Nutrient Availability in Tropical Rain
Forests: The Paradigm of Phosphorus
Limitation
James W. Dalling, Katherine Heineman, Omar R. Lopez,
S. Joseph Wright and Benjamin L. Turner
Abstract A long-standing paradigm in tropical ecology is that phosphorus
(P) availability limits the productivity of most lowland forests, with the largest pool
of plant-available P resident in biomass. Evidence that P limits components of
productivity is particularly strong for sites in Panama and the Amazon basin.
Analyses of forest communities in Panama also show that tree species distributions
are strongly affected by P availability at the regional scale, but that their local
distributions in a single site on Barro Colorado Island (BCI) are as frequently
correlated with base cations as with P. Traits associated with species sensitivity to P
availability require more detailed exploration, but appear to show little similarity
with those associated with N limitation in temperate forests. Recent research
indicates that a large fraction of P in tropical forests exists as organic and microbial
J.W. Dalling (&)
Department of Plant Biology, University of Illinois at Urbana-Champaign,
505 S. Goodwin Avenue, Urbana, IL 61801, USA
e-mail: dalling@illinois.edu
J.W. Dalling 
 O.R. Lopez
Smithsonian Tropical Research Institute, Apartado Postal,
0843-03092 Panama, Republic of Panama
e-mail: olopez@indicasat.org.pa
K. Heineman
Program in Ecology, Evolution and Conservation Biology,
University of Illinois at Urbana-Champaign, 505 S. Goodwin Avenue,
Urbana, IL 61801 USA
e-mail: kheineman@life.illinois.edu
O.R. Lopez
Instituto de Investigaciones Científicas y Servicios de Alta Tecnología,
Apartado Postal, 0843-01103 Ciudad de Saber, Panama, Republic of Panama
S.J. Wright 
 B.L. Turner
Smithsonian Tropical Research Institute, Apartado Postal,
0843-03092 Balboa, Panama, Republic of Panama
e-mail: WRIGHTJ@si.edu
B.L. Turner
e-mail: TurnerBL@si.edu
© Springer International Publishing Switzerland 2016
G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_12
261
P in the soil; plant adaptations to access organic P, including the synthesis of
phosphatase enzymes, likely represent critical adaptations to low P environments.
Plants also cope with low P availability through increases in P use-efficiency
resulting from increased retention time of P in biomass and decreased tissue P
concentration. Although foliar P responds strongly to P addition, we show here that
foliar P and N:P are highly variable within communities, and at BCI correlate with
regional species distributional affinity for P. An improved understanding of P
limitation, and in particular the plasticity of responses to P availability, will be
critical to predicting community and ecosystem responses of tropical forests to
climate change.
Keywords Ecosystem nutrient budget 
 Fertilization experiments 
 Nutrient
uptake 
 Physiological traits 
 Soil nutrients
Introduction
Humid low elevation tropical forests support among the highest above-ground
biomass and net primary productivity of any ecosystem (Scurlock and Olson 2002;
Houghton 2005). Yet, many tropical forests that have been cleared for agriculture
fail to support crop yields for more than a few years without large fertilizer inputs
(Nye and Greenland 1960; Sanchez et al. 1983; Lal 1986). This apparent paradox
suggested that much of the nutrient reserve of tropical forests is stored in plant
tissue, resulting in critical nutrient limitation once biomass is removed. A synthesis
of datasets on nutrient concentrations in leaves and senescent tissue returning to the
ecosystem as litterfall highlighted phosphorus (P) as the nutrient that most clearly
distinguishes the stoichiometry of tropical from temperate forests, leading to the
paradigm that P availability constrains the productivity of most lowland tropical
forests (Vitousek 1984). Here we review the evidence for this paradigm, high-
lighting the insights gained over the past three decades on the distribution of P in
tropical ecosystems, its availability to plants, adaptations of plants for P acquisition
and use, and evidence that plant growth and forest diversity reflects not only P
supply, but also co-limitation by nitrogen (N) and base cations.
