Skip to main content

Advertisement

Log in

Arbuscular mycorrhizae, a tool to enhance the recovery and re-introduction of Juglans venezuelensis Manning, an endemic tree on the brink of extinction

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

A pot experiment was conducted to evaluate the effects of two arbuscular mycorrhizal fungi (AMF), Dentiscutata heterogama and Rhizophagus manihotis on the growth and nutrition of Juglans venezuelensis Manning. This species is currently considered a threatened tree species and the successful restoration of its populations depends on an increased understanding of the ecological and physiological aspects of its response to inoculation with AMF. In general, shoot and total dry weight, and leaf area were significantly higher in seedlings inoculated with AMF than in non-inoculated ones. Differences in height and leaf number between the inoculated and non-inoculated treatments become apparent after 30 days of plant growth. Inoculated plants had a greater leaf area as the result of the higher allocation of resources to leaf biomass (leaf mass ratio, LMR). The fraction allocated to the roots (RMR) was not significantly different between treatments. Differences between vital stain (SDH) and non-vital trypan blue stain (TB) showed that the D. heterogama colonization was almost entirely active compared to the R. manihotis colonization. The relative responsiveness (RR) of J. venezuelensis to inoculation with D. heterogama and R. manihotis was 21.8 and 25.4 % respectively, but colonization values were never greater than 45 %, despite low P content in the soils used. The growth and physiological responses of J. venezuelensis to inoculation with two AMF species indicate that these microorganisms should be employed when propagating this threatened species for its subsequence reintroduction into its natural habitat.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Abdel-Fattah GM (2001) Measurement of the viability of arbuscular mycorrhizal fungi using three different stains; relation to growth and metabolic acivities of soybean plants. Microbiol Res 156:359–367

    Article  CAS  PubMed  Google Scholar 

  • Abdel-Fattah GM, Asrar AA (2012) Arbuscular mycorrhizal fungal application to improve growth and tolerance af wheat (Triticum aestivum L.) plants grown in saline soil. Acta Physiol Plant 34:267–277

    Article  CAS  Google Scholar 

  • Al-Karaki GN, Hammad R, Rusan M (2001) Response of two tomato cultivars differing in salt tolerance to inoculation with mycorrhizal fungi under salt stress. Mycorrhiza 11:43–47

    Article  CAS  Google Scholar 

  • Allen SE (1989) Chemical analysis of ecological materials. Blackwell Sci. Pub, Osney

    Google Scholar 

  • Aradhya MK, Potter D, Gao F, Simon CJ (2007) Molecular phylogeny of Juglans (Juglandaceae): a biogeographic perspective. Tree Genet Genomes 3:363–378

    Article  Google Scholar 

  • Barroetavena C, Gisler SD, Luoma DL, Meinke RJ (1998) Mycorrhizal status of the endangered species Astragalus applegatei Peck as determined from a soil bioassay. Mycorrhiza 8:117–119

    Article  Google Scholar 

  • Bathia NP, Sundari K, Adholeya A (1996) Diversity and selective dominance of vesicular-arbuscular mycorrhizal fungi. In: Mukerji KG (ed) Concepts in mycorrhizal research, Kluwer Academic Publishers, pp 133–178

  • Bothe H, Turnau K, Regvar M (2010) The potential role of arbuscular mycorrhizal fungi in protecting endangered plants and habitats. Mycorrhiza 20:445–457

    Article  PubMed  Google Scholar 

  • Bressano M, Curreti M, Giocherona L, Gil SV, Cabello M, March G, Duccase DA, Luna CM (2010) Mycorrhizal fungi symbiosis as a strategy againts oxidative sress in soybean plants. J Plant Physiol 167:1622–1626

    Article  CAS  PubMed  Google Scholar 

  • Bruinsma J (1963) The quantitative analysis of chlorophylls a and b in plant extract. Photoch Photobio Sci 2:241–249

    Article  CAS  Google Scholar 

  • Brundrett M, Melville L, Peterson L (1994) Practical methods in mycorrhiza research. Mycologue Publications, Canada

    Google Scholar 

  • Cáceres A, Cuenca G (2006) Response of seedlings of two tropical species Clusia minor and Clusia multiflora to mycorrhizal inoculation in two soils with different pH. Trees Struct Funct 20:593–600

    Article  Google Scholar 

  • Chazdon RL, Fetcher N (1984) Photosynthesis light environment in a lowland tropical rain forest in Costa Rica. J Ecol 72:553–564

    Article  Google Scholar 

  • Cuenca G, De Andrade Z, Lovera M, Fajardo L, Meneses E, Márquez M, Machuca R (2003) Pre-selección de plantas nativas y producción de inóculos de hongos micorrízicos arbusculares (HMA) de relevancia en la rehabilitación de áreas degradadas de La Gran Sabana, Estado Bolívar, Venezuela. Ecotropicos 16:27–40

