Ecology, 91(11), 2010, pp.

32523260
2010 by the Ecological Society of America

Niche complementarity due to plasticity in resource use:

plant partitioning of chemical N forms
ISABEL W. ASHTON,1,6 AMY E. MILLER,2,3 WILLIAM D. BOWMAN,3,4 AND KATHARINE N. SUDING5
1
Inventory and Monitoring Program, Rocky Mountain Network, National Park Service, Fort Collins, Colorado 80525 USA
2
Inventory and Monitoring Program, Southwest Alaska Network, National Park Service, Anchorage, Alaska 99501 USA
3
Institute of Arctic and Alpine Research, University of Colorado, Boulder, Colorado 80309-0450 USA
4
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado 80309-0334 USA
5
Department of Environmental Science Policy and Management, University of California, Berkeley, California 94720-3114 USA

Abstract. Niche complementarity, in which coexisting species use different forms of a

resource, has been widely invoked to explain some of the most debated patterns in ecology,
including maintenance of diversity and relationships between diversity and ecosystem
function. However, classical models assume resource specialization in the form of distinct
niches, which does not obviously apply to the broadly overlapping resource use in plant
communities. Here we utilize an experimental framework based on competition theory to test
whether plants partition resources via classical niche differentiation or via plasticity in
resource use. We explore two alternatives: niche preemption, in which individuals respond to a
superior competitor by switching to an alternative, less-used resource, and dominant
plasticity, in which superior competitors exhibit high resource use plasticity and shift resource
use depending on the competitive environment. We determined competitive ability by
measuring growth responses with and without neighbors over a growing season and then used
15
N tracer techniques to measure uptake of different nitrogen (N) forms in a eld setting. We
show that four alpine plant species of differing competitive abilities have statistically
indistinguishable uptake patterns (nitrate . ammonium . glycine) in their fundamental niche
(without competitors) but differ in whether they shift these uptake patterns in their realized
niche (with competitors). Competitively superior species increased their uptake of the most
available N form, ammonium, when in competition with the rarer, competitively inferior
species. In contrast, the competitively inferior species did not alter its N uptake pattern in
competition. The existence of plasticity in resource use among the dominant species provides a
mechanism that helps to explain the manner by which plant species with broadly overlapping
resource use might coexist.
Key words: alpine dry meadow; biodiversity; chemical nitrogen forms; competition; Niwot Ridge,
Colorado, USA; phenotypic plasticity; resource partitioning.

INTRODUCTION tions, and an increased chance of species invasion

Niche complementarity has been invoked to explain
some of the most actively debated questions in ecology,
including species coexistence (Chase and Leibold 2003,
Silvertown 2004), the positive effect of species diversity
on ecosystem function (Petchey 2003), and invasion
resistance (Kennedy et al. 2002, Tilman 2004), despite
alternative explanations (e.g., Hubbell 2001). Niche
complementarity predicts that species that differ in their
resource use are more likely to coexist, even in highly
variable environments (Pacala and Tilman 1994, Holt
2008), due to less intense competitive interactions
(Schoener 1974, Chesson 2000, Silvertown 2004). The
theory also predicts that when specialists are lost from a
system, their niches remain unoccupied, leading to
reduced resource utilization, declining ecosystem func-
Manuscript received 12 October 2009; revised 3 March 2010;
accepted 9 March 2010. Corresponding Editor: J. M. Levine.
6 E-mail: isabel_ashton@nps.gov
3252
(Loreau 2000, Chase and Leibold 2003).
Niche complementarity among plants has received
strong indirect support. For example, statistical analyses
reveal overyielding in diverse communities, in which the
aggregate primary productivity exceeds productivity
expected from the weighted averages of the component
plant species grown in monocultures (Hector et al. 1999,
Hooper et al. 2005). Mixtures of different functional
groups, assumed to represent different resource use
patterns, often show the greatest overyielding (Hooper
and Dukes 2004, Petchey 2004) and are able to resist
invasion of additional species (Dukes 2001). Although
these patterns can often be attributed to complementar-
ity in resource use (Loreau and Hector 2001, Petchey
2003), they are based on statistical inference. Thus,
despite the large body of work suggesting niche
complementarity, we have virtually no empirical evi-
dence of it as a mechanism of resource use differenti-
ation in plants (Petchey 2003, Silvertown 2004).