Nutrient Limitation in Tropical Forests
Many tropical soils are strongly weathered, reflecting warm, moist conditions acting
on stable land surfaces that were not directly affected by Quaternary glaciations
(Baillie 1996). These older, well-weathered ‘Oxisol’ (Soil Taxonomy system; Soil
262 J.W. Dalling et al.
Survey Staff 1999) or ‘Ferralsol’ soils (IUSS Working Group WRB 2014) are
characterized by a moderately organically enriched surface horizon, and deep,
relatively uniform yellow-red subsoils, reflecting weathering of clay minerals into
ferric sesquioxides (Baillie 1996). Chemically, these soils are acidic, highly lea-
ched, with a low cation exchange capacity and high aluminum saturation. Beyond
this broad generalization, however, lies a diversity of soil physical properties
(notably influencing drainage patterns and water-holding capacity) and chemical
properties reflecting heterogeneous parent materials, substrate age, and topographic
effects on soil development. Nonetheless, a feature of many soil orders associated
with tropical forests is limited P availability and low total P, resulting from long
periods of leaching and strong adsorption or occlusion of P with iron and alu-
minium oxides (summarized in Table 10.12 in Baillie 1996).
The central importance of P limitation to the productivity of lowland forests
reached prominence after comparisons of litterfall in temperate and tropical forests
(Vitousek 1984). If P is a key limiting nutrient, then plants might be expected either
to function with less of it (reflected in lower tissue P concentrations), or to cycle it
more efficiently (reflected in part in higher resorption efficiency of P as tissues
senesce). Analysis of nutrient concentrations and nutrient ratios in leaf litter is
consistent with both mechanisms. Litterfall from lowland tropical forests, particu-
larly those on older, more weathered soils of the Amazon basin, had low P con-
centrations, whereas tissue N and Ca concentrations were mostly comparable to
temperate forests (Vitousek 1984). This study also highlighted differences in nu-
trient limitation between lowland and montane tropical forests. In montane forests,
P availability can be low, and foliar P generally declines with elevation (Tanner
et al. 1998; Benner et al. 2010). However, N limitation appears to be much more
important in the mountains than in the lowlands, probably due to temperature and
moisture effects on rates of mineralization (e.g. Grubb 1977; Vitousek et al. 1994;
reviewed in Benner et al. 2010).
Fertilization experiments have generally supported the view of P limitation in
lowland forests, and N or N and P limitation in montane forests (reviewed by Sayer
and Banin, this volume, Dalling et al. 2015). However, insights from fertilization
experiments are incomplete with regard to the scale and generality of nutrient
limitation. This is because factorial fertilization experiments are expensive to
establish and therefore restricted in the number of nutrient addition treatments that
can be included, and may take many years to yield clear treatment effects (Sullivan
et al. 2014). Fertilization experiments may therefore miss co-limitation scenarios
that could arise either because productivity in different plant size classes or tissue
types have different and distinct nutrient requirements (as seen in responses to
growth vs. litterfall responses to N, P and K in the Gigante fertilization experiment;
Wright et al. 2011), or because the limited scale and replication of fertilization
experiments precludes analyses of the individual species responses that contribute
to heterogeneous nutrient limitation (Alvarez-Clare et al. 2013; Dalling et al. 2015).
Nutrient Availability in Tropical Rain Forests … 263
Mixed Evidence of Phosphorus Limitation at the Local Scale
If P availability alone governs forest growth and productivity then we would predict
that, at the community level, N:P would be relatively tightly constrained, with
ratios >16 (the Redfield ratio; Koerselman and Mueleman 1996) reflecting selection
for efficient P use. However, evidence from community-wide analyses of foliar N:P
do not support this prediction, with very wide variation in N:P in lowland forests,
but declining N:P with elevation (Fig. 1). In an analysis compiling published
datasets of foliar nutrients from neotropical sites, Townsend et al. (2007) found
limited evidence for environmental control over N:P. Instead, they found large
interspecific variation in N:P among species in lowland forests, suggesting coex-
isting tree species are likely to differ widely in their nutrient requirements (see also
Hättenschwiler et al. 2008; Hedin et al. 2009).
