Journal of
Ecology 2005
93, 113–126
Multiple resources limit plant growth and function in
a saline-alkaline desert community
Blackwell Publishing, Ltd.
J. J. JAMES, R. L. TILLER and J. H. RICHARDS
Department of Land, Air and Water Resources, University of California Davis, One Shields Avenue, Davis, CA 95616–
8627, USA
Summary
1 We investigated resource limitations in a saltbrush scrub community along a salinityalkalinity gradient in the Mojave Desert of North America. Previous studies have shown
that, as productivity declines with increasing soil stress, there are parallel declines in leaf
Ca and Mg, suggesting availability of these resources may limit growth in addition to
water, N and P limitations expected in deserts.
2 To determine which soil resources limited growth of the dominant shrub, Atriplex
parryi, and whether this differed along the soil stress gradient or among life stages, water
and nutrients were applied in combination at different rates to plants at high- and low-stress
sites. We developed and applied a conceptual model to identify resource limitations
from this experiment. We also investigated how those limitations interacted to influence
A. parryi growth and physiological function at the high-stress site.
3 Availability of soil N and P limited growth at the low-stress site and N, P and Mg limited
growth at the high-stress site for both adult and juvenile life stages. There was no evidence that availability of water alone or K, Ca or other nutrients, or increasing soil Na
and B, limited growth along the soil stress gradient.
4 When N, P, Mg and water were supplied in combination, plant growth increased more
than 16-fold. Supply of these resources interacted to influence both plant growth and
function. Because of the high demand for N relative to other resources, N supply rate
was the major driver of these interactions, influencing the magnitude by which P and
Mg affected growth. The major mechanism behind these growth responses was an
increase in allocation to leaves relative to fine roots, rather than nutrient or water effects
on water relations, photosynthesis or water use efficiency.
5 Multiple, interacting resources limit the growth and distribution of A. parryi on a
saline, alkaline Mojave Desert site. Similar interactions between multiple limiting
resources are likely to be instrumental in shaping community and species distributions
along other abiotic stress gradients.
Key-words: alkalinity, Atriplex parryi, desert shrub, nutrient limitation, salinity
Journal of Ecology (2005) 93, 113–126
doi: 10.1111/j.1365-2745.2004.00948.x
Introduction
Resource limitations influence plant community properties, such as structure and species distribution, as well
as ecosystem functions, such as productivity and nutrient cycling. Although multiple-factor limitations have
long been recognized, few studies have investigated
individual plant or community responses to such
limitations (Chapin et al. 1987; Field et al. 1992; Shaw
et al. 2002; Ho et al. 2004). This lack of information
© 2004 British
Ecological Society
Correspondence: Jeremy J. James (tel. 530 752 2878;
530 823 2284; fax 530 752 1552; e-mail [email protected]).
may be related to the large number of treatments
needed to evaluate responses to both single resource
limitations and their interactions with other factors.
Additionally, individual species within a community
may be limited by different resources, making community level and individual plant responses in species-rich
communities difficult to interpret (Aerts & Chapin
2000; Drenovsky & Richards 2004). Despite these challenges, such insight is essential for understanding how
individual species and communities are impacted
following natural and anthropogenic perturbations, as
these are inherently multifactorial (Chapin & Shaver
1985; Press et al. 1998; Shaver et al. 1998; Shaw et al. 2002).
114
J. J. James,
R. L. Tiller &
J. H. Richards
© 2004 British
Ecological Society,
Journal of Ecology,
93, 113–126
Desert plant communities are excellent model systems
in which to investigate multiple resource limitations
to growth due to their simple structure, their low, but
highly variable, annual productivity and their limited,
heterogeneous supply of soil resources. Productivity
patterns in deserts are thought to be driven mainly
by low and infrequent precipitation inputs (Noy-Meir
1973; Hadley & Szarek 1981). In addition to the direct
effect of precipitation on plant growth, low and variable water supply reduces soil nutrient availability by
limiting the weathering of parent material, organic
matter production and mineralization (Fisher et al.
1987; Burke 1989; Schlesinger 1997). Studies in several
desert systems have shown that N or P can limit growth
once water limitations are removed (Smith et al. 1997;
Drenovsky & Richards 2004). Additionally, large
temporal and spatial heterogeneity of soil resources
compounds the effects of low soil nutrient supply on
productivity. For example, soil inorganic N concentrations can vary three- to tenfold within a site through the
season (Burke 1989; Ryel et al. 1996; Xie & Steinberger
2001; Z. Aanderud et al., unpublished data). Significant spatial variation has also been reported for N, P,
Ca, Mg, pH and organic matter in a range of desert systems (Jackson & Caldwell 1993; Schlesinger et al. 1996;
Cross & Schlesinger 1999).
While most research has focused on water limitations in deserts and how this interacts with low soil N
availability, there is evidence that the availability of
other soil resources may limit productivity in deserts,
particularly in highly saline-alkaline systems. Topographic gradients across interior drainage basins in
arid western North America are paralleled by gradients of decreasing soil fertility and increasing salinity,
pH and toxic ion concentrations (e.g. Na, B) at lower
positions. Thus, at lower topographic positions, productivity and diversity decline and, eventually, monospecific stands develop at the most stressful sites (West
1983; Donovan & Richards 2000), probably as a combined result of several factors. Increasing salinity not
only increases plant nutrient requirements, but it can
interfere with uptake of nutrient cations such as K+,
Ca2+ and Mg2+ (Flowers et al. 1977; Marschner 1995;
Drenovsky & Richards 2003). Likewise, increasing
alkalinity is expected to further reduce N availability
+
through volatilization of mineralized NH 4 and to
decrease P, Ca and Mg solubility (Lajtha & Schlesinger
1988; Schlesinger & Peterjohn 1991; Lambers et al.
1998).
Evidence for multiple resource limitations in salinealkaline deserts is, however, inconsistent. In a survey of
widespread Great Basin and Mojave Desert species
that establish on the lower portions of the topographic
gradients (including Atriplex parryi, the species that we
focus on here), Snyder et al. (2004) found that water
addition alone had minimal effects on productivity or
on physiological functions such as photosynthesis.
When soil organic matter and nutrients are available,
water addition should increase mineralization and
nutrient mobility (Birch 1960; Fisher et al. 1987; Cui &
Caldwell 1997), but no changes in leaf nutrient concentrations were observed. It was therefore suggested that
plant growth was co-limited by soil nutrient availability.