November 2010 NICHE COMPLEMENTARITY IN ALPINE PLANTS
Most expectations of niche complementarity, partic-
ularly due to resource use partitioning mechanisms, stem
from traditional models of coexistence explained by
specialization in the form of distinct niches (Futuyma
and Moreno 1988, Dayan and Simberloff 2005, Abrams
2006). While resource use specialization is quite
common, particularly among vertebrates and insects,
the framework does not obviously apply to species that
use essentially the same resources, such as generalist
herbivores (Behmer and Joern 2008) or most plant
species (Silvertown 2004). In the case of plants, several
modes of differentiation have been proposed, including
phenology, rooting depth, nitrogen xation, and chem-
ical form of nitrogen used (Dukes 2001, Jumpponen et
al. 2002, McKane et al. 2002, Spehn et al. 2002,
Fargione and Tilman 2005, Kahmen et al. 2006).
However, these forms of differentiation, with the
exception of N xation, often only represent partial
specialization (genetically constrained character dis-
placement; Futuyma 1998) based on the fundamental
niche. Instead, much of the differentiation is due to
phenotypic plasticity (facultative character displace-
ment; Pfennig and Murphy 2002) based on conditions
of the realized niche (Aerts et al. 1991, Casper and
Jackson 1997, DeWitt et al. 1998).
There are at least two ways in which plasticity in
resource use could lead to niche complementarity in
plant communities. First, resource partitioning may
occur via niche preemption, in which individuals
respond to the presence of a superior competitor by
switching to an alternative, less-used resource (May and
MacArthur 1972, Hector et al. 1999; Fig. 1A). This
mechanism is supported by theory that suggests that
generalists that switch foraging behavior in order to
capitalize on the more rewarding resource can coexist
with competitively superior specialists (Abrams 2006).
Second, plasticity in resource use may enhance compet-
itive ability, as has been shown for plasticity in other
traits (Aerts et al. 1991, Casper and Jackson 1997). In
this case of dominant plasticity, superior competitors
exhibit high resource use plasticity while inferior
competitors are unable to shift resource use (Fig. 1B).
These two scenarios are alternatives to the more
traditional concept of niche complementarity, in which
resource use differentiation occurs in both the funda-
mental and realized niche (Fig. 1C).
We employed an experimental approach grounded in
competition theory to test the importance of these
mechanisms for differential resource use of organic and
inorganic nitrogen (N) forms among alpine dry meadow
plant species in the Rocky Mountains of Colorado. In
this system (Miller and Bowman 2002, 2003, Miller et al.
2007), as in others (McKane et al. 2002, Weigelt et al.
2005, James et al. 2008), species-specic differences in
the usage of chemical forms of N could provide a
mechanism for plants to partition a limited soil N pool,
facilitating species coexistence and maintaining diversi-
ty. Plant growth is limited by N availability (Bowman et
3253
FIG. 1. Mechanisms of resource use differentiation for
niche complementarity. While not typically considered a
mechanism leading to niche complementarity, plasticity in
resource use could be an important mechanism for resource
partitioning, particularly for groups that have broadly over-
lapping resource use patterns such as plants. We show resource
use of two different resources (gray, white) for two species
according to their fundamental niches (no competitive interac-
tions) or realized niches (with competition). Total resource use
is indicated by the size of the circles, with the superior
competitor the leftmost of the pair and overlap in resource
use between the two species indicated by the degree of overlap
of the circles. Three alternative scenarios are depicted: (A) niche
preemption, in which individuals respond to a superior
competitor by switching to an alternative less-used resource;
(B) dominant plasticity, in which superior competitors exhibit
high plasticity in resource use and shift resource use depending
on the competitive environment; and (C) more strictly canalized
niches, in which species resource use differs in both the
fundamental and realized niches and little plasticity in resource
use occurs. This last scenario is most classically assumed in
complementarity theory. In all scenarios, niche complementar-
ity is indicated, as total resource use increases in the realized
niche with both species together.
al. 1993), organic N is an important component of the N
resource for plants (Lipson et al. 2001), and glycine is
the most abundant amino acid in the soil (Raab et al.
1999). We focused on four alpine plant species that
varied in abundance, providing direct experimental
examination of resource use by manipulating competi-
tive interactions. We manipulated the intensity of
competition among three abundant species and one
rarer species by isolating naturally occurring individuals
(each of the four species alone) and species pairs (each of
the three abundant species with the rarer species) in eld
microcosms that served as belowground competition
arenas. We quantied competitive ability as the effect
of neighbors on a target species biomass. A year after
the seven competition treatments were initiated, we
injected one of three chemical forms of 15N-labeled N
(glycine, ammonium, nitrate) to measure plant and
microbial uptake of different N sources and to test for
complementarity in resource use.