Similarly, analyses of species distributions within large forest dynamics plots
show correlations with a multitude of soil nutrients, with no clear preference for P
(John et al. 2007). For example, at Barro Colorado Island (BCI), Panama, 40 % of
10
20
30
40
Lowland (BCI) Montane (Fortuna)
Sp
ec
ie
s 
M
ea
n 
Fo
lia
r N
:P
Fig. 1 The distribution of species mean foliar N:P ratios for 281 lowland tree species sampled on
Barro Colorado Island (BCI) in the Panama Canal and 91 montane tree species sampled at Fortuna
Forest Reserve in western Panama (800–1300 m a.s.l). The hinges of the boxplot represent the
interquartile range (IQR), and the whiskers extend to the largest and smallest values within
1.5 * IQR. Community mean N:P ratio was significantly higher on BCI (NP = 22.8) than Fortuna
(NP = 19.5; t = 5.65, df = 179.3, P < 0.001). However, variance did not differ significantly between
sites (levene test, F = 2.8; df = 1,370; P = 0.093). The line at N:P = 15 represents the Redfield
Ratio, which is the empirically derived threshold between N and P limitation in terrestrial
ecosystems
264 J.W. Dalling et al.
the 258 most common tree species in the 50 ha forest dynamics plot show a
significant association in their local distribution patterns with at least one principal
component axis representing variation in soil chemical variables (John et al. 2007).
Analysis of individual soil variables shows a relatively even distribution in the
frequency of associations across soil variables (Fig. 2), with as many species
showing significant distributional associations with boron (B), calcium (Ca),
potassium (K), and zinc (Zn) as with P.
The lack of a clear pattern of association between tree species distributions and
soil P could reflect insufficient variability in P availability at the plot level, strong
spatial autocorrelation among soil nutrients, or strong similarity among species in P
requirements. Despite its location on a relatively flat andesite plateau, nutrient
availability within the BCI plot is quite variable. Soil P, extracted using Mehlich III
and analyzed using ICP, ranged from 0.45 to 6.8 mg/kg (10th–90th percentiles).
Although as a group base cations were strongly positively correlated at BCI
(defining the first principal component of soil chemical variation), P concentration
was only weakly correlated with base cations and instead loaded most strongly on a
second principal component axis. Although it might therefore be tempting to
conclude that demographic rates, and therefore distributions of species on BCI are
not primarily differentiated by P requirements, species distributions across the
Panama Canal area forests suggest otherwise.
Fig. 2 Frequency of association of 258 tree species with 12 soils variables measured at 300
locations in the 50 ha forest dynamics plot on Barro Colorado Island, Panama. Positive and
negative associations indicate that species occurred at sites with higher and lower than expected
concentrations (p < 0.05) of that variable based on assessment using the Poisson Cluster Method
(John et al. 2007)
Nutrient Availability in Tropical Rain Forests … 265
Evidence for Phosphorus Limitation at Landscape
and Regional Scales
Analysis of tree communities in 72 forest plots distributed across the 66 km-wide
Isthmus of Panama surrounding BCI has revealed a much stronger imprint of soil P
on species distributions. Condit et al. (2013) examined whether the distribution of
550 tree species in this regional species pool showed distributional associations
with seven environmental variables measured at each plot, and with dry season
moisture availability estimated from a network of rain gauges. This analysis con-
firmed that dry season rainfall was the strongest environmental predictor of tree
distributions, with strong effects on 66 % of species, reflecting a steep gradient in
dry season intensity from the Caribbean to Pacific coasts of Panama. More of a
surprise, however, was that P availability affected nearly as many species (58 %),
revealing a previously unrecognized environmental filter acting on the composition
of these forests. Furthermore, species partitioned a gradient of P availability rela-
tively evenly, with 23 % of species showing affinity for high P and 35 % for low P
soils.
Phosphorus effects on tree community composition may be particularly strong in
central Panama because of the remarkable variation in P availability (resin
extractable P varies from <0.1 to 22.8 mg P kg−1; Condit et al. 2013); comparable
in magnitude to that of the entire lowland tropics (Condit et al. 2013 and references
therein). However, other soil nutrients, notably calcium, were associated with the
distribution of 35 % of tree species, raising the possibility that observed associa-
tions are at least in part driven by other correlated resources. To test whether species
associations reflect differences in growth response to P availability, we have begun
measuring seedling growth rates in a pot experiment manipulating P availability.
