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Pervasive phosphorus limitation of tree species but not communities in tropical forests

A Publisher Correction to this article was published on 02 May 2018

This article has been updated

Abstract

Phosphorus availability is widely assumed to limit primary productivity in tropical forests1,2, but support for this paradigm is equivocal3. Although biogeochemical theory predicts that phosphorus limitation should be prevalent on old, strongly weathered soils4,5, experimental manipulations have failed to detect a consistent response to phosphorus addition in species-rich lowland tropical forests6,7,8,9. Here we show, by quantifying the growth of 541 tropical tree species across a steep natural phosphorus gradient in Panama, that phosphorus limitation is widespread at the level of individual species and strengthens markedly below a threshold of two parts per million exchangeable soil phosphate. However, this pervasive species-specific phosphorus limitation does not translate into a community-wide response, because some species grow rapidly on infertile soils despite extremely low phosphorus availability. These results redefine our understanding of nutrient limitation in diverse plant communities and have important implications for attempts to predict the response of tropical forests to environmental change.

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Figure 1: Tree growth responses to phosphorus and moisture.
Figure 2: A threshold for strong phosphorus limitation in lowland tropical forests.
Figure 3: Predicted growth rates and growth responses to increasing soil phosphorus for individual common species as a function of their phosphorus affinity.
Figure 4: Observed community-wide growth rates as a function of resin phosphate concentration.

Change history

  • 02 May 2018

    Please see accompanying Publisher correction (https://doi.org/10.1038/s41586-018-0099-x). In this Letter, the y axis of the right-hand panel of Fig. 2a was mislabelled 'Phosphomonoesterase' instead of 'Phosphodiesterase'. This error has been corrected online.

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Acknowledgements

We thank R. Pérez, S. Aguilar and the many field assistants who helped in collection of the plot data; staff at the STRI Soils Laboratory for assistance in the collection and analysis of soils; and J. Dalling, E. Laliberté, M. Sheldrake and G. Zemunik for comments on the manuscript.

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Contributions

R.C. collected tree growth data, B.L.T. collected soil data, T.B.-A. and R.C. conducted statistical analysis, and B.L.T. wrote the manuscript with input from T.B.-A. and R.C.

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Correspondence to Benjamin L. Turner.

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Extended data figures and tables

Extended Data Figure 1 Growth responses of individual species to resin phosphate.

ad, Blue points represent the observed growth of individual trees, and blue triangles the species mean growth in a plot. The solid blue line is the modelled species response to resin phosphate, and the dashed black line is the fixed response of the entire community (as in Fig. 1). The four species are among the most abundant and widespread in the two size classes: Faramea occidentalis (Rubiaceae), an understory evergreen tree/shrub (a); Sorocea affinis (Moraceae), an understory deciduous tree (b); Gustavia superba (Lecythidaceae), an understory tree (c); and Alseis blackiana (Rubiaceae), a canopy tree (d). Saplings (a, c) include all individuals ≥ 10 mm and <50 mm dbh; the dashed black line is the community-wide estimate at 30 mm dbh. Trees (b, d) include all individuals ≥ 100 mm dbh; the dashed black line is the community-wide estimate at the mean dbh of all trees ≥ 100 mm dbh. Both the y axes (growth in mm y−1) and x axes (resin phosphate in mg P kg−1) are plotted on logarithmic scales. The number of individuals were: 398 saplings (F. occidentalis), 328 saplings (S. affinis), 620 trees (G. superba) and 253 trees (A. blackiana).