3254 ISABEL W. ASHTON ET AL.
MATERIALS AND METHODS
Study system
We conducted this work during the 2005 and 2006
growing seasons in dry meadow alpine tundra at Niwot
Ridge, Colorado, USA (40803 0 N, 105835 0 W; 3500 m
above sea level), a Long-Term Ecological Research
(LTER) site and a United Nations Educational,
Scientic and Cultural Organization (UNESCO) Bio-
sphere Reserve. The alpine dry meadow community is
highly diverse compared to other herbaceous communi-
ties and averages 2025 species/m2 (Gough et al. 2000).
Our study focused on three dominant species and one
rarer species: the sedge Kobresia myosuroides (Vill.)
Fiori.; the rosaceous forb Geum rossii (R. Br.) C.L.
Hitchc. (formerly Acomastylis rossii ); another sedge,
Carex rupestris All; and Mertensia lanceolata (Pursh)
DC, a forb in the Borage family. We hereafter use genus
names to refer to all species. Kobresia is consistently the
most dominant species in the dry meadow of this area,
ranging from 43% 6 4.9% (mean 6 SE; Niwot Ridge
LTER 2010) to 47% 6 0.3% cover (Theodose and
Bowman 1997). Carex is often the second most
dominant species, averaging between 8% 6 1.4% cover
(Theodose and Bowman 1997) and 14% 6 2.1% (Niwot
Ridge LTER 2010). Geum is widespread and abundant
across the alpine; in the dry meadow it can make up
from 3% 6 0.3% (Theodose and Bowman 1997) to 12%
6 2.1% cover (Niwot Ridge LTER 2010). Finally,
Mertensia is consistently ,1% in relative abundance
(Theodose and Bowman 1997, Niwot Ridge LTER
2010).
Field competition experiment
We manipulated plant interactions by creating plant
competition arenas in the eld. In June 2005, 168 of unlabeled forms to detect N uptake, but at a low
Mertensia plants with a nearest neighbor of Geum,
Carex, or Kobresia were identied in the eld. A PVC
tube (7.62 cm diameter 3 7.5 cm deep) with a beveled
edge was sunk into ground to a depth of 7 cm around
each species pair. In the dry meadow, the majority of
plant roots are within the top 5 cm of soil (Webber and
May 1977). The arenas were designed to limit interac-
tions of the focal plants and plants outside the arena and
focus interactions between the plants within the arena.
To allow for surface water drainage, each tube had two
holes drilled within the top 1 cm. The bottoms and tops
of the tubes were open, allowing for drainage and access
into the arena by soil microbes and invertebrates. All
PVC tubes were installed within a 0.5-ha area, separated
into two blocks in which one was slightly upslope of the
other. By selectively harvesting and clipping nontarget
plants within the competition arenas, seven species
competition treatments were created: Mertensia alone,
Kobresia alone, Geum alone, Carex alone, Mertensia
with Kobresia, Mertensia with Geum, and Mertensia
with Carex. Each competition treatment was replicated
12 times in each of two blocks. Within the rst two
Ecology, Vol. 91, No. 11
weeks of placing the PVC tubes in the eld, replicates
that had died from the manipulation were replaced.
Nontarget clipped biomass was collected, dried at 708C,
and weighed. To maintain treatments, nontarget plants
were clipped three additional times within the 2005
growing season. In spring of 2006, 36 of the 148 arenas
to be used for the 15N tracer experiment (24%)
contained a plant that did not survive the winter. We
assume that stress from severed roots was the main
cause of mortality. To replace lost replicates, 36
additional species pairs were found and isolated in early
June 2006. Nontarget plants were clipped from all
replicates again in early June 2006, and clipped biomass
was dried and weighed.
