Nitrogen uptake strategies of edaphically specialized
Bornean tree species
Sabrina E. Russo ? Amy Kochsiek ?
Jocelyn Olney ? Lauren Thompson ?
Amy E. Miller ? Sylvester Tan
Received: 13 August 2013 / Accepted: 19 September 2013 / Published online: 25 September 2013
 Springer Science+Business Media Dordrecht 2013
Abstract The association of tree species with par-
ticular soil types contributes to high b diversity in
forests, but the mechanisms producing such distribu-
tions are still debated. Soil nitrogen (N) often limits
growth and occurs in differentially available chemical
forms. In a Bornean forest where tree species compo-
sition changes dramatically along a soil gradient
varying in supplies of different N-forms, we investi-
gated whether tree species? N-uptake and soil special-
ization strategies covaried. We analyzed foliar 15N
natural abundance for a total of 216 tree species on
clay or sandy loam (the soils at the gradient?s
extremes) and conducted a 15N-tracer experiment
with nine specialist and generalist species to test
whether species displayed flexible or differential
uptake of ammonium and nitrate. Despite variation
in ammonium and nitrate supplies and nearly 4 %
difference in foliar d15N between most soil specialists
and populations of generalists on these soils, our 15N
tracer experiment showed little support for the
hypothesis that soil specialists vary in N-form use or
the ratios in which they use these forms. Instead, our
results indicate that these species possess flexible
capacities to take up different inorganic N forms.
Variation between soil specialists in uptake of differ-
ent N forms is thus unlikely to cause the soil
associations of tree species and high b diversity
characteristic of this Bornean rain forest. Flexible
uptake strategies would facilitate N-acquisition when
supply rates of N-forms exhibit spatiotemporal vari-
ation and suggest that these species may be function-
ally redundant in their responses to N gradients and
influences on ecosystem N-cycles.
Keywords Ammonium  15-N  Malaysia 
Nitrate  Soil gradient  Stable isotope tracer
experiment  Tropical forest
Introduction
b diversity, or the diversity contributed by turnover of
species along environmental gradients, arises in
forests because many tree species occur only in
particular habitats, defined by the availability of above
and belowground resources and interactions with
herbivores and pathogens (Whittaker 1956; Ashton
1964; Janzen 1974; Whitmore 1978). Although much
S. E. Russo (&)  A. Kochsiek  J. Olney  L. Thompson
School of Biological Sciences, Manter Hall, University of
Nebraska, Lincoln, NE 68588-0118, USA
e-mail: srusso2@unl.edu
S. E. Russo  S. Tan
Center for Tropical Forest Science, Arnold Arboretum
Asia Program, Harvard University, Cambridge,
MA 02138, USA
A. E. Miller
Southwest Alaska Network, U.S. National Park Service,
Anchorage, AK 99501, USA
123
Plant Ecol (2013) 214:1405?1416
DOI 10.1007/s11258-013-0260-4
research has demonstrated how light availability
affects tree species? distributions (e.g., Chazdon
1986; Kobe et al. 1995; Dalling and Hubbell 2002),
the mechanisms contributing to tree species? special-
ization to particular soil habitats are still debated. Most
hypothesized mechanisms involve species? differen-
tial requirements for and responses to variation in soil
nutrient or water availability (Grime 1979; Tilman
1982; Chapin et al. 1986, 1993).
Nitrogen (N) often limits or co-limits plant growth,
and is critical to photosynthetic carbon gain (Field and
Mooney 1990; Marschner 1995). Soil N occurs in a
variety of organic and inorganic forms that are
differentially available to plant roots (Marschner
1995). Complex organic N in litter is mineralized by
microorganisms, producing ammonium (NH?4 ) that is
converted to nitrate (NO3 ). Plants are often flexible in
their capacity to take up the chemical forms of N that
are the most readily available (Scott and Rothstein
2011), but some species also display preferences for
particular forms of N (von Wire?n et al. 1997). It is still
unclear how prevalent generalized versus specialized
N-uptake strategies are among plant species and to
what extent strategies vary among ecosystems, soil
environments, and plant functional groups.
Competition in the rhizosphere for different forms of
N can affect the partitioning of soil N among plant
species and is thus expected to influence plant species
coexistence and community composition (Kahmen et al.
2006). Evidence from a variety of ecosystems indicates
that N-partitioning through preferential uptake of partic-
ular N forms is not uncommon. Early and late succes-
sional tree species have been found to display differential
uptake of NO3 versus NH
?
4 , respectively, which, due
to variation in the availability of these N-forms along
successional gradients, affects tree distributions
(Stewart et al. 1988; Kronzucker et al. 1997; Aidar
et al. 2003). In N-limited arctic and alpine tundra plant
communities, species composition was found to
correlate with the partitioning of differentially avail-
able forms of N, with dominance being linked to a
species? ability to exploit the most abundant N-form
(McKane et al. 2002; Ashton et al. 2010). Preference
for different N-forms has not, however, always been
linked to plant species? distributions (e.g., Aanderud
and Bledsoe 2009; von Felten et al. 2009). Although
the distributions of understory palm species along a
soil gradient in a Panamanian tropical forest were
more closely linked to nutrient availability than to
either rainfall or light (Andersen et al. 2012), no
species showed a significant preference for forms of N
that were most abundant in the soils in which they
grew. Instead, species? distributions were related to
total N-uptake rates (Andersen and Turner 2013).