Other work supports the prediction that low nutrient
availability regulates plant growth response to water in
such environments. Along gradients of increasing soil
salinity and alkalinity in the Great Basin and Mojave,
both growth and leaf Ca and Mg concentrations of
dominant shrubs, including Sarcobatus vermiculatus
and A. parryi, declined in parallel with soil Ca and
Mg availability (Richards 1994; Donovan et al. 1997).
Although N and P are expected to be limiting in deserts,
no relationship was observed between growth and leaf
N or P concentration. Macro- and micronutrient additions
at one site, however, demonstrated that S. vermiculatus
growth was stimulated by N (Drenovsky 2002), but
not by P, Ca or Mg, supporting earlier experimental
work in deserts (see Smith et al. 1997 for review).
The discord between these different approaches to
determining resource limitations in deserts could be
due to methodology. For example, nutrient addition
may not significantly increase soil fertility if nutrients
are fixed by soil chemical reactions (Chapin et al. 1986).
Without dose-response curves it is not possible to
determine if a lack of response is because the resource
was not limiting or because supply rates were insufficient to overcome limitations or soil fixation. Of more
fundamental importance, however, is the need to consider how multiple limitations may interact to influence
plant response. Current models of allocation predict
that multiple resources will be limiting, but differences
in acquisition costs and absolute demand for resources
should interact to influence plant response to changes
in resource supply. In these models, small increases in
resources that are in high demand, such as N, which is
required in large quantities, result in significant reallocation to other functions (Bloom et al. 1985; Gleeson
& Tilman 1992; Gleeson & Good 2003). The magnitude
of this re-allocation should therefore influence plant
response to other resources or resource manipulation.
We determined whether single or multiple resources
(water, N, P, Mg and Ca) limit productivity of A. parryi
in the saltbrush scrub community it dominates. We
had two specific objectives. The first was to determine
experimentally which soil resources limit productivity
of A. parryi and to evaluate if these limitations differed
along a soil stress gradient or between life stages
(reproductive adults vs. pre-reproductive juveniles).
We applied resources in combination at different supply rates in two A. parryi stands, one at a high-stress site
and the other at a more species-diverse, low-stress site.
We then developed and applied a conceptual model
of plant response to resource addition to evaluate
patterns of nutrient limitations (Fig. 1). Treatments were
applied to adult plants at both the low and high stress
sites and to juvenile plants at the high stress site
because juvenile plants may be less tolerant of soil
stress (Donovan & Ehleringer 1994; Richards 1994).
115
Multiple resource
limitations in
deserts
Fig. 1 Conceptual model for determining nutrient limitations.
Nutrient limitations are inferred if both plant biomass and
nutrient concentration increase following resource addition.
Other permutations of the response variables include sufficient
supply (biomass increases but nutrient concentrations remain
constant), dilution (biomass increases but nutrient concentration declines) and luxury consumption (nutrient accumulates
but no biomass increase occurs). (Model modified from
Timmer and Morrow 1984).
The second objective was to investigate how resource
limitations interact to influence plant growth and function.
We used a full factorial approach to investigate how
resource limitations identified in the first experiment
interact to influence plant growth and function ( biomass
allocation, gas exchange, water relations) at the highstress end of the gradient.
Materials and methods
 
© 2004 British
Ecological Society,
Journal of Ecology,
93, 113–126
Both experiments were conducted on the southwestern shore of Owens Lake, California, USA (36°21.5′ N,
118° W; 1085 –1087 m a.s.l.). Owens Lake is in a closed
hydrologic basin at the north-western edge of the
Mojave Desert and has been dry since 1926 as a result
of urban water diversion (Saint-Amand et al. 1986).
Previous soil sampling along transects in this basin,
from the densely vegetated, non-saline dunes, through
the historic shoreline, to the barren playa surface, has
demonstrated steep gradients in soil nutrient availability,
salinity and alkalinity ( Dahlgren et al. 1997). Because
the higher topographic sites have been exposed longer,
allowing more weathering and leaching to occur, their
soils generally have higher nutrient concentrations,
lower pH and lower salinity levels. Sites located closer
to the playa have very nutrient-poor soils that are quite
−
saline and alkaline. Along the transects, soil NO3 in the
10 – 40 cm depth layer, where the highest concentration
of roots is found, ranges from 8 to less than 1 µg g−1. In
saturated paste extracts, soil P ranges from 5.1 to 0.01 m,
K from 40 to 1 m , Ca from 6 to 1 m and Mg from
0.45 to 0.05 m . Soil salinity (Na concentration)
increases from less than 10 to over 500 m and soil pH
increases from 8.5 to over 10 (Dahlgren et al. 1997).
The mean annual precipitation is 149 mm year−1, with
over 80% of the precipitation occurring between
October and April. Total precipitation in 2001 and
2002 was 196 and 138 mm. From January to August
2003 precipitation totalled 164 mm.
Two sites that differed in soil stress were selected
along an E-W transect. The low-stress site on the historic
shoreline of Owens Lake (Shoreline) and the highstress site below it on the recently exposed playa surface
(Playa) encompass the ecological range of Atriplex parryi
S. Watson in this community. This C4, non-mycorrhizal
shrub, forms a sparse (6% cover) but monospecific
stand at the high-stress site and is the dominant species
(23% cover) at the low-stress site (Table 1). At the lowstress site, the less stress-tolerant shrubs Sarcobatus vermiculatus, Atriplex confertifolia and Distichlis spicata
add 4% perennial cover and quickly replace A. parryi at
higher topographic positions, while at lower locations
no vegetation is able to establish. These sites correspond
to the LM4 and LM7 sampling locations of Richards
(1994) and Dahlgren et al. (1997).