    Google Scholar 

  • Cuenca G, Caceres A, Oirdobro G, Hasmy Z, Urdaneta C (2007) Las micorrizas arbusculares como alternativa para una agricultura sustentable en áreas tropicales. Interciencia 32:23–29

    Google Scholar 

  • Day PR (1965) Particle fractionation and particle size analysis. In: Black CA (ed) Methods of soil analysis. Part 1. Physical and Mineralogical Properties. ASA-SSSA, Madison, pp 545–567

    Google Scholar 

  • Debrot H (1989) El bosque urbano caraqueño. Acta Bot Venez 15:47–70

    Google Scholar 

  • Dixon R (1988) Seed source and vesicular-arbuscular mycorrhizal symbiont affects growth of Juglans nigra seedlings. New Forest 2:203–211

    Article  Google Scholar 

  • Ferrazzano S, Williamson PS (2013) Benefits of mycorrhizal inoculation in reintroduction of endangered plant species under drought conditions. J Arid Environ 98:123–125

    Article  Google Scholar 

  • Fisher JB, Jayachandran K (2005) Presence of arbuscular mycorrhizal fungi in South Florida native plants. Mycorrhiza 15:580–588

    Article  PubMed  Google Scholar 

  • Fuchs B, Haselwandter K (2008) Arbuscular mycorrhiza of endangered plant species: potential impacts on restoration strategies. In: Varma A (ed) Mycorrhiza: genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics, third edition. Springer-Verlag, Berlin

    Google Scholar 

  • Gemma JN, Koske RE, Habte M (2002) Mycorrhizal dependency of some endemic and endangered Hawaiian plant species. Am J Bot 89:337–345

    Article  CAS  PubMed  Google Scholar 

  • Grandcourt A, Epron D, Montpied P, Louisinna E, Beraeu M, Garbaye J, Guelh JM (2004) Contrasting response to mycorrhizal inoculation and phosphorus availability in seedlings of two tropical rainforest tree species. New Phytol 161:865–875

    Article  Google Scholar 

  • Grimoldi AA, Karanová M, Lattanzi FA, Schnyder H (2005) Phosphorus nutrition-mediated effects of arbuscular mycorrhiza on leaf morphology and carbon allocation in perennial ryegrass. New Phytol 168:435–444

    Article  CAS  PubMed  Google Scholar 

  • Hamel E, Fyles H, Smith DL (1990) Measurement of development of endomycorrhizal mycelium using tree different stains. New Phytol 155:297–302

    Article  Google Scholar 

  • Haug I, Wubet T, Weib M, Aguirre N, Weber M, Günter S, Kottke I (2010) Species-rich but distinct arbuscular mycorrhizal communities in reforestation plots on degraded pastures and in neighboring pristine tropical mountain rain forest. Trop Ecol 51:125–148

    CAS  Google Scholar 

  • Huante P, Rincón E, Acosta I (1995) Nutrient availability and growth rate of 34 woody species from a tropical deciduous forest in Mexico. Funct Ecol 9:849–858

    Article  Google Scholar 

  • Janos DP (1980) Mycorrhizae influence tropical succession. Biotropica 12:56–64

    Article  Google Scholar 

  • Kitajima K (2002) Do shade-tolerent tropical tree seedlings depend longer on seed reserves? Functional growth analysis of three Bignonaceae species. Do shade-tolerent tropical tree seedlings depend longer on seed reserves? Functional growth analysis of three Bignonaceae species 16: 433–444

  • Kormanik PP, Schultz RC, Bryan WC (1982) The influence of vesicular-arbuscular mycorrhizae on the growth and development of eight hardwood tree species. Forest Sci 28:531–539

    Google Scholar 

  • Kough JL, Gianinazzi-Pearson V (1986) Physiological aspects of VA mycorrhizal hyphae in root tissue and soil. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA publications, Paris, pp 223–226

    Google Scholar 

  • Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes an ecological consecuences. Adv Bot Res 23:187–261

    CAS  Google Scholar 

  • Llamozas S, de Stefano RD, Meier W, Riina R, Stauffer F, Aymard G, Huber O, Ortiz R (2003) Libro rojo de la flora venezolana. PROVITA, Fundación Polar, Fundación Instituto Botánico de Venezuela “Dr. Tobías Lasser. Conservación Internacional, Caracas

    Google Scholar 

  • McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  • Melichar MW, Garret HE, Cox GS (1986) Mycorrhizae benefit growth and development of eastern black walnut seedlings. North J Appl For 3:151–153

    Google Scholar 

  • Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphore in natural waters. Anal Chem Acta 27:31–36

    Article  CAS  Google Scholar 

  • Ortiz R, Salazar A (2004) El Nogal de Caracas. Património emblemático de la ciudad. Ministerio del Ambiente y de los Recursos Naturales, Caracas