Flexibility in the use of different N forms has also
been demonstrated in a range of ecosystems. In alpine
tundra, some plant species have been found to absorb
all N forms supplied, but alter uptake of them
depending on the intensity of competition for N and
the identity of neighboring plants (Miller and Bowman
2002; Miller et al. 2007). Similarly, based on 15N
natural abundance in vegetation and soils, tree species
in Hawaiian tropical forests along a rainfall gradient
did not appear to specialize on different soil N pools,
but rather responded to changes in the availability of
soil N to exploit the most abundant N-form (Houlton
et al. 2007).
The capacity of plants to take up different N forms
should be adaptive, assuming that costs of such
plasticity are not high (Scheiner and Berrigan 1998).
However, if specialization on particular forms enables
dramatically more efficient uptake, then between-
species differences in N uptake strategies may lead to
niche partitioning across edaphic gradients varying in
supply rates of N forms, which would facilitate species
coexistence (Tilman 1982). Work to date testing this
hypothesis in tropical forests has focused on relating
tree species? traits (e.g., foliar N and d15N, nitrate
reductase activity) to the availability and isotopic
signature of different N-forms (Aidar et al. 2003;
Schimann et al. 2008; Andersen et al. 2012) and rates
of microbial transformations of N in soil (Schimann
et al. 2008; Andersen et al. 2012). Few studies have
directly quantified differences among tropical tree
species in the capacity to take up different forms of N,
with the exception of Andersen and Turner (2013),
who limited their work to understory palms. We
sought to fill this gap by testing whether tree species in
a Bornean rain forest display differential uptake of
different chemical forms of N using both 15N natural
abundance (d15N) and a 15N tracer experiment. In this
forest, most tree species? distributions are tightly
correlated with soil resources, causing forest compo-
sition to vary dramatically between soil types along an
edaphic gradient, resulting in high b diversity (Davies
et al. 2005) that contributes to the exceptionally high
1406 Plant Ecol (2013) 214:1405?1416
123
species richness of this region (Ashton and Hall 1992).
We focused on the two soil types at the extremes of the
edaphic gradient, clay and sandy loam (Baillie et al.
2006). These soils share the same climate, due to their
close proximity, but differ in supply rates of N-forms,
with greater supplies of NO3 than NH
?
4 in clay and
greater supplies of NH?4 than NO

3 in sandy loam
(Kochsiek et al. 2013).
twWe hypothesized that edaphic specialization in
this Bornean forest may arise due to variation among
tree species? in the capacity to take up different
chemical forms of N that are differentially available
along the soil gradient. To the extent that differential
uptake of N forms is a proxy for variation between
species in resource use ratios (i.e., resource consump-
tion vectors sensu Tilman (1982)), then differences
between species in N-form uptake may be a mechanism
promoting high b diversity. To test this hypothesis, we
used foliar d15N as a first step towards identifying
whether trees on sandy loam and clay access different
N-forms. We also related foliar d15N to C, N, and P
concentrations to help evaluate the growth demand for
N of trees on the two soil types, which affects foliar
d15N. Second, we conducted a stable isotope tracer
experiment with 15N-labelled ammonium and nitrate
using seedlings of nine species with contrasting soil
associations in the Dipterocarpaceae, the dominant
angiosperm family in this forest. We expected sandy
loam specialists to exhibit a greater capacity to absorb
NH?4 , relative to clay specialists, and clay specialists
to exhibit greater capacity to absorb NO3 , relative to
sandy loam specialists, reflecting the availability of
these N forms in each soil type. Generalist tree species
were expected to exhibit no difference in their
capacity to take up either NO3 or NH
?
4 .
Methods
Study site and supply rates of N-forms
Lambir Hills National Park (4110N, 114010E) in
Sarawak, Malaysian Borneo, consists of 6,952 ha of
lowland mixed dipterocarp rainforest, has the highest
tree species richness recorded in the Paleotropics
(Ashton and Hall 1992), and is dominated by trees in
the Dipterocarpaceae (Lee et al. 2002b). Lambir receives
3,000 mm of rainfall per year, with [100 mm in all
months (Watson 1985), and is the site of a 52-ha long-
term research plot (Lee et al. 2002a). All trees C1 cm
in diameter at breast height (DBH) have been identified
to species and are censused ca. every 5 year for
survival and DBH.
Soil types within the 52-ha plot experience the
same rainfall regime and are sandstone or shale-
derived. Sandstone-derived soils are humult utisols or
sandy haplic acrisols with substantial surficial raw
humus and root mat and relatively low nutrient and
water retention. Shale-derived soils are clay-rich
ultisols generally lacking a humus layer and root mat
and have greater nutrient and moisture retention
(Baillie et al. 2006). Four soil types have been
described based on differences in soil chemistry (C,
N and P and exchangeable K, Ca and Mg) and
elevation (Davies et al. 2005). Davies et al. (2005)
found that of the abundant species at Lambir, 73 %
had distributions significantly aggregated on at least
one of the four soil types. Here we focus on two soil
types, clay and sandy loam, at the extremes of this
gradient that differ most in soil properties (Baillie et al.