Extended Data Figure 2 Responses to resin phosphate above and below ground.

a, Modelled responses of common species to resin phosphate as adult trees and saplings. Trees were defined as being 100 mm dbh and saplings were defined as being 10 mm dbh. The responses of trees and saplings are unrelated by simple linear regression (R2 = 0.006; P = 0.74). As trees 90% of species have a positive response to increasing resin phosphate concentrations (points above the horizontal dotted line), and as saplings 84% of species have a positive response to increasing resin phosphate concentrations (points to the right of the vertical dotted line). Only three common species responded negatively as both small and large trees. b, Piecewise linear regression model using common widespread species, showing the relationship fitted to the response of growth (log-transformed) to resin phosphate concentration for trees >100 mm dbh (top) and saplings <100 mm dbh (bottom). The black line is the community-wide mean, or fixed response. Each grey line is the fit for one species and blue dots are the growth rates of individual trees. For trees, the break point between large and small responses to phosphorus is at 1.6 mg P kg−1 resin phosphate (red dashed vertical line; 95% credible interval 1.3–2.0). To the left of this break, s1 = 0.16 (95% credible interval 0.06–0.28) and to the right, s2 = 0.01 (−0.01–0.03). For saplings, s2 was significantly positive. However, the two slopes had widely overlapping credible intervals, forcing us to accept the null hypothesis of no change in slope. c, Specific phosphatase activity and resin phosphate for 83 sites under lowland tropical forest in Panama, showing phosphomonoesterase activity and phosphodiesterase activity expressed on the basis of the soil microbial biomass carbon (left) and total soil organic carbon (right). For both transformations, the relationships are almost identical to those for non-standardized activities, but the models explain a slightly smaller proportion of the variance. The hydrolysis product is methylumbelliferone and model fits are exponential functions determined by nonlinear regression. d, The proportion of the widespread species at a site that have negative or positive associations with soil phosphorus, against the resin phosphate concentration for 72 lowland tropical forests in Panama. Species with negative associations with soil phosphorus (low-phosphorus affinity), open blue circles and blue line; species with positive associations with soil phosphorus (high-phosphorus affinity), red circles and red line. The point at which the proportion of low-affinity species equals the proportion of high-affinity species corresponds to a resin phosphate concentration of 2.18 mg P kg−1.

Extended Data Figure 3 Growth responses to phosphorus at the species and community levels.

a, Similarity in the growth rates of individual common species as predicted by the hierarchical model at three different resin phosphate concentrations. Each point represents the growth rate of a single species as estimated from the model, assuming intermediate moisture and a tree of 100 mm dbh. The graphs show the predicted species responses at intermediate resin phosphate (x axis, predicted growth − midP; as shown in Fig. 2a) against the predicted responses at low resin phosphate (predicted growth – lowP; left) and high resin phosphate (predicted growth – highP; right) concentrations. Only species that are common in the dataset (growth data available for >20 individuals) are plotted. The relative estimated responses are virtually identical across the entire phosphorus gradient. b, Observed growth rates as a function of species phosphorus affinities, with growth rates of individual trees ≥ 100 mm dbh shown in black and species-level median growth for the 362 species with estimated phosphorus affinities in blue. The y axis (growth) is log-transformed. The blue line shows a standard linear regression between log-transformed growth and phosphorus affinity (effect size), using median species growth (n = 362), weighted by species abundance. The slope (−0.13) is significantly different from zero (P = 0.00014), demonstrating that growth rates were greater for species with low-phosphorus affinity. c, Standing above-ground biomass (AGB) (top) and annual relative AGB growth (that is, standardized by the total AGB) (bottom) as a function of resin phosphate concentration. Data are from 32 plots across the phosphorus gradient in Panama. The resin phosphate scale is logarithmic. The linear regression relating standing AGB to log(resin phosphate), dry-season intensity and successional state revealed a slight negative but non-significant effect of phosphorus on biomass (slope = −7.9, P = 0.37). The same regression for relative AGB growth was likewise negative but not significant (slope = −0.002, P = 0.09). Biomass was significantly and negatively related to dry-season intensity (that is, more biomass at wetter sites) (P = 0.003), but relative biomass growth was not correlated with dry season intensity (P = 0.07).

