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Cultured arbuscular mycorrhizal fungi and native soil inocula improve seedling development of two pioneer trees in the Andean region

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The tree species Alnus acuminata and Morella pubescens, native to South America, are candidates for soil quality improvement and afforestation of degraded areas and may serve as nurse trees for later inter-planting of other trees, including native crop trees. Both species not only form symbioses with arbuscular mycorrhizal fungi (AMF) and ectomycorrhizal fungi (EMF), but also with N2-fixing actinobacteria. Because tree seedlings inoculated with appropriate mycorrhizal fungi in the nursery resist transplanting stress better than non-mycorrhizal seedlings, we evaluated for A. acuminata and M. pubescens the potential of inoculation with mycorrhizal fungi for obtaining robust tree seedlings. For the first time, a laboratory-produced mixed AMF inoculum was tested in comparison with native soil from stands of both tree species, which contains AMF and EMF. Seedlings of both tree species reacted positively to both types of inocula and showed an increase in height, root collar diameter and above- and belowground biomass production, although mycorrhizal root colonization was rather low in M. pubescens. After 6 months, biomass was significantly higher for all mycorrhizal treatments when compared to control treatments, whereas aboveground biomass was approximately doubled for most treatments. To test whether mycorrhiza formation positively influences plant performance under reduced water supply the experiment was conducted under two irrigation regimes. There was no strong response to different levels of watering. Overall, application of native soil inoculum improved growth most. It contained sufficient AMF propagules but potentially also other soil microorganisms that synergistically enhance plant growth performance. However, the AMF inoculum pot-produced under controlled conditions was an efficient alternative for better management of A. acuminata and M. pubescens in the nursery, which in the future may be combined with defined EMF and Frankia inocula for improved management practices.

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References

  • Aguirre N, Palomeque X, Weber M, Stimm B, Günter S (2011) Reforestation and natural succession as tools for restoration on abandoned pastures in the Andes of South Ecuador. In: Günter S, Weber M, Stimm B (eds) Tropical forestry 8, pp 513–524

  • Akthar MS, Siddiqui ZA (2008) Arbuscular mycorrhizal fungi as potential bioprotectants against plant pathogens. In: Siddiqui ZA, Akhtar MS, Futai K (eds) Mycorrhizae: sustainable agriculture and forestry. Springer, Dordrecht, pp 61–97

    Google Scholar 

  • Allen MF, Allen EB, Gómez-Pompa A (2005) Effects of mycorrhizae and nontarget organisms on restoration of a seasonal tropical forest in Quintana Roo, Mexico: factors limiting tree establishment. Restor Ecol 13:325–333

    Article  Google Scholar 

  • Aristizabal C (2008) Arbuscular mycorrhizal fungi enhance the acquisition of mineral nutrients from leaf litter by Morella cerifera. Dissertation University of Miami, Florida

  • Audet P, Charest C (2010) Identification of constraining experimental-design factors in mycorrhizal pot-growth studies. J Bot 2010. Article ID 718013. doi:10.1155/2010/718013

  • Augé RM (2001) Water relations, drought and vesicular–arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Averby A, Ulf G (1998) Occurrence and succession of mycorrhizas in Alnus incana. Swed J Agric Res 28:117–127

    Google Scholar 

  • Becerra A, Cabello M (2007) Micorrizas arbusculares en plantines de Alnus acuminata (Betulaceae) inoculados con Glomus intraradices (Glomaceae). Bol Soc Argent Bot 42:155–158

    Google Scholar 

  • Becerra A, Zak M (2011) The ectomycorrhizal symbiosis in South America: morphology, colonization, and diversity. In: Rai M, Varma A (eds) Diversity and biotechnology of ectomycorrhizae. Soil Biol 25:19–41

  • Becerra A, Pritsch K, Arrigo N, Palma M, Bartoloni N (2005a) Ectomycorrhizal colonization of Alnus acuminata Kunth in northwestern Argentina in relation to season and soil parameters. Ann For Sci 62:325–332

    Article  Google Scholar 

  • Becerra A, Zak R, Horton T, Micolini J (2005b) Ectomycorrhizal and arbuscular mycorrhizal colonization of Alnus acuminata from Calilegua National Park (Argentina). Mycorrhiza 15:525–531

    Article  PubMed  Google Scholar 

  • Becerra A, Cabello M, Zak M, Bartoloni N (2009) Arbuscular mycorrhizae of dominant plant species in Yungas forests, Argentina. Mycologia 101:612–621

