Skip to main content Accessibility help

Arbuscular mycorrhizas increase survival, precocity and flowering of herbaceous and shrubby species of early stages of tropical succession in pot cultivation

  • Artur Berbel Lirio Rondina (a1) (a2), Luis Eduardo Azevedo Marques Lescano (a1) (a3), Ricardo de Almeida Alves (a1) (a2), Enio Massao Matsuura (a1) (a2), Marco Antonio Nogueira (a3) (a4) and Waldemar Zangaro (a1) (a2)...


Arbuscular mycorrhizal fungi (AMF) are an important biotic factor that influences tropical ecological succession and differently affect the woody species belonging to different successional stages. However, little is known about the influence of AMF on growth and reproduction of herbaceous and shrubby species of early phases of tropical succession. Thus, we assessed the effect of AMF on the development of 27 heliophilous herbaceous and shrubby tropical species. Plants were grown in greenhouse, in low- and high-fertility soils, with or without AMF, for 100 d. Most species grown with AMF exhibited high root infection intensity (≈80%), irrespective of soil fertility. In the low-fertility soil, non-mycorrhizal plants exhibited about 88% less shoot dry mass (SDM) than mycorrhizal plants, and AMF were crucial for the survival of most species. Non-mycorrhizal plants also had lower relative growth rate (RGR), total leaf area (TLA), leaf area expansion (LAE) and total root length (TRL). Six species flowered in the low-fertility soil, and flowering increased with AMF in one plant species and four species only flowered when mycorrhizal. In the high-fertility soil, non-mycorrhizal plants exhibited about 13% less SDM than mycorrhizal plants and also exhibited lower TLA, LAE, and nutrient concentrations in shoots. On the other hand, no major changes were observed for RGR, TRL and root dry mass for most of the species. Sixteen plant species flowered in the high-fertility soil, but most had earlier (11) and more abundant (10) flowering when mycorrhizal. Thus, AMF have different influences on the survival, growth and flowering of herbaceous and shrubby tropical species, depending on soil fertility: in low-fertility soil, AMF especially affect the survival, growth and flowering, whereas in high-fertility soil, AMF mainly influence the shoot nutrient concentrations and flowering.


Corresponding author

1Corresponding author. Email:


