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Biological Nitrogen Fixation and Mycorrhizal Associations in Agroforestry

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Tropical Agroforestry

Abstract

Biological nitrogen fixation is performed through both symbiotic and non-symbiotic means. Symbiotically, the most common association is that of roots and Rhizobium bacteria or filamentous actinomycete Frankia. Nearly all legumes used in alley cropping fix significant amounts of nitrogen in association with Rhizobium. Non-legume shrubs or trees such as Casuarinas and alders also fix significant amounts of nitrogen in association with Frankia. The amount of nitrogen fixed by legumes is variable. Leucaena leucocephala, which forms abundant nodulation, fixes between 100 and 550 kg of nitrogen per ha per year. The potential for nitrogen fixation by Acacia is also high, with up to 200 kg per ha per year. The contributions of fixed nitrogen to native as well as managed ecosystems by the actinorhizal symbioses (Frankia-non legume symbioses) are comparable to those of the more extensively studied Rhizobium-legume interactions. For instance, the roots of Casuarina equisetifolia and C. junghuhnina produce nodules where the bacteria fix atmospheric nitrogen (362 kg ha-1 year-1). The main selection criteria for provenances or species for introduction into an agroforestry system include the rate of nitrogen fixation. The species selected should have the highest possible rate for a range of climatic conditions, and must also be able to tolerate environmental constraints such as pests and low nitrogen levels in the soil. Agroforestry species form symbiotic associations with mycorrhiza, typically arbuscular mycorrhizas, to enhance nutrient and water uptake and plant growth. Possible topics of interest to researchers in agroforestry are the efficient use of ecologically adapted biofertilizers (nitrogen fixing and mycorrhizal inoculants) in relation to plant species and soil fertility (N and P availability), the quality assurance of commercial inoculants, as well as the response to inoculation (improvement of methods to estimate nitrogen fixation and P uptake).

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Bibliography

  • Akinnifesi FK, Ajayi OC, Sileshi G, Chirwa PW, Chianu J (2010) Fertiliser trees for sustainable food security in the maize-based production systems of East and Southern Africa. A review. Agron. Sustain. Dev 30:615–629

    Google Scholar 

  • Akkermans ADL, Houvers H (1983) Morphology of nitrogen fixers in forest ecosystems. In: Gordon JC, Wheeler CT (eds) Biological Nitrogen Fixation in Forest Ecosystems: Foundations and Applications. Njihoff/Junk, The Hague, The Netherlands, pp 7–53

    Google Scholar 

  • Allen ON, Allen EK (1981) The Leguminosae. A source Book of Characteristics, Uses, and Nodulation. University of Wisconsin Press, Madison, WI, USA.

    Google Scholar 

  • Andrade ACS, Queiroz MH, Hermes RAL, Oliveira VL (2000) Mycorrhizal status of some plants of the Araucaria forests and the Atlantic rainforest in santa Catarina, Brazil. Mycorrhiza 10:131–136

    Google Scholar 

  • Atayese MO, Awotoye OO, Osonubi O, Mulongoy K (1993) Comparisons of the influence of vesicular-arbuscular mycorrhiza on the productivity of hedgerow woody legumes and cassava at the top and the base of a hillslope in alley cropping system. Biol Fert Soils 16:198–204

    Google Scholar 

  • Bagyaraj DJ, Byra Reddy MS, Nalini PA (1989) Selection of an efficient inoculant VA mycorrhizal fungus for Leucaena. For Ecol Manag 27:81–85

    Google Scholar 

  • Bakarr MI, Janos DP (1996) Mycorrhizal associations of tropical legume trees in Sierra Leone, West Africa. For Ecol Manag 89:89–92

    Google Scholar 

  • Bala A, Giller KE (2001) Symbiotic specificity of tropical tree rhizobia for host legumes. New Phytol 149(3):495–507

    Google Scholar 

  • Bergersen FJ (1980) Methods for evaluating nitrogen fixation. John Wiley, New York, USA

    Google Scholar 

  • Bergersen FJ (1988) Measurements of dinitrogen fixation. In: Shamsuddin ZH, Othman WMW, Marziah M, Sundram J (eds) Biotechnology of Nitrogen Fixation in the Tropics. Universiti pertanian Malaysia, Serdang, Malaysia, pp 105–115

    Google Scholar 

  • Bond G (1983) Taxonomy and distribution of non-legume nitrogen-fixing systems. In: Gordon JC, Wheeler TC (eds), Biological Nitrogen Fixation in Forest Ecosystems: Foundations and Applications. Njihoff/Junk, The Hague, The Netherlands, pp 55–87

    Google Scholar 

  • Brady NC, Weir RR (2010) Elements of the nature and properties of soils. 3rd edn. Prentice Hall, Upper Saddle River, New Jersey, USA,p 614 with index

    Google Scholar 

  • Brewbaker JL (1987) Significant nitrogen fixing trees in agroforestry systems. In: Gholz HL (ed) Agroforestry: realities, possibilities and potentials. Martinus Njihoff, Dordrecht, The Netherlands, pp 31–45

    Google Scholar 

  • Budowski G (1983) An attempt to quantify some current agroforestry practices in Costa Rica. In: Huxley PA (ed) Plant Research and Agroforestry. ICRAF, Nairobi, Kenya, pp 43–62

    Google Scholar 

  • Busse MD (2000) Suitability and use of the 15N-isotope dilution method to estimate nitrogen fixation by actinorhizal shrubs. For Ecol Manag 136(1–3):85–95