   

Experiment 1
To determine which resources limit growth, we selected
40 widely spaced, similar-sized adult A. parryi shrubs
(canopy dimensions c. 20 × 20 × 35 cm and c.10 × 10 ×
10 cm at the low- and high-stress sites) at each site in
spring 2001. Additionally, 40 subplots, consisting of
three juvenile A. parryi plants (c. 5 × 5 × 8 cm each),
were selected at the Playa site. We selected shrubs and
subplots that had no neighbouring plants present
within a 1-m2 area. There were insufficient similar-sized
juveniles at the Shoreline site to allow treatment replication there, but it was more important to compare the
response of the two different life stages at the highstress site because juveniles may be more sensitive to
soil stress than adult plants (Donovan & Ehleringer
1994; Richards 1994). In each of five blocks, eight treatments (control, water, three rates of NPK addition with
water and three different Ca : Mg ratios with NPK and
water, Table 2) were randomly assigned to the eight
adult plants and eight juvenile subplots. Slow-release
KNO3 fertilizer was used to control the duration of N
−
and K availability and limit NO3 leaching (Apex® 120-42, Simplot, Lathrop, CA, USA). Nutrients were applied
in spring of 2001 and 2002 in the same locations in two
40-cm-deep holes on opposite sides of the canopy of
each adult plant and by auguring one 40-cm-deep hole
in the centre of each cluster of juvenile plants. The
nutrients were mixed with the excavated soil and holes
back-filled. Treatments receiving water were dripirrigated bi-weekly throughout the growing season
(March–June). The average amount of water applied
116
J. J. James,
R. L. Tiller &
J. H. Richards
Table 1 Comparison of plant community and soil characteristics at the Shoreline (low-stress) and Playa (high-stress) sites and
effects of water addition on soil characteristics. Soil samples were collected during August 2001 (5 months after start of water
treatments). Analyses were performed on saturated paste extracts. Soil values (mean ± SE, n = 5) are from 10 to 40 cm depth. All
−
+
−
2−
elemental data are in m. N is inorganic N ( NO 3 + NH 4 ) and P is inorganic P ( H2PO4 + HPO4 ). Different letters within a soil
characteristic (e.g. pH) indicate significantly different mean values as determined by  and subsequent multiple range tests
Shoreline
Playa
Plant community characteristics
Total cover
A. parryi cover (%)
A. parryi density (plants m−2)
A. parryi height (cm)
27 ± 2
23 ± 2
2.1 ± 0.4
36 ± 2
6±1
6±1
0.8 ± 0.1
10 ± 2
Soil characteristics
pH
Control
Water
8.58 ± 0.05b
8.39 ± 0.13b
9.04 ± 0.04a
8.47 ± 0.03b
EC (dS m−1)
Control
Water
2.41 ± 0.67b
0.85 ± 0.25b
6.33 ± 0.61a
1.32 ± 0.22b
Na
Control
Water
27.28 ± 8.13b
9.73 ± 3.71b
78.38 ± 7.47a
14.71 ± 2.53b
B
Control
Water
1.020 ± 0.381b
0.644 ± 0.413b
2.605 ± 0.196a
0.945 ± 0.201b
N
Control
Water
0.111 ± 0.052a
0.079 ± 0.024a
0.036 ± 0.008a
0.171 ± 0.049a
P
Control
Water
0.032 ± 0.011b
0.014 ± 0.006b
0.063 ± 0.006a
0.019 ± 0.005b
Mg
Control
Water
0.027 ± 0.003a
0.091 ± 0.057a
0.029 ± 0.005a
0.076 ± 0.018a
Ca
Control
Water
0.166 ± 0.031a
0.061 ± 0.012a
0.155 ± 0.016a
0.097 ± 0.027a
K
Control
Water
3.05 ± 0.56b
0.95 ± 0.09c
4.72 ± 0.45a
0.86 ± 0.11c
per replicate per year was equivalent to 330 mm of rainfall for adult plants and 310 mm of rainfall for juvenile
plants. Nutrient limitations can only be confidently
assessed if geochemical processes that reduce nutrient
availability are saturated, allowing plant nutrient requirements to be met (Chapin et al. 1986). To overcome
geochemical fixation in these highly alkaline soils, we
applied high rates of P, Ca and Mg so that a small
amount of the added resources would remain in a
soluble form long enough to be accessed by the shrubs.
Fertilizer addition increased nutrient availability to
levels within ranges sampled in adjacent upland stands
that are dominated by less stress-tolerant vegetation.
Similarly, applying water at a high rate ensured that water
Table 2 Fertilizer addition rates for treatments in experiments 1 and 2. Values are g of nutrient replicate −1 year−1. The three different NPK and Ca : Mg
−
−
doses are indicated by L (low), M (mid) and H (high) rates. Soil NO3 samples were collected 5 months after fertilization. Values are in µg N as NO3 per
g dry soil (mean ± SE, n = 10). In experiment 1 all treatments except control received water (W)
Treatment
Experiment 1
Control
W
W + LNPK
W + MNPK
W + HNPK
W + HNPK + LCa : Mg
W + HNPK + MCa : Mg
W + HNPK + HCa : Mg
Experiment 2
© 2004 British
N
Ecological Society,
P
Journal of Ecology,
Mg
93, 113–126
N(KNO3)
P(P2O5)
Adult
Juvenile
Adult
0
0
20
60
120
120
120
120
0
0
4
12
24
24
24
24
0
0
9
30
60
60
60
60
24
0
0
−
K(KNO3)
Mg(MgSO4)
Ca(CaSO4)
Soil N ( NO3 )
Juvenile
Adult
Juvenile
Adult
Juvenile
Adult
Juvenile
Adults
0
0
2
6
12
12
12
12
0
0
70
210
420
420
420
420
0
0
14
42
84
84
84
84
0
0
0
0
0
323
323
0
0
0
0
0
0
65
65
0
0
0
0
0
0
0
1764
1764
0
0
0
0
0
0
352
352
1.4 ± 0.2
1.7 ± 0.3
6.8 ± 0.9
56.8 ± 7.4
83.9 ± 12.8
0
12
0
84
0
0
0
0
65
0
117
Multiple resource
limitations in
deserts
limitations were removed, allowing additional effects
of nutrient limitations to growth to be determined.
The sandy, well-drained soils and wide plant spacing
prevented soil resources from overlapping into other
treatments.
Experiment 2
To determine how multiple resource limitations interact
to influence A. parryi growth and function, we selected
80 similar-sized juvenile plants at the Playa site in March
2003. Neighbour plants within a 1-m2 area around the
target shrubs were removed. Four soil resources (water,
N, P, Mg), each at two levels (+ or –), were applied in a
complete factorial design. The control treatment received
no additional resources (i.e. water, N, P, Mg). The 16
treatment combinations were randomly assigned to
plants in each of five blocks. Fertilizer and irrigation
applications and rates were similar to those applied in
experiment 1 (Table 2) but application rates per plant were
therefore three times higher in this second experiment.
    
Biomass and tissue nutrient samples were collected in
July 2002 for experiment 1 and July 2003 for experiment
2. In experiment 1 leaf biomass was sampled by harvesting one-quarter of the hemispherical canopy from
each adult plant (Messina et al. 2002; Snyder et al. 2004).