    Article  PubMed  Google Scholar 

  • Beck E, Richter M (2008) Ecological aspects of a biodiversity hotspot in the Andes of southern Ecuador. In: Gradstein SR, Homeier J, Gansert J (eds) The tropical mountain forest: patterns and processes in a biodiversity hotspot. Biodivers Ecol Ser 2:195–217

  • Berliner R, Torrey JG (1988) On tripartite Frankia-mycorrhizal associations in the Myricaceae. Can J Bot 67:1708–1712

    Article  Google Scholar 

  • Botero C, Dussán J (2001) La micorrización del aliso Alnus acuminata H.B.K. sub sp. acuminata con suelos nativos y sobre el crecimiento. Actual Biol 23:33–40

    Google Scholar 

  • Brummitt N, Lughadha EN (2003) Biodiversity: where’s hot and where’s not. Conserv Biol 17:1442–1448

    Article  Google Scholar 

  • Carú A, Becerra D, Sepúlveda A, Cabello A (2000) Isolation of infective and effective Frankia strains from root nodules of Alnus acuminata (Betulaceae). World J Microbiol Biotech 16:647–651

    Article  Google Scholar 

  • Cervantes E, Rodríguez-Barrueco C (1992) Relationships between the mycorrhizal and actinorhizal symbioses in nonlegumes. In: Norris J, Read D, Varma A (eds) Techniques for the study of mycorrhizae, methods in microbiology, vol 24. Academic Press, New York, pp 417–432

    Google Scholar 

  • Chatarpaul L, Chakravarty P, Subramaniam P (1989) Studies in tetrapartite symbioses I. Role of ecto-and endomycorrhizal fungi and Frankia on the growth performance of Alnus incana. Plant Soil 118:145–150

    Article  Google Scholar 

  • Core Team R (2012) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna

    Google Scholar 

  • Daft M (1983) The influence of mixed inocula on endomycorrhizal development. Plant Soil 73:331–337

    Article  Google Scholar 

  • Davies F, Calderón C, Huaman Z, Gómez R (2005) Influence of a flavonoid (formononetin) on mycorrhizal activity and potato crop productivity in the highlands of Peru. Sci Hortic-Amsterdam 106:318–329

    Article  CAS  Google Scholar 

  • de Mendiburu F (2012) Agricolae: statistical procedures for agricultural research. R package version 1.1-2. http://CRAN.R-project.org/package=agricolae

  • Dehgan B, Sheehan TJ, Sylvia DM, Kane M, Loope BC, Niederhofer M (1987) Propagation and mycorrhizal inoculation of indigenous Florida plants for phosphate mine revegetation: final report. Florida Institute of Phosphate Research, Bartow

    Google Scholar 

  • FAO (2006) Progress towards sustainable forest management. In: Global forest resources assessment 2005. FAO, Rome

  • Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, London

    Google Scholar 

  • Gardner IC, Clelland DM, Scott A (1984) Mycorrhizal improvement in non-leguminous nitrogen-fixing associations with particular reference to Hippophae rhamnoides L. Plant Soil 78:189–199

  • Grace C, Stribley D (1991) A safer procedure for routine staining of vesicular arbuscular mycorrhizal fungi. Mycol Res 95:1160–1162

    Article  Google Scholar 

  • Grau A (1985) La expansión del aliso del cerro (Alnus acuminata H.B.K. subsp. acuminata) en el noroeste de Argentina. Lilloa 36:237–247

    Google Scholar 

  • Graves S, Piepho H-P, Selzer L (2011) MultcompView: visualizations of paired comparisons. R package version 0.1-5. http://CRAN.R-project.org/package=multcompView

  • Günter S, Gonzalez P, Álvarez G, Aguirre N, Palomeque X, Haubrich F, Weber M (2009) Determinants for successful reforestation of abandoned pastures in the Andes: soil conditions and vegetation cover. For Ecol Manag 258:81–91

    Article  Google Scholar 

  • Hall R, McNabb S, Maynard C, Green L (1979) Toward development of optimal Alnus glutinosa symbioses. Bot Gaz 140:120–126

    Article  Google Scholar 

  • Halloy S (1991) South American pioneer. Grow Today 4:22–24

    Google Scholar 

  • Harley JL, Harley EL (1987) A check-list of mycorrhiza in the British flora. New Phytol 105:1–102

    Article  Google Scholar 

  • Homeier J, Breckle S-W, Günter S, Rollenbeck RT, Leuschner C (2009) Tree diversity, forest structure and productivity along altitudinal and topographical gradients in a species-rich Ecuadorian montane rain forest. Biotropica 42:140–148