15
N tracer addition
One year after competition treatments were initiated
(approximately at peak biomass, late June 2006), we
added 15N tracers to the plots. The tracer addition
consisted of the three N forms (NH4, NO3, and
glycine) in combination, with one form labeled with 15N
and the remaining two forms unlabeled, as described in
Miller et al. (2007). Glycine was used as the organic
form of N because it is the most abundant amino acid in
these soils (Raab et al. 1996) and because plants appear
to compete well for glycine relative to more complex
forms (Lipson et al. 1999). Soils were injected with 0.6
mmol/L solutions of 15N-NH4 (98% atom enrichment),
15
N-NO3 (98% atom enrichment), or 15N-22[2]-13C
glycine (98% atom enrichment 15N, 99% atom enrich-
ment 13C-2), in combination with equal parts of 0.2
mmol/L unlabeled N, for a total solution concentration
of 1.0 mmol/L N. We used a 15N-labeled N source that
was three times more concentrated than the unlabeled N
because we wanted to deliver enough 15N in the presence
enough overall N concentration to avoid a fertilization
effect. A 3-mL solution of the 15N tracer was injected to
a depth of 7.5 cm at six points within the competition
arena, delivering ;2.4 lg 15N/g dry soil. With each
injection, the needle was slowly withdrawn to uniformly
label the soil depth column. At the time of labeling, this
addition represented ;10% of the extractable inorganic
N pool. Our calculations assumed a bulk density of 0.6
g/cm3, based on previous work at this site.
We added the label in the rst block between 07:00
and 09:00 on 20 June 2006 and the second block was
labeled in a similar manner the morning of 26 June 2006.
For each block, within approximately six hours of the
label addition we harvested the plant and soils within
each arena, separated plants from the soil, and began
soil extractions. The six-hour period was chosen to
minimize the potential for microbial transformation of
the added N forms (NH4, glycine-N).
Plant competition arenas were harvested in the eld
by removing the PVC tube and collecting the soil plug
containing all soil and target plants to 7.5 cm depth.
After removal, the soil plugs were placed on ice and
November 2010 NICHE COMPLEMENTARITY IN ALPINE PLANTS
transported immediately to the laboratory where the
plant material was separated from the soils. The focal
plants were separated into live aboveground (leaves,
stems, inorescences) and belowground (root, rhizome)
tissue. Plants were washed in tap water to remove soil,
immersed in 0.5 mmol/L CaCl2 1.0 mmol/L KCl for 2
3 minutes to remove adsorbed 15N, and rinsed well with
deionized water. We dried plants at 708C and weighed
the root and shoot biomass. Dried and ground plant
tissue was analyzed on a mass spectrometer (SerCon,
Cheshire, UK) for 15N at the Stable Isotope Facility,
University of California, Davis.
In addition to following the tracer in plant tissue, we
also determined the 15N concentration in three soil
pools: exchangeable inorganic N (NH4 and NO3),
exchangeable dissolved organic N (DON), and CHCl3-
labile microbial N. The soil samples were sieved
through a 2-mm mesh screen to remove excess rocks
and large debris. Soils were then extracted in 0.5 mol/L
K2SO4 for inorganic N and total N (TN). Samples were
measured for inorganic N by colorimetry on a
continuous ow autoanalyzer (QuikChem 8000, La-
chat, Loveland, Colorado, USA) and extractable TN
and CHCL3-N colorimetrically as inorganic N follow-
ing high-temperature persulfate digestion in the Kiowa
Environmental Chemistry Laboratory, University of
Colorado at Boulder (Seibold 2007). We calculated N
concentrations and 15N enrichments of extractable
DON as the extractable TN minus extractable inor-
ganic N. Chloroform-labile N was determined using the
chloroform fumigation extraction technique for three
days and then soils were extracted with 0.5 mol/L
K2SO4 as above. We calculated microbial N as the
CHCL3-labile N minus extractable TN, divided by a
factor of 0.54 to correct for chloroform labile N
extraction efciency (Brookes et al. 1985, Jenkinson
et al. 2004). To measure recovery of 15N, we diffused
the inorganic N, total N, and CHCL3-N soil extracts
for ve days with Devardas alloy onto acidied disks
(Brooks et al. 1989), which were analyzed using an
automated Rittenberg apparatus mass spectrometer
(Mulvaney et al. 1990) at the 15N Analysis Service at
the University of Illinois, UrbanaChampaign.
We used concentration of 15N in plant pools to
estimate 15N uptake, calculated as F [T(AS  AB)]/AF
where T is the mass of N in the sample, AS is the atom%
excess 15N in sample, AB is the atom% excess 15N in
background, and AF is the atom% excess 15N in the
tracer. Background enrichment was assumed to be
0.3663 atom%15N. The quantity F was divided by the
sample mass to determine 15N concentration in the
sample (Hauck and Bremner 1976). Plant 15N pools
were calculated as the sum of above- and belowground
tissue 15N concentrations multiplied by the above- and
belowground mass of the labeled individuals. Plant
uptake rate was calculated as the 15N pool divided by
the incubation time (time of label to addition to time
sample was refrigerated). Uptake of 15N by soil
3255
microbes was calculated by multiplying the 15N concen-
tration of the microbial N pool by the size of the pool
and dividing by the incubation time.