Seedlings of fifteen species with contrasting distributions across the Isthmus were
transplanted to a low P soil (0.13 mg kg−1 resin extractable P) and fertilized weekly
with a full nutrient solution either with or without added P. The magnitude of
species growth increase in the P addition treatment was significantly positively
correlated with the degree to which species distributions were skewed towards high
P soils (determined from the Condit et al. (2013) dataset).
Phosphorus Limitation: Links to Functional
and Physiological Traits
Species distributional affinity for P is also likely to be correlated with plant func-
tional traits that potentially impact ecosystem processes. In another pot experiment
exploring how Panamanian tree species respond to P availability, Vargas and Lopez
(unpublished data), found that Hura crepitans, a species with affinity for high P
soils, showed significantly higher leaf specific hydraulic conductance (KL) when
grown under high P conditions, suggesting the potential for P availability to
266 J.W. Dalling et al.
influence ecosystem water balance. Higher KL under high P might be the result of
increased xylem vessel diameter or a by-product of shifts in allocation patterns, and
reduction in wood density (Goldstein et al. 2013).
More broadly, soil P availability is often correlated with foliar P concentration
(Vitousek and Sandford 1983), with effects on decomposition rates and therefore
nutrient cycling (reviewed in Cornwell et al. 2008). While foliar P concentration is
a plastic trait that responds to P fertilization (e.g., Santiago et al. 2012; Mayor et al.
2014), community wide foliar P values may also reflect the wider distribution
patterns of constituent species. We compared foliar N and P concentrations mea-
sured in shade leaves of three individuals of each of 137 species collected on BCI
(Wright and Turner, unpublished data) with species distributional affinity for P from
Condit et al. (2013). Foliar P was significantly positively correlated with distribu-
tional affinity for P (Fig. 3; r = 0.45, p < 0.001), and foliar N:P was significantly
-1 0 1 2
-1 0 1 2
-1 0 1 2
Species P Affinity
10
20
30
40
10
20
30
40
0.
5
1.
0
1.
5
2.
0
2.
5
Fo
ila
r N
:P
Fo
ila
r N
 (m
g/g
)
Fo
ila
r P
 (m
g/g
)
Fig. 3 Relationship between
foliar N, P, and N:P of shade
leaves of 137 tree species
collected on Barro Colorado
Island, Panama, and the index
score of species affinity for P,
based on the distribution of
the same species across 72
sites across the Isthmus of
Panama varying in
resin-extractable P. Positive P
affinity index scores indicate
that species were associated
with sites with high
resin-extractable P
Nutrient Availability in Tropical Rain Forests … 267
negatively correlated (r = –0.38, p < 0.001). Foliar N was not significantly corre-
lated with P affinity (r = 0.17). Interspecific variation in foliar nutrient concentration
may, in turn, be expected to correlate with juvenile and adult growth rates, however
no significant relationships were found between foliar N, P and N:P with sapling
(>1 cm DBH) or juvenile and adult (>10 cm DBH) growth rates of the same 137
species in the BCI 50 ha plot.
Elsewhere, an affinity for low P soils has been found to correlate with a high
P use-efficiency (PUE; a measure of biomass increment per unit P). In Queensland,
Australia, Gleason et al. (2009) found that tree species that were specialists on
P-poor schist-derived soils had twice the PUE of generalist species. High PUE in
turn was related to lower wood P concentrations and to higher retention time of P in
the canopy, but was unrelated to above-ground net primary productivity (sum of
radial growth and litter production). In contrast, along a steeper gradient of soil
P availability spanning the eastern slope of the Andes to the highly weathered and P
impoverished soils of the Guiana Shield, total soil P correlates positively with foliar
P concentration (Fyllas et al. 2009) and wood production, and inversely with wood
density (Mercado et al. 2011; Quesada et al. 2012).
Phosphorus Pools in Soil and Biomass
Much of our understanding of the chemistry of P limitation is based on temperate
chronosequences (Walker and Syers 1976). These studies generally show that given
sufficient time for pedogenesis, a decline in the total P pool size occurs, and is
accompanied by a decline in primary mineral P, and a corresponding increase in the
proportion of the total P occurring in occluded and organic forms. Similar shifts
between inorganic and organic P pools have been observed in the Hawaiian island
chronosequence (Crews et al. 1995), and are likely to be more generally reflected in
wet tropical forests (although no long-term chronosequence has been identified in
species-rich lowland tropical rain forest).