    Article  Google Scholar 

  • Hurd TM, Schwintzer CR (1997) Formation of cluster roots and mycorrhizal status of Comptonia peregrina and Myrica pensylvanica in Maine, USA. Physiol Plant 99:680–689

    Article  CAS  Google Scholar 

  • Janos D (1980) Vesicular–arbuscular mycorrhizae affect lowland tropical rain forest plant growth. Ecology 61:151–162

    Article  Google Scholar 

  • Knoke T, Calvas B, Aguirre N, Román-Cuesta RM, Günter S, Stimm B, Weber M, Mosandl R (2009) Can tropical farmers reconcile subsistence needs with forest conservation? Front Ecol Environ 7:548–554

    Article  Google Scholar 

  • Kottke I, Haug I (2004) The significance of mycorrhizal diversity of trees in the tropical mountain forest of southern Ecuador. Iyonia 7:49–56

    Google Scholar 

  • Marx D, Marrs L, Cordell C (2002) Practical use of mycorrhizal fungal technology in forestry, reclamation, arboriculture, agriculture and horticulture. Dendrobiology 47:29–42

    Google Scholar 

  • Miller S, Koo D, Molina R (1992) Early colonization of red alder and Douglas-fir by ectomycorrhizal fungi and Frankia in soils from the Oregon coast range. Mycorrhiza 2:53–61

    Article  Google Scholar 

  • Molina R, Myrold D, Li C (1994) Root symbioses of red alder: technological opportunities for enhanced regeneration and soil improvement. In: Hibbs D, Bell D, Tarrant R (eds) The biology and management of red alder. Oregon State University Press, Oregon

    Google Scholar 

  • Morris M, Eveleigh D, Riggs S, Tiffney W (1974) Nitrogen fixation in the bayberry (Myrica pensylvanica) and its role in coastal succession. Am J Bot 61:867–870

    Article  Google Scholar 

  • Mosandl R, Günter S, Stimm B, Weber M (2008) Ecuador suffers the highest deforestation rate in South America. In: Beck E, Bendix J, Kottke I, Makeschin F, Mosandl R (eds) Gradients in a tropical mountain ecosystem of Ecuador. Ecol Stud 198. Springer, Berlin, pp 431–441

  • 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 939

  • Palomeque X (2012) Natural succession and tree plantation as alternatives for restoring abandoned lands in the Andes of Southern Ecuador: aspects of facilitation and competition. Dissertation, Technische Universität Mϋnchen, Munich. urn:nbn:de:bvb:91-diss-20121012-1111870-0-1

  • Parolly G, Kürschner H, Schäfer-Verwimp A, Gradstein SR (2004) Cryptogams of the Reserva Biológica San Francisco (Province Zamora-Chinchipe, Southern Ecuador). III. Bryophytes: additions and new species. Cryptogamie Bryologie 25:271–289

    Google Scholar 

  • Parra O (2002) New combinations in South American Myricaceae. Brittonia 54:322–326

    Article  Google Scholar 

  • Põlme S, Bahram M, Yamanaka T, Nara K, Dai Y, Grebenc T, Kraigher H, Toivonen M, Wang P-H, Matsuda Y, Naadel T, Kennedy P, Kõljalg U, Tedersoo L (2013) Biogeography of ectomycorrhizal fungi associated with alders (Alnus spp.) in relation to biotic and abiotic variables at the global scale. New Phytol 198:1239–1249

    Article  PubMed  Google Scholar 

  • Poole BC, Sylvia DM (1990) Companion plants affect colonization of Myrica cerifera by vesicular–arbuscular mycorrhizal fungi. Can J Bot 68:2703–2707

    Article  Google Scholar 

  • Pritsch K, Munch J, Buscot F (1997) Morphological and anatomical characterisation of black alder Alnus glutinosa (L.) Gaertn. ectomycorrhizas. Mycorrhiza 7:201–216

    Article  Google Scholar 

  • Rivera EL, Campos R, de Yunda AL, Martínez R (2000) Mycotrophic status of wax laurel useful for the recuperation of eroded soils in Tomine reservoir-Colombia. Suelos Ecuatoriales 30:188–193

    Google Scholar 

  • Rose SL (1980) Mycorrhizal associations of some actinomycete nodulated nitrogen-fixing plants. Can J Bot 58:1449–1454

    Article  Google Scholar 

  • Rosendahl S, McGee P, Morton JB (2009) Lack of global population genetic differentiation in the arbuscular mycorrhizal fungus Glomus mosseae suggests a recent range expansion which may have coincided with the spread of agriculture. Mol Ecol 18:4316–4329