2006). Supply rates of NH?4 and NO

3 in surface soil
(top 10 cm) of clay and sandy loam were quantified in
the 52-ha plot over a 5-week period using anion and
cation exchange resins as part of a separate study
(Kochsiek et al. 2013). Supply rates were expressed as
Fig. 1 Differences in ion-exchangeable ammonium (NH?4 ) and
nitrate (NO3 ) supply rates (mg/L extractant/g resin/mo)
between clay and sandy loam surface soils underlying Bornean
rainforest. Error bars are one standard error; letters indicate
significant differences between soil types in the supply rate of
each N-form, and numbers indicate significant differences
between N-forms in their supply on each soil type (P \ 0.05).
Data are from Kochsiek et al. (2013)
Plant Ecol (2013) 214:1405?1416 1407
123
nutrient concentration in the solution per dry mass of
resin per month burial time. Differences between soil
types in supply rates were tested using a linear mixed-
effects model with a random effect for location. Clay
soil provided significantly greater supply rates of NO3
and total inorganic N than sandy loam, but the supply
rate of NH?4 in sandy loam was not significantly
greater than that in clay (Fig. 1). Within soils, the
supply rate of NO3 was significantly greater than NH
?
4
in clay, whereas the supply rate of NH?4 was signif-
icantly greater than NO3 in sandy loam.
Foliar 15N natural abundance
Foliar d15N is viewed as an integrator of terrestrial
N-cycling and is known to vary systematically with
N-availability to plants, differential N-form use, and
relative limitation by N versus other nutrients
(Robinson 2001; Craine et al. 2009; Evans 2001).
As part of a survey data collection effort to quantify
soil-related variation in leaf functional traits, foliar
15N natural abundance (d15N) was measured for 212
tree species (n = 1?7 trees per species, n = 1?6
canopy leaves per tree, DBH range 1?126 cm)
growing on sandy loam (n = 129 species) or clay
(n = 83 species). Species were non-N2-fixing Angio-
sperms (91 genera, 43 families) that are canopy or
subcanopy trees. As part of another study examining
leaf functional trait variation of soil specialists and
generalists (Russo et al. 2010), d15N was measured
for 31 non-N2-fixing tree species at Lambir in 13
genera (11 Angiosperm families; Table 1): 26 spe-
cies were congeners specializing on either sandy
loam or clay soil, and five species (one for each of
five of the 13 genera) were generalists that were
sampled on both sandy loam and clay. For each
species (specialists) or population (generalists), 1?3
recent, fully expanded leaves were collected from 9
to 11 saplings (1?3 cm DBH) growing in either clay
or sandy loam soils in the 52-ha forest plot. Leaves
were dried for [72 h at 60 C, ground to a uniform,
fine powder using a ball mill, and packed into tin
capsules. Nitrogen isotope ratio (15N/14N) and total N
and C were determined at the University of Arkansas
Stable Isotope Laboratory using a NC2500 Finnegan
elemental analyzer coupled with a DeltaPlus Ther-
moquest/Finnegan isotope ratio mass spectrom-
eter. Values are expressed as d15N = [(Rsample/
Rstandard) - 1] 9 1,000 where R is
15N/14N. Foliar
P concentrations were determined with a nitric acid
digest followed by analysis with inductively coupled
plasma emission spectroscopy (ARCOS, SpectroAn-
alytical) at the University of Arkansas Agricultural
Diagnostics Laboratory.
15N Isotope tracer experiment
Uptake rates of ammonium and nitrate were quantified
for seedlings of nine species (Table 1) using a 15N
tracer experiment. The experimental species were
confined to Dipterocarpaceae due to the availability of
seed near Lambir during a masting event in 2009.
Species comprised four congeneric pairs specializing
on either clay or sandy loam soil, two additional sandy
loam specialists, and two generalist species. Seeds
were planted in polyethylene bags (5 9 7-in size,
except S. macrophylla, 6 9 9-in size) filled with a 2:1
clay:sand potting mixture created by blending native
clay soil collected from the forest at Lambir with
washed river sand as 2 parts clay:1 part sand by
volume. Thus, seedlings of all species experienced the
same soil medium as in a common-garden. Because all
polybags of each size were filled with approximately
equal volumes of the potting mixture, all seedlings
planted in the same sized polybags were exposed to the
same ambient nitrogen levels. Seedlings were grown
in a shade house, and all received ambient rainfall that
was supplemented during dry periods. At the time of
the tracer addition, when all seedlings had been
established for a least 6 mos, a total of 376 seedlings
were randomly treated with 10 mL of one of three
solutions: K15NO3 (0.509 mM
15N; 98 at.% 15N),
15NH?4 Cl (2.865 mM
15N; 98 at.% 15N), or distilled,
deionized water (control). For each species, 7?10
individuals received one of the two 15N treatments,
and five seedlings were controls. A syringe with a 10-
cm needle was used to inject 2 mL of solution
uniformly through a depth range of 0?7 cm at each
of five injection points per polybag (a total of 10 mL
per polybag). At the time of injection, seedlings? root
systems occupied most of the volume of the polybag,
so we consider the injections to have supplied the
isotope solutions uniformly within the rooting zone.