Nonetheless, a traditional view of P cycling in tropical forests holds that the
biological uptake of P is tightly coupled with the deposition of labile P via canopy
litterfall and relies very little on soil organic and inorganic P pools. According to
this hypothesis, nearly all the biologically available P in tropical forests should be
sequestered in plant biomass. This view is supported by the observation that while
intact tropical forests are highly productive, forested land cleared and converted to
pasture is often P-impoverished and frequently abandoned within a few years of
conversion (Serrao et al. 1996). Furthermore, Stark and Jordan (1978) provided
evidence for “direct-cycling” of P by demonstrating that only 0.1 % of
isotopically-labeled P and calcium applied directly soil surface was lost beyond the
root mat in a Venezuelan rainforest, indicating that there should be little chance that
organic P is leached from the ecosystem, or sequestered to iron or aluminum oxides
in the soil.
268 J.W. Dalling et al.
Recent studies, however, provide increasing evidence that soil organic P pools,
which constitute about 25 % of total soil P in tropical forests (Turner and
Engelbrecht 2011), are more dynamic and chemically variable than previously
thought. For example, total soil organic P concentrations decline markedly (up to
25 %) during the dry season (Turner et al. 2015), while Vincent et al. (2010)
showed that organic P contained in DNA and phosphate monoesters declined in
response to experimental litter removal and increased in response to litter addition.
These studies indicate that there are more persistent pools of accessible organic P in
the soil beyond those directly re-assimilated from litter into plant biomass. In broad
terms, the pool of organic P available to plants can be considered to constitute three
groups: (1) recently senesced plant or microbial material, (2) P sequestered in live
microbial biomass and (3) “stable” organic P bound to iron or aluminum oxides.
Soil microbial biomass, characterized by low C:P ratios relative to plant biomass, is
an important P sink in forested ecosystems, and can represent a large fraction of the
total biomass-associated P (Turner et al. 2013). In a lowland tropical forest in
Panama, microbial P was estimated to account for approximately two thirds of the
total soil organic P (Turner et al. 2015). While microbes may compete with vascular
plants for P, microbial sequestration of P prevents the loss of ecosystem P to more
permanent geochemical sinks (Oberson et al. 1997), and facilitates the mineral-
ization of organic P to plant available phosphate (Richardson and Simpson 2011).
A recent detailed ecosystem P budget for sites representing a five-fold range in total
P storage in a Panamanian montane forest reveals that the amount of available P
contained in soil microbial and non microbial pools greatly exceeds the amount of P
sequestered in foliar and woody plant tissues at all sites (Heineman unpublished
data), contrary to the paradigm that labile P is sequestered primarily in plant
biomass.
Acquisition of Organic Phosphorus in Tropical Forests
Adaptations of plants to low P environments may reflect alterations both in P use
efficiency and in the ability to acquire P from less readily available sources. Turner
(2008) suggested that a gradient of biological availability of soil organic P exists,
which is determined by the investment cost to plants of producing an array of
enzymes required to catalyze the hydrolysis and release of phosphate. At one
extreme, plants can take up dissolved phosphate directly from the soil solution or
via mycorrhizas. Simple phosphate monoesters, such as glucose 6-phosphate
however require hydrolysis using phosphomonoesterase enzymes. Phosphate die-
sters, including phospholipids and nucleic acids, require both phosphomonoesterase
and phosphodiesterase enzymes to release phosphate. Finally, inositol hexak-
isphosphates require both solubilization from organic matter or clay minerals and
hydrolysis by phytase enzymes. Turner (2008) further suggested that differences in
the enzymatic capacity of plants confronted with an array of potential P sources
could represent an axis of resource partitioning among plant species.
Nutrient Availability in Tropical Rain Forests … 269
Consistent with the hypothesis that species partition P sources, pools of organic
P differ in composition across a gradient in total soil P (Turner and Engelbrecht
2011) with a higher ratio of phosphomonoesters to phosphodiesters in sites with
higher total P. Nonetheless, to date, little evidence has emerged to suggest that
plants from P impoverished tropical forests differ in their capacity to produce
phosphatase enzymes when compared to those from more P-rich sites. In lower
montane forest at Fortuna, Panama, Steidinger et al. (2015) measured the produc-
tion of phosphomonoesterase and phosphodiesterase of excised roots of arbuscular
mycorrhizal (AM), ectomycorrhizal (EM) and non-mycorrhizal (NM) plant species.