    Google Scholar 

  • Camargo-Ricalde SL, Dhillion SS (2003) Endemic Mimosa species can serve as mycorrhizal ‘resource islands’ within semiarid communities of The Tehuacán-Cuicatlán Valley, Mexico. Mycorrhiza 13:129–136

    PubMed  Google Scholar 

  • Camargo-Ricalde SL, Montaño NM, Reyes-Jaramillo I, Jimenéz-González C, Dhillion SS (2010) Effects of mycorrhizae on seedlings on six endemic Mimosa L. species (Leguminosae-Mimosoideae) from the semi-arid Tehuacán-Cuicatlán Valley, Mexico. Trees 24:67–78

    CAS  Google Scholar 

  • Campagnac E, Piché Y, Khasa DP (2013) Relationship between genetic variability in Rhizophagus irregularis and tolerance to saline conditions. Mycorrhiza (In révision)

    Google Scholar 

  • Cardoso IM, Boddington C, Janssen BH, Oenema O, Kuyper TW (2003) Distribution of mycorrhizal fungal spores in soils under agroforestry and monocultural cropping systems in Brazil. Agrofor Syst 58:33–43

    Google Scholar 

  • Caru M, Becerra A, Sepulveda D, Cabello A (2000) Isolation of infective and effective Frankia strains from root nodules of Alnus acuminata (Betulaceae). World J Microb Biot 16:647–651

    Google Scholar 

  • Chaia EE, Wall LG, Huss-Danell K (2010) Life in soil by the actinorhizal root nodule endophyte Frankia. A review. Symbiosis 51:201–226

    Google Scholar 

  • Chakravarty P, Mishra RR (1986) The influence of VA mycorrhizae on the wilting of Albizia procera and Dalbergia sissoo. Eur J Forest Pathol 16:91–97

    Google Scholar 

  • Chen WX, Yan GH, Li JL (1988) Numerical taxonomic study of fast-growing soybean rhizobia and a proposal that Rhizobium fredii be assigned to Sinorhizobium gen. nov. Int J Syst Bacteriol 38:392–397

    Google Scholar 

  • Cooperband LR, Boerner REJ, Logan TJ (1994) Humid tropical leguminous tree and pasture grass responsiveness to vesicular-arbuscular mycorrhizal infection. Mycorrhiza 4:233–239

    Google Scholar 

  • Cornet F, Diem HG, Dommergues YR (1982) Effet de l’inoculation avec Glomus mosseae sur la croissance d’Acacia holosericea en pepiniere et apres transplantation sur le terrain. In: Les Mycorhizes : Biologie et Utilisation. INRA, Paris, France

    Google Scholar 

  • Chen W-M, Faria SM de, Straliotto R, Pitard RM, Simões-Araùjo JL, Chou J-H, Yi-Ju C, Barrios E, Prescott AR, Elliott GN, Sprent JI, Young JPW, James EK (2005) Proof that Burkholderia strains form effective symbioses with legumes: a study of novel Mimosa-nodulating strains from South America. Appl Environ Microbiol 71(11):7461–7471

    PubMed  CAS  Google Scholar 

  • Cuenca G, Azcón R (1994) Effects of ammonium and nitrate on the growth of vesicular-arbuscular mycorrhizal Erythrina poeppigiana O.I. Cook seedlings. Biol Fert Soils 18:249–254

    Google Scholar 

  • Danso SKA (1985) Methods for estimating biological nitrogen fixation. In: Sali H, Keya SO (eds) Biological Nitrogen Fixation in Africa. MIRCENS, Nairobi, Kenya pp 213–234

    Google Scholar 

  • Danso SKA, Bowen GD, Sanginga N (1992) Biological nitrogen fixation in trees in agro-ecosystems. PlantSoil 141:177–196

    CAS  Google Scholar 

  • de Carvalho AMX, de CTavarerR, Cardoso IM, Kuyper TW (2010) Mycorrhizal associations in agroforestry systems. In: Dion P (ed) Soil Biology and Agriculture in the Tropics, Soil Biology 21. doi:10.1007/978–3-642–05076-3_9. Springer-Verlag, Berlin Heidelberg

    Google Scholar 

  • De LCruzRE, Zarate JT, Aggangan NS, Lorilla EB (1992) Differential mycorrhizai dependency of some agricultural, horticultural and forestry crops to inoculation with arbuscular mycorrhizal fungi. In: Jasper D, Thomson B (eds) International Symposium on Management of Mycorrhizas in Agriculture, Forestry and Horticulture, 28 September–2 October 1992, Perth, W. Australia, Abstracts, p 54

    Google Scholar 

  • De SMoreiraFM, Soares deCT, Siqueira JO (2010) Effect of fertilizers, lime, and inoculation with rhizobia and mychorrhizal fungi on the growth of four leguminous tree species in a low-fertility soil. Biol Fertil Soils 46:771–779

    Google Scholar 

  • Diagne O, Ingleby K, Deans JD, Lindley DK, Diaite I, Neyra M (2001) Mycorrhizal inoculum potential of soils from alley cropping plots in Senegal. For Ecol Manag 146:35–43

    Google Scholar 

  • Diem HG, Gauthier D, Dommergues YR (1982) Isolation of Frankia from nodules of Casuarina equisitifolia. Canadian J Microbiol 28:526–530

    Google Scholar 

  • Diem HG, Gauthier D, Dommergues YR (1983) An effective strain of Frankia from Casuarina sp. Canadian J Botany 61:2815–2821

    Google Scholar 

  • Diouf A, Diop TA, Ndoye I, Gueye M (2008) Response of Gliricidia sepium tree to phosphorus application and inoculations with Glomus aggregatum and rhizobial strains in a sub-Saharian sandy soil. Afr J Biotechnol 7(6):766–771