The solutions applied 15N at rates that were approx-
imately 2 % (15NO3 ) and 11 % (
15NH?4 ) of the total
available inorganic N pool in 5 9 7-in polybags and
1408 Plant Ecol (2013) 214:1405?1416
123
1 % (15NO3 ) and 7 % (
15NH?4 ) in 6 9 9-in polybags,
as our goal was to produce a 15N-tracer signal without
inducing a fertilization effect. Our calculations are
based on NH?4 and NO

3 concentrations from 1 M KCl
extracts of the clay soil (S.E. Russo, unpub. data),
adjusted for volume in the potting mixture, and a bulk
density of 1.23 g/cm3 for the mixture. We calculated
dilution of the 15N tracer in each N pool (NH?4 ; NO

3 )
using the same set of soil values (see ??Calculations
and statistical analysis?? section).
One leaf per plant was harvested at 24 h as a check
on 15N recovery. Seedlings were harvested in their
Table 1 Taxonomy, growth form, and soil specialization pattern of study tree species in Bornean rain forest measured for foliar
natural abundance d15N (31 species) and used in the 15N tracer experiment (9 species)
Species Family Growth form Soil specialization Study
Anisoptera grossivenia Sloot. Dipterocarpaceae Canopy Generalist Tracer
Aporusa hosei Merr. Phyllanthaceae Subcanopy Sandy loam d15N
Aporusa sarawakensis A. Schott Phyllanthaceae Subcanopy Clay d15N
Calophyllum ferrugineum Merr. Clusiaceae Canopy/subcanopy Sandy loam d15N
Calophyllum gracilipes Merr. Clusiaceae Canopy/subcanopy Clay d15N
Dacryodes rostrata (Bl.)Lam. forma cuspidata (Bl.) Lam. Burseraceae Canopy/subcanopy Clay d15N
Dacryodes expansa (Ridl.) H.J. Lam Burseraceae Canopy/subcanopy Sandy loam d15N
Diospyros decipiens C.B. Clarke Ebenaceae Canopy/subcanopy Clay d15N
Diospyros ferruginescens Bakh. Ebenaceae Canopy/subcanopy Sandy loam d15N
Diospyros pendula Hasselt ex Hassk. Ebenaceae Canopy/subcanopy Generalist d15N
Dipterocarpus confertus Sloot. Dipterocarpaceae Canopy Generalist d15N
Dipterocarpus globosus Vesque Dipterocarpaceae Canopy Sandy loam d15N, tracer
Dipterocarpus kunstleri King Dipterocarpaceae Canopy/subcanopy Clay d15N
Dryobalanops aromatica C.F. Gaertn. Dipterocarpaceae Canopy Sandy loam d15N, tracer
Dryobalanops lanceolata Burck Dipterocarpaceae Canopy Clay d15N, tracer
Knema latericia Elm. Myristicaceae Subcanopy Generalist d15N
Knema elmeri Merrill Myristicaceae Subcanopy Clay d15N
Knema galeata J. Sinclair Myristicaceae Subcanopy Sandy loam d15N
Macaranga lamellata Whitmore Euphorbiaceae Subcanopy Sandy loam d15N
Macaranga umbrosa S.J.Davies Euphorbiaceae Subcanopy Clay d15N
Palaquium cryptocariifolium P.Royen Sapotaceae Canopy/subcanopy Sandy loam D15N
Palaquium dasyphyllum Pierre ex Dubard Sapotaceae Canopy/subcanopy Clay d15N
Polyalthia clavigera King Annonaceae Canopy/subcanopy Sandy loam d15N
Polyalthia sarawakensis Diels Annonaceae Subcanopy Clay d15N
Polyalthia rumphii (Bl.) Merrill Annonaceae Subcanopy Generalist d15N
Rinorea bengalensis (Wall.) Kuntze Violaceae Subcanopy Clay d15N
Rinorea lanceolata Kuntze Violaceae Subcanopy Sandy loam d15N
Shorea beccariana Burck Dipterocarpaceae Canopy Sandy loam Tracer
Shorea inappendiculata Burck Dipterocarpaceae Canopy Clay d15N
Shorea laxa Slooten Dipterocarpaceae Canopy Sandy loam d15N, tracer
Shorea patoiensis Ashton Dipterocarpaceae Canopy Generalist d15N
Shorea macrophylla de Vries (Ashton) Dipterocarpaceae Canopy Clay Tracer
Shorea xanthophylla Sym. Dipterocarpaceae Canopy Clay Tracer
Syzygium cf. grande (Wight) Walp. Myrtaceae Canopy/subcanopy Sandy loam d15N
Syzygium kingii (Merr.) Merr. and L.M.Perry Myrtaceae Canopy/subcanopy Clay d15N
Vatica nitens King Dipterocarpaceae Canopy/subcanopy Sandy loam Tracer
None of the study species fixes N2
Plant Ecol (2013) 214:1405?1416 1409
123
entirety 48 h following 15N tracer addition and
separated into below- and aboveground tissue and
dried at 60 C for 2 weeks. Dried leaf samples were
weighed and ground to a uniform, fine powder using a
ball mill. A mass of 4?5 mg of each ground sample
was packed in tin capsules for 15N and total N analysis
at the University of California-Davis, with a PDZ
Europa ANCA-GSL elemental analyzer coupled with
a PDZ Europa 20?20 isotope ratio mass spectrometer
(Sercon Ltd., Cheshire, UK).