    Article  PubMed  Google Scholar 

  • Russo R (1989) Evaluating alder-endophyte (Alnus acuminata-Frankia-mycorrhizae) interactions. Plant Soil 118:151–155

    Article  Google Scholar 

  • Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Schwartz MW, Hoeksema JD, Gehring CA, Johnson NC, Klironomos JN, Abbott LK, Pringle A (2006) The promise and the potential consequences of the global transport of mycorrhizal fungal inoculum. Ecol Lett 9:501–515

    Article  PubMed  Google Scholar 

  • Siqueira J, Saggin-Júnior O (2001) Dependency on arbuscular mycorrhizal fungi and responsiveness of some Brazilian native woody species. Mycorrhiza 11:245–255

    Article  CAS  Google Scholar 

  • Siqueira JO, Carneiro MAC, Curi N, Rosado SCDS, Davide AC (1998) Mycorrhizal colonization and mycotrophic growth of native woody species as related to successional groups in Southeastern Brazil. For Ecol Manag 107:241–252

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, London

    Google Scholar 

  • Smith JE, Johnsonke KA, Cázares E (1998) Vesicular mycorrhizal colonization of seedlings of Pinaceae and Betulaceae after spore inoculation with Glomus intraradices. Mycorrhiza 7:279–285

    Article  Google Scholar 

  • Stimm B, Beck E, Günter S, Aguirre N, Cueva E, Mosandl R, Weber M (2008) Reforestation of abandoned pastures: seed ecology of native species and production of indigenous plant material. In: Beck E, Bendix J, Kottke I, Makeschin F, Mosandl R (eds) Gradients in a tropical mountain ecosystem of Ecuador. Ecol Stud 198. Springer, Berlin, pp 433–446

  • Tedersoo L, Bahram M, Toots M, Diédhiou AG, Henkel TW, Kjøller R, Morris MH, Nara K, Nouhra E, Peay KG, Põlme S, Ryberg M, Smith ME, Kõljalg U (2012) Towards global patterns in the diversity and community structure of ectomycorrhizal fungi. Mol Ecol 17:4160–4170

    Article  Google Scholar 

  • Urgiles N, Loján P, Aguirre N, Blaschke H, Günter S, Stimm B, Kottke I (2009) Application of mycorrhizal roots improves growth of tropical tree seedlings in the nursery: a step towards reforestation with native species in the Andes of Ecuador. New For 38:229–239

    Article  Google Scholar 

  • Vannette L, Rasmann S (2012) Arbuscular mycorrhizal fungi mediate below-ground plant–herbivore interactions: a phylogenetic study. Funct Ecol 26:1365–2435

    Article  Google Scholar 

  • Walker C, Vestberg M (1994) A simple and inexpensive method for producing and maintaining closed pot cultures of arbuscular mycorrhizal fungi. Agric Sci Finland 3:233–240

    Google Scholar 

  • Walkley A, Black IA (1934) An examination of different method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci 37:29–37

    Article  CAS  Google Scholar 

  • Weber M, Günter S, Aguirre N, Stimm B, Mosandl R (2008) Reforestation of abandoned pastures: silvicultural means to accelerate forest recovery and biodiversity. In: Beck E, Bendix J, Kottke I, Makeschin F, Mosandl R (eds) Gradients in a tropical mountain ecosystem of Ecuador. Ecol Stud 198. Springer, Berlin, pp 431–441

  • Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82:1198–1227

    Article  Google Scholar 

  • Zangaro W, Bononi VLR, Trufen SB (2000) Mycorrhizal dependency, inoculum potential and habitat preference of native woody species in South Brazil. J Trop Ecol 16:603–622

    Article  Google Scholar 

  • Zangaro W, Nisizaki SMA, Domingos JCB, Nakano EM (2003) Mycorrhizal response and successional status in 80 woody species from south Brazil. J Trop Ecol 19:315–324

    Article  Google Scholar 

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Acknowledgments

The authors thank the German Research Foundation (DFG) for the Grant SCHU1203/10 in the Research Unit 816 and Claudia Krüger for help with the inoculum production. The authors declare that they have no conflict of interest.

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Urgiles, N., Strauß, A., Loján, P. et al. Cultured arbuscular mycorrhizal fungi and native soil inocula improve seedling development of two pioneer trees in the Andean region. New Forests 45, 859–874 (2014). https://doi.org/10.1007/s11056-014-9442-8

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