In experiment 2 the entire canopy was harvested and
roots were sampled by excavating a 45 cm wide × 45 cm
deep hole around each plant. Previous sampling demonstrated that A. parryi rooting density is highest in this
soil layer (Dahlgren et al. 1997). All excavated soil was
placed in a basin and washed to separate roots from
the sandy soil. Before grinding and analysis, root samples
were triple rinsed with deionized water and all coarse
roots (> 2 mm), dead roots and non-root material
were removed. A similar triple rinsing procedure was
followed for leaf samples to remove dust and surface
salts. Plant tissue was analysed for N content by microDumas combustion with a Carlo Erba NA1500 elemental
analyser (Milan, Italy). For all other elements, samples
were microwave digested with nitric acid following
the method of Sah & Miller (1992) and analysed by
inductively coupled-plasma atomic-emission spectrophotometry (Thermo Jarrell Ash Corp., Franklin, MA,
USA).
   
© 2004 British
Ecological Society,
Journal of Ecology,
93, 113–126
Soils were sampled from the 10 –40 cm depth layer in
experiment 1 in all treatments. Three subsample cores
were taken directly under the edge of the canopy of each
adult plant and combined. Soil characteristics were
measured on saturated paste extracts. Na+ and K+ were
analysed by atomic absorption spectrophotometry and
Ca2+ and Mg2+ by atomic emission spectrophotometry.
−
+
Soil NO3 and NH 4 were analysed following Carlson
(1978), P and B were analysed colourimetrically
following Murphey & Riley (1962) and Keren (1996).
   
  
Instantaneous gas exchange and predawn (Ψpd) and
midday (Ψmd) water potentials were measured on juvenile plants in experiment 2 only. Leaf gas-exchange was
measured from 09.00 to 11.00 hours on all treatments
using a LI-6400 (LiCor Inc., Lincoln, NE, USA) in midspring (23 and 24 May) and early summer (1 and 2 July)
2003. Sample CO2 was 370 µ mol mol−1, PPFD was maintained at an average ambient rate for the sampling
period (1800 µ mol m−2 s−1), cuvette temperature was set
to 28 °C, and relative humidity tracked ambient levels.
Leaves within the cuvette were excised and scanned for
leaf area using a desktop scanner and image analysis
software (Scion Corp., 2000, Frederick, MD, USA,
and Win RHIZO vs. 5.0 A software, Regent Instruments Inc., Saint-Foy, Canada). Treatment effects on
gas exchange and on Ψpd and Ψmd were assessed only
for the Control, Water, NPMg and Water + NPMg
treatments. Measurements of plant water status were
made on terminal leafy stems with a Scholander-type
pressure chamber (PMS, Corvallis, OR, USA) following the procedures of Turner (1988) to minimize errors.
Water potential measurements were made on the same
days and plants used for gas exchange measurements.
 
The main objective of the first experiment was to determine which resources were limiting plant growth by
fitting treatment effects on leaf biomass and nutrient
concentration to a conceptual model (Fig. 1). In this
model the primary focus is how the relationship between
individual nutrients and biomass changes across resource
addition treatments rather than the interaction of
all five response variables. Although this univariate
approach allows for a direct application of our conceptual model, we first evaluated treatment effects on all
leaf response variables (i.e. leaf biomass, N, P, K, Ca
and Mg concentration) using multivariate analysis
of variance () and contrasts because the
response variables were strongly correlated. Because
these comparisons were not orthogonal, sequential
Bonferroni corrections were made to maintain an
experiment-wise error rate of α = 0.05 (Rice 1989). When
these  contrasts indicated significant differences
between treatments, univariate  models were run
on each of the five leaf response variables followed by
univariate contrasts (Scheiner 1993; Tabachnick &
Fidell 1996). Normality of residuals was evaluated
using Shapiro Wilk tests on individual univariate
models. Because  is robust against heterogeneity
of covariance matrices (Scheiner 1993), particularly
when cell sizes are equal (Tabachnick & Fidell 1996), no
remedial measures were taken to correct univariate
118
J. J. James,
R. L. Tiller &
J. H. Richards
heterogeneity of variance in the  models.
However, when univariate approaches were used, the
 models were weighted by the inverse of the variance to correct for heterogeneous variances among
treatments (Neter et al. 1990).
Measured variables in experiment 2 that did not
involve repeated sampling (i.e. biomass and nutrient
concentrations) were analysed using . Assumptions of  were tested and corrected following the
same procedures used in experiment 1. Repeated-measures  was used for variables that involved repeated
sampling of individual plants through the season (i.e.
gas exchange and water potential) (Gurevitch & Chester
1986). Between-subject effects were block, water and
NPMg. Within-subject effects were season and the
interactions of season with the between-subject effects.
Univariate analyses were used to test within-subject
effects. When there were more than two levels of the
within-subject factor and assumptions of sphericity
were violated, Huynh-Feldt adjusted P-values were used
to evaluate within-subject effects. Data were analysed
with SAS (SAS Institute 2001).
Results

1
Soils
Soil salinity (EC and Na), B and pH were higher at the
Playa site than the Shoreline site (P < 0.05, Table 1).
Values for soil stress factors and nutrient concentration
in the control plots are similar to those previously
reported from this study site (Dahlgren et al. 1997).
Water addition lowered pH, EC, Na and B in both
plots, reducing differences in soil stress factors between
sites. Soil nutrient concentrations were low at both sites
and were generally unaffected by water addition. An
exception to this was the relatively high inorganic P
found in soil solution at both sites. Due to the high soil
pH, however, the majority of this P was in the form of
2−
−
HPO 4 as opposed to the more plant available H 2 PO 4
(Kochian 2000). Application of slow-release KNO3 created
−
large differences in soil NO3 availability (Table 2), and
at the highest dose saturated paste K+ increased from
0.95 to 6.23 m . At the highest P dose, saturated paste
inorganic P increased from 0.014 to 0.06 m. Saturated
paste concentrations of Ca and Mg rose from 0.09 to
0.2 m and from 0.06 to 0.3 m , respectively, when
these elements were added. These increases in soil nutrient
levels are within the range documented in adjacent,
upland stands that are dominated by less stress-tolerant
vegetation.
Plant growth and nutrient relations
Multivariate comparison of treatment effects on
adult and juvenile plants within sites Because limitations
within sites were of primary interest, treatment effects
on the leaf response variables (i.e. total leaf biomass,
and leaf N, P, K, Mg and Ca concentrations) were
analysed separately for the Shoreline and Playa sites
(Table 3). Control and watered adult plants did not differ significantly at either site and this comparison was
therefore excluded from the subsequent univariate
analyses. Both NPK supply and soil Ca : Mg and addition rates, however, significantly affected the leaf response
variables of adult plants at both sites. Juvenile plants
showed similar responses to both water and nutrient
addition.