Species growth rates
Growth rates were estimated for the nine study species
included in the 15N tracer experiment using census
data from the 52-ha plot at Lambir. Mean stem
diameter growth rate (cm/year) for each species was
estimated based on the change in DBH between 1992
and 2003 for trees 1?3 cm in diameter, divided by the
time period in fractional years between censuses.
Calculations and statistical analysis
We used 15N recovery in shoots to examine species?
capacities for NH?4 and NO

3 uptake, as in previous
studies (e.g., McKane et al. 2002; Miller and Bowman
2002). Only leaves harvested at 48 h (e.g., Andersen
and Turner 2013) were used in our analysis due to the
low 15N recovery in leaves harvested at 24 h.
Although microbial transformation of the added N
forms could have occurred within the 48 h incubation
period, we interpret our 15N uptake results as an
estimate of the capacity of plants to take up N from
NH?4 to NO

3 sources, and not as an indication of
preference for those forms, per se. Uptake of the 15N
labeled solutions was estimated from the following
formula, which calculates F, the mass (lg) of 15N that
was derived from the tracer for each analyzed sample
(i.e., used in the isotopic analysis): F = (N 9 (A -
C))/98, where N is the total N in the analyzed sample,
A = 15N at.% in the sample minus the natural
abundance of 15N (0.3663 %), C is the average 15N
at.% in the control samples minus 0.3663, and 98
represents the at.% of the added isotope (Hauck and
Bremner 1976). Uptake rate of 15N, UL (lg
15N/g dry
leaf tissue/h), was calculated as (F/(M 9 T)), where
F is as above, M is the dry mass (g) of the analyzed
sample, and T is number of hours of incubation before
harvesting the leaves (48 h). Uptake rates were also
calculated per unit tissue N, to account for interspe-
cific differences in foliar N, in which case M would be
mass of N (mg) in the analyzed sample.
We accounted for dilution of the 15N tracer using a
mixing model in which the uptake of the unlabeled N-
form corresponding to the treatment 15N label (UU)
was estimated as UL 9 (mU/mL), where mL is the mass
of 15N-labelled nitrogen injected per treatment, and
mU is the mass of the available N-form corresponding
to the treatment estimated to be within the rooting
zone, and UL is the uptake rate from the labeled N-
form (mL), and UU is uptake from the source mU
(McKane et al. 2002). Based on these calculations, we
estimate that approximately 7 % of the ambient NO3
pool and 15 % of the NH?4 pool were labeled in the
5 9 7-in polybags, and 5 % (NO3 ) and 9 % (NH
?
4 ) of
the target N pools were labeled in the 6 9 9-in bags.
Uptake of total inorganic N was estimated as the sum
of the uptake rates for NH?4 and NO

3 .
Statistical analyses were done in R statistical
software (R Core Development Team 2011). Differ-
ences in foliar d15N signatures between trees growing
on sandy loam versus clay (survey data) were tested
based on species? mean values using a Student?s t test.
Differences in foliar d15N signatures between soil
specialists in each genus and between populations of
generalists growing on each soil type were analyzed
using separate linear models for specialists and
generalists in R. For specialists, soil specialization
(clay or sandy loam) was nested within genus, as
specialists were only sampled on their home soil type,
with genus as a fixed effect. For generalists, the model
structure was similar, except that the population (clay
or sandy loam) was nested within species, with species
as a fixed effect. For the survey data, species? mean
foliar d15N values were correlated with foliar N, P,
C:N, and N:P using Spearman rank correlation tests.
Differences in uptake rates for each N- form (NH?4 vs.
NO3 ) were analyzed using separate generalized least
squares linear models for each species. Treatment
group was a fixed factor, total seedling dry mass was a
covariate (to account for any influence of seedling size
on N-uptake), and the variance of the error distribution
(Gaussian) was fit for each group due to heterosced-
asticity (gls function in R; Pinheiro and Bates 2000).
Resource use ratios (sensu Tilman 1982) of specialists
were estimated as ratio of species? mean uptake rates
1410 Plant Ecol (2013) 214:1405?1416
123
of NH?4 and NO

3 . The difference between clay and
sandy loam specialists in resource use ratio was tested
using a Student?s t test. Species? mean uptake rates
were correlated with mean foliar N concentrations and
mean diameter growth rates from the 52-ha plot using
Spearman rank correlation tests.
Results
Foliar d15N signatures were significantly more nega-
tive (depleted) in trees growing on sandy loam
compared to clay (t = 5.812, df = 196, P \ 0.001;
Fig. 2). Foliar d15N signatures also varied signifi-
cantly between specialists of sandy loam and clay and
between populations of generalists on each soil type.