    Google Scholar 

  • Diouf D, Duponnois R, Tidiane Ba A, Neyra M, Lesueur D (2005) Symbiosis of Acacia auriculiformis and Acacia mangium with mycorrhizal fungi and Bradyrhizobium spp. improves salt tolerance in greenhouse conditions. Funct Plant Biol 32:1143–1152

    CAS  Google Scholar 

  • Dixon RK, Garg VK, Rao MV (1993) Inoculation of Leucaena and Prosopis seedlings with Glomus and Rhizobium species in saline soils: rhizosphere relations and seedling growth. Arid Soil Res Rehab 7(2):133–144

    Google Scholar 

  • Dobereiner J (1984) Nodulation and nitrogen fixation in legume trees. Pesqui Agropecu Bras 19:83–90

    Google Scholar 

  • Domingo I (1983) Nitrogen fixation in Southeast Asian forestry research and practice. In: Gordon JC, Wheeler CT (eds) Biological Nitrogen Fixation in Forest Ecosystems: Foundations and Applications. Njihoff/Junk, The Hague, The Netherlands, pp 295–313

    Google Scholar 

  • Dommergues YR (1997) Contribution of actinorhizal plants to tropical soil productivity and rehabilitation. Soil Biol Biochem 29(5/6):931–941

    CAS  Google Scholar 

  • Dreyfus BL, Dommergues YR (1981) Nodulation of Acacia species by fast- and slow-growing tropical strains. Appl Environm Microbiol 41:97–99

    CAS  Google Scholar 

  • Dreyfus B, Garcia JL, Gillis M (1988) Characterization of Azorhizobium caulinodans gen. nov., sp. nov., a stem-nodulating nitrogen-fixing bacterium isolated from Sesbania rostrata. Int J Syst Bacteriol 38:89–98

    CAS  Google Scholar 

  • Duguma B, Tonye J (1994) Screening of multipurpose tree a nd shrub species for agroforestry in the humid lowlands of Cameroon. For Ecol Manag 64(2–3):135–143

    Google Scholar 

  • Elkan GH (1984) Taxonomy and metabolism of Rhizobium and its genetic relationships. In: Alexander M (ed) Biological Nitrogen Fixation, Ecology, Technology, and Physiology. Plenum Press, New York, USA, pp 1–38

    Google Scholar 

  • Elliott GN, Chen W-M, Chou J-H, Wang H-C, Sheu S-Y, Perin L, Reis VM, Moulin L, Simon MF, Bontemps C, Sutherland JM, Bessi R, De Faria SM, Trinick MJ, Prescott AR, Sprent JI, James EK (2007) Burkholderia phymatum is a highly effective nitrogen-fixing symbiont of Mimosa spp., and fixes ex planta. New Phytol 173(1):168–180

    PubMed  CAS  Google Scholar 

  • Evans DO, Rotar PP (1987) Sesbania in Agriculture. Westview Press, Boulder, CO, USA

    Google Scholar 

  • Fagbola O, Osonubi O, Mulongoy K, Odunfa SA (2001) Effects of drought stress and arbuscular mycorrhiza on the growth of Gliricidia sepium (Jacq). Walp, and Leucaena leucocephala (Lam.) de Wit. in simulated eroded soil conditions. Mycorrhiza 11:215–223

    Google Scholar 

  • Founoune H, Duponnois R, Ba AM, Sall S, Branget I, Lorquin J, Neyra M, Chotte JL (2002) Mycorrhiza Helper Bacteria stimulate ectomycorrhizal symbiosis of Acacia holoricea with Pisolithus alba. New Phytol 153:81–89

    Google Scholar 

  • Fried M, Danso SK, Zapata AF (1983) The methodology of measurement of N2 fixation by nonlegumes as inferred from field experiments with legumes. Can J Microbiol 29:1053–1062

    Google Scholar 

  • Franco AA (1984) Nitrogen fixation in trees and soil fertility. Pesqui Agropecu Bras 19:253–261

    CAS  Google Scholar 

  • Franco AA, De Faria SM (1997) The contribution of N2-fixing tree legumes to land reclamation and sustainability in the tropics. Soil Biol Biogeochem 29(5/6):897–903

    CAS  Google Scholar 

  • Ganry F, Diem HG, Wey J, Dommergues YR (1985) Inoculation with Glomus mosseae improves N2 fixation by field-grown soybeans. Biol Fertil Soils 1:15–23

    Google Scholar 

  • Gathumbi SM, Cadisch G, Giller KE (2002) 15N natural abundance as a tool for assessing N2-fixation of herbaceous, shrub and tree legume in improved fallows. Soil Biol Biogeochem 34(8):1059–1071

    CAS  Google Scholar 

  • Gauthier DL, Diem HG, Dommergues YR (1984) Tropical and subtropical actinorhizal plants. Pesqui Agropec Bras 19:119–136

    CAS  Google Scholar 

  • Gauthier DL, Diem HG, Dommergues YR, Ganry F (1985) Assessment of N2 fixation by Casuarina equisitifolia inoculated with Frankia ORS021001 using 15N methods. Soil Biol Biochem 17:375–379

    CAS  Google Scholar 

  • Gehring C, Vlek PLG (2004) Limitations of the 15N natural abundance method for estimating biological nitrogen fixation in Amazonian forest legumes. Basic Appl Ecol 5(6):567–580

    CAS  Google Scholar 

  • Ghosh S, Verma NK (2006) Growth and mycorrhizal dependency of Acacia mangium Willd. inoculated with three vesicular arbuscular mycorrhizal fungi in lateritic soils. New Forest 31:75–81

