Skip to main content Accessibility help

Plant–microbe interactions along a gradient of soil fertility in tropical dry forest

  • Bonnie G. Waring (a1), Maria G. Gei (a1), Lisa Rosenthal (a1) and Jennifer S. Powers (a1) (a2)


Theoretical models predict that plant interactions with free-living soil microbes, pathogens and fungal symbionts are regulated by nutrient availability. Working along a steep natural gradient of soil fertility in a Costa Rican tropical dry forest, we examined how soil nutrients affect plant–microbe interactions using two complementary approaches. First, we measured mycorrhizal colonization of roots and soil P availability in 18 permanent plots spanning the soil fertility gradient. We measured root production, root colonization by mycorrhizal fungi, phosphatase activity and Bray P in each of 144 soil cores. Next, in a full-factorial manipulation of soil type and microbial community origin, tree seedlings of Albizia guachapele and Swietenia macrophylla were grown in sterilized high-, intermediate- and low-fertility soils paired with microbial inoculum from each soil type. Seedling growth, biomass allocation and root colonization by mycorrhizas were quantified after 2 mo. In the field, root colonization by mycorrhizal fungi was unrelated to soil phosphorus across a five-fold gradient of P availability. In the shadehouse, inoculation with soil microbes had either neutral or positive effects on plant growth, suggesting that positive effects of mycorrhizal symbionts outweighed negative effects of soil pathogens. The presence of soil microbes had a greater effect on plant biomass than variation in soil nutrient concentrations (although both effects were modest), and plant responses to mycorrhizal inoculation were not dependent on soil nutrients. Taken together, our results emphasize that soil microbial communities can influence plant growth and morphology independently of soil fertility.


Corresponding author

1Corresponding author. Email:


Hide All
ALLEN, M. 2011. Linking water and nutrients through the vadose zone: a fungal interface between the soil and plant systems. Journal of Arid Lands 3:155163.
ALLISON, S. D. & VITOUSEK, P. M. 2005. Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biology and Biochemistry 37:937944.
AUGÉ, R. 2001. Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:342.
BECKNELL, J. M. & POWERS, J. S. 2014. Stand age and soils as drivers of plant functional traits and aboveground biomass in secondary tropical dry forest. Canadian Journal of Forest Research 44:604613.
BEVER, J. D., DICKIE, I. A., FACELLI, E., FACELLI, J. M., KLIRONOMOS, J., MOORA, M., RILLIG, M. C., STOCK, W. D., TIBBETT, M. & ZOBEL, M. 2010. Rooting theories of plant community ecology in microbial interactions. Trends in Ecology and Evolution 25:468478.
CAMENZIND, T., HEMPEL, S., HOMEIER, J., HORN, S., VELESCU, A., WILCKE, W. & RILLIG, M. C. 2014. Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Global Change Biology 20:36463659.
CASPER, B. B., BENTIVENGA, S. P., JI, B., DOHERTY, J. H., EDENBORN, H. M. & GUSTAFSON, D. J. 2008. Plant-soil feedback: testing the generality with the same grasses in serpentine and prairie soils. Ecology 89:21542164.
CORNELISSEN, J., LAVOREL, S., GARNIER, E., DIAZ, S., BUCHMANN, N., GURVICH, D., REICH, P. B., TER STEEGE, H., MOGAN, H. D. & VAN DER HEIJDEN, M. G. A. 2003. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany 51:335380.
FIERER, N., STRICKLAND, M. S., LIPTZIN, D., BRADFORD, M. A. & CLEVELAND, C. C. 2009. Global patterns in belowground communities. Ecology Letters 12:12381249.
GEI, M. G. & POWERS, J. S. 2014. Nutrient cycling in tropical dry forests. Pp. 141155 in Sanchez-Azofeifa, G. A., Powers, J. S., Fernandes, G. W. & Quesada, M. (eds.). Tropical dry forests in the Americas: ecology, conservation, and management. CRC Press, Boca Raton.
GRMAN, E. 2012. Plant species differ in their ability to reduce allocation to non-beneficial arbuscular mycorrhizal fungi. Ecology 93:711718.
JOHNSON, N. C. 2010. Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytologist 185:631647.
JOHNSON, N., WILSON, G., WILSON, J., MILLER, R. & BOWKER, M. 2015. Mycorrhizal phenotypes and the Law of the Minimum. New Phytologist 205:14731484.
KAYE, J. P. & HART, S. C. 1997. Competition for nitrogen between plants and soil microorganisms. Trends in Ecology and Evolution 12:139143.
KIERS, E., DUHAMEL, M., BEESETTY, Y., MENSAH, J., 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. & BUCKING, H. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880882.
KOSKE, R. & GEMMA, J. 1989. A modified procedure for staining roots to detect VA mycorrhizas. Mycological Research 92:486488.
LAJTHA, K., DRISCOLL, C. T., JARELL, W. M. & ELLIOT, E. T. 1999. Soil phosphorus: characterization and total element analysis. Pp. 115142 in Robertson, G. P., Coleman, D. C., Bledsoe, C. S. & Sollins, P. (eds.). Standard soil methods for long-term ecological research. Oxford University Press, New York.
LAVOREL, S. & GARNIER, E. 2002. Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Functional Ecology 16:545556.
LAWRENCE, D. 2003. The response of tropical tree seedlings to nutrient supply: meta-analysis for understanding a changing tropical landscape. Journal of Tropical Ecology 19:239250.
LOVELOCK, C., ANDERSEN, K. & MORTON, J. 2003. Arbuscular mycorrhizal communities in tropical forests are affected by host tree species and environment. Oecologia 135:268279.
MCGONIGLE, T., MILLER, M., EVANS, D., FAIRCHILD, G. & SWAN, J. 1990. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist 115:495501.
NEUHAUSER, C. & FARGIONE, J. 2004. A mutualism–parasitism continuum model and its application to plant–mycorrhizae interactions. Ecological Modelling 177:337352.
PAINE, C. E., MARTHEWS, T. R., VOGT, D. R., PURVES, D., REES, M., HECTOR, A. & TURNBULL, L. A. 2012. How to fit nonlinear plant growth models and calculate growth rates: an update for ecologists. Methods in Ecology and Evolution 3:245256.
POORTER, H., NIKLAS, K., REICH, P., OLEKSYN, J., POOT, P. & MOMMER, L. 2012. Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytologist 193:3050.
POWERS, J. S., TRESEDER, K. K. & LERDAU, M. 2005. Fine roots, arbuscular mycorrhizal hyphae and soil nutrients in four neotropical rain forests: patterns across large geographic distances. New Phytologist 165:913921.
POWERS, J. S., BECKNELL, J. M., IRVING, J. & PEREZ-AVILES, D. 2009. Diversity and structure of regenerating tropical dry forests in Costa Rica: geographic patterns and environmental drivers. Forest Ecology and Management 258:959970.
RUIZ-LOZANO, J. M. & AZCON, R. 1995. Hyphal contribution to water uptake in mycorrhizal plants as affected by the fungal species and water status. Physiologia Plantarum 95:472478.
SCHEUBLIN, T., RIDGWAY, K., YOUNG, J. & VAN DER HEIJDEN, M. 2004. Nonlegumes, legumes and root nodules harbor different arbuscular mycorrhizal fungal communities. Applied and Environmental Microbiology 70:62406242.
SINSABAUGH, R. L., ANTIBUS, R. K., LINKINS, A. E., MCCLAUGHERTY, C. A., RAYBURN, L., REPERT, D. & WEILAND, T. 1993. Wood decomposition: nitrogen and phosphorus dynamics in relation to extracellular enzyme activity. Ecology 74:15861593.
SIQUEIRA, J. & SAGGIN-JÚNIOR, O. 2001. Dependency on arbuscular mycorrhizal fungi and responsiveness of some Brazilian native woody species. Mycorrhiza 11:245255.
TRESEDER, K. K. 2004. A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytologist 164:347355.
TRESEDER, K. K. & ALLEN, M. E. 2002. Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test. New Phytologist 155:507515.
VAN DER HEIJDEN, M. G. A., BARDGETT, R. D. & VAN STRAALEN, N. M. 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 11:296310.
VAN DER PUTTEN, W., BARDGETT, R., BEVER, J. D., BEZEMER, M., CASPER, B. B., FUKAMI, T., KARDOL, P., KLIRONOMOS, J. N., KULMATISKI, A., SCHWEITZER, J. A., SUDING, K. N., VAN DE VOORDE, T. F. J. & WARDLE, D. A. 2013. Plant-soil feedbacks: the past, the present, and future challenges. Journal of Ecology 101:265276.
WARING, B. G., BECKNELL, J. M. & POWERS, J. S. 2015. Nitrogen, phosphorus, and cation use efficiency in stands of regenerating tropical dry forest. Oecologia 178:887897.
WARING, B. G., ADAMS, R., BRANCO, S. & POWERS, J. S. 2016. Scale-dependent variation in nitrogen cycling and soil fungal communities along gradients of forest composition and age in regenerating tropical dry forests. New Phytologist 209:845854.
WOOD, S. N. 2011. Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society B 73:336.


Related content

Powered by UNSILO

Plant–microbe interactions along a gradient of soil fertility in tropical dry forest

  • Bonnie G. Waring (a1), Maria G. Gei (a1), Lisa Rosenthal (a1) and Jennifer S. Powers (a1) (a2)


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.