Extended Data Figure 4 Relationships between resin phosphate and other measures of soil phosphorus.

a, Comparison of resin phosphate concentration and two common extraction procedures for plant-available phosphorus, showing values for 1,184 fresh (field-moist) soil samples at depths of up to 100 cm in lowland tropical forests of Panama. Relationships are shown for Bray-1 phosphate (top) and Mehlich-III phosphate (bottom). For both extractions, phosphate was determined in the extracts by automated molybdate colorimetry. Resin phosphate is strongly correlated to Bray-1 phosphate (Pearson product–moment correlation 0.81, P < 0.0001) and Mehlich-III phosphate (Pearson product–moment correlation 0.87, P < 0.0001). b, Relationship between resin phosphate concentration and total phosphorus (top) and organic phosphorus (bottom). Data are from soils from 83 sites in central Panama, with each value being the mean of multiple individual soil samples at a single site. The relationships are described by the following equations, derived from linear regression of log-transformed data: total phosphorus: y = 342.43 × (x0.3821), R2 = 0.68, P < 0.001; organic phosphorus: y = 106.01 × (x0.4136), R2 = 0.66, P < 0.001.

Extended Data Figure 5 Phosphorus limitation threshold for total phosphorus.

a, Relationships between phosphatase activities and total phosphorus concentrations in soils from 83 sites under lowland tropical forest in Panama. The figure shows phosphomonoesterase activity (blue circles, left) and phosphodiesterase activity (red circles, right). The hydrolysis product is methylumbelliferone and the model fits are negative exponential functions determined by nonlinear regression. The activity of both phosphatases decreases markedly at total phosphorus concentrations >400 mg P kg−1. b, The proportion of species at a site that has a negative association with soil phosphorus (low-phosphorus affinity, blue circles and blue line) or positive association with soil phosphorus (high-phosphorus affinity, red circles and red line) against total soil phosphorus for 72 lowland tropical forests in Panama. The models are sigmoidal fits and phosphorus associations are defined as effect sizes >0.8 (positive affinity) or <−0.8 (negative affinity). The point at which the proportion of low-affinity species exceeds the proportion of high-affinity species corresponds to a total phosphorus concentration of 435 mg P kg−1.

Extended Data Table 1 Results of the full model used for analysis of the effect of resin on tree growth
Extended Data Table 2 Models evaluating the effects of moisture and nutrients on tree growth
Extended Data Table 3 Model evaluating the effect on tree growth of resin phosphate and Mehlich calcium
Extended Data Table 4 Additional model runs to examine the influence of plot-level parameters on tree growth response to phosphorus

Supplementary information

Life Sciences Reporting Summary (PDF 72 kb)

Supplementary Table 1

This file contains information on 32 forest census plots used in the hierarchical model. (XLSX 20 kb)

Supplementary Table 2

This file contains correlations among soil properties, including dry season moisture deficit, extractable nutrients, organic matter, and texture, in 32 plots in tropical forest in Panama. Significant correlations are in bold text (p < 0.05). Results for the broader set of sites involved in the determination of species distributional associations were reported previously14. (XLSX 11 kb)

Supplementary Table 3

This file contains information on 83 study sites in the phosphatase analysis. Seventy-two of the sites were used to generate phosphorus and moisture affinities of tree species in Condit et al.14. (XLSX 15 kb)

Supplementary Table 4

This file contains species information and affinities to moisture and phosphorus from Condit et al.14. (XLSX 62 kb)

Supplementary Table 5

This file contains species-specific growth rates and responses to phosphorus and moisture in the hierarchical model, obtained from random effects. (XLSX 136 kb)

Supplementary Table 6

This file contains growth responses to phosphorus for small and large trees of 175 common species, defined as those with > 20 individuals with growth data across the plot network. (XLSX 23 kb)

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Turner, B., Brenes-Arguedas, T. & Condit, R. Pervasive phosphorus limitation of tree species but not communities in tropical forests. Nature 555, 367–370 (2018). https://doi.org/10.1038/nature25789

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