    Google Scholar 

  • Gibson AH, Dreyfus BL, Dommergues YR (1982) Nitrogen fixation by legumes. In: Dommergues YR, Diem HG (eds) Microbiology of Tropical soils and Plant Productivity. Martinus Njhoff, The Hague, The Netherlands, pp 37–73

    Google Scholar 

  • Grossman JM, Sheaffer C, Wyse D, Bucciarelli B, Vance C, Graham PH (2006) An assessment of nodulation and nitrogen fixation in inoculated Inga oerstediana, a nitrogen-fixing tree shading organically grown coffee in Chiapas, Mexico. Soil Biol Biogeochem 38(4):769–784

    CAS  Google Scholar 

  • Habte M, Aziz T (1985) Response of Sesbania grandiflora to inoculation of soil with vesicular-arbuscular mycorrhizal fungi. Appl Environ Microbiol 50(3):701–703

    PubMed  CAS  Google Scholar 

  • Habte M, Manjunath A (1987) Soil solution phosphorus status and mycorrhizal dependency in Leucaena leucocephala. Applied Environ. Microbiol 43:797–801

    Google Scholar 

  • Habte M, Musoko M (1994) Changes in the vesicular-arbuscular mycorrhizal dependency of Albizia ferruginea and Enterolobium cyclocarpum in response to soil phosphorus concentration. J Plant Nutr 17(10):1768–1780

    Google Scholar 

  • Halliday J (1984) Register of nodulation reports for leguminous trees and other arboreal genera with nitrogen-fixing trees. Nitrogen-Fixing Tree Research Reports 4:38–45

    Google Scholar 

  • Halliday J, Somasegaran P (1983) Nodulation, nitrogen fixation, and Rhizobium and strain affinities in the genus Leucaena. In: Leucaena Research in the Asia-Pacific region. IDRC, Ottawa, Canada

    Google Scholar 

  • Haselwandter K, Bowen GD (1996) Mycorrhizal relations in trees for agroforestry and land rehabilitation. For Ecol Manag 81:1–17

    Google Scholar 

  • Hayman DS (1986) Mycchorhizae of nitrogen-fixing legumes. MIRCEN J 2:121–145

    Google Scholar 

  • Herridge DF (1982) A whole-system approach to quantifying biological nitrogen fixation by legumes and associated gains and losses of nitrogen in agricultural systems. In: Graham PH, Harris SC (eds) Biological nitrogen fixation technology for tropical agriculture. CIAT, Cali, Colombia

    Google Scholar 

  • Herridge DF, Bergersen FJ, Peoples MB (1990) Measurement of nitrogen fixation by soybean in the field using the ureide and natural 15N abundance methods. Plant Physiol 93:708–716

    PubMed  CAS  Google Scholar 

  • Higo M, Isobe K, Kang D-J, Maekawa T, Ishii R (2011) Molecular diversity and spore density of indigenous arbuscular mycorrhizal fungi in acid sulfate soil in Thailand. Ann Microbiol 61:383–389

    Google Scholar 

  • Högberg P, Kvarnström M (1982) Nitrogen fixation by the woody legume Leucaena leucocephala. Plant Soil 66:21–28

    Google Scholar 

  • Hu TW, Kiang T (1983) Leucaena research in Taiwan. In: Leucaena Research in the Asian-Pacific Region. IDRC, Ottawa, Canada

    Google Scholar 

  • Huang RS, Smith WK, Yost RS (1985) Influence of vesicular-arbuscular mycorrhiza on growth, water relations and leaf orientation in Leucaena leucocephala (LAM.) de Wit. New Phytol 99:229–243

    Google Scholar 

  • Hutton EM (1984) Breeding and selecting Leucaena for acid tropical soils. Pesqu Agropecu Bras 19:263–274

    CAS  Google Scholar 

  • Iglesias L, Salas E, Leblanc HA, Nygren P (2011) Response of Theobroma cacao and Inga edulis seedlings to cross-inoculated populations of arbuscular mycorrhizal fungi. Agrofor Syst. doi: 10.1007/s10457–011-9400–9

    Google Scholar 

  • Ingleby K, Diagne O, Deans JD, Lindley DK, Neyra M, Ducousso M (1997) Distribution of roots, arbuscular mycorrhizal colonisation and spores around fast-growing tree species in Senegal. For Ecol Manag 90:19–27

    Google Scholar 

  • Ingleby K, Wilson J, Munro RC, Cavers S (2007) Mycorrhizas in agroforestry: spread and sharing of arbuscular mycorrhizal fungi between trees and crops: complementary use of molecular and microscopic approaches. Plant Soil 294:125–136

    CAS  Google Scholar 

  • IRRI (1988) Green manure in rice farming: Proceedings of a symposium on sustainable agriculture. International Rice Research Institute, Los Banos, The Philippines

    Google Scholar 

  • Jalonen R, Nygren P, Sierra J (2009) Transfer of nitrogen from a tropical legume tree to an associated fodder grass via root exudation and common mycelial networks. Plant. Cell Environ 32:1366–1376

    CAS  Google Scholar 

  • Jefwa JM, Sinclair R, Maghembe JA (2006) Diversity of glomalean mycorrhizal fungi in maize/sesbania intercrops and maize monocrop in southern Malawi. Agrofor Syst 67:107–114

    Google Scholar 

  • Kernaghan G, Hambling B, Fung M, Khasa DP (2002) In vitro selection of boreal ectomycorrhizal fungi for use in reclamation of saline-alkaline habitats. Restor Ecol 10:43–51

    Google Scholar 

  • Kessel C, Naskao P (1986) The use of nitrogen-15-depleted ammonium sulfate for estimating nitrogen fixation by leguminous trees. Agron J 78:549–551

    Google Scholar 

  • Khasa DP, Furlan V, Fortin JA (1992) Response of some tropical plant species to endomycorrhizal fungi under field condition. Trop Agr 69:279–283

    Google Scholar 

  • Khasa DP, Vallée G, Bousquet J (1994) Biological considerations in the utilization of Racosperma auriculiforme and R. mangium in tropical countries with emphasis on Zaire. J Trop Forest Res 6:422–443

    Google Scholar 

  • Khurma UR, Mangotra A (2004) Screening of some Leguminosae seeds for nematicidal activity. The South Pacific J Nat Sci 22(1):51–53

    Google Scholar 

  • Knowles R (1983) Nitrogen fixation in natural plant communities and soils. In: Bergersen FJ (ed) Methods for evaluating biological nitrogen fixation. John Wiley, New York, USA

    Google Scholar 

  • Ladha JK, Peoples MB, Garrity DP, Capuno VT, Dart PJ (1993) Estimating dinitrogen fixation of hedgerow vegetation using the nitrogen-15 natural abundance method. Soil Sci Soc Am J 57(3):732–737

    CAS  Google Scholar 

  • La Malfa S, Tribulato E, Ventura M, Gioacchini P, Tagliavini M (2010) 15N natural abundance technique does not reveal the presence of nitrogen from biological fixation in field grown Carob (Ceratonia siliqua L.) trees. Acta Hort. (ISHS) 868:191–196

    Google Scholar 

  • Lambers H (2003) Dryland salinity: a key environmental issue in southern Australia. Plant Soil 257:v–vii

    CAS  Google Scholar 

  • LaRue TA, Patterson TG (1981) How much nitrogen do legumes fix? Adv Agron 34:15–38

    CAS  Google Scholar 

  • Lesueur D, Ingleby K, Odee D, Chamberlain J, Wilson J, Tiki-Manga T, Sarrailh J-M, Pottinger A (2001) Improvement of forage production in Calliandra calothyrsus: methodology for the identification of an effective inoculum containing Rhizobium strains and arbuscular mychorrizal inoculates. J Biotechnol 91(2–3):269–282

    PubMed  CAS  Google Scholar 

  • Lesueur D, Sarr A (2008) Effects of single and dual inoculation with selected microsymbionts (rhizobia and arbuscular mycorrhizal fungi) on field growth and nitrogen fixation of Calliandra calothyrsus Meissn. Agrofor Syst 73:37–45

    Google Scholar 

  • Liang Z (1986) Vegetative propagation and selection of Casuarina for resistance to bacterial wilt. Tropical Forestry (Science and Technology) Guangazhou 2:1–6

    Google Scholar 

  • Ligon JM, Nakas JP (1987) Isolation and characterization of Frankia sp. Strain FaC1 genes involved in nitrogen fixation. Appl Environ Microbiol 53(10):2321–2327

    PubMed  CAS  Google Scholar 

  • Lindbald P, Russo R (1986) C2H2-reduction by Erythrina poeppigiana in a Costa Rican coffee plantation. Agrofor Syst 4:33–37

    Google Scholar 

  • Lulandala LLL, Hall JB (1986) Leucaena’s leucocephala’s biological nitrogen fixation: A promising substitute for inorganic nitrogen fertilization in agroforestry systems. In: Shamsuddin ZH, Othman WMW, Marziah M, Sundram J (eds) Biotechnology of nitrogen fixation in the tropics (BIOnifT), proceedings of UNESCO regional symposium and workshop. Universiti Pertanian Malaysia, Serdang, Malaysia

    Google Scholar 

  • Maia J, Scotti MR (2010) Growth of Inga vera Willd. Subsp. Affinis under rizobia inoculation. R. C. Suelo Nutr. Veg 10(2):139–149

    Google Scholar 

  • Mansour SR, Baker DD (1994) Selection trials for effective N2-fixing Casuarina-Frankia combinations in Egypt. Soil Biol Biogeochem 26(5):655–658

    Google Scholar 

  • Martinez-Romero E, Segovia L, Martins Mercante F, Antonio Franco A, Graham P, Pardo MA (1991) Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena leucocephala trees. Int J Syst Evol Microbiol 41:417–426

    CAS  Google Scholar 

  • Michelsen A, Rosendahl S (1990) The effect of VA mycorrhizal fungi, phosphorus and drought stress on the growth of Acacia nilotica and Leucaena leucocephala seedlings. Plant Soil 124:7–13

    CAS  Google Scholar 

  • Milnystki F, Frioni L, Agius F (1997) Characterization of rhizobia that nodulate native legume trees from Uruguay. Soil Biol Biogeochem 29(5–6):989–992

    Google Scholar 

  • Moreira FMS, Cruz L, Faria SM, Marsh T, Martinez-Romero E, Pedrosa FO, Pitard RM, Young JPW (2006) Azorhizobium doebereinerae sp. Nov. Microsymbiont of Sesbania virgata (Caz.) Pers Syst Appl Microbiol 29:197–206

    Google Scholar 

  • Muleta D, Assefa F, Nemomissa S, Granhall U (2008) Distribution of arbuscular mycorrhizal fungi spores in soils of smallholder agroforestry and monocultural coffee systems in southwestern Ethiopia. Biol Fertil Soil 44:653–659