On 4 July 2006, we harvested an additional set of the
plant competition arenas to determine ambient N pools
and to examine effects of competition on growth. The
plant competition arenas were harvested and soil
extractable ammonium, nitrate, and dissolved organic
nitrogen were determined in the same manner as above.
We found ammonium was the most available form of N
(n 46, 22.1 6 1.37 lg N/g dry soil) and NO3 and
dissolved organic N (of which glycine only makes up a
portion) are less abundant (11.8 6 1.66 and 0.9 6 0.20
lg N/g dry soil, respectively). Uptake of available N was
estimated for each form using the approach of McKane
and colleagues (2002), where unlabelled uptake labeled
uptake 3 (mass of the N form pool/mass of the labeled
N form added). The mass of the glycine pool was
approximated by that of total dissolved organic N pool.
We calculated competitive response based on plant
biomass using (biomass of plant grown with neighbor 4
mean biomass of plant grown without neighbor from the
same block). Likewise, we calculated the competitive
response per gram of neighbor biomass in order to
account for differences in biomass among individuals,
i.e., log((biomass of plant grown with neighbor 4
biomass of plant grown without neighbor)/neighbor
biomass). To test whether this response was signicantly
greater than zero, where zero represents the point at
which growth is not changed by the presence of a
neighbor, t tests were used; positive values indicate a
facilitation of growth and negative values indicate
competition.
Differences in 15N uptake between species when
grown in isolation were analyzed using a two-way
ANOVA with species and N form as main effects.
Extreme outliers and loss of some replicates in the eld
harvest and throughout the analytical process resulted in
the nal sample size for each plant combinationlabel
treatment represented by 48 replicates. Uptake rates
were log-transformed to meet assumptions of normality
and heteroscedasticity. We tested for differences among
means using Tukeys studentized range (honestly signif-
icant difference [hsd]) tests. Differences in the domi-
nants response to the presence of Mertensia were
analyzed using a three-way ANOVA with species,
competition (with or without Mertensia neighbor), and
N form as main effects. The response of Mertensia to the
presence of the dominants was analyzed with N form
and competition as main effects. A separate model with
species and N form was used to determine the effects of
different species on Mertensia uptake. To examine the
differences in uptake rates of 15N in soil microbial N
pools we analyzed the data using ANOVA with main
effects of species combination and N form. Block effects
were not signicant and did not improve model t and
so were not included. All analyses were repeated using
the amount of clipped biomass from all plots as a
3256 ISABEL W. ASHTON ET AL.
FIG. 2. The competitive response of abundant and rare
species in the dry meadow alpine tundra at Niwot Ridge,
Colorado, USA. Competitive responses of the three abundant
species (Kobresia, Kob; Carex, Car; and Geum, Geu; in gray)
and the rare species Mertensia (white) were strongly asymmet-
ric. Competitive response is the log-transformed ratio of the
mass of an individual grown with a neighbor for one year
relative to the mass of an individual grown without a neighbor.
Zero represents the point at which growth is not changed by the
presence of a neighbor, positive values indicate a facilitation of
growth, and negative values indicate competition. Bars indicate
mean 6 SE, n 48 replicates for each plant combinationlabel
treatment, and asterisks indicate responses signicantly differ-
ent from zero (* P  0.05; ** P  0.01). While Mertensia did
not affect the growth of any of the abundant species
(competitive response not signicantly different from zero; P
0.56, P 0.57, P 0.21, respectively), the three abundant
species inhibited the growth of Mertensia (competitive response
signicantly less than zero; P 0.004, P 0.018, P 0.017,
respectively).
covariate, but since results were qualitatively equivalent
and clipped biomass did not correlate with 15N uptake,
we report analyses without this factor.