In 12 of 13 congeneric comparisons, saplings of sandy
loam specialists had significantly more depleted foliar
d15N, compared to clay specialists in the same genus
(Fig. 3). A similar pattern was seen in four out of five
comparisons of generalist species? populations on
sandy loam and clay (Fig. 3). Across species, foliar
d15N correlated negatively with foliar C:N (r =
-0.25, S = 1,198,289, P \ 0.001, n = 179) and N:P
(r = -0.20, S = 1,167,715, P = 0.007, n = 180)
and positively with foliar N (r = 0.30, S = 684,314,
P \ 0.001, n = 180) and P (r = 0.35, S = 634,990,
P \ 0.001, n = 180) concentrations.
All species used both inorganic forms of N, but
contrary to expectations, sandy loam and clay spe-
cialists did not show differential uptake of either
chemical form of N (Table 2; Fig. 4). Sandy loam
specialists did not show significantly greater uptake of
NH?4 over NO

3 , nor did clay specialists exhibit greater
uptake of NO3 over NH
?
4 (Fig. 4). As with the
specialists, the one generalist that we tested did not
exhibit a significant difference in its capacity to take
up NH?4 or NO

3 (Fig. 4). Our estimates of uptake rate
calculated per unit mass of N in leaf tissue showed the
same patterns as those calculated per unit leaf dry mass
(Table 2). Sandy loam and clay specialists did not
differ significantly in their mean resource use ratios
(t = -0.827, df = 5.9, P = 0.441). Across species
stem diameter growth rates were not correlated with
the uptake rate of either N form across species (NH?4 :
r = -0.48, S = 178, P = 0. 194; NO3 : r = -0.55,
S = 186, P = 0.133; n = 9), nor with total inorganic
N-uptake (r = -0.43, S = 172, P = 0.250, n = 9).
However, foliar N concentration was positively cor-
related with total inorganic N-uptake rate across
species (r = 0.68, S = 38, P = 0.050, n = 9). The
greatest differences among species were in total
inorganic N-uptake rate, with Vatica micrantha (sandy
loam specialist) and Anisoptera grossivenia (general-
ist) showing the fastest rates.
Discussion
Despite variation in the supply rates of ammonium and
nitrate in the clay and sandy loam soils underlying this
Bornean rain forest and the nearly 4 % difference in
foliar d15N between most soil specialists and popula-
tions of generalists, the results of our 15N tracer
experiment showed little support for the hypothesis
that tree species associated with these soils vary
consistently in their use of different inorganic N forms
or in the ratio in which these forms are used. Instead of
distinct strategies of N-form use, our results support
the idea that these tree species have evolved similar,
flexible capacities to take up different forms of
inorganic N. Few studies have experimentally tested
Fig. 2 Variation in community-level foliar d15N (%) of
Bornean tree species growing on sandy loam (129 species;
white) or clay (83 species; gray). Error bars are ? 1 SE. The
difference in d15N between soil types was significant
(P \ 0.001)
Plant Ecol (2013) 214:1405?1416 1411
123
for differential N-form use among tropical plants. Our
findings are consistent with a small but growing body
evidence demonstrating flexible N-use among tropical
plants, including a 15N tracer experiment in
Panamanian forest that also found limited evidence
for N-form preferences of understory palm species
distributed on different soil types (Andersen and
Turner 2013) and studies suggesting flexibility in
Fig. 3 Variation in foliar
d15N (%) of 31 Bornean tree
species in 13 genera:
pairwise comparisons of
congeneric soil specialist
species and soil generalist
populations on sandy loam
(white) or clay (gray) soil.
Error bars are ? 1 SE;
asterisks indicate genera (or
species) with significant
differences (P \ 0.05)
between soils based on post-
hoc comparisons following
a signficant effect of genus
(specialists) or species
(generalists) in linear
models. Study species are
listed in Table 1
Table 2 Analysis of variance tables for each Bornean dip-
terocarp species showing the effect of N-form treatment on
rates of nitrogen uptake, calculated per unit leaf dry mass (dry
mass basis; lg 15N/g dry leaf tissue/h) and per unit total N in
leaf tissue (total N basis; lg 15N/mgN in leaf tissue/h)
Ndf,
Ddf
Dry mass
basis
Leaf N basis
F P F P
Sandy loam specialists
Dipterocarpus
globosus
1, 14 0.663 0.429 0.769 0.395
Dryobalanops
aromatica
1, 17 0.565 0.463 0.555 0.467
Shorea beccariana 1, 16 0.001 0.981 0.011 0.919
Shorea laxa 1, 10 0.138 0.718 0.031 0.865
Vatica nitens 1, 13 1.551 0.235 1.857 0.196
Clay specialists
Dryobalanops
lanceolata
1, 17 0.634 0.437 0.252 0.622
Shorea macrophylla 1, 15 0.685 0.421 0.803 0.384
Shorea xanthophylla 1, 13 0.014 0.908 0.053 0.822
Generalist
Anisoptera
grossivenia
1, 17 0.901 0.356 0.746 0.400
The numerator and denominator degrees of freedom (Ndf, Ddf),
F-statistic (F), and probability (P) of each test are listed
Fig. 4 Differences in relative uptake rates of ammonium
(NH?4 ) and nitrate (NO

3 ) for nine Bornean tree species that
specialize on sandy loam or clay soil types (specialists) or show
no soil association (generalist). Error bars are ? 1 SE; there
were no statistically significant differences in uptake rates of the
two N forms for any species (Table 2)
1412 Plant Ecol (2013) 214:1405?1416
123
N-form use by Hawaiian plant species (Houlton et al.