    Google Scholar 

  • Muthukumar T, Senthilkumar M, Rajangam M, Udaiyan K (2006) Arbuscular mycorrhizal morphology and dark septate fungal associations in medicinal and aromatic plants of Western Ghats, Southern India. Mycorrhiza 17:11–24

    PubMed  CAS  Google Scholar 

  • NAS (1984) Casuarinas: Nitrogen-Fixing Trees for Adverse Sites. National Academy of Sciences, Washington, DC, USA

    Google Scholar 

  • Ndiaye F, Manga A, Diagne-Leye G, Ndiaye Samba SA, Diop TA (2009) Effects of rockphosphate and arbuscular mycorrhiza fungi on growth and nutrition of Sesbania sesban and Gliricidia sepium. Afr J Microbiol Res 3(5):305–309

    Google Scholar 

  • Ndoye I, Dreyfus B (1988) N2 fixation by Sesbania rostrata and Sesbania sesban using 15N and total N difference methods. Soil Biol Biogeochem 20(2):209–213

    CAS  Google Scholar 

  • Ndoye I, Gueye M, Danso SKA, Dreyfus B (1995) Nitrogen fixation in Faidherbia albida, Acacia raddiana, Acacia Senegal and Acacia seyal estimated using the 15N isotope dilution technique. Plant Soil 172:175–180

    CAS  Google Scholar 

  • Nichols JD, Carpentier FL (2006) Interplanting Inga edulis yields nitrogen benefits to Terminalia amazonia. For Ecol Manag 233(2–3):344–351

    Google Scholar 

  • Nick G, Paget E, Simonet P, Moiroud A, Normand P (1992) The nodular endophytes of Coriaria spp. form a distinct lineage within the genus Frankia. Mol Ecol 1:175–181

    PubMed  CAS  Google Scholar 

  • Nygren P, Ramirez C (1995) Production and turnover of N2 fixing nodules in relation to foliage development in periodically pruned Erythrina poeppigiana (Leguminosae) tress. For Ecol Manag 73(1–3):59–73

    Google Scholar 

  • Okon IE (2011) Field response of two cassava genotypes inoculated with arbuscular mycorrhizal fungus to Gliricidia sepium mulch in a tropical Alfisol. Bot Res Int 4(1):04–08

    Google Scholar 

  • Okon IE, Osonubi O, Sanginga N (1996) Vesicular-arbuscular mycorrhiza effects on Gliricidia sepium and Senna siamea in a fallowed alley cropping system. Agrofor Syst 33:165–175

    Google Scholar 

  • Oliveira RS, Castro PML, Dodd JC, Vosatka M (2005) Synergistic effects of Glomus intraradices and Frankia spp on the growth and stress recovery of Alnus glutinosa in an alkaline anthropogenic sediment. Chemosphere 60(10):1462–1470

    PubMed  CAS  Google Scholar 

  • Orchard ER, Darby GD (1956) Fertility changes under continued wattle culture with special reference to nitrogen fixation and base status of the soil. In: Comptes Rendus du sixième Congrès. International Science du Sol, Paris, France

    Google Scholar 

  • Osonubi O, Atayese MO, Mulongoy K (1995) The effect of vesicular-arbuscular mycorrhizal inoculation on nutrient uptake and yield of alley-cropped in a degraded Alfisol of southwestern Nigeria. Biol Fertil Soil 20:70–76

    Google Scholar 

  • Osonubi O, Bakare ON, Mulongoy K (1992) Interactions between drought stress and vesicular-arbuscular mycorrhiza on the growth of Faidherbia albida (syn. Acacia albida) and Acacia nilotica in sterile and non-sterile soils. Biol Fertil Soil 14:159–165

    Google Scholar 

  • Osonubi O, Mulongoy K, Awotoye OO, Atayese MO, Okali DUU (1991) Effects of ectomycorrhizal and vesicular-arbuscular mycorrhizal fungi on drought tolerance of four leguminous woody seedlings. Plant Soil 136:131–143

    Google Scholar 

  • Peoples MB, Herridge DF (1990) Nitrogen fixation by legumes in tropical and subtropical agriculture. Adv Agron 44:155–223

    CAS  Google Scholar 

  • Peoples MB, Faizah AW, Rerkasem B, Herridge DF (1989) Methods for Evaluating Nitrogen Fixation by Nodulated Legumes in the Field. Monograph No 11, ACIAR, Canberra, Australia

    Google Scholar 

  • Pindi KP (2011a) Influence of bioinoculants on the growth of Albizia lebbeck in nursery conditions. Res J Agr Sci 2(2):265–268

    Google Scholar 

  • Pindi KP (2011b) Influence of bioinoculants on establishment of micropropagated plantlets of Sesbania grandiflora. Res J Agr Sci 2(1):114–118

    Google Scholar 

  • Pindi KP, Reddy SR, Reddy SM (2000) Mycorrhizal dependency of some agroforestry tree species. Indian Forest 126(4):397–402

    Google Scholar 

  • Puppo A, Dimitrevic L, Diem HG, Dommergues YR (1985) Homogeneity of superoxide dismutase patterns in Frankia strains from Casuarinaceae. FEMS Microbiol Lett 30:43–46

    CAS  Google Scholar 

  • Purcino AAC, Lurlarp C, Lynd JQ (1986) Mycorrhizal and soil fertility effects with growth, nodulation and nitrogen fixation of leucaena grown on a typic eutrustox. Commun Soil Sci Plan 17(5):473–489

    Google Scholar 

  • Purwantari ND, Date RA, Dart PJ (1995) Nodulation and N2-fixation by Calliandra calothyrsus and Sesbania sesban grown at different room temperatures. Soil Biol Biogeochem 27(4–5):421–425