They found only weak evidence for differences in enzymatic activity among these
groups, with no difference in activity between AM and EM taxa but significantly
higher phosphodiesterase activity in the NM taxon. A second experiment with the
same taxa compared growth rates of seedlings infected with mycorrhizas and grown
in acid-washed sand fertilized with inorganic phosphate, glucose phosphate, RNA
and phytate as the sole P source. Again, AM and EM species did not differ in their
response to organic sources of P, but the NM taxon, Roupala montana (Proteaceae)
was the only species capable of exploiting phytate as a P source. At Fortuna EM
and AM taxa, as well as Roupala occur in multiple sites that differ in P availability
(as determined by resin-extractable P and total P). Although the difference in P
source use between Roupala and other taxa suggests P source partitioning could
occur, its ecological significance in tropical forests requires further exploration,
including greater species replication of mycorrhizal groups.
Investment in phosphatase enzymes, however, may explain the abundance of N
fixing legumes, which can account for a large fraction of stems and basal area in
lowland tropical forests (Losos and Leigh 2004) and on occasions form mon-
odominant stands (Connell and Lowman 1989). The dominance of nitrogen fixers
in ecosystems where P is considered to limit forest productivity suggests that
increasing N availability may indirectly impact P acquisition. Houlton et al. (2008)
pointed out that phosphatase production is nitrogen-intensive (up to 15 % N by
mass), and that N2 fixing plants might therefore be able to increase allocation to
phosphatase relative to non-fixers. Evidence generally supports the Houlton
hypothesis, with higher phosphatase activity in soil beneath N2 fixing plants
(Houlton et al. 2008), higher root phosphatase activity (and AM infection) in N2
fixing lowland tropical trees (Nasto et al. 2014), and an increase in the phospho-
monoesterase activity of N2 fixing legumes relative non-fixers with declining soil P
along a chronosequence in Western Australia (Png et al. 2014).
Conclusions and Future Directions
The consequences of P limitation from the individual to the whole community-level
remains a relatively poorly studied aspect of tropical plant ecophysiology and forest
ecology. Just as N availability can limit the productivity of temperate plants under
elevated CO2 (e.g., Long et al. 2004; Norby et al. 2010; but see Drake et al. 2011),
270 J.W. Dalling et al.
chronic P limitation has the potential to constrain the response of tropical forest
plants to rising CO2, particularly if reduced transpiration rates also reduce P uptake
(Cernusak et al. 2011). Despite this, experimental data to explore how CO2 and P
interact to influence the growth of tropical plants remains extremely scarce
(Cernusak et al. 2013). Likewise, an understanding of how tropical forest plants
have adapted to low P environments, either through increases in P-use efficiency or
phosphate-acquisition efficiency, can provide insights into how to manage P inputs
more efficiently in agricultural settings to maximize crop yields while minimizing P
exports from the system (Veneklaas et al. 2012).
References
Alvarez-Clare S, Mack MC, Brooks M (2013) A direct test of nitrogen and phosphorus limitation
to net primary productivity in a lowland tropical wet forest. Ecology 94:1540–1551
Baillie IC (1996) Soils of the humid tropics. In: Richards PW (ed) The tropical rain forest.
