiose quadripartite chez l’Aulne glutineux). PhD Thesis, Annaba University, Algeria (unpublished).

Benabderrahmane, M.C. & Chenchouni, H. 2010. Assessing environmental sensitivity areas to desertification in eastern Algeria using Mediterranean desertification and land use “MEDALUS” model. Int. J. Sust. Water Environ. Syst. 1(1): 5-10.

Bethlenfalvay, G.J. & Schuëpp, H. 1994. Arbuscular mycorrhizas and agrosystem stability. In Impact of Arbuscular Mycorrhizas on Sustainable Agriculture and Natural Ecosystems, edited by Gianinazzi, S. & Schuëp, H. Basel: Birkhaüser Verlag. pp. 171-313.

Bever, J., Schultz, P., Pringle, A. & Morton, J. 2001. Arbuscular mycorrhizal fungi: More diverse than meets the eye, and the ecological tale of why. BioScience 51(11): 923-932.

Biró, B., Köves-Péchy, K., Tsimilli-Michael, M. & Strasser, R.J. 2006. Role of beneficial microsymbionts on the plant performance and plant fitness. In Microbial Activity in the Rhizosphere (vol. 7), edited by Mukerji, K.G., Manoharachary, C. & Singh, J. Berlin, Heidelberg: Springer. pp. 265-296.

Błaszkowski, J. 2003. Glomus intraradices In Arbuscular Mycorrhizal Fungi (Glomeromycota), Endogone, and Complexipes Species deposited in the Department of Plant Pathology, University of Agriculture in Szczecin, Poland. Available at: www.agro.ar.szczecin.pl/~jblaszkowski/ Glomus%20intraradices.html.

Bohrer, K., Friese, C. & Amon, J. 2004. Seasonal dynamics of arbuscular mycorrhizal fungi in differing wetland habitats. Mycorrhiza 14(5): 329-337.

Boomsma, C. & Vyn, T. 2008. Maize drought tolerance: Potential improvements through arbuscular mycorrhizal symbiosis. Field Crop Res. 108(1): 14-31.

Bradai, L., Bissati, S. & Chenchouni, H. 2014. Desert truffles of the North Algerian Sahara: Diversity and bioecology. Emir. J. Food Agric. 26(5): 425-435.

Bradai, L., Bissati, S., Chenchouni, H. & Amrani, K. 2015. Effects of climate on the productivity of desert truffles beneath hyper-arid conditions. Int. J. Biometeorol. 59 doi: 10.1007/s00484- 014-0891-8 (In Press).

Brundrett, M.C., Ashwath, N. & Jasper, D.A. 1996. Mycorrhizae in the Kakadu region of tropical Australia. Part II. Propagules of mycorrhizal fungi in disturbed habitats. Plant and Soil 184(1): 173-184.

Caravaca, F., Figueroa, D., Azcon-Aguilar, C., Barea, J.M. & Roldan, A. 2003. Medium-term effects of mycorrhizal inoculation and composted municipal waste addition on the establishment of two Mediterranean shrub species under semiarid field conditions. Agr. Ecosyst. Environ. 97(1): 95-105.

Carrillo-Garcia, Á., La Luz, D., León, J.L., Bashan, Y. & Bethlenfalvay, G.J. 1999. Nurse plants, mycorrhizae and plant establishment in a disturbed area of the Sonoran Desert. Restor. Ecol. 7(4): 321-335.

Chafi, M.E. & Fortas, Z. 1999. Les mycorhizes des plantes des zones arides algériennes. Bois Forêts Trop. 262: 77-79.

Chmura, D. & Gucwa-Przepióra, E. 2012. Interactions between arbuscular mycorrhiza and the growth of the invasive alien annual Impatiens parviflora DC: A study of forest type and soil properties in nature reserves (S Poland). Appl. Soil Ecol. 62(1): 71-80.