    CAS  Google Scholar 

  • Rahman MK, Parsons JW (1997) Effects of inoculation with Glomus mosseae, Azorhizobium caulinodans and rock phosphate on the growth of and nitrogen and phosphorus accumulation in Sesbania rostrata. Biol Fertil Soil 25:47–52

    CAS  Google Scholar 

  • Reddell PW (1986) Management of nitrogen fixation by Casuarina. ACIAR Forest Newslett 2:1–3

    Google Scholar 

  • Reddell PW, Bowen GD, Robson AD (1986) Nodulation of Casuarinaceae in relation to host species and soil properties. Aust J Bot 34:435–444

    Google Scholar 

  • Reed SC, Cleveland CC, Townsend AR (2007) Controls over leaf litter and soil nitrogen fixation in two lowland tropical rainforests. Biotropica 39(5):585–592

    Google Scholar 

  • Reena J, Bagyaraj DJ (1990) Response of Acacia nilotica and Calliandra calothyrsus to different VA mycorrhizal fungi. Arid Soil Res Rehab 4:261–268

    Google Scholar 

  • Rodriguez-Echeverria S, Crisostomo JA, Freitas H (2007) Genetic diversity of rhizobia associated with Acacia longifolia in two-stages of invasion of coastal sand dunes. Appl. Environ. Microbiol. doi: 10.1128/AEM.00613–07

    Google Scholar 

  • Roskoski JP (1981) Nodulation and N2 fixation by Inga jinicuil, a woody legume in coffee plantations. I. Measurements of nodule biomass and field C2H2 reduction rates. Plant Soil 59:201–206

    CAS  Google Scholar 

  • Roskoski JP (1982) Nitrogen fixation in a Mexican coffee plantation. In: Robertson GP, Herrera R, Roswall T (eds) Nitrogen Cycling in Ecosystems of Latin America and the Caribbean. Martinus Njihoff, The Hague, The Netherlands, pp 283–292

    Google Scholar 

  • Roskoski JP (1986) Future directions in biological nitrogen fixation research. In: Shamsuddin ZH, Othman WMW, Marziah M, Sundram J (eds) Biotechnology of Nitrogen Fixation in the Tropics. Universiti Pertanian Malaysia, Serdang, Malaysia

    Google Scholar 

  • Roskoski JP, Kessel C van, Castilleja G (1982) Nitrogen fixation by tropical woody legumes: Potential source of soil enrichment. In: Graham PH (ed) Biological Nitrogen Fixation Technology for Tropical Agriculture. CIAT, Cali, Colombia, pp 447–454

    Google Scholar 

  • Rouvier C, Prin Y, Reddell P, Normand P, Simonet P (1996) Genetic diversity among Frankia strains nodulating members of the family Casuarinaceae in Australia revealed by PCR and restriction fragment length polymorphism analysis with crushed root nodules. Appl Environ Microbiol 62(3):979–985

    PubMed  CAS  Google Scholar 

  • Roy S, Khasa DP, Greer CW (2007) Combining alders, frankiae, and mycorrhizae for the revegetation and remediation of contaminated ecosystems. Can J Bot 85:237–251

    CAS  Google Scholar 

  • Russo RO (1989) Evaluating alder-endophyte (Alnus acuminata-Frankia-Mycorrhizae) interactions. I. Acetylene reduction in seedlings inoculated with Frankia strain ArI3 and Glomus intra-radices, under three phosphorus levels. Plant Soil 118:151–155

    Google Scholar 

  • Sanginga P, Danso SKA, Bowen GD (1992) Variation in growth, sources of nitrogen and N-use efficiency by provenances of Gliricidia sepium. Soil Biol Biogeochem 24(10):1021–1026

    Google Scholar 

  • Sanginga N, Mulongoy K, Ayanaba A (1985) Effect of inoculation and mineral nutrients on nodulation and growth of Leucaena leucocephala. In: Ssali H, and Keys SO (eds) Biological Nitrogen Fixation in Africa. MIRCEN, Nairobi, Kenya

    Google Scholar 

  • Sanginga N, Mulongoy K, Ayanaba A (1986) Inoculation of Leucaena leucocephala (Lam.) de Wet with Rhizobium and its nitrogen contribution to a subsequent maize crop. Biol agric Hortic 3:347–352

    Google Scholar 

  • Sanginga N, Mulongoy K, Ayanaba A (1988) N contribution of leucaena/rhizobium symbiosis to soil and and a subsequent maize crop. Plant Soil 112:137–141

    CAS  Google Scholar 

  • Sanginga N, Mulongoy K, Ayanaba A (1989) Nitrogen fixation of field-inoculated Leucaena leucocephala (Lam) de Wit estimated by the 15N and difference methods. Plant Soil 117:269–274

    Google Scholar 

  • Sanginga N, Zapata F, Danso SKA, Bowen GD (1990) Effects of successive cuttings on uptake and partitioning of 15N among plant parts of Leucaena leucocephala. Biol Fertil Soil 9:37–42

    Google Scholar 

  • Schenck NC (1982) Methods and principles of mycorrhizal research. American Phytopathological Society, Saint-Paul, Minnesota, USA

    Google Scholar 

  • Sebuliba E, Nyeko P, Majaliwa JGM, Kizza LC, Eilu G, Adipala E (2010) Effect of selected arbuscular mycorrhiza fungi on the growth of Calliandra calothyrsus and Sorghum bicolor in eastern Uganda. Second RUFORUM Biennial Meeting 20–24 September 2010, Entebbe, Uganda