    Google Scholar 

  • Panwar J, Vyas A (2002) AM fungi: a biological approach towards conservation of endangered plants in Thar desert, India. Curr Sci 82:576–578

    CAS  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Article  Google Scholar 

  • Pieters AJ, Lawlor DW (2001) Low sink demands limits photosynthesis under Pi deficiency. J Exp Bot 52:1083–1091

    Article  CAS  PubMed  Google Scholar 

  • Plenchette C, Fortin JA, 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 Soil 70:199–209

    Article  CAS  Google Scholar 

  • Poorter H, Remkes C (1990) Leaf area ratio and net assimilation rate of 24 wild species differing in relatived growth rate. Leaf area ratio and net assimilation rate of 24 wild species differing in relatived growth rate. Oecologia 83:533–559

    Article  Google Scholar 

  • Pope PE, Chaney WR, Rhodes JD, Woodhead SH (1983) The mycorrhizal dependency of four hardwood tree species. Can J Bot 61:412–417

    Article  Google Scholar 

  • Porters L (2001) Light-dependent changes in biomass allocation and their importance for growth of rain forest tree species. Funct Ecol 15:113–123

    Article  Google Scholar 

  • Ríos-Marín MC (2011) Aspectos ecológicos de la regeneración natural del Nogal de Caracas (Juglans venezuelensis). Implicaciones para su conservación y recuperación. Master’s Thesis, Instituto Venezolano de Investigaciones Científicas

  • Sieverding E (1991) Vesicular arbuscular mycorrhiza management in tropical agrosystems. Deutsche Gesellschaft für Technische Zusammenarbeit (GTZ), Eschborn

    Google Scholar 

  • Smith SE, Read DJ (2008) The mycorrhizal symbiosis. Academic Press, Great Britain

    Google Scholar 

  • Smith SE, Smith FA (1996) Mutualism and parasitism: diversity in function and structure in the arbuscular (VA) mycorrhizal symbiosis. Adv Bot Res 22:1–43

    Article  Google Scholar 

  • Sukesh K, Sharma MS, Chandrashekar KR (2013) Inoculation effect of arbuscular mycorrhizal fungi on the growth of Vatica chinensis L.: a critically endangered species of Western Ghats. Trees-Struct Funct 28:381–388

    Article  Google Scholar 

  • Tawaraya K (2003) Arbuscular mycorrhizal dependency of different plant species and cultivars. Soil Sci Plant Nutr 49:655–668

    Article  Google Scholar 

  • Tian YH, Lai YB, Zheng YL, Cai ZQ (2013) Sinergistic effect of colonization with arbuscular mycorrhizal fungi improves growth and drought tolerence of Plukenetia volubilis seedlings. Acta Physiol Plant 35:687–696

    Article  CAS  Google Scholar 

  • Tiessen H, Moir J (1993) Characterization of available P by sequential extraction. Soil Samp Meth Anal 10:75–86

    Google Scholar 

  • Walkley A, Black IA (1934) An examination of Degtjareff 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 

  • Wang YY, Vestberg M, Walker C, Huarme T, Zhang X, Lindström K (2008) Diversity and infectivity of arbuscular mycorrhizal fungi in agricultural soils of the Sichuan Province of mainland China. Mycorrhiza 18:59–68

    Article  PubMed  Google Scholar 

  • Zandavalli RB, Dillenburg LR, de Souza PV (2004) Growth responses of Araucaria angustifolia (Araucariaceae) to inoculation with the mycorrizal fungus Glomus clarum. App Soil Ecol 25:245–255

    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 

  • Zubek S, Turnau K, Tsimilli-Michael M, Strasser RJ (2009) Response of endangered plant species to inoculation with arbuscular mycorrhizal fungi and soil bacteria. Mycorrhiza 19:113–123

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was funded by the Instituto Venezolano de Investigaciones Científicas (IVIC) through a project titled “Use of the arbuscular mycorrhiza in the propagation of threatened tree species” (project number 943). We thank to Ramón Capote and Héctor Linares for your field assistance and work at the greenhouse. Likewise, we want to thank to Elizabeth Rengifo from Laboratory of Ecophysiology of the Ecology Center (IVIC), for having provided the AM-200 Leaf Area Meter and to Maiella Rangel for her assistance in the physical and chemical determinations of the seedlings and soil samples. Finally, we also want to thank to Milagros Lovera for revision of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Laurie Fajardo.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fajardo, L., Cáceres, A. & Arrindell, P. Arbuscular mycorrhizae, a tool to enhance the recovery and re-introduction of Juglans venezuelensis Manning, an endemic tree on the brink of extinction. Symbiosis 64, 63–71 (2014). https://doi.org/10.1007/s13199-014-0304-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-014-0304-0

Keywords

Navigation