RESULTS
Competitive interactions, the degree to which neigh-
bors inhibited growth, were strongly asymmetric. The
presence of Mertensia did not affect the biomass of
Kobresia, Carex, or Geum (competitive response was not
signicantly different from zero in a t test: P 0.56, P
0.57, P 0.21, respectively; Fig. 2), but all three
abundant species decreased the growth of Mertensia
(signicantly negative competitive response: P 0.004, P
0.017, P 0.018, respectively; Fig. 2). Results were
qualitatively similar when competitive response was
calculated as response per gram of neighbor biomass
where the growth of the dominant species, Kobresia,
Carex, and Geum, was not affected by the presence of
Mertensia (t test, P 0.52, P 0.69, P 0.21,
respectively) and the presence of the abundant species
decreased the growth of Mertensia (t test, P 0.036, P
0.004, P 0.014, respectively).
In the absence of competitive interactions, an
estimation of the fundamental niche for N form use,
all four species preferred nitrate to glycine and
ammonium (ANOVA, N form, F2,71 15.9, P ,
0.001; Fig. 3A) and took up N at equivalent rates
Ecology, Vol. 91, No. 11
across all chemical forms (ANOVA N form 3 species,
F3,71 0.81, P 0.49). With competitors, Mertensia did
not affect the growth of the other species, but it did
affect the N forms they used (Fig. 3B). Kobresia, Carex,
and Geum increased their uptake of ammonium in the
presence of Mertensia (ANOVA competition, F1, 105
4.2, P 0.043; competition 3 N form, F2, 105 5.6, P
0.005; post hoc test indicates a signicant increase of
ammonium uptake in the presence of neighbors, F1, 105
14.7, P , 0.001; N form 3 species 3 competition, F4, 105
0.9, P 0.47). The shift to greater ammonium use was
not accompanied by a relative decrease in uptake of
nitrate or glycine in the presence of Mertensia (Fig. 3B).
While Carex did not signicantly increase total N
uptake (nitrogen response did not differ from zero; P
0.65; Fig. 4), Kobresia and Geum increased total 15N
uptake when grown with Mertensia (nitrogen response
signicantly greater than zero; P 0.003 and P 0.012,
respectively; Fig. 4).
In contrast to the plasticity of N form use of the
abundant species, the rare species and poorer compet-
itor, Mertensia, did not shift its preference from nitrate
to other N forms (ANOVA, competition 3 N form, F2,75
0.02, P 0.97; Fig. 3C) or alter its uptake rates
(ANOVA, competition, F1,75 0.6, P 0.45) when in
competition. Mertensias cumulative N uptake did not
change signicantly in the presence of the abundant
species (nitrogen response did not differ from zero; P
0.90, P 0.89, P 0.33, respectively; Fig. 4).
Qualitatively, the relative effect of neighbors on
Mertensia uptake followed abundance patterns, with
strongest effects from Kobresia and Carex and weakest
effects in the presence of Geum (Fig. 4), the least
effective competitor (Fig. 2) of the three. Mertensias
lack of plasticity in resource uptake likely translated to
reduced growth in competition (Fig. 2).
When the size of unlabeled pools are known, plant
15
N uptake can be used to estimate the potential
contribution of the native unlabeled N pools (cf.
McKane et al. 2002). With this approach, we found
that ammonium uptake was increased by a multiplier of
9, nitrate a multiplier of 5, and glycine uptake was
reduced by a multiplier of 0.4. However, estimates of
plant 15N uptake remained qualitatively similar between
the measured 15N uptake rates and calculated uptake
rates that accounted for uptake of N from unlabeled
pools. For instance, when grown alone, all species still
preferred nitrate to ammonium and glycine (signicant
N form F2,71 78.85, P , 0.0001). However, because of
uncertainty associated with our glycine estimates (i.e.,
unlabeled soil glycine pools approximated by DON
pools), we report all results as uptake of labeled N. We
also found that replicates established in 2006 had lower
rates of 15N uptake than older replicates (F1,69 6.7, P
0.0119), but including replicate year as a factor in
statistical models did not change results.
Microbial uptake rates differed across N forms
(ANOVA, F2, 106 66.4, P , 0.0001; Appendix) where
November 2010 NICHE COMPLEMENTARITY IN ALPINE PLANTS 3257

FIG. 3. Measurements of plant 15N uptake rate of three abundant and one rare species in the alpine and the effect of neighbors
on uptake. Cumulative plant 15N uptake rate of 15N-glycine, 15N-ammonium, and 15N-nitrate when (A) all species were grown
without neighbors (dark gray); (B) when abundant species were grown with Mertensia (light gray); and (C) when Mertensia was
grown with neighbors (white). When grown alone, species had similar N preferences (ANOVA, F3,71 0.81, P 0.49) where all
preferred nitrate (F2,71 15.9, P , 0.001). All three of the more abundant competitively superior species responded to the presence
of Mertensia by increasing ammonium uptake (F1, 105 14.7, P , 0.001), which translated to an increase in total N uptake in the
presence of a neighbor (F1, 105 4.2, P 0.043). Mertensia, on the other hand, was unable to shift its preference from nitrate to
other N forms (F2,75 0.02, P 0.97) or increase its total N uptake rates (F1,75 0.6, P 0.45) in the presence of the other species.