Cambridge University Press, Cambridge, pp 256–285
Benner J, Vitousek PM, Ostertag R (2010) Nutrient cycling and nutrient limitation in tropical
montane cloud forest. In: Bruijnzeel LA, Scatena FN, Hamilton LS (eds) tropical montane
cloud forest. Cambridge University Press, Cambridge, pp 90–100
Cernusak L, Winter K, Turner BL (2011) Transpiration modulates phosphorus acquisition in
tropical tree seedlings. Tree Phys 31:878–885
Cernusak L, Winter K, Dalling JW et al (2013) Tropical forest responses to increasing [CO2]:
current knowledge and opportunities for future research Func. Plant Biol 40:531–551
Condit R, Engelbrecht BMJ, Pino D et al (2013) Species distributions in response to individual soil
nutrients and seasonal drought across a community of tropical trees. P Natl Acad Sci
110:5064–5068
Connell JH, Lowman MD (1989) Low-diversity tropical rain forests: some possible mechanisms
for their existence. Am Nat 134:19–88
Cornwell WK, Cornelissen JH, Amatangelo K et al (2008) Plant species traits are the predominant
control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–1071
Crews TE, Kitayama K, Fownes JH et al (1995) Changes in soil-phosphorus fractions and
ecosystem dynamics across a long chronosequence in Hawaii. Ecology 76:1407–1424
Dalling JW, Heineman K, González G et al (2015) Geographic, environmental and biotic sources
of variation in the nutrient relations of tropical montane forests. J Trop Ecol in press
Drake JE, Gallet-Budynek A, Hofmockel KS et al (2011) Increases in the flux of carbon
belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest
productivity under elevated CO2. Ecol Lett 14:349–357
Fyllas NM, Patino S, Baker TR et al (2009) Basin-wide variations in foliar properties of
Amazonian forest: phylogeny, soils and climate. Biogeosciences 6:2677–2708
Gleason SM, Read J, Ares A et al (2009) Phosphorus economics of tropical rainforest species and
stands across soil contrasts in Queensland, Australia: understanding the effects of soil
specialization and trait plasticity. Func Ecol 23:1157–1166
Goldstein G, Bucci SJ, Scholz FG (2013) Why do trees adjust water relations and hydraulic
architecture in response to nutrient availability? Tree Phys 33:238–240
Grubb PJ (1977) Control of forest growth and distribution on wet tropical mountains: with special
reference to mineral nutrition. Ann Rev Ecol Syst 8:83–107
Hättenschwiler S, Aeschlimann B, Coûteaux MM et al (2008) High variation in foliage and leaf
litter chemistry among 45 tree species of a neotropical rainforest community. New Phytol
179:165–175
Nutrient Availability in Tropical Rain Forests … 271
Hedin LO, Brookshire ENJ, Menge DNL et al (2009) The nitrogen paradox in tropical forest
ecosystems. Ann Rev Ecol Evol Syst 40:613–635
Houghton RA (2005) Above-ground forest biomass and the global carbon balance. Global Change
Bio 11:945–958
Houlton BZ, Wang Y-P, Vitousek PM et al (2008) A unifying framework for dinitrogen fixation in
the terrestrial biosphere. Nature 454:327–331
IUSS Working Group WRB (2014) World Reference Base for Soil Resources 2014. International
soil classification system for naming soils and creating legends for soil maps. World Soil
Resources Reports No. 106. FAO, Rome
John RC, Dalling JW, Harms KE et al (2007) Soil nutrients influence spatial distributions of
tropical tree species. P Natl Acad Sci 104:864–869
Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature
of nutrient limitation. J Appl Ecol 33:1441–1450
Lal R (1986) Conversion of tropical rainforest: agronomic potential and ecological consequences.
Adv Agron 39:173–264
Long SP, Ainsworth EA, Rogers A et al (2004) Rising atmospheric carbon dioxide: plants face the
future. Ann Rev Plant Biol 55:591–628
Losos EC, Leigh EG (2004) Tropical forest diversity and dynamism: findings from a large-scale
plot network. University Chicago Press, Chicago
Mayor JR, Wright SJ, Turner BL (2014) Species-specific responses of foliar nutrients to long-term
nitrogen and phosphorus additions in a lowland tropical forest. J Ecol 102:36–44
Mercado LM, Patiño S, Domingues TF et al (2011) Variations in Amazon forest productivity
correlated with foliar nutrients and modelled rates of photosynthetic carbon supply. Phil Trans
Royal Soc Series B 366:3316–3329
Nasto MK, Alvarez-Clare S, Lekburg Y et al (2014) Interactions among nitrogen fixation and soil
P acquisition strategies in lowland tropical forest. Ecol Lett 17:1282–1289
Norby RJ, Warren JM, Iversen CM et al (2010) CO2 enhancement of forest productivity
constrained by limited nitrogen availability. P Natl Acad Sci 107:19368–19373
Nye PH, Greenland DJ (1960) The soil under shifting cultivation. Commonwealth Bureau of Soils,
Harpenden UK. Tech Comm 51:73–126
Oberson A, Friesen DK, Morel C et al (1997) Determination of phosphorus released by chloroform
fumigation from microbial biomass in high P sorbing tropical soils. Soil Biol Biochem
29:1579–1583
Png GK, Laliberté E, Hayes PE et al (2014) Do N2-fixing plants show higher root phosphatase
activity on P-poor soils? In: Mucina L, Price JN, Kalwij JM (eds) Biodiversity and vegetation:
patterns, processes, conservation. Kwongan Foundation, Perth, p 255
Quesada CA, Phillips OL, Schwarz M et al (2012) Basin-wide variations in Amazon forest
structure and function are mediated by both soils and climate. Biogeosciences 9:2203–2246
Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability. Plant
Phys 156:989–996
Sanchez PA, Villachica JH, Bandy DE (1983) Soil fertility dynamics after clearing a tropical
rainforest in Peru. Soil Sci Soc Am J 47:1171–1178
Santiago LS, Wright SJ, Harms KE et al (2012) Tropical tree seedling growth responses to
nitrogen, phosphorus and potassium addition. J Ecol 100:309–316
Scurlock JMO, Olson RJ (2002) Terrestrial net primary productivity—a brief history and a new
worldwide database. Env Rev 10:91–109
Serrao EAS, Nepstad D, Walker R (1996) Upland agricultural and forestry development in the
Amazon: sustainability, criticality and resilience. Ecol Econ 18:3–13
Soil Survey Staff (1999) Soil taxonomy: a basic system of soil classification for making and
interpreting soil surveys. United States Department of Agriculture-Natural Resources
Conservation Service, Lincoln
Stark NM, Jordan CF (1978) Nutrient retention by the root mat of an Amazonian rain
forest. Ecology: 434–437
272 J.W. Dalling et al.
Steidinger BS, Turner BL, Corrales A et al (2015) Variability in potential to exploit different soil
organic phosphorus compounds among tropical montane tree species. Func Ecol 29:121–130
Sullivan BW, Alvarez-Clare S, Castle SC et al (2014) Assessing nutrient limitation in complex
forested ecosystems: alternatives to large-scale fertilization experiments. Ecology 95:668–681
Tanner EVJ, Vitousek PM, Cuevas E (1998) Experimental investigation of nutrient limitation of
forest growth on wet tropical mountains. Ecology 79:10–22
Townsend AR, Cleveland CC, Asner GP et al (2007) Controls over foliar N:P ratios in tropical
rain forests. Ecology 88:107–118
Turner BL (2008) Resource partitioning for soil phosphorus: a hypothesis. J Ecol 96:698–702
Turner BL, Lambers H, Condron LM et al (2013) Soil microbial biomass and the fate of
phosphorus during long-term ecosystem development. Plant Soil 367:225–234
Turner BL, Engelbrecht BM (2011) Soil organic phosphorus in lowland tropical rain forests.
Biogeochemistry 103:297–315
Turner BL, Yavitt JB, Harms KE et al (2015) Seasonal changes in soil organic matter after a
decade of nutrient addition in a lowland tropical forest Biogeochemistry (in press)
Veneklaas EJ, Lambers H, Bragg J et al (2012) Opportunities for improving P-use efficiency in
crop plants. New Phytol 195:306–320
Vincent AG, Turner BL, Tanner EVJ (2010) Soil organic phosphorus dynamics following
perturbation of litter cycling in a tropical moist forest. Eur J Soil Sci 61:48–57
Vitousek PM (1984) Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology
65:285–298
Vitousek PM, Sanford RL (1983) Nutrient cycling in moist tropical forest. Ann Rev Ecol Syst
17:137–167
Vitousek PM, Turner DR, Parton WJ et al (1994) Litter decomposition on the Mauna Loa
environmental matrix, Hawaii – patterns, mechanisms, and models. Ecology 75:418–429
Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderm 15:1–19
Wright SJ, Yavitt JB, Wurzburger N et al (2011) Potassium, phosphorus and nitrogen limit forest
plants growing on a relatively fertile soil in the lowland tropics. Ecology 92:1616–1625
Nutrient Availability in Tropical Rain Forests … 273