2007) and Jamaican tree species (Brearley 2013).
Plasticity in the use of different N forms may be
adaptive if it allows for more effective competition for
N resources at the root-level, where availability of
different forms can fluctuate on small spatial and
temporal scales due to variation in, e.g., mineralization
rates, soil moisture, and differential diffusion (Nye
1977; Owen and Jones 2001; Miller and Cramer
2004), as well as competition with neighboring plants
and microorganisms (Schimel and Bennett 2004;
Harrison et al. 2007; Miller et al. 2007). Variation
among tree species in the capacity to take up
differentially available inorganic N forms is thus
unlikely to be a dominant mechanism influencing their
distributions across soil types in this Bornean rain
forest. However, our foliar d15N results nevertheless
showed significant soil-related variation, suggesting
that trees on the two soil types have access to N with
different d15N.
Nitrogen use strategies inferred from 15N natural
abundance
Uptake of N by plants is not considered to cause
appreciable isotopic fractionation (Hogberg 1997;
Dawson et al. 2002), and fractionation associated
with translocation within the plant is considered
minimal (Dawson et al. 2002), so foliar d15N is often
assumed to be similar to the d15N of the N source used
by plants (Houlton et al. 2007). The depleted foliar
d15N values among Bornean trees growing on sandy
loam and their negative relationships with foliar C:N
suggest decreased N-availability to plants on sandy
loam compared to clay (Craine et al. 2009). In all but
one congeneric comparison (Rinorea), foliar d15N
values were also significantly depleted in sandy loam,
compared to clay, specialists, as well as in populations
of generalists growing on sandy loam compared to
clay. There is no obvious explanation as to why
Rinorea differed from the other genera. However,
there are at least three plausible explanations for the
otherwise dominant patterns: (1) these tree species are
not using a common source of N across soil types; (2)
they are using a common source of N, but the d15N of
that source varies between soil types; or (3) both
factors may be contributing to the observed differ-
ences in foliar d15N. Although we cannot definitively
distinguish between these alternatives with our data,
the tracer experiment revealed little evidence of
differential uptake of inorganic N for any species.
Our findings are thus consistent with the hypothesis
that these species may be able to use whichever
inorganic N-form is in greatest supply and that the
d15N of the N form(s) accessed by trees on sandy loam
and clay likely differs.
Differences in d15N in bulk soils along gradients are
influenced by N-isotope fractionation associated with
microbial processes, including nitrification and deni-
trification, and with gaseous losses (Hogberg 1997;
Robinson 2001; Houlton et al. 2006). These pathways
tend to cause enrichment of the remaining soil 15N
pool, leading to enriched foliar d15N. One explanation
of our results is that differences between soil types in
these fractionating processes could produce variation
in the bulk soil d15N, which is then reflected in foliar
d15N signatures of trees on the two soil types. In N-
limited systems with tighter N-cycling, pathways for
N loss are reduced, resulting in depleted foliar d15N
(Hogberg 1997). Although total soil N does not differ
between soil types (Baillie et al. 2006), and N may not
be a primary limiting nutrient in this forest (Kochsiek
et al. 2013), the dominance of NH?4 , the well-
developed, recalcitrant organic layer, and slower litter
decomposition rates in sandy loam (Baillie et al. 2006)
suggest tighter nutrient cycling, and lower N avail-
ability to plants than in clay, consistent with the
depleted foliar d15N signatures seen in trees growing
on this soil type. A survey of foliar d15N among
tropical forests also found more depleted values in
forests with low N-availability, such as those on
sandier soils (Martinelli et al. 1999). Indeed, our foliar
d15N values from sandy loam are similar to those from
an N-limited Brazilian savanna (Bustamante et al.
2004), and three sandy loam specialists had foliar d15N
values as low as those observed in strongly N-limited
Hawaiian forests (Vitousek et al. 1989). The soil-
related differences in foliar d15N we found also
paralleled variation between mor and mull soils in
Jamaican montane forest. The mor soil, with a thick,
acidic humus layer, resembling that on the sandy loam
in our site, exhibited relatively depleted foliar and soil
d15N, interpreted as evidence of a tighter N-cycle
(Brearley 2013). Along a gradient of N-availability in
forests on Mount Kinabalu, Borneo, foliar d15N
correlated positively with soil NO3 availability, and
Plant Ecol (2013) 214:1405?1416 1413
123
negatively with NH?4 availability, in parallel to our
findings, a result the authors attribute to leaching
losses of NO3 (Kitayama and Iwamoto 2001).