Hide All
AARSSEN, L. W. & TAYLOR, D. R. 1992. Fecundity allocation in herbaceous plants. Oikos 65:225232.
AUGÉ, R. M. 2001. Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:342.
BRUNDRETT, M., BEEGHER, N., DELL, B., GROOVE, T. & MALAJCZUK, N. 1996. Working with mycorrhizas in forestry and agriculture. ACIAR Monograph, Canberra. 374 pp.
BUSBY, R. R., GEBHART, D. L., STROMBERGER, M. E., MEIMAN, P. J. & PASCHKE, M. W. 2011. Early seral plant species’ interactions with an arbuscular mycorrhizal fungi community are highly variable. Applied Soil Ecology 48:257262.
COMAS, L. H. & EISSENSTAT, D. M. 2004. Linking fine root traits to maximum potential growth rate among 11 mature temperate tree species. Functional Ecology 18:388397.
DEFILIPPO, B. V. & RIBEIRO, A. C. 1997. Análise química do solo – metodologia. Universidade Federal de Viçosa, Viçosa. 26 pp.
FAO. 1994. Soil map of the world. FAO-UNESCO, Rome. 140 pp.
GANGE, A. C. & SMITH, A. K. 2005. Arbuscular mycorrhizal fungi influence visitation rates of pollinating insects. Ecological Entomology 30:600606.
GRMAN, E. 2012. Plant species differ in their ability to reduce allocation to non-beneficial arbuscular mycorrhizal fungi. Ecology 93:711718.
GUARIGUATA, M. R. & OSTERTAG, R. 2001. Neotropical secondary forest succession: changes in structural and functional characteristics. Forest Ecology and Management 148:185206.
HEPPELL, K. B., SHUMWAY, D. L. & KOIDE, R. T. 1998. The effect of mycorrhizal infection of Abutilon theophrasti on competitiveness of offspring. Functional Ecology 12:171175.
HUNT, R. 1982. Plant growth curves: the functional approach to plant growth analysis. University Park Press, Baltimore. 248 pp.
JOHNSON, N. C. 2010. Resource stoichiometry elucidates structure and function of arbuscular mycorrhizas across scales. New Phytologist 185:631647.
JOHNSON, N. C., GRAHAM, J. H. & SMITH, F. A. 1997. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytologist 135:575585.
KALINHOFF, C., CÁCERES, A. & LUGO, L. 2009. Mudanças na biomassa de raízes e micorrizas arbusculares em cultivos itinerantes do Amazonas Venezolano. Interciencia 34:571576.
KEENEY, D. R. & NELSON, D. W. 1982. Nitrogen inorganic forms. Pp. 643698 in Page, A. L., Miller, R. H. & Keeney, D.R. (eds.). Methods of soil analysis: chemical and microbiological properties. American Society of Agronomy, Madison.
KHURANA, E. & SINGH, J. S. 2006. Impact of life-history traits on response of seedlings of five tree species of tropical dry forest to shade. Journal of Tropical Ecology 22:653661.
KIERS, E. T., DUHAMEL, M., BEESETTY, Y., MENSAH, J. A., FRANKEN, O., VERBRUGGEN, E., FELLBAUM, C. R., KOWALCHUK, G. A., HART, M. M., BAGO, A., PALMER, T. M., WEST, S. A., VANDENKOORNHUYSE, P., JANSA, J. & BÜCKING, H. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880882.
KLIRONOMOS, J. N. 2003. Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:22922301.
KOIDE, R. T. & DICKIE, I. A. 2002. Effects of mycorrhizal fungi on plant populations. Plant and Soil 244:307317.
KRANZ, W. M., FONSECA JUNIOR, N. S., PASSINI, T. & MARTINS, N. M. B. 2009. Ocorrência e distribuição de plantas daninhas no Paraná. Iapar, Londrina. 283 pp.
LEITÃO FILHO, H. F., ARANHA, C. & BACCHI, O. 1972. Plantas invasoras de culturas no Estado de São Paulo. Hucitec, São Paulo. 291 pp.
LEKBERG, Y., KOIDE, R. T. & TWOMLOW, S. J. 2008. Effect of agricultural management practices on arbuscular mycorrhizal fungal abundance in low-input cropping systems of southern Africa: a case study from Zimbabwe. Biology and Fertility of Soils 44:917923.
LI, H., SMITH, F. A., DICKSON, S., HOLLOWAY, R. E. & SMITH, S. E. 2008. Plant growth depressions in arbuscular mycorrhizal symbioses: not just caused by carbon drain? New Phytologist 178:852862.
LORENZI, H. 2000. Plantas daninhas do Brasil: terrestres, aquáticas, parasitas e tóxicas. Instituto Plantarum, Nova Odessa. 608 pp.
LU, X. & KOIDE, R. T. 1994. The effects of mycorrhizal infection on components of plant growth and reproduction. New Phytologist 128:211218.
LUSK, C. H., REICH, P. B., MONTGOMERY, R. A., ACKERLY, D. D. & CAVENDER-BARES, J. 2008. Why are evergreen leaves so contrary about shade? Trends in Ecology and Evolution 23:299303.
LYNCH, J. P. & HO, M. D. 2005. Rhizoeconomics: carbon costs of phosphorus acquisition. Plant and Soil 269:4556.
MANGAN, S. A., EOM, A., ADLER, G. H., YAVITT, J. B. & HERRE, E. A. 2004. Diversity of arbuscular mycorrhizal fungi across a fragmented forest in Panama: insular spores communities differ from mainland communities. Oecologia 141:687700.
McGONIGLE, T. P., EVANS, D. G. & MILLER, M. H. 1990. Effect of degree of soil disturbance on mycorrhizal colonization and phosphorus absorption by maize in growth chamber and field experiments. New Phytologist 116:629636.
MUTHUKUMAR, T. & PRAKASH, S. 2009. Arbuscular mycorrhizal morphology in crops and associated weeds in tropical agro-ecosystems. Mycoscience 50:233239.
NEWELL, S. J. & TRAMER, E. J. 1978. Reproductive strategies in herbaceous plant communities during succession. Ecology 59:228234.
NORRIS, R. F. 2007. Weed fecundity: current status and future needs. Crop Protection 26:182188.
PAVAN, M. A., BLOCH, M. F., ZEMPULSKI, H. C., MIYAZAWA, M. & ZOCOLER, D.C. 1992. Manual de análise química de solo e controle de qualidade. IAPAR, Londrina. 40 pp.