Univariate responses of leaf N, P, K, Mg and Ca and relationship with leaf biomass Univariate contrasts were
run on the six leaf response variables (i.e. leaf biomass,
Table 3 Experiment 1:  contrasts of leaf response variables (i.e. biomass and leaf N, P, K, Mg and Ca concentrations)
between treatments within sites. Wilks’ lambda, exact F-values and P-values are presented (numerator d.f., denominator d.f. = 5,
24). Significant comparisons are indicated with bold P-values. Average NPK and average Ca : Mg contrasts compare the
appropriate control treatment with the average responses produced by the three dose treatments for the respective nutrients. The
linear contrasts test if there is a significant linear response of the leaf variables to increasing rates of NPK or Ca : Mg addition
© 2004 British
Ecological Society,
Journal of Ecology,
93, 113–126
Site
Stage
Treatment comparison
Wilks’ lambda
F
P
Shoreline
Adult
Control vs. Water
Water vs. average NPK
High NPK vs. average Ca : Mg
Linear response to NPK
Linear response to Ca : Mg
0.768
0.152
0.185
0.116
0.099
1.45
26.63
21.04
36.32
43.23
0.2435
< 0.0001
< 0.0001
< 0.0001
< 0.0001
Playa
Adult
Control vs. Water
Water vs. average NPK
High NPK vs. average Ca : Mg
Linear response to NPK
Linear response to Ca : Mg
0.64
0.281
0.506
0.18
0.316
2.69
12.26
4.67
21.41
10.38
0.0457
< 0.0001
0.004
< 0.0001
< 0.0001
Juvenile
Control vs. Water
Water vs. average NPK
High NPK vs. average Ca : Mg
Linear response to NPK
Linear response to Ca : Mg
0.792
0.504
0.665
0.382
0.2366
1.26
4.72
2.41
7.75
15.48
0.3122
0.0038
0.0661
0.0002
< 0.0001
119
Multiple resource
limitations in
deserts
Fig. 2 Effects of resource addition treatments on leaf biomass and nutrient concentration (mean ± SE; n = 5). Treatments were:
water (no added fertilizer) three rates of NPK addition [low (LNPK), mid (MNPK), high (HNPK)], and three rates of Ca and Mg
addition to give different ratios [low (LCa : Mg), mid (MCa : Mg), high (HCa : Mg)] in combination with high NPK addition. All fertilizer
treatments included water addition. Different letters indicate significant univariate differences, as indicated by linear contrasts (see
methods). Differences in leaf nutrient concentration (x-axis) are indicated by letters x–z on all graphs and differences between leaf biomass
(y-axis) are indicated by letters a– d on the first graph within a row. Dashed lines on the x and y axis delineate these statistical
differences between groups of treatments and facilitate interpretation of responses with our conceptual model (Fig. 1 and see text).
© 2004 British
Ecological Society,
Journal of Ecology,
93, 113–126
and leaf N, P, K, Mg and Ca concentrations) and treatment
effects on these responses were fitted to our conceptual
model to evaluate nutrient limitations (Fig. 1).
At the Shoreline site, leaf N and leaf biomass both
increased with higher rates of NPK supply (Fig. 2a).
Both biomass and N concentration increased up to the
mid rate of N supply but further increases in leaf biomass were not associated with concurrent increases in
leaf N, indicating that N limitations had been overcome. Leaf biomass and P concentration also increased
at higher rates of NPK supply, but the increase was
only significant at the highest rate, indicating that P
availability was limiting at lower rates. Leaf Mg concentrations increased significantly with increasing soil
Mg supply (i.e. decreasing soil Ca : Mg) but the lack of
an effect on growth suggests that soil Mg was not limiting.
The absence of increases in leaf K and Ca concentration when these elements were added also suggests that
their supply was not limiting growth of adult A. parryi
at this site.
Adult plants at the Playa site increased both leaf
biomass and N and P concentrations when NPK was
added at the lowest rate (Fig. 2b). Further increases in
NPK supply resulted in increased growth but not leaf
N, indicating that N supply was sufficient at the lowest
rate, whereas leaf P continued to increase, indicating
that P availability continued to limit growth. Both biomass and leaf Mg increased at higher soil Mg supply
rates (i.e. decreasing soil Ca : Mg), suggesting that Mg
was limiting growth once N and P limitations were
removed. Increased plant growth due to increased NPK
supply also resulted in a significant dilution of leaf Mg,
with Mg concentrations declining over 1.6-fold with
NPK addition. Increasing soil K and Ca again had
no effect, suggesting that, as at the Shoreline site, they
were not limiting growth.
Juvenile plants at the Playa plot increased leaf biomass and leaf N and P concentrations when soil NPK
supply was increased (Fig. 2c), but the effect was only
significant at the highest rate. It was not therefore
indicating that plant uptake and allocation of Mg2+,
Ca2+ and K+ to leaves relative to Na+ increased as relative soil availability declined (Fig. 3). S[Ca,Mg] remained
constant between the sites.
120
J. J. James,
R. L. Tiller &
J. H. Richards

2
Above-ground biomass
Fig. 3 Selectivity coefficients (leaf / soil) for Mg2+, Ca2+ and
K+ relative to Na+, and Ca2+ relative to Mg2+ for control adult
Atriplex parryi plants growing at the shoreline and playa sites
and control juvenile plants growing at the playa site (mean ±
SE; n = 5). Coefficients are calculated as the leaf molar ratio
divided by the soil molar ratio of a pair of elements.
possible to determine if N and P limitations were overcome. The addition rates per plant may have been too
low to create a significant dose response (adult leaf N
concentrations exceeded 2%, even at the mid N supply
rate, while juvenile concentrations never exceeded 1.5%).
At the highest rate of NPK supply leaf Mg increased
but no significant growth responses were observed,
suggesting low N and P availability continued to be the
primary growth limitation. Consistent with the adult
plants, increasing soil K and Ca did not result in any
significant change in leaf nutrient concentrations or
biomass, suggesting soil K and Ca was not limiting growth.
Cation selectivity
Cation selectivity coefficients are an integrated measure of nutrient acquisition and allocation to leaves in
different soil environments, such as declining nutrient
availability and /or increasing salinity (Donovan et al.