The dominant family of trees in this forest, Diptero-
carpaceae, form ectomycorrhizal associations,
although trees forming arbuscular mycorrhizal associ-
ations are also present and were represented in our
survey data. Mycorrhizal associations are often more
common in N- and P-poor soils and can result in
depleted foliar d15N values relative to bulk soil d15N,
with more negative values for ectomycorrhizal than
arbuscular mycorrhizal associations (Hogberg 1997;
Michelsen et al. 1998; Hobbie and Colpaert 2003;
Craine et al. 2009). Hence, another explanation for the
soil-related differences in foliar d15N in this forest is
that trees on sandy loam may rely more heavily on
mycorrhizal sources of N, relative to trees on clay, a
mechanism that can operate independently of soil-type-
related differences in the bulk soil d15N. Furthermore,
the magnitude of the soil-related difference in foliar
d15N varied among generalist species, suggesting that
foliar d15N of these species is not a simple function of
bulk soil d15N. Instead, differences in competitive
interactions among trees and with microorganisms for
N or differences in mycorrhizal associations between
soil types may also operate to produce variability in
foliar d15N. More detailed comparative data on d15N of
N forms in soil, microbial N mineralization rates, N loss
rates, and mycorrhizal infection in sandy loam and clay
soil would help to further elucidate the underlying
causes of these soil-related differences in foliar d15N.
Lack of nitrogen-form preference: Possible
ecological interpretations
We cannot rule out the possibility that plants receiving
the 15N-NH?4 tracer took up both forms of N (NH
?
4 and
NO3 ), since NH
?
4 could have been retained in the clay
fraction and subsequently nitrified to NO3 . However,
in this study and a similar one by Andersen and Turner
(2013), one or more species showed a trend of greater
mean uptake of 15N-NO3 , suggesting that even if N
was better retained in the NH?4 treatment, our exper-
iment had the capacity to detect differential use of
N-forms.
Many, but not all, studies testing for variation in N
uptake among plant species find evidence of species?
preference for different forms of N (see Introduction).
Those that find evidence of preference are often from
markedly N-limited systems, such as arctic, alpine, and
N-poor grasslands. One possible explanation for our
finding of lack of differential uptake of N-forms is that
tree growth in this Bornean forest may not be primarily
limited by inorganic N. If so, then selection for
adaptations to partition inorganic N resources between
species may be weak. Some evidence points towards this
hypothesis. First, a study of in situ standing biomass and
growth rates of fine roots at Lambir demonstrated that
PO34 and K
? are likely to limit tree growth (Kochsiek
et al. 2013). Nitrate and ammonium supply rates in soil
did not correlate strongly with either standing biomass
or growth rates of fine roots, signifying that inorganic
N may only be secondarily limiting or that acquisition
of N via mycorrhizal associations may be more
important. Second, foliar d15N was negatively related
to N:P ratio, consistent with other studies of P-limited
systems (McKee et al. 2002; Clarkson et al. 2005;
Wanek and Zotz 2011). Although trees may store
excess P in leaves, foliar N:P ratios are considered an
indicator of the relative limitation of plant growth by
N versus P (Gu?sewell 2004). To the extent that this is
true, greater N:P ratios should be associated with more
depleted foliar d15N, since due to limitation by P, not
all bulk soil N that is available in the system is
assimilated, resulting in greater opportunity for dis-
crimination (Evans 2001). Third, studies in N-limited
systems often find a significant relationship between
plant growth and N-use strategy, with the fastest
growing, dominant species often exhibiting preference
for the most abundant N form (McKane et al. 2002;
Ashton et al. 2010; Scott and Rothstein 2011).
Although foliar N concentration correlated with
N-uptake rates of seedlings across species, we found
no correlation between uptake and diameter growth
rates of saplings, which would be expected if N
resource partitioning between species was a strong
determinant of carbon acquisition and growth.
Conclusions
Differential use of inorganic N forms does not appear
to be an overriding mechanism producing the
observed soil-specific distributions of tree species
and high b diversity across the edaphic gradient in this
rainforest. Instead, our results imply that these
1414 Plant Ecol (2013) 214:1405?1416
123
Bornean tree species display considerable flexibility
both in the uptake of different inorganic N forms and,
potentially, in reliance on ectomycorrhizal associa-
tions for N-supply. That flexibility would facilitate N
acquisition when the availability of N forms in the
rhizosphere varies in space and time and could
potentially result in functional redundancy among
tree species in their responses to nitrogen gradients
and their influence on ecosystem N-cycles.
Acknowledgments The authors thank the Sarawak Forest
Department, National Parks, and Forest Research Corporation
for their kind permission to conduct research in Lambir Hills
National Park. This research was made possible by funds from
the US National Science Foundation (NSF) award DEB-
0919136 to SER, including an NSF-Research Experiences for
Undergraduates supplementary award, the Center for Tropical
Forest Science, and from the University of Nebraska?Lincoln
Undergraduate Creative Activities and Research Experiences
Program. The 52-ha plot is a collaborative project of the Center
for Tropical Forest Science, Forest Department of Sarawak,
Malaysia, Harvard University, USA (NSF awards DEB-
9107247 and DEB-9629601 to P. S. Ashton), and Osaka City
University, Japan (Monbusho grant 06041094 to T. Yamakura,
08NP0901 to S. Tamura and 09NP0901 to S. Sasaki). The
authors thank Lela Ali and Aimee Koenig for field assistance,
Ramesh Laungani for helpful discussions about stable isotope
tracer experiments, and David Wedin for comments on an
earlier version of this manuscript.
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