Bars indicate mean 6 SE, n 48 replicates for each plant combinationlabel treatment.

rates of glycine uptake were higher than ammonium and
nitrate (Tukey hsd, P , 0.05; n 49, 47, and 51; 1.9 6
0.11, 1.6 6 0.20, and 0.3 6 0.04 lg15Ng1d1,
respectively) and the rate of ammonium uptake was
higher than nitrate (Tukey hsd, P , 0.05). In arenas
with Mertensia and Kobresia, whether alone or in
combination, microbes preference between glycine and
ammonium was not signicantly different, resulting in a
signicant species combination 3 N form interaction
(F12, 106 2.2, P 0.018).
DISCUSSION
Our research documents resource use plasticity as a
mechanism of niche complementarity among plants.
Specically, we show that superior competitors exhibit
higher resource use plasticity of chemical forms of N
than the inferior competitor, which did not shift
resource use. While most theoretical or empirical
considerations of niche complementarity do not consid-
er plasticity in resource use, plasticity could provide a
general and important mechanism for resource parti-
tioning, particularly for species that have broadly
overlapping resource use patterns.
Much theory relating to niche complementarity
assumes evolutionary specialization in the form of
distinct niches. However, based on resource use
patterns in the absence of competitors, we did not nd
evidence for distinct fundamental niches in the use of
3258 ISABEL W. ASHTON ET AL.
FIG. 4. The nitrogen response of three abundant (Kobresia,
Kob; Carex, Car; and Geum, Geu) and one rare species (Mer,
Mertensia) in the dry meadow alpine. Cumulative 15N uptake
data were used to derive the relative response in terms of N
uptake of the abundant species when grown with Mertensia and
Mertensia when grown with each of the abundant species.
Nitrogen response is the logged ratio of N uptake of an
individual grown with a neighbor relative to the uptake of an
individual grown without a neighbor and used to normalize
uptake rates. Zero represents the point at which uptake is not
changed by the presence of a neighbor, positive values indicate
an increased uptake, and negative values indicate a decline.
Bars indicate mean 6 SE, n 48 replicates for each plant
combinationlabel treatment, and asterisks indicate responses
signicantly different from zero (* P  0.05; ** P  0.01).
When grown with Mertensia, Kobresia and Geum increased
their cumulative uptake of 15N (nitrogen response signicantly
greater than zero; P 0.003 and P 0.012, respectively). Carex
did not alter uptake rates in the presence of Mertensia, and the
uptake rates of Mertensia were not altered by the presence of
Kobresia, Carex, or Geum (competitive response not signi-
cantly different from zero; P 0.65, P 0.90, P 0.89, P 0.33,
respectively).
chemical N form among the four species we studied.
While this result could be specic to the species we
studied or to the usage of chemical N forms, we feel
that it is likely generalizable, as other studies have also
found large overlap in traits related to resource use
among coexisting species (Mahdi et al. 1989, Kahmen
et al. 2006, Schamp et al. 2008). However, because very
few studies examine resource use differentiation in
terms of fundamental and realized niches in plants, it is
not clear whether studies without competitive manip-
ulations mistake resource use plasticity for strict niche
differentiation.
Plasticity in resource use could be an important
mechanism for resource partitioning in plants. Plasticity
has been documented to have substantial ecological
consequences by directly altering tness of a species
(Sultan 2004, Miner et al. 2005) and indirectly affecting
species interactions (e.g., trait-mediated indirect inter-
actions; Werner and Peacor 2003). There is a rich body
of evidence that individual plants change their resource
use traits based on neighbor identity (DAntonio and
Mahall 1991, Jumpponen et al. 2002, Miller et al. 2007),
indicating potentially strong consequences for plant
communities (Callaway et al. 2003). This is the rst
Ecology, Vol. 91, No. 11
study to show that plasticity in N form use varies among
species that differ in their competitive dominance. As we
present results for only one set of species in the alpine,
further work is necessary to test whether these dynamics
often relate to competitive rankings and abundance
patterns.
Species abundance is generally thought to be corre-
lated with superior use of the most available resource
(McKane et al. 2002). We found that abundant species
did increase their use of the most abundant N form,
ammonium, when in competition (Fig. 3b). However, N
form use was not a static phenomenon, as all species
preferred nitrate to ammonium in the absence of
competition. Nitrate may be preferred, despite being
less available than ammonium, because it diffuses more
rapidly to the roots though soil water and is less toxic
when stored in plant tissue (Lambers et al. 1998). This
preference in the absence of plant competition may also
be due to preemptive competition by the microbial
community. In our study, microbes preferred glycine to
ammonium and nitrate and took up all forms of N up to
two orders of magnitude faster than plants.
We found that the presence of competitors increased
individual N uptake rates. This seemingly counterintu-
itive result is consistent with our past work in the alpine
(Miller et al. 2007, Ashton et al. 2008), as well as animal
systems (Peacor 2002), and could be due to the increased
density of two species mixtures in which the uptake of
alternative N forms is induced by crowding or via
indirect effects on foraging behavior (Abrams 1992).
While we did not quantify foraging behavior, it is likely
that the presence of a competitor could stimulate root
foraging activity (de Kroon and Mommer 2006). In this
case, the ability to switch N form preferences allowed
exible generalists to maintain growth while in proxim-
ity to Mertensia and facilitated increased uptake of N.
Further research is needed to determine whether the
response could be induced by intraspecic competition,
if it changes at different levels of resource availability,
and if the response of resource generalists differs when
different subordinate species are present. The long-term
repercussions of this short-term response in 15N uptake
are also unknown.
Where net primary productivity is limited by N and
the chemical form and abundance of N varies both
spatially and temporally, such as in our study system
(Raab et al. 1996), plasticity in N form use may be
particularly important in determining plant abundance
and diversity patterns. Here, species that were able to
switch their resource use patterns in response to
competition were superior competitors in terms of
growth, which in turn appeared to be associated with
high abundance. At the community level, resource
partitioning should reduce competitive exclusion and
increase persistence of rarer, potentially less plastic,
species. Our study did not address coexistence mecha-
nisms among the abundant species, which would require
a broader set of pairwise interactions.
November 2010 NICHE COMPLEMENTARITY IN ALPINE PLANTS
Environmental change is expected to alter patterns of
resource availability, including the availability of differ-
ent chemical forms of N. The patterns of N use that we
have shown here are likely to inuence the response of
biodiversity to future forecasted environmental variabil-
ity (Houlton et al. 2007). In the alpine of the Rocky
Mountains, atmospheric deposition of inorganic N is
currently increasing and the majority of the deposition is
in the form of nitrate (NADP 2009). These high nitrate
inputs have the potential to diminish the spatial and
temporal variability in N forms as N accumulates in the
system. As nitrate inputs increase and soil N availability
becomes less heterogeneous, resource use may more
closely follow niche preemption expectations, leaving
species with exible niche breadths at a competitive
disadvantage. While still rare, Mertensia has increased in
abundance in the alpine over the past two decades (from
,0.01% in 1990 to 0.5% cover in 2006; Niwot Ridge
LTER 2010) and shows a consistent positive response to
N fertilization experiments (Theodose and Bowman
1997). We expect other species with narrow nitrate
preferences to respond positively as well (Bowman et al.
2006). Patterns in resource heterogeneity and plasticity
of resource use may help explain the variability in
coexistence mechanisms across different ecosystems and
contribute to differential species responses to N depo-
sition or other environmental changes (Weigelt et al.
2005, Clark et al. 2007).
ACKNOWLEDGMENTS
We thank those who helped with eld work and laboratory
analyses, including M. Spasojevic, J. G. Smith, R. Winkleman,
M. Khosh, R. Aicher, H. McGray, J. Esclamado, W. Schlegel,
O. Plume, and R. Mulvaney at the University of Illinois, D.
Harris at the University of CaliforniaDavis Stable Isotope
Facility, and C. Seibold at Kiowa Laboratory. We are grateful
for funding from the Andrew W. Mellon Foundation and the
NSF-sponsored Niwot Ridge LTER program. The manuscript
was much improved by comments from J. Martiny, S. Harpole,
M. Lerdau, C. Stein, C. Meier, A. Darrouzet-Nardi, and K. Tea.
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