Collier, S., Yarnes, C. & Peter Herman, R. 2003. Mycorrhizal dependency of Chihuahuan Desert plants is influenced by life history strategy and root morphology. J. Arid Environ. 55: 223-229.

Cui, M. & Nobel, P.S. 1992. Nutrient status, water uptake and gas exchange for three desert succulents infected with mycorrhizal fungi. New Phytol. 122(4): 643-649.

Degens, B.P., Sparling, G.P. & Abbott, L.K. 1999. Increasing the length of hyphae in a sandy soil increases the amount of water-stable aggregates. Appl. Soil Ecol. 3(2): 149-159.

Dhillion, S.S. & Friese, C.F. 1992. The occurrence of mycorrhizas in prairies: Application to ecological restoration. In Proceedings of the 13th North American Prairie Conference: Spirit of the Land, our Prairie Legacy, edited by Wickett, R.G., Lewis, P.D., Woodliffe, A. & Pratt, P. Canada: University of Windsor. pp. 103-114.

Escudero, V. & Mendoza, R. 2005. Seasonal variation of arbuscular mycorrhizal fungi in temperate grasslands along a wide hydrologic gradient. Mycorrhiza 15(4): 291-299.

Evelin, H., Kapoor, R. & Giri, B. 2009. Arbuscular mycorrhizal fungi in alleviation of salt stress: A review. Ann. Bot. 104(7): 1263-1280.

Ferrol, N., Calvente, R., Cano, C., Barea, T.M. & Azcon-Aguilar, C. 2004. Analysing arbuscular mycorrhizal fungal diversity in shrub-associated resource islands from a desertification threatened semiarid Mediterranean ecosystem. Appl. Soil Ecol. 25(2): 123-133.

Fitter, A.H. & Hay, R.K. 2012. Environmental Physiology of Plants. 3rd edition. New York: Academic Press.

Fox, J. 2008. Generalized linear models. In Applied Regression Analysis and Generalized Linear Models. 2nd ed., Chapter 15, edited by Fox, J. SAGE Publications. pp. 379-424.

Fraga-Beddiar, A. & Abda, S. 2002. Statut mycorhizien du chêne liège (Quercus suber L.) et dynamique de la symbiose au cours des saisons. Synthèse 11: 108-114.

Fraga-Beddiar, A. & Le Tacon, F. 1990. Interactions between a V.A. mycorrhizal fungus and Frankia associated with alder (Alnus glutinosa L. Gaertn.). Symbiosis 9(1–3): 247-258.

Frey-Klett, P., Chavatte, M., Clausse, M.L., Courrier, S., Roux, C.L., Raaijmakers, J. & Garbaye, J., 2005. Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads. New Phytol. 165(1): 317-328.

García, I. & Mendoza, R.E. 2008. Relationships among soil properties, plant nutrition and arbuscular mycorrhizal fungi-plant symbioses in a temperate grassland along hydrologic, saline and sodic gradients. FEMS Microbiol. Ecol. 63(3): 359-371.

Gui, M. & Nobel, P.S. 1992. Nutrient status, water uptake and gas exchange for three desert succulents infected with mycorrhizal fungi. New Phytol. 122(4): 643-649.

Guissou, T., Ba, A.M., Ouadba, J.M., Guinko, S. & Duponnois, R. 1988. Responses of Parkia biglobosa (Jacq.) Benth, Tamarindus indica L. and Zizyphus mauritiana Lam. to arbuscular mycorrhizal fungi in a phosphorus-deficient sandy soil. Biol. Fert. Soils 26(3): 194-198.

Hart, M.M., Reader, R.J. & Klironomos, J.N. 2001. Life-history strategies of arbuscular mycorrhizal fungi in relation to their successional dynamics. Mycologia 93(6): 1186-1194.

Hartnett, D.C. & Wilson, G.W. 1999. Mycorrhizae influence plant community structure and diversity in tallgrass prairie. Ecology 80(4): 1187-1195.

Jeffries, P., Gianinazzi, S., Perotto, S., Turnau, K. & Barea, J.M. 2003. The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol. Fert. Soils 37(1): 1-16.

Kessler, M., Jonas, R., Strasberg, D. & Lehnert, M. 2010. Mycorrhizal colonizations of ferns and lycophytes on the island of La Réunion in relation to nutrient availability. Basic Appl. Ecol. 11(4): 329-336.

Koske, R.E. & Halvorson, W.L. 1981. Ecological studies of vesicular-arbuscular mycorrhizae in a barrier sand dune. Can. J. Bot. 59(8): 1413-1422.

Lingfei, L., Anna, Y. & Zhiwei, Z. 2005. Seasonality of arbuscular mycorrhizal symbiosis and dark septate endophytes in a grassland site in southwest China. FEMS Microbiol. Ecol. 54(3): 367-373.

Meddad-Hamza, A., Beddiar, A., Golotte, A., Lemoine, M.C., Kuszala, C. & Gianinazzi, S. 2010. Arbuscular mycorrhizal fungi improve the growth of olive trees and their resistance to transplantation stress. Afr. J. Biotech. 9(8): 1159-1167.

Mejstřík, V.K. & Cudlín, P. 1983. Mycorrhiza in some plant desert species in Algeria. Plant Soil 71(1–3): 363-366.

Mekahlia, M.N., Beddiar, A. & Chenchouni, H. 2013. Mycorrhizal dependency in the olive tree (Olea europaea) across a xeric climatic gradient. Adv. Environ. Biol. 7(9): 2166-2174.

Montiel, S.D. & Olivares, O.J. 1997. Presencia de la micorriza vesõculo-arbuscular en cuatro cultivares de nopal (Opuntia spp.) en Hichapan, Hidalgo. In Conocimiento y Aprovechamiento del Nopal, edited by Vazquez-Alvarado, R.E., Galle-Gos-Vazquez, C., Trevin Hernandez, N. & Dõaz-Torres, Y. Memorias del VII Congreso Nacional y V Internacional. Fac. de Agronomõa, UANL, Monterrey, N.L. Mexico.

Muthukumar, T. & Udaiyan, K. 2002. Seasonality of vesicular-arbuscular mycorrhizae in sedges in a semi-arid tropical grassland. Acta Oecologica 23(5): 337-347.

Neffar, S. 2012. Étude de l’effet de l’âge des plantations de figuier de Barbarie (Opuntia ficus-indica L. Miller) sur la variation des ressources naturelles (sol et végétation) des steppes algériennes de l’Est. Cas de Souk Ahras et Tébessa. PhD Thesis, Univ. Annaba, Algeria (unpublished).

Neffar, S., Beddiar, A., Redjel, N. & Boulkheloua, J. 2011. Effets de l’âge des plantations de figuier de Barbarie (Opuntia ficus indica f. inermis) sur les propriétés du sol et la végétation à Tébessa (zone semi-aride de l’est algérien). Ecologia Mediterranea 37(1): 5-15.

Neffar, S., Chenchouni, H., Beddiar, A. & Redjel, N. 2014. Rehabilitation of degraded rangeland in drylands by Prickly pear (Opuntia ficus-indica L.) plantations: Effect on soil and spontaneous vegetation. Ecol. Balkanica 5(2): 63-76.

Nicolson, T.H. 1960. Mycorrhiza in the Gramineae. II. Development in different habitats, particularly sand dunes. Trans. Br. Mycol. Soc. 43(1): 132-145.

North, G.B. & Nobel, P.S. 1992. Drought-induced changes in hydraulic conductivity and structure in roots of Ferocactus acanthodes and Opuntia ficus-indica. New Phytol. 120(1): 9-19.

Owen, N.A. & Griffiths, H. 2014. Marginal land bioethanol yield potential of four crassulacean acid metabolism candidates (Agave fourcroydes, Agave salmiana, Agave tequilana and Opuntia ficus-indica) in Australia. GCB Bioenergy 6(6): 687-703.

Owens, H., LaFantasie, J. & Adler, P. 2012. Mycorrhization rates of two grasses following alterations in moisture inputs in a southern mixed grass prairie. Appl. Soil Ecol. 60(1): 56-60.

Pande, M. & Tarafdar, J.C. 2004. Arbuscular mycorrhizal fungal diversity in neem-based agroforestry systems in Rajasthan. Appl. Soil Ecol. 26(3): 233-241.

Pansu, M. & Gautheyrou, J. 2006. Handbook of Soil Analysis: Mineralogical, Organic and Inorganic Methods. Heidelberg: Springer-Verlag Berlin.

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. Trans. Br. Mycol. Soc. 55(1): 159-161.

Pimienta-Barrios, E., Pimienta-Barrios, E., Salas-Galvan, M., Zanudo-Hernandez, J. & Nobel, P. 2002. Growth and reproductive characteristics of the columnar cactus Stenocereus queretaroensis and their relationships with environmental factors and colonization by arbuscular mycorrhizae. Tree Physiol. 22(9): 667-674.

R Development Core Team. 2014. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: http:// www.R-project.org/.

Requena, N., Jeffries, P. & Barea, J.M. 1996. Assessment of natural mycorrhizal potential in a desertified semiarid ecosystem. Appl. Environ. Microbiol. 62(3): 842-847.

Sanon, A. 2009. Le concept de niche écologique associé à la coexistence des espèces végétales: Mise en évidence du rôle de la symbiose mycorhizienne et de sa microflore associée dans la structuration de la strate herbacée en milieu tropical. PhD Thesis, University of Nancy (unpublished).

Smith, S.E. & Read, D.J. 2008. Mycorrhizal Symbiosis. New York: Academic Press.

Snyman, H.A. 2006. A greenhouse study of root dynamics of cactus pears, Opuntia ficus-indica and O. robusta. J. Arid Environ. 65(4): 529-542.

Tilman, D., Wedin, D. & Knops, J. 1996. Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379(6567): 718-720.

Trouvelot, A., Kouche, J. & Gianinazzi-Pearson, V. 1986. Mesure du taux de mycorhization VA d’un système radiculaire: Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Les mycorhizes: Physiologie et Génétiques. Proceedings of 1st European Conference on Mycorrhizae. INRA, Dijon, Paris. pp. 217-221.

van der Heijden, M.G.A., Boller, T., Wiemken, A. & Sanders, I.R. 1998. Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79(6): 2082-2091.

Wang, G.M., Stribley, D.P., Tinker, P.G. & Walker, C. 1985. Soil pH and vesicular-arbuscular mycorrhizae, In Ecological Interactions in Soil, edited by Fitter, A.H. Oxford: Blackwell Publication. pp. 219-224.

West, N.E., Stark, J.M., Johnson, D.W., Abrams, M.M., Wight, J.R., Heggem, D. & Peck, S. 1994. Effects of climatic change on the edaphic features of arid and semi-arid lands of western North-America. Arid Soil Res. Rehabil. 8(4): 307-351.

Zañudo-Hernández, J., González del Castillo Aranda, E., Ramírez-Hernández, B.C., Pimienta-Barrios, E., Castillo- Cruz, I. & Pimienta-Barrios, E. 2010. Ecophysiological responses of Opuntia to water stress under various semi-arid environments. J. Prof. Ass. Cactus Dev. 12: 20-36.

Zhu, X.C., Song, F.B. & Xu, H.W. 2010. Arbuscular mycorrhizae improves low temperature stress in maize via alterations in host water status and photosynthesis. Plant Soil 331(1-2): 129-137.

 

 

*Corresponding author; email: neffarsouad@gmail.com

 

 

previous