1997). Selectivity coefficients are calculated as the leaf
molar ratio of an elemental pair divided by their soil
molar ratio (e.g. S[Mg,Na] = Leaf[Mg,Na] /Soil[Mg,Na]). In control plants, S[Mg,Na], S[Ca,Na] and S[K,Na] increased five-, fourand twofold between the Shoreline and Playa sites,
© 2004 British
Ecological Society,
Journal of Ecology,
93, 113–126
Plant growth was significantly affected by factorial
alteration of the four soil resources (P < 0.0001). Over
one growing season above-ground biomass of juvenile
A. parryi increased over 16-fold when the supplies of
water, N, P and Mg were increased (Fig. 4). These
growth responses were driven by both effects of single
resource manipulations and the interaction of multiple
resource additions.
Effects of single resource manipulations Increasing N,
P or Mg supply without water addition significantly
increased shoot mass (P < 0.0001, P = 0.02, P = 0.0004,
Fig. 4). There was no significant effect of water addition alone on shoot mass (P > 0.05).
Interaction of resources The effects of increasing supply of any resource on shoot mass depended on the
supply rate of other soil resources (Fig. 5a–d; all four
three-way interactions were significant, W × N × P (P =
0.03), W × P × Mg (P < 0.001), N × P × Mg (P < 0.001),
W × N × Mg (P = 0.001), while the four-way interaction was not significant (P = 0.35)). For example, Mg
addition significantly increased growth at both low and
high rates of N and P supply (P = 0.0001, P < 0.0001,
Fig. 5a) but the response was greater when both N and
P were supplied at high rates relative to when either
was supplied at lower rates (P < 0.0001). Similarly, the
response to Mg addition was greatest when high rates
of water and P were combined (Fig. 5c).
Although all the soil resources interacted to influence
growth, soil N availability, as determined both by the
rate of N and water supply, had the largest effect and
was thus a major driver of most interactions (Fig. 5b,d).
Fig. 4 Effects of water, N, P, and Mg addition, indicated by hatched bars along base of figure, on Atriplex parryi shoot mass
(mean ± SE; n = 5). Treatments are arranged by magnitude of growth response to facilitate interpretation of resource effects.
other resources were manipulated concurrently (see
data in Appendix S1 and statistics in Appendix S2 in
Supplementary Material). Plants receiving water and
N had 1.5-fold higher leaf N concentration than plants
only receiving N, but water alone had no effect on leaf
P and Mg. Increasing soil Mg predictably lowered leaf
Ca : Mg but this decline was due to both an increase in
leaf Mg concentration and a decline in leaf Ca. Leaf K
increased in treatments receiving water and N (N was
supplied as KNO3). These resource effects on leaf K,
however, were moderate, increasing less than 1.2-fold.
Treatment effects on root nutrient concentrations were
less pronounced than effects on leaf nutrient concentrations. N addition did not alter root N concentration
significantly (P > 0.05, Appendices S1 and S2), although
P and Mg additions raised root concentrations of these
elements (P < 0.0001, P = 0.01). Altering soil Ca : Mg
supply did not change root Ca : Mg and there were no consistent treatment effects on root Ca or K concentrations.
Leaf and fine root Na and B concentrations significantly decreased with water addition (P < 0.0001) but
there was no effect of increasing N, P or Mg supply,
either with or without water, on leaf and root Na or B.
Leaf concentrations of Na and B, respectively, were:
–W, 75.2 ± 1.0 g kg−1 and 305 ± 8 mg kg−1; +W 65.2 ±
1.2 g kg−1 and 219 ± 9 mg kg−1 (means ± SE, n = 40).
Root Na and B concentrations, respectively, were: –W,
8.3 ± 0.5 g kg−1, 138 ± 10 mg kg, +W 6.2 ± 0.2 g kg−1,
80 ± 3 mg kg−1. Storage patterns were similar between
treatments and elements; leaf tissue had > nine- and
twofold higher Na and B concentrations than roots.
Effects of salinity on leaf cation nutrition were
examined by calculating molar ratios of cation nutrients,
Mg and Ca, relative to Na. Leaching of Na through
irrigation increased leaf Mg : Na and Ca : Na (see data
and statistics in Appendices S1 and S2). Treatment
differences beyond the irrigation effects were mainly
due to the differential effects of N, P and Mg addition
on leaf nutrient status, rather than differences in leaf Na.
121
Multiple resource
limitations in
deserts
Fig. 5 Interactions of water, N, P, and Mg addition on juvenile
Atriplex parryi shoot mass (mean ± SE; n = 5). Treatments
were applied in a factorial design. Minus (−) symbols indicates
ambient resource supply rates and plus (+) indicates elevated
supply rates (see Table 1). Simple effects in the four three-way
interactions (N × P × Mg, W × N × Mg, W × P × Mg, W × N × P;
all were significant for shoot mass) are shown in Fig. 5a– d
respectively. Results of statistical analysis are given in
Appendix S2.
For example, when both N and water were supplied, Mg
addition resulted in a 1.6-fold increase in growth but
Mg addition had no effect on growth when N supply
was increased without water addition (Fig. 5b).
Tissue nutrient and toxic ion concentrations
© 2004 British
Ecological Society,
Journal of Ecology,
93, 113–126
N, P and Mg addition all significantly increased concentration of the respective element in leaf tissue, but in
general, leaf nutrient concentrations depended on what
Leaf and fine root allocation
Plant leaf : fine root biomass was significantly affected
by soil water and NPMg availability and this effect differed depending on the rate of water and NPMg supply
(P = 0.005, Fig. 6). All plants receiving treatments
without NPMg had a significantly lower leaf : fine root
biomass than plants that received NPMg addition (P <
0.0001). Furthermore, plants that received NPMg and
water had a significantly higher leaf : fine root biomass
than plants that received NPMg alone (P = 0.005). Water
addition alone, however, had no effect on leaf : fine
root biomass (P > 0.05).
   
 
Instantaneous photosynthesis and conductance were
not significantly affected by water addition alone in
122
J. J. James,
R. L. Tiller &
J. H. Richards
Fig. 6 Effects of water and NPMg addition on Atriplex parryi
allocation to leaf and fine root biomass (mean ± SE; n = 20).
periods (P > 0.05). Changes in photosynthetic rate were
small, increasing approximately 1.2-fold with NPMg
addition. Photosynthetic water use efficiency (WUE)
significantly increased with both water and NPMg
addition (P ≤ 0.05). These resource effects on WUE
were similar across the season (P > 0.05) and were
moderate, with approximately 1.5-fold increases in
treatments receiving NPMg only relative to control
plants. Water addition significantly improved Ψpd and
Ψmd in both May and June (P < 0.05); there was no
effect of plant nutrient status on Ψpd and Ψmd at either
high or low water supply (P > 0.05) (Fig. 7). Although
there was a significant decline in both Ψ pd and Ψmd
through the season (main effect of season, P < 0.001)
there was not a significant season × treatment interaction (P = 0.29), indicating plants experienced similar
changes in Ψ pd and Ψmd through the season in all
treatments.
Discussion
    
Fig. 7 Effects of water and NPMg addition on Atriplex parryi
midday leaf instantaneous photosynthetic rate, stomatal
conductance, photosynthetic water use efficiency (WUE), and
predawn and midday xylem water potentials on 23 and 24
May and 1 and 2 July 2003 (mean ± SE; n = 5).
© 2004 British
Ecological Society,
Journal of Ecology,
93, 113–126
either May or July (P > 0.05) (Fig. 7). Photosynthesis
increased with NPMg addition (P = 0.01) but this
effect was similar regardless of water addition (P > 0.05)
and did not differ between May and July sampling
Water, N and P limitations to plant growth in deserts
have been demonstrated (Smith et al. 1997; Drenovsky
& Richards 2004). Our results are consistent with N
and P limitations but demonstrate an additional limitation of Mg at the most saline-alkaline site. Although
Ca limitations were predicted by earlier studies in this
community and in a similar system in the Great Basin
(Richards 1994; Donovan et al. 1997), increasing Ca
supply did not result in Ca accumulation or growth
at either site or life stage. A similar lack of effect of K
addition suggests that low soil K, or high soil Na+ relative to K+, was not limiting growth. Although there
was no direct manipulation of other plant macro- or
micronutrients, no significant changes of these elements
occurred with plant growth, suggesting their availability did not limit growth (data not presented). Although
there were gradients in soil toxic ions (Na and B)
through the community, the high leaf concentrations
of these elements do not appear to be major limiting
factors to A. parryi growth. Leaching of soil Na and B
in the water addition treatment decreased Na and B
concentrations in juvenile A. parryi leaves as well as in
adults (data not presented) but no positive effect on
growth was observed. Leaf toxic ion levels in all treatments, for all life stages, were well below tolerance
limits measured in sand culture (Richards 1994).
Unlike other work in deserts, our results suggest that
water availability alone does not limit growth (Noy-Meir
1973; Fisher et al. 1988; Smith et al. 1997; Reynolds
et al. 1999; but see Hooper & Johnson 1999). Experiment
1 encompassed wet and dry years, but no significant
effects of water addition on growth or leaf nutrient concentrations were observed. Significant improvement in
pre-dawn water status confirms that plants acquired
water but did not use it to increase growth. A parallel
123
Multiple resource
limitations in
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study indicates that nutrient, but not water, addition
increased A. parryi seed production and viability (A.N.
Breen and J.H. Richards, unpublished data) and that
seeds produced by fertilized plants were larger, germinated
faster and resulted in seedlings that had higher survival
rates under stressful soil conditions. Nutrients, N, P
and Mg, which limit growth in this system, are therefore
likely also to play a role in establishment and survival
of seedlings.
The concept of resource limitations was developed in
agricultural systems and has been utilized in many ecological studies to understand the major factors limiting
individual plant, community and ecosystem processes.
This approach requires high rates of resource addition
to overcome soil biogeochemical fixation and abiotic
loss, allowing enough resources to remain available
to meet plant resource demand. However, measured
responses represent the maximum potential for resource
limitation, and resource manipulations must be compared with the natural resource dynamics of the study
system. Our water additions in both experiments
represented more than twice the amount of rainfall
normally received but the absence of effects on growth,
allocation or leaf-level physiology makes it likely that
smaller, more ecologically relevant increases in water
availability would not affect A. parryi performance.
Although we applied nutrients at a high rate, water
extractable nutrient pools only increased moderately.
−
Soil NO3 increased approximately sixfold from the low
N addition rate (which was sufficient to saturate plant
−
N demand) and the observed increase in soil NO3 was
similar to what occurs following spring precipitation
pulses and N mineralization preceded by several drought
years (Cui & Caldwell 1997; Z. Aanderud et al., unpublished data). The other nutrients (P, K, Ca, Mg)
that are mainly supplied through weathering of parent
material also increased (approximately four-, six-, fiveand twofold, respectively) well within documented levels. Although a detailed understanding of community
nutrient dynamics requires both measurements of pool
sizes and estimates of pool turnover rates, our results
indicate that changes in soil N availability that occur
seasonally with varying precipitation inputs may interact strongly with changes in P and Mg availability that
occur over successional time periods to influence the
distribution of A. parryi specifically and the species
composition and structure of saline-alkaline desert
plant communities in general.
  
    
© 2004 British
Ecological Society,
Journal of Ecology,
93, 113–126
At the high-stress site, plant growth increased when the
three nutrients, N, P and Mg were added individually
(Fig. 4), as predicted by the model and experiment 1
results (Figs 1 and 2). While some treatment combinations, such as NMg, resulted in growth that was similar
to the average response when N and Mg were supplied
individually, factorial application of nutrients and
water demonstrated that effects of resource addition on
A. parryi growth were not strictly additive (Fig. 5). The
supply rate of N, as determined by both rate of N addition and soil water availability, appeared to be a primary
driver of these interactions, and therefore a major
determinant of plant response to other resource limitations. For example, when NPMg was supplied, growth
increased more than 3.5-fold relative to PMg addition.
When water was supplied with NPMg, there was an
additional threefold increase in growth. In general, the
effect of Mg and P on growth depended on the supply
rate of N, which in turn was influenced by soil water status.
Not all interactions were positive. Some treatment
combinations, such as PMg, resulted in lower growth
responses than if either resource was supplied individually.
These results demonstrate that the magnitude of response
to altering the supply of one resource can influence
plant response to other resource manipulations.
Low nutrient availability in desert soils is compounded by salinity and pH effects on nutrient availability (Lajtha & Schlesinger 1988; Marschner 1995;
Lambers et al. 1998). While nutrient sufficiency levels
are not well established for desert plants, leaf N and P
levels in control plants were low relative to other reported
values for desert plants (El-Ghonemy et al. 1978;
Wentworth & Davidson 1987; Donovan et al. 1997).
Although addition of limiting nutrients resulted in
significant increases in leaf nutrient concentrations of the
respective elements, there were both synergistic and
antagonistic effects of nutrient addition on concentrations of other nutrients. For example, N addition
stimulated P and Mg acquisition but P addition decreased
Mg and Ca concentrations. Similar nutrient interactions are widely documented in agricultural systems
but poorly understood in natural systems (Marschner
1995). In this experiment, it was not possible to determine if these responses were due to changes in soil
chemical properties as a result of fertilization or plant
physiological responses to nutrient imbalance. Concentrations of cation macronutrients relative to Na were
consistent with reported values for other halophytic
desert shrubs (Donovan et al. 1997), supporting the
conclusion that salinity per se has little effect on
growth, nutrient status or other plant functions in this
system dominated by salt-tolerant halophytes.
  
Increasing levels of the four soil resources in this experiment resulted in over a 16-fold increase in above-ground
biomass in a single growing season. The major mechanism driving these growth responses appears to be
changes in biomass allocation between leaves and fine
roots. The ratio of leaf to fine root biomass is a sensitive
measure of functional allocation because it quantifies
the amount of resource dedicated to instantaneous leaf
photosynthetic rate relative to nutrient and water
absorption in these perennial shrubs. In this study, water
addition alone did not change allocation between leaf
124
J. J. James,
R. L. Tiller &
J. H. Richards
and fine roots, while NPMg addition resulted in a fourfold increase in allocation to leaves relative to fine root
biomass. When water was added with N, allocation to
leaves increased over sixfold.
In contrast, changes in leaf level responses do not
appear to be key mechanisms contributing to these growth
responses. Although increasing soil water availability
improved plant water status through the growing season,
it did not increase instantaneous leaf photosynthetic
rate or conductance. Increasing nutrient availability
stimulated instantaneous leaf photosynthetic rate only
slightly (c. 20%). For plants not receiving water, instantaneous WUE increased 1.5-fold in fertilized plants.
Photosynthetic nitrogen use efficiency (PNUE) declined,
however, because leaf N concentration increased 1.4fold with only small changes in instantaneous leaf photosynthetic rate. This is consistent with the expected
trade-off between leaf-level WUE and PNUE (Field
et al. 1983). These changes in instantaneous WUE, like
instantaneous photosynthesis, were moderate, consistent
with the expectation of tight internal controls on photosynthesis in desert environments (Smith et al. 1997).
Taken together, these results suggest both that soil
nutrient availability is the major driver of leaf vs. fine
root allocation patterns and that changes in allocation
appear to be much more important than changes in
photosynthetic rates per unit leaf area or leaf level
instantaneous WUE. A key functional trait of stresstolerant plants, according to life-history theory, is slow,
tightly regulated growth, in order to balance plant demand
with the low resource supply rates typical in stressful
systems. While similar nutrient-driven responses are
well documented in systems dominated by fast-growing
plants (Marschner 1995; Aerts & Chapin 2000), the
magnitude of changes observed in allocation in this
nutrient-poor environment were substantially greater
than expected based on traditional life-history theory
(Aerts & Chapin 2000; Grime 2001). However, similar
large changes (threefold) in above-ground / belowground allocation were also observed in transplants
of Sarcobatus vermiculatus grown for 2 years at sites
differing in nutrient availability in a Great Basin playa
ecosystem (Donovan & Richards 2000).
Increased allocation to root growth to minimize N
limitations might be expected to increase capture of the
less limiting resources P and Mg, potentially resulting in a single limitation. However, nutrient-specific
components to allocation have been demonstrated in
nutrient-poor soils (Marschner 1995; Hinsinger 2001)
and, although not directly quantified, may well occur in
our system. For example, although high concentrations
of Na and K can drastically reduce Mg uptake, A. parryi
minimized limitation along the soil stress gradient by
increasing selectivity for Mg relative to Na, similar to
the cold desert halophyte S. vermiculatus (Donovan
et al. 1997). Likewise, when all nutrients were supplied
simultaneously, Ca uptake did not increase, while
uptake of P and Mg did. This supports the idea that
plant demand regulates nutrient uptake through changes
in selectivity and that root growth does not necessarily
result in simultaneous capture of multiple nutrients
(Marschner 1995).
These observed patterns of resource limitations have
major implications for understanding arid ecosystem
responses to environmental change. Although there
is strong evidence that soil nutrient availability is the
major limitation to plant growth, our results suggest
that the various nutrients interact to influence plant
growth, physiology and allocation patterns. This suggests
that perturbations that change nutrient availability
will have the largest impacts on these desert plant communities, contrasting with expectations that changes
in water availability or efficiency of water utilization
will be most important in altering community and
ecosystem properties (Melillo et al. 1993; Brown et al.
1997; Smith et al. 2000). It is therefore likely that desert
plant community responses to accelerated N deposition,
such as changes in productivity, stability and invasibility,
will strongly depend on the relative availability of water
and other nutrients. Multiple interacting resources
limit the growth and distribution of A. parryi at our
Mojave Desert site. We predict that similar interactions
between multiple limiting resources may be instrumental in shaping community and species distributions
along other abiotic stress gradients and are potentially
important in defining ecotonal areas between major communities in resource-poor ecosystems.

© 2004 British
Ecological Society,
Journal of Ecology,
93, 113–126
Our results are consistent with current models that
predict optimal allocation will balance resource supply
and plant demand, resulting in multiple resource
limitations (Bloom et al. 1985; Gleeson & Tilman 1992;
Gleeson & Good 2003; Ho et al. 2004). A hierarchy of
limiting resources, with N limitations producing the
largest growth responses and P and Mg limitations producing equivalent, substantially smaller, growth responses,
was apparent. A large N response, as reflected in both
significant plant growth and increases in leaf : fine root
biomass, is not surprising given the high demand and
acquisition costs of N and extremely low N concentrations in desert soils.
Supplementary material
The following material is available from
http://www.blackwellpublishing.com/products/
journals/suppmat/JEC/JEC948/JEC948sm.htm
Appendix S1 Experiment 2 treatment effects on Atriplex
parryi leaf and fine root nutrient concentrations and
nutrient cation molar ratios.
Appendix S2 Experiment 2 treatment effects of water,
N, P and Mg addition (source) on Atriplex parryi shoot
mass, leaf elemental concentrations and leaf cation
molar ratios.
125
Multiple resource
limitations in
deserts
Acknowledgements
We thank R. Batha, S. Blazej, A. Breen, M. Caird, R.
O’Dell, N. Parchman, and J. Pfeiff for help with field
and laboratory work and R. Drenovsky, L. Jackson
and T. Young for manuscript review. This research was
supported by the CA State Lands Commission (C99017),
The Los Angeles Department of Water and Power, and
NSF grant IBN-99–03004. Additional support was
provided by the CA-AES.
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© 2004 British
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Journal of Ecology,
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Received 4 July 2004
revision accepted 20 September 2004
Handling Editor: Paul Adam