    Google Scholar 

  • Shepherd KD, Jefwa J, Wilson J, Ndufa JK, Ingleby K, Mbuthia KW (1996) Infection potential of farm soils as mycorrhizal inocula for Leucaena leucocephala. Biol Fertil Soil 22:16–21

    Google Scholar 

  • Shepherd M, Nguyen L, Jones ME, Nichols JD, Carpenter FL (2007) A method for assessing arbuscular mycorrhizal fungi group distribution in tree roots by intergenic transcribed sequence variation. Plant Soil 290:259–268

    CAS  Google Scholar 

  • Sogo A, Setoguchi H, Noguchi J, Jaffre T, Tobe H (2001) Molecular phylogeny of Casuarinaceae based on rbcL and matK gene sequences. J Plant Res 114:459–464

    CAS  Google Scholar 

  • Subhan S, Sharmila P, Pardha Saradhi P (1998) Glomus fasciculatum alleviates transplantation shock of micropropagated Sesbania sesban. Plant Cell Rep 17:268–272

    CAS  Google Scholar 

  • Staal M, te Lintel-HekkertS, Harren F, Stal L (2001) Nitrogenase activity in cyanobacteria measured by the acetylene reduction assay: a comparison between batch incubation and on-line monitoring. Environ Monit 3(5):343–351

    CAS  Google Scholar 

  • Stamford NP, Ortega AD, Temprano F, Santos DR (1997) Effects of phosphorus fertilization and inoculation of Bradyrhizobium and mycorrhizal fungi on the growth of Mimosa caesalpiniaefolia in acid soil. Soil Biol Biochem 9(5/6):959–964

    Google Scholar 

  • Virginia RA, Jarrell WM, Kohl DH, Shearer GB (1981) Symbiotic nitrogen fixation in Prosopis (Leguminosae) dominated ecosystems. In: Gibbson AH, Newton WE (eds) Current Perspectives in Nitrogen Fixation. Australian Academy of Sciences, Canberra, Australia

    Google Scholar 

  • Waring HD (1985) Chemical fertilization and its economic aspects. In: Burnley J, Stewart JL (eds) Increasing Productivity of Multipurpose Species. IUFRO, Vienna, Austria

    Google Scholar 

  • Wang ET, Martinez-Romero J, Martinez-Romero E (1999) Genetic diversity of rhizobia from Leucaena leucocephala nodules in Mexican soils. Mol Ecol 8(5):711–724

    Google Scholar 

  • Wang ET, Tan ZY, Willems AY, Fernandez-Lopez M, Reinhold-Hurek B, Martinez-Romero E (2002) Sinorhizobium morelense sp. Nov. , a Leucaena leucocephala-associated bacterium that is highly resistant to multiple antibiotics. Int J Syst Evol Micr 52:1687–1693

    CAS  Google Scholar 

  • Warembourg FR (1993) Nitrogen fixation in soil and plant systems. In: Knowles R, Blackburn TH (eds) Nitrogen isotope techniques. Academic Press, San Diego, USA, pp 127–156

    Google Scholar 

  • West JB, HilleRisLambers J, Lee TD, Hobbie SE, Reich PB (2005) Legume species identity and soil nitrogen supply determine symbiotic nitrogen-fixation responses to elevated atmospheric [CO2]. New Phytol 167:523–530

    PubMed  CAS  Google Scholar 

  • Whitbeck JL (2001) Effects of light environment on vesicular-arbuscular mycorrhiza development in Inga leiocalycina, a tropical wet forest tree. Biotropica 33(2):303–311

    Google Scholar 

  • Williams PK (1984) Current use of legume inoculant technology. In: Alexander M (ed) Biological Nitrogen Fixation: ecology, technology and physiology. Plenum Press, New York, USA, pp 173–200

    Google Scholar 

  • Witty JF, Minchin FR (1988) Measurements of nitrogen fixation by acetylene reductions assay: myths and mysteries. In: Beck DP, Materon LA (eds) Nitrogen fixation: achievements and objectives. Chapman and Hall, New York, pp 285–292

    Google Scholar 

  • Woldemeskel E, Singlair FL (1998) Variation in seedling growth, nodulation and nitrogen fixation of Acacia nilotica inoculated with eight rhizobial strains. For Ecol Manag 104(1–3):239–247

    Google Scholar 

  • Wubet T, Kottke I, Teketay D, Oberwinkler F (2003) Mycorrhizal status of indigenous trees in dry Afromontane forests of Ethiopia. For Ecol Manag 179:387–399

    Google Scholar 

  • Yadav JSP (1983) Soil limitations for successful establishment and growth of Casuarina plantations. In: Midgley SJ, Turnbull JW, Johnson RD (eds) Casuarina Ecology: Management and Utilization. CSIRO, Melbourne, Australia, pp 138–157

    Google Scholar 

  • Zangaro W, Nishidate FR, Camargo FRS, Romagnoli GG, Vandressen J (2005) Relationships among arbuscular mycorrhizas, root morphology and seedling growth of tropical native woody species in southern Brazil. J Trop Ecol 21:529–540

    Google Scholar 

  • Zhang Z, Lopez MF, Torrey JG (1984) A comparison of cultural characteristics and infectivity of Frankia isolates from root nodules of Casuarina species. Plant Soil 78:79–90

    Google Scholar 

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Atangana, A., Khasa, D., Chang, S., Degrande, A. (2014). Biological Nitrogen Fixation and Mycorrhizal Associations in Agroforestry. In: Tropical Agroforestry. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7723-1_8

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