PENG, S., EISSENSTAT, D. M., GRAHAM, J. H., WILLIAMS, K. & HODGE, N. C. 1993. Growth depression in mycorrhizal citrus at high-phosphorus supply. Plant Physiology 101:10631071.
PERNER, H., SCHWARTZ, D., BRUNS, C., MÄDER, P. & GEORGE, E. 2007. Effect of arbuscular mycorrhizal colonization and two levels of compost supply on nutrient uptake and flowering of pelargonium plants. Mycorrhiza 17:469474.
PLENCHETTE, C., FORTIN, J. A. & FURLAN, V. 1983. Growth response of several plants species to mycorrhiza in a soil of moderate P fertility. I. Mycorrhizal dependency under field conditions. Plant and Soil 70:191209.
POORTER, L. & ROZENDAAL, D. M. A. 2008. Leaf size and leaf display of thirty-eight tropical tree species. Oecologia 158:3546.
POULTON, J. L., BRYLA, D., KOIDE, R. T. & STEPHENSON, A. G. 2002. Mycorrhizal infection and high soil phosphorus improve vegetative growth and the female and male functions in tomato. New Phytologist 154:255264.
REICH, P. B. 1998. Variation among plant species in leaf turnover rates and associated traits: implications for growth at all life stages. Pp. 467487 in Cambers, H., Porter, H. & van Vuuren, M. M. I. (eds.). Physiological mechanisms and ecological consequences. Backhuys Publishing, Leiden.
RYAN, M. H., VAN HERWAARDEN, A. F., ANGUS, J. F. & KIRKEGAARD, J. A. 2005. Reduced growth of autumn-sown wheat in a low-P is associated with high colonization by arbuscular mycorrhizal fungi. Plant and Soil 270:275286.
SILVA, F. C. 1999. Manual de análises químicas de solos, plantas e fertilizantes. Embrapa, Brasilia. 370 pp.
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 182:347358.
SMITH, S. E. & READ, D. J. 2008. Mycorrhizal symbiosis. Academic Press, London. 797 pp.
SMITH, S. E., JAKOBSEN, I., GRØLUND, M. & SMITH, F. A. 2011. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiology 156:10501057.
STANLEY, M. R., KOIDE, R. T. & SHUMWAY, D. L. 1993. Mycorrhizal symbiosis increases growth, reproduction and recruitment of Abutilon theophrasti Medic. in the field. Oecologia 94:3035.
STÜRMER, S. L. & SIQUEIRA, J. O. 2011. Species richness and spore abundance of arbuscular mycorrhizal fungi across distinct land uses in Western Brazilian Amazon. Mycorrhiza 21:255267.
TENNANT, D. 1975. A test of modified line intersect method of estimating root length. Journal of Ecology 63:9951001.
VEIGA, R. S. L., JANSA, J., FROSSARD, E. & VAN DER HEIJDEN, M. G. A. 2011. Can arbuscular mycorrhizal fungi reduce the growth of agricultural weeds? PloS ONE 6:e27825. doi: 10.1371/journal.pone.0027825.
WEHNER, J., ANTUNES, P. M., POWELL, J. R., MAZUKATOW, J. & RILLING, M. C. 2010. Plant pathogen protection by arbuscular mycorrhizas: a role for fungal diversity? Pedobiologia 53:197201.
WILSON, G. W. T. & HARTNETT, D. C. 1998. Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. American Journal of Botany 85:17321738.
WRIGHT, D. P., SCHOLES, J. D. & READ, D. J. 1998. Effects of VA mycorrhizal colonization on photosynthesis and biomass production of Trifolium repens L. Plant Cell and Environment 21:209216.
YOLANDA, N. G., CERRATO, R. F. & SANTAMARÍA, R. F. 2012. Glomus intraradices attenuates the negative effect of low Pi supply on photosynthesis and growth of papaya Maradol plants. Journal of Botany 2012:ID129591. doi: 10.1155/2012/129591
ZANGARO, W., BONONI, V. L. R. & TRUFEM, S. B. 2000. Mycorrhizal dependency, inoculum potential and habitat preference of native woody species in South Brazil. Journal of Tropical Ecology 16:603622.
ZANGARO, W., NISHIDATE, F. R., VANDRESEN, J., ANDRADE, G. & NOGUEIRA, M. A. 2007. Root mycorrhizal colonization and plant responsiveness are related to root plasticity, soil fertility and successional status of native woody species in southern Brazil. Journal of Tropical Ecology 23:5362.
ZANGARO, W., ASSIS, R. L., ROSTIROLA, L. V., SOUZA, P. B., GONÇALVES, M. C., ANDRADE, G. & NOGUEIRA, M. A. 2008. Changes in arbuscular mycorrhizal associations and fine root traits in sites under different plant successional phases in southern Brazil. Mycorrhiza 19:3745.
ZANGARO, W., ALVES, R. A., LESCANO, L. E., ANSANELO, A. P. & NOGUEIRA, M. A. 2012a. Investment in fine roots and arbuscular mycorrhizal fungi decrease during succession in three Brazilian ecosystems. Biotropica 44:141150.
ZANGARO, W., ANSANELO, A. P., LESCANO, L. E. A. M., ALVES, R. A., RONDINA, A. B. L. & NOGUEIRA, M. A. 2012b. Infection intensity, spore density and inoculum potential of arbuscular mycorrhizal fungi decrease during secondary succession in tropical Brazilian ecosystems. Journal of Tropical Ecology 28:453462.
ZANGARO, W., ROSTIROLA, L. V., SOUZA, P. B., ALVES, R. A., LESCANO, L. E. A. M., RONDINA, A. B. L., NOGUEIRA, M. A. & CARRENHO, R. 2013. Root colonization and spore abundance of arbuscular mycorrhizal fungi in distinct successional stages from an Atlantic rainforest biome in southern Brazil. Mycorrhiza 23:221233.
ZANGARO, W., ALVES, R. A., SOUZA, P. B., ROSTIROLA, L. V., LESCANO, L. E. A. M., RONDINA, A. B. L. & NOGUEIRA, M. A. 2014. Succession and environmental variation influence soil exploration potential by fine roots and mycorrhizal fungi in an Atlantic ecosystem in southern Brazil. Journal of Tropical Ecology 30:237248.



Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed