Ecology, 91(7), 2010, pp. 2141–2150� 2010 by the Ecological Society of America
Spatial niches and coexistence: testing theory with tarweeds
SUSAN HARRISON, HOWARD CORNELL,1 AND KARA A. MOORE
Department of Environmental Science and Policy, University of California, Davis, California USA 95616
Abstract. Competitive coexistence in a spatially heterogeneous environment is tradition-ally attributed to niche differences, but several recent theories have proposed importantadditional roles for propagule limitation and chance (e.g., neutral theory, stochastic nichetheory, spatial storage effect). We tested whether propagule supply and timing of disturbanceaffected the coexistence of three ecologically similar plants that replace one another withpartial overlap along a local soil gradient. We asked what prevents the species that dominatesthe most common habitat (Holocarpha virgata, open hillsides) from invading the habitatswhere the other two species are dominant (Calycadenia pauciflora, rocky hilltops; Hemizoniacongesta, clay-rich bottomlands). We added abundant Holocarpha seeds into Calycadenia andHemizonia habitats that were experimentally disturbed at different times of year. InitialHolocarpha seedling densities in Calycadenia and Hemizonia habitats equaled or exceededthose in unmanipulatedHolocarpha habitat, butHolocarpha survival, adult size, and fecunditywere much lower outside its own habitat. Holocarpha persisted in Calycadenia and Hemizoniahabitats for three years, and springtime disturbance promoted this expansion. However,outside its own habitat Holocarpha showed below-replacement fitness and little competitiveeffect on the other two species. Our results were most consistent with a deterministic view ofspatial niches. Nonetheless, chance events may often cause natural communities to includesome transient populations at any given time, leading them to appear ‘‘unsaturated’’ withspecies.
Key words: Calycadenia pauciflora; competition; disturbance; Hemizonia congesta; Holocarphavirgata; Hutchinsonian niche; neutral theory; seed addition; serpentine; spatial storage effect; stochasticniche; tarweed.
INTRODUCTION
Spatial heterogeneity in the environment clearly
affects competitive coexistence and community assem-
bly, but the precise mechanisms and their larger
implications are debated. In traditional Hutchinsonian
theory, species coexist because they cannot compete
successfully in one another’s niches. In some cases niche
differentiation is spatial, such as when each competitor is
more effective at acquiring the same limiting resource(s)
under a slightly different set of biotic or abiotic
conditions that vary among localities (Amarasekare
2003). Distinct spatial niches lead to the apparent
paradox of competitors that ‘‘coexist’’ at the regional
or metacommunity scale, within which the environment
is heterogeneous, by virtue of being relatively segregated
at the scale of more homogeneous local sites (Levine and
Rees 2002, Amarasekare 2003, Levine and Murrell 2003,
Tilman 2004, Gravel et al. 2006, Kadmon and Allouche
2007). In communities where spatial niche differentiation
is an important mechanism of coexistence, species
composition varies predictably along continuous gradi-
ents of biotic or abiotic conditions that affect relative
competitive abilities (Chave 2004, Tilman 2004). One
weakness of the niche-based perspective, however, is its
failure to address the random or contingent aspects of
community structure. For example, the openness of
many communities to new species has been demonstrated
by seed addition experiments (Tilman 1997, Zobel et al.
2000, Munzbergova 2004, Ehrlen et al. 2006; but see
Turnbull et al. 2000, Wilsey and Polley 2003), linear
local–regional richness relationships (Harrison and
Cornell 2008), and positive native–exotic richness
correlations (Davies et al. 2005, 2007, Sax and Gaines
2008, Stohlgren et al. 2008), evidence that argues against
an overly deterministic view of competitive communities.
Neutral theory (Hubbell 1997) represents an opposite
extreme, in which nonequilibrial coexistence arises from
competitive equality, no niche differences exist, and any
spatial patterning in community composition arises only
from chance and dispersal limitation. Neutral theory is
compatible with the evidence for stochastic aspects of
community structure, and highlights the importance of
random processes in community assembly. However, a
purely neutral perspective is not consistent with the
ubiquitous correlations that are observed between
community composition, species traits, and environ-
mental gradients (Chave 2004, Tilman 2004). In an
attempt to reconcile the niche-based and neutral
viewpoints, Tilman (2004) proposed stochastic niche
Manuscript received 29 April 2009; revised 25 September2009; accepted 19 October 2009. Corresponding Editor: J.Weiner.
1 Corresponding author. E-mail: [email protected]
2141
theory, in which random processes interact with spatial
heterogeneity and niche differences to shape communi-
ties. According to this theory, competition occurs
primarily at recruitment, whereas established adults
are relatively resistant to competitive exclusion. Niche
expansion and community enrichment are possible when
propagule arrival coincides with disturbances that create
pulses of unused resources. Although community
composition should still vary somewhat predictably
along environmental gradients, it is more affected by
chance processes than in the traditional view.
The spatial storage effect (Chesson 2000) has also been
proposed as a general theory of competition in spatially
heterogeneous environments that incorporates niches,
propagule limitation, and stochastic effects. In this
model, spatial heterogeneity permits competitors to
coexist when, first, each species has higher fitness than
the other(s) in some portion of the environment, and
second, each species is most strongly self-limited through
intraspecific competition in the environment where it has
the highest fitness. The second condition is required
because this model implicitly assumes that the most
successful competitor in a widespread habitat (i.e., the
species with the highest overall fitness in the landscape)
could otherwise export unlimited propagules into the
nearby habitats of other species, which would overcome
these species’ local fitness advantages and cause it to
become competitively dominant everywhere. Self-limita-
tion of propagule production by each species within its
optimal habitat is thus necessary for coexistence.
While many empirical studies have demonstrated the
existence of propagule limitation, few have tested
specific theories for how it interacts with spatial
environmental heterogeneity to determine niche bound-
aries, coexistence, and/or the structure of natural
communities (Turnbull et al. 2000, Levine and Murrell
2003, Vandvik and Goldberg 2005). Using common
elements of the neutral, stochastic niche, and spatial
storage effect theories as a conceptual foundation, we
examined coexistence in three ecologically similar
annual tarweeds (Asteraceae, subtribe Madiinae; Carl-
quist et al. 2003) whose distributions are spatially
segregated with partial overlap across a heterogeneous
5003 550-m grassland study site (as well as elsewhere in
the region). Holocarpha virgata is dominant in the most
common habitat, open hillsides, while Calycadenia
pauciflora is most abundant on rocky hilltops, and
Hemizonia congesta is most abundant in clay-rich
bottomlands. We assume that these species are potential
competitors and that their partial segregation contrib-
utes to their coexistence within this heterogeneous
environment. Thus, to better understand their coexis-
tence at this larger scale, we asked what conditions
would allow the widespread Holocarpha to invade and/
or outcompete Calycadenia and Hemizonia within their
more specialized local habitats.
All three theories predict that the arrival of large
numbers of propagules should, at least under some
circumstances, permit Holocarpha to invade and persist
in Calycadenia and Hemizonia habitats. Under stochas-
tic niche theory, an additional prediction is that
propagule arrival must coincide with a pulse of limiting
resources, such as might be provided by an appropri-
ately timed disturbance. Under the spatial storage effect
model, we expect that relaxing dispersal limitation
through experimental propagule addition should allow
Holocarpha not only to persist in Calycadenia and
Hemizonia habitats, but to outcompete these species
within their own habitats (note that this is an underlying
assumption, rather than an explicit prediction, of the
spatial storage effect model). Under neutral theory,
which seems unlikely a priori given the apparent
correlations of these species distributions with environ-
mental gradients, an additional prediction is that
Holocarpha will not only persist in Calycadenia and
Hemizonia habitats but will show equal fitness in all
three habitats. In contrast, under a traditional view of
the spatial niche, even a large influx of propagules will
not allow Holocarpha to invade and persist in Calyca-
denia or Hemizonia habitats, either because it cannot
tolerate the abiotic conditions (fundamental niche) or
because it is competitively inferior in these habitats
(realized niche).
We emphasize that the neutral, stochastic niche, and
spatial storage effect theories are not mutually exclusive,
and that our study is not intended as a definitive test of
all of the assumptions or predictions of any of them,
which would require quantification of model parame-
ters. Our primary focus is on testing the shared
qualitative assumption made by all three of these
theories (as well as others) that relaxation of propagule
limitation can lead to broadening of the spatial niche.
Secondarily, by testing additional predictions of each of
the theories, our goal is to identify the most promising
conceptual framework for better understanding the
controls over spatial distributions in this system.
We used a one-time Holocarpha propagule addition
into Hemizonia and Calycadenia habitats, with and
without disturbance, followed by 3.5 years of observa-
tion of the growth, survival, and recruitment of
transplants and natural controls. As our principal
measure of Holocarpha success under different treat-
ments, we used an index of population-level fitness
(number of mature plants times mean flowers per plant).
We also examined individual fitness components and
yearly population replacement rates.
METHODS
Study system
Our study site at the Donald and Sylvia McLaughlin
University of California Reserve is a heterogeneous
mosaic of vegetation including grasslands, oak wood-
lands, and chaparral (available online).2 The site
2 hhttp://nrs.ucdavis.edu/McL/index.htmli
SUSAN HARRISON ET AL.2142 Ecology, Vol. 91, No. 7
comprises a complex of rocks and soils that includes
serpentine, which is relatively infertile because of low
primary nutrients and Ca, low water availability, and
excess Mg (Alexander et al. 2006). The Ca:Mg ratio is
often considered an indicator of the harshness of
serpentine soils, with ratios �1.0 representing the
harshest soils (Kruckeberg 1984, Harrison 1999). At
our study site, grasslands on shallow rocky serpentine
soils with low Ca:Mg are low in biomass and rich in
native forbs, while those on deeper soils or those with
higher Ca:Mg are dominated by exotic annual grasses
and forbs (Harrison 1999, Davies et al. 2005, Elmendorf
and Moore 2007).
Tarweeds (Madiinae) are a tribe within the Asteraceae
that diversified greatly in the California Floristic
Province and that share a distinctive set of traits,
including resinous glandular foliage, late-summer flow-
ering phenology, and deep roots (Carlquist et al. 2003).
At our study site, as well as elsewhere in California,
tarweeds are among the latest-flowering species (and
often the only abundant native late-flowering species)
within grasslands that are otherwise dominated by
winter-germinating annual grasses and vernal annual
forbs.
Three tarweeds are found at our study site in
grasslands where the soil is partly or completely formed
from serpentine. The most abundant is Holocarpha
virgata, which is widespread on open hillsides and is
sometimes considered a rangeland pest (Perrier et al.
1981, 1982). The others are Calycadenia pauciflora,
which is found on rocky hilltops and is a serpentine
endemic, and Hemizonia congesta, which is found in
clay-rich bottomlands. They flower late in the growing
season (July–September), forming nearly monospecific
stands at a time when few species other than sparse
perennials (e.g., Nassella pulchra, Poaceae and Eriogo-
num nudum, Polygonaceae) are still active. Both
Holocarpha and Hemizonia are known to have the
capacity for multi-year seed dormancy (Perrier et al.
1981, 1982, Gulmon et al. 1983); seed dormancy in
Calycadenia has not been studied. The tarweeds appear
to replace one another, sometimes at sharp boundaries,
along a soil gradient from rocky serpentine hilltops
through hillsides to bottomlands (see Plate 1). Where the
serpentine soil influence ends, Holocarpha and Hemi-
zonia often give way to the exotic yellow starthistle
(Centaurea solstitialis, Asteraceae), which has a similar
late-flowering phenology.
Observational data
To identify niche differences among the three
tarweeds, we used observational data from Davies et
al. (2005; see also Moore and Elmendorf 2006,
Elmendorf and Moore 2007). In a 0.33-km2 area
selected for its substantial heterogeneity, a grid of 132
sampling sites spaced 50 m apart was established in
2000. At each sampling site, presence or absence of all
vascular plant species was recorded annually in four 1-
m2 quadrats from 2001 to 2003. In 2001, one value of
mean soil depth and one bulked soil sample were taken
from each site; samples were analyzed for soil chemistry
at A and L Western Laboratories (Modesto, California,
USA). For our present analyses, we used only the 81
sampling points located in open grassland, excluding the
51 points that were shaded either by dense chaparral or
oak canopy.
Based on previous studies and our observations, we
predicted that soil depth, texture, and Ca:Mg ratio
would distinguish the sites occupied by the three tarweed
species. Specifically, we expected Holocarpha habitats to
be intermediate between the habitats of Calycadenia
(shallow soils, low clay content, low Ca:Mg) and
Hemizonia (deep soils, high clay content, high Ca:Mg).
Of a large suite of other available soil variables,
including NO3-N, NH4-N, Bray-P, cation exchange
capacity, and pH, none had significant predictive power
in this study or others using the same study sites and soil
data (Davies et al. 2005, Moore and Elmendorf 2006,
Elmendorf and Moore 2007; S. Harrison, unpublished
data).
We first used Pearson’s chi-square tests of association
to determine whether occurrences of each pair of the
three tarweeds were significantly negatively associated
with each other. We then used multivariate analysis of
variance (MANOVA) to test for significant differences
in soil depth, percentage clay, and Ca:Mg among the
sites occupied by each species. Replicates were the
occurrence of each species at each site, and species was
the sole independent variable. Separate univariate
ANOVAs were then used to test for differences among
species for each environmental factor. Analyses were
performed in JMP version 5.1 (SAS Institute 2004).
Field experiment
To test whether propagule arrival and/or appropri-
ately timed disturbance would permit Holocarpha to
invade and persist in Calycadenia and Hemizonia
habitats, we conducted a field experiment from fall
2005 to spring 2009. Within the same area studied by
Davies et al. (2005), we established 10 experimental sites
in Calycadenia stands, 10 experimental sites in Hemi-
zonia stands, and 20 natural control sites in Holocarpha
stands. Sites were chosen haphazardly within stands of
relatively uniform and high density of each species, with
the three types of sites well interspersed spatially. At
each of the 40 sites we established one 1 3 2-m plot
comprising eight 0.5 3 0.5-m subplots. At the 20
experimental sites we randomly assigned the eight 0.5
3 0.5-m subplots to two levels of propagule addition
(control, addition) crossed with four levels of distur-
bance (control, fall clearing, fallþ early spring clearing,
fall þ late spring clearing).
The four levels of the disturbance treatment were
designed to ensure that disturbance occurred at what-
ever time it is most effective at promoting Holocarpha
invasion into its competitors’ habitats; we had no
July 2010 2143SPATIAL NICHES AND COEXISTENCE
specific a priori hypothesis about which time of
disturbance would be the most effective. We combined
fall (preemergence) clearing with early and late spring
(postemergence) clearing to ensure that enough Holo-
carpha seedlings would emerge at the beginning of the
experiment (spring 2006) to make further data collection
possible. Fall clearing consisted of clipping and remov-
ing all biomass, which was mostly dead annual grasses,
to within 1 cm of the soil (8 September 2005). Spring
clearing consisted of carefully clipping and removing all
live biomass except forHolocarpha; most of this biomass
was live vernal annuals in the early spring (16 April
2006), and senescing vernal annuals plus live juvenile
tarweeds in the late spring (24 May 2006). Biomass of
vernal annuals consisted predominantly of exotic annual
grasses (e.g., Avena fatua, Bromus hordeaceus, Taenia-
therum caput-medusae).
The propagule addition treatment was designed to
ensure that initial recruitment of Holocarpha in Calyca-
denia and Hemizonia habitats was at least as high as in
its own habitat, to allow an adequate test of treatment
effects. We collected Holocarpha seeds and added them
to the experimental plots by harvesting flower heads
from adjacent Holocarpha stands at a time when seeds
were ripe but had not dropped (27 September 2005). We
added all seed-containing flower heads from 1 3 1 m of
dense Holocarpha to each 503 50-cm experimental plot,
thus producing a seed density approximately four times
higher than a high natural seed rain.
We counted Holocarpha seedlings in March 2006 and
adults in August 2006 in each experimental subplot in
Calycadenia and Hemizonia habitat and in each of four
randomly chosen subplots of the natural control plots
within Holocarpha habitat. In August, we also randomly
chose three Holocarpha adults from each subplot and
measured their heights and numbers of flowers, and
counted and weighed seeds from 10 flowers per plant. In
2007–2009 we again counted seedlings in March. In 2007
and 2008 we again counted and measured adults in
August, and also counted and measured competitor
(Calycadenia and Hemizonia) adults in August (which
we could not do in 2006 because they had been removed
from the disturbed subplots).
Data analyses
To determine the effects of propagule addition and
disturbance on the performance of Holocarpha in
Calycadenia and Hemizonia habitats, we analyzed the
2006 experimental data using a split-plot ANOVA. An
index of population-level fitness (number of adult
Holocarpha 3 mean number of flowers/plant) was the
dependent variable, and disturbance treatment, habitat
(Calycadenia or Hemizonia), and treatment by habitat
interaction were the independent variables.
The performance of Holocarpha was further analyzed
with two additional split-plot ANOVAs using emer-
gence (number of seedlings) and survival (ratio of adult
plants to seedlings) as dependent variables, and the same
independent variables as the population-level fitness
analysis. We could not combine these into a singleanalysis because lack of emergence in some subplots led
to unequal sample sizes (e.g., it is not meaningful tomeasure seedling survival in a plot with no seedlings).
Also, too few plants survived in some treatments toallow a comparison of flowers per plant or othermeasures of adult plant size.
To compare the performance ofHolocarpha in its ownhabitat vs. in Calycadenia and Hemizonia habitats, we
analyzed data from the 20 natural control plots vs. the20 experimental plots in 2006. We used a simple
ANOVA with population-level fitness as the dependentvariable, and habitat (Holocarpha, Calycadenia, or
Hemizonia) as the independent variable.To decompose this second analysis into its demo-
graphic components, we used simple ANOVAs withemergence (numbers of seedlings) and survival (ratio of
adults to seedlings) as dependent variables, and habitat(Holocarpha, Calycadenia, or Hemizonia) as the inde-
pendent variable. We used a simple MANOVA to testthe effect of habitat on measures of plant size (height,
flower number, seeds per flower, seed mass).To determine the persistence of the effects of
disturbance, habitat, and propagule addition, we re-peated the analyses of Holocarpha performance using
the 2007 and 2008 data. We also calculated populationgrowth rate (k2007¼ seedlings 2007/seedlings 2006, k2008
¼ seedlings 2008/seedlings 2007, k2009 ¼ seedlings 2009/
seedlings 2008) as a way to compare populationtrajectories in the three habitats.
To test for competitive effects of introduced Holo-carpha on resident Calycadenia and Hemizonia in 2007
and 2008, we used a simple ANOVA with population-level fitness of the latter two species as the dependent
variable, and population-level fitness of Holocarpha, aswell as its interaction with habitat (Calycadenia or
Hemizonia) as the independent variables.
RESULTS
Observational data
The distributions of the three species overlapped atthe scale of presence or absence in sampling sites (i.e.,
clusters of four 1-m2 quadrats distributed at 50-mintervals across the grassland portion of the 0.33-km2
study area); Holocarpha was present in 45% of samplingsites containing Calycadenia and 32% of sites containing
Hemizonia. Chi-square tests found a significant negativeassociation between Holocarpha and Hemizonia at this
scale (v281 ¼ 0.0246, P ¼ 0.0237), while Calycadenia was
not significantly associated with eitherHolocarpha (v281¼
0.1619, P ¼ 0.1237) or Hemizonia (v281 ¼ 0.0943, P ¼
0.1059).
Soils in quadrats occupied by the three target speciesdiffered significantly in the predicted directions, with
clay content increasing from Calycadenia to Holocarphato Hemizonia sites; also, soil depths were greater inHemizonia sites than Holocarpha or Calycadenia sites
SUSAN HARRISON ET AL.2144 Ecology, Vol. 91, No. 7
(Table 1). Mean soil Ca:Mg ratios also differed in the
predicted direction, with the lowest values (i.e., most
serpentine influence) in Calycadenia sites, but this
difference was not significant.
Effects of experimental disturbance and propagule
addition on Holocarpha success in Calycadenia
and Hemizonia habitats
Throughout the experiment, Holocarpha abundance
was close to zero in subplots in Calycadenia and
Hemizonia habitats to which no Holocarpha seeds were
added, so these control subplots were not used in any
analyses.
Population-level fitness of Holocarpha introduced into
Calycadenia and Hemizonia habitats was significantly
affected by disturbance and habitat in 2006 (Fig. 1).
Fitness was highest in the fall þ early spring clearing
treatment and in Calycadenia habitat, and no interaction
between the habitat effect and the disturbance effect.
This disturbance effect was significant in 2007 but not
2008, while the habitat effect remained significant in
both years (Table 2).
Considering individual fitness components, seedling
emergence in 2006 was not significantly affected by
disturbance or by the interaction between disturbance
and habitat (ANOVA, P . 0.10 for all effects), although
there was marginally higher (P ¼ 0.08) emergence in
Calycadenia than Hemizonia habitat. Survival from
seedling to adult was improved by fall þ early spring
clearing and was higher in Calycadenia than Hemizonia
habitat, with no interaction between these effects
(Tables 3 and 4).
Holocarpha performance in its own habitat vs.
in Calycadenia and Hemizonia habitats
Population-level fitness of Holocarpha in 2006 was
significantly higher in the natural controls in Holocarpha
habitat than in the experimental plots with Holocarpha
seed addition in either Calycadenia or Hemizonia
habitats (Fig. 2; ANOVA, F ¼ 40.1, df ¼ 2, 157, P ,
0.0001; Fisher’s least significant difference test, P ,
0.0001 for comparisons of natural controls and the other
two habitats).
TABLE 1. Site conditions (mean with SE in parentheses) for the three focal species of tarweeds(Asteraceae) at 81 observation sites within the study area at the Donald and Sylvia McLaughlinUC Reserve, California, USA.
Dependentvariable
Holocarpha Hemizonia CalycadeniaF2, 108 P(n ¼ 64) (n ¼ 33) (n ¼ 14)
Ca:Mg 0.99 (0.13) 1.05 (0.27) 0.50 (0.11) 0.0203 0.3372Clay (%) 29.83a (1.58) 35.87b (2.19) 19.43c (1.96) 0.1699 0.0002�Soil depth (cm) 31.23
a(2.36) 41.39
b(3.40) 25.16
a(4.50) 0.0875 0.0108�
Note: Overall variation among site type was significant in a MANOVA (Pillai’s trace F6, 214 ¼4.0383, P¼ 0.0007).
� Rows in boldface highlight factors showing significant variation (P � 0.01) in univariateANOVA models comparing species; pairwise differences are indicated by different superscriptletters.
FIG. 1. Competitive relationships among three ecologicallysimilar annual tarweeds (Asteraceae) on a soil gradient in theDonald and Sylvia McLaughlin University of CaliforniaReserve, showing effects of experimental disturbance atdifferent times of the year on population-level fitness (meanwith 95% CI; number of plants 3 mean flowers/plant) ofHolocarpha planted in Calycadenia and Hemizonia habitat in2006. Different letters above bars indicate significant differencesamong habitats (P , 0.05).
TABLE 2. Effects of experimental disturbance and habitat(Calycadenia or Hemizonia) on population-level fitness ofHolocarpha.
Source SS df F P
2006
Habitat 36.9 1 6.5 0.02Disturbance 20.2 3 6.7 0.03Habitat 3 disturbance 7.9 3 1.3 0.29Plot(habitat) 102.9 18Disturbance 3 plot(habitat) 109.1 54
2007
Habitat 54.8 1 11.7 0.003Disturbance 15.7 3 4.1 0.01Habitat 3 disturbance 7.8 3 2.0 0.12Plot(habitat) 84.4 18Disturbance 3 plot(habitat) 69.4 54
2008
Habitat 65.1 1 18.8 0.0004Disturbance 3.6 3 1.1 0.39Habitat 3 disturbance 3.9 3 1.2 0.35Plot(habitat) 62.4 18Disturbance 3 plot(habitat) 61.2 54
Notes: Sources are from a split-plot ANOVA. Populationfitness is measured as number of plants 3 mean flowers/plant.
July 2010 2145SPATIAL NICHES AND COEXISTENCE
This difference remained significant when comparing
natural controls to just the fall þ early spring distur-
bance plots which exhibited the highest fitness
(ANOVA, F¼ 5.8, df¼ 2, 97, P , 0.005). The difference
between natural and experimental plots remained
significant in 2007 and 2008 (2007, F ¼ 99.7, df ¼ 2,
128; 2008, F ¼ 36.9, df ¼ 2, 96).
Considering individual fitness components, initial
seedling emergence in 2006 was higher in Calycadenia
habitat than in Hemizonia habitat or natural controls,
with no significant difference between the latter two
(Fig. 3; ANOVA, F ¼ 13.7, df ¼ 2, 158, P ¼ 0.0001;
Fisher’s least significant difference test, P , 0.0001 for
comparisons of Calycadenia habitat and the other two
habitats). Survival from seedling to adult was lower in
Hemizonia habitat than in either Calycadenia habitat or
natural controls, with no significant difference between
the latter two (ANOVA, F ¼ 17.2, df ¼ 2, 124, P ¼0.0001; Fisher’s least significant difference test, P ,
0.0001 for comparisons of Hemizonia habitat and the
other two habitats).
All measures of plant size (height, flowers per plant,
seeds per flower, seed mass) were significantly higher in
natural controls than in Calycadenia or Hemizonia
habitats in 2006 (Fig. 4; MANOVA, Pillai’s trace ¼1.7, F ¼ 31.4, df ¼ 412, 303, P , 0.0001, followed by
univariate F tests, all P , 0.0001). The height and flower
number differences remained significant in 2007 (MAN-
OVA, Pillai’s trace ¼ 1.4, F ¼ 80.6, df ¼ 6, 256, P ,
0.0001) and 2008 (MANOVA, Pillai’s trace ¼ 1.5, F ¼128.6, df ¼ 6, 192, P , 0.0001); we did not repeat the
seed number or seed mass measurements in 2007 or
2008.
Long-term persistence of Holocarpha in Calycadenia
and Hemizonia habitats
During the first year following establishment, Holo-
carpha populations increased significantly in the natural
controls (k2007 ¼ seedlings 2007/seedlings 2006 . 1.0),
but decreased significantly in the other two habitats
(k2007 , 1.0; one-sample t tests, P , 0.001). Populationsize change (k2007) was not significantly affected by the
2005 disturbance treatments (ANOVA, N¼ 80 subplots,
F ¼ 0.68, df ¼ 3, 54, P ¼ 0.41). Population size changewas significantly higher in natural controls than in
Calycadenia habitat, and in Calycadenia habitat than
Hemizonia habitat (Fig. 5; ANOVA, N¼ 155, F¼ 30.0,
df ¼ 2, 152, P ¼ 0.0001; Fisher’s least significantdifference test, P ¼ 0.0001 for natural controls vs.
Calycadenia habitat and P ¼ 0.035 for Calycadenia vs.
Hemizonia habitats).
In the second post-establishment year, populationsdeclined significantly in all habitats (k2008 ¼ seedlings
2008/seedlings 2007 , 1.0; one-sample t tests, P ,
0.001). Population change (k2008) was again unaffectedby the 2005 disturbance treatments (ANOVA, N¼ 45, F
¼ 0.055, df ¼ 3, 37, P ¼ 0.39) and was not significantly
different among the three habitats (Fig. 5; ANOVA, N¼124, F ¼ 1.634, df ¼ 2, 121, P ¼ 0.51). Sample sizes arelower than for the first post-establishment year because
populations in some subplots (mainly Calycadenia and
Hemizonia subplots) went permanently extinct.
In the third post-establishment year, populationsincreased significantly in the natural controls (k2009 ¼seedlings 2009/seedlings 2008 . 1.0; one-sample t test, P
, 0.001), and again decreased in Calycadenia andHemizonia habitats, but not significantly so (k2009 ,
1.0; one-sample t tests, P . 0.264 and 0.173, respective-
ly). Population change was significantly higher in
natural controls than in Calycadenia and Hemizonia
TABLE 3. Effects of experimental disturbance and habitat(Calycadenia or Hemizonia) on survival of Holocarpha, 2006.
Source SS df F P
Habitat 4.0 1 15.6 0.0009Disturbance 1.8 3 5.5 0.002Habitat 3 disturbance 0.1 3 0.2 0.87Plot(habitat) 4.6 18Disturbance 3 plot(habitat) 5.9 54
Notes: Sources are from a split-plot ANOVA. Survival ismeasured as number of adults/number of seedlings.
FIG. 2. Population-level fitness (mean with 95% CI; numberof plants 3 mean flowers/plant) of Holocarpha in naturalcontrols in Holocarpha habitat vs. in experimental plots inCalycadenia and Hemizonia habitat in 2006. Different lettersabove bars indicate significant differences among habitats (P ,0.05). For simplicity, all disturbance treatments are combinedhere and in Figs. 3–5.
TABLE 4. Pairwise contrasts of disturbance treatment using Fisher’s LSD test.
Season ofdisturbance
Control Fall Fall þ early spring
Meandifference Probability
Meandifference Probability
Meandifference Probability
Fall �0.09 0.52Fall þ early spring 0.28 0.04 0.37 0.01Fall þ late spring �0.08 0.58 0.01 0.92 �0.36 0.01
SUSAN HARRISON ET AL.2146 Ecology, Vol. 91, No. 7
habitat but was not different between the latter two (Fig.
5; ANOVA, N¼ 113, F¼ 13.94, df¼ 2, 110, P¼ 0.0001;
Fisher’s least significant difference test, P ¼ 0.0001 for
natural controls vs. Calycadenia and Hemizonia habitat
and P ¼ 0.73 for Calycadenia vs. Hemizonia habitats).
Population change (k2009) was again unaffected by the
2005 disturbance treatments (ANOVA, N ¼ 36, F ¼0.397, df¼ 6, 29, P¼ 0.88). Sample sizes are again lower
than for the first and second post-establishment years
because additional populations in some Calycadenia and
Hemizonia subplots went permanently extinct.
Frequencies of Holocarpha seedlings in experimental
Calycadenia plots declined from 100% in 2006 to 98%,
68%, and 70% in 2007–2009, respectively; frequencies of
Holocarpha seedlings in experimental Hemizonia plots
changed from 100% in 2006 to 14%, 10%, and 18% in
2007–2009, respectively.
Competitive effects of Holocarpha on Calycadenia
and Hemizonia
In 2007, there was no evidence for an effect of the
population-level fitness of Holocarpha on the popula-
tion-level fitness of its two competitors, or vice versa
(ANOVA, P ¼ 0.79), and no significant interaction
between the effects of Holocarpha and species (Calyca-
denia vs. Hemizonia). However, a trend toward compe-
tition was suggested by negative correlations between
the numbers of Holocarpha and the mean heights and
flower numbers of its competitors (Pearson r ¼�0.31,�0.33), as well as between the number of Holocarpha
and the mean heights and flower numbers of Holocarpha
(Pearson r ¼�0.24,�0.20).In 2008, there was a significant positive association
between the population-level fitness of Holocarpha and
those of its competitors (ANOVA, F¼19.1, df¼51, 1, P
,0.0001), with no significant interaction between the
effects of Holocarpha and species (Calycadenia vs.
Hemizonia). Numbers of Holocarpha and the mean
heights and flower numbers of its competitors were less
negatively correlated than in 2007 (Pearson r ¼ �0.01
and�0.19, respectively), and the numbers of Holocarpha
and the numbers of its competitors were positively
correlated (Pearson r ¼ 0.44). Negative correlations
persisted between the numbers of Holocarpha and the
mean heights and flower numbers of Holocarpha
(Pearson r ¼�0.22, �0.34).
DISCUSSION
Species occurrence and environmental data supported
our initial observations that the three tarweed species
have different although partly overlapping spatial
niches. Distributions of the two more common species,
Holocarpha and Hemizonia, showed a significant nega-
tive association with one another at the scale of four 1-
FIG. 3. Number of Holocarpha seedlings emerging (meanwith 95% CI) per 0.25-m2 subplot in natural controls inHolocarpha habitat vs. in experimental subplots (approximatelyequal numbers of seeds added in all experimental seed additionsubplots) in Calycadenia and Hemizonia habitat in 2006.Different letters above bars indicate significant differencesamong habitats (P , 0.05).
FIG. 4. Height, number of flowers/plant, number of seeds/flower, and seed mass (mean with 95% CI) of Holocarpha innatural controls in Holocarpha habitat vs. in experimentalplots in Calycadenia or Hemizonia habitat in 2006. Differentletters above bars indicate significant differences amonghabitats (P , 0.05).
July 2010 2147SPATIAL NICHES AND COEXISTENCE
m2 sampling units spaced 50 m apart. The distribution
of the less common species, Calycadenia, was not
significantly negatively associated with those of the
other two species, perhaps because of its small number
of occurrences (N¼ 14). However, soil differences were
found to separate Calycadenia, Holocarpha, and Hemi-
zonia sites. As we expected, soil texture and depth are
key indicators that differentiate the habitats of the three
species along the gradient from rocky hilltops to
bottomlands.
Consistent with recent theories emphasizing the role
of propagule limitation within a spatially heterogeneous
environment, we found that the addition of a large
quantity of seeds allowed Holocarpha virgata to
establish and persist for several generations in habitats
dominated by its competitors Calycadenia pauciflora and
Hemizonia congesta. Consistent with stochastic niche
theory (Tilman 2004), in particular, the ability of
Holocarpha to establish in Calycadenia and Hemizonia
habitats depended on appropriately timed disturbance.
In both of these habitats, the critical disturbance was the
removal of competing vernal annual plants in early
spring when Holocarpha seedlings were small, whereas
there was little effect of removal of either dead biomass
in the fall, or senescing vernal annuals plus live summer-
flowering annuals in the late spring. Under the
framework of stochastic niche theory, these results
suggest that in undisturbed Calycadenia and Hemizonia
habitats, established vernal annuals play a key role in
preventing enough resources from being available to
allow seedlings of Holocarpha to reach maturity. Also
consistent with this theory, the ability of Holocarpha to
establish in these two habitats appeared to be facilitated
by its attainment of reproductive maturity at very small
sizes (Fig. 4).
While the effect of early spring disturbance on
Holocarpha establishment was significant in both
Calycadenia and Hemizonia habitats, there was a trend
toward a weaker effect in rocky, unproductive Calyca-
denia habitat than in more productiveHemizonia habitat
(Fig. 1). These results support the idea that stochastic
aboveground disturbance plays a greater role in
facilitating community enrichment in productive than
unproductive environments, an idea that has received
previous experimental support in the same grasslands
(Elmendorf and Moore 2007) as well as others (e.g.,
Foster 2001).
Our results suggest that coexistence among these
species is not well explained by the spatial storage effect
model (Chesson 2000), in which the dominant compet-
itor in the most common habitat can outcompete all
other species if the propagule limitation imposed by
intraspecific competition within its optimal habitat is
relaxed. We found that, although an abundant propa-
gule influx did allow Holocarpha to establish in
Calycadenia and Hemizonia habitats, there was no
evidence that it suppressed the abundances of either
species. This is not surprising, given that Holocarpha
individuals were considerably smaller at maturity in
Calycadenia and Hemizonia habitats than in Holocarpha
habitat (Fig. 4). For our system, then, only the first
condition of the spatial storage effect model (distinct
spatial niches) appears to be required for coexistence;
the second condition (self-limitation of the dominant
competitor within the optimal habitat) appears not to be
necessary. The spatial storage effect model assumes that
spatial environmental heterogeneity affects the relative
fitnesses of competing species but does not change their
per capita competitive effects on one another (e.g., the
aij’s of the Lotka-Volterra model). However, per capita
competitive effects for plants may depend on relative
plant sizes (Weiner 1985), and thus it may be common
for a species to be a strong competitor in its optimal
habitat where it is large, but a weak one in suboptimal
habitats where it is smaller.
As we expected, the results were inconsistent with
neutral theory (Hubbell 1997) because niche differences
among the three species are clearly present. Despite its
ability to invade and persist in Calycadenia and Hemi-
zonia habitats when seeds were added, Holocarpha was
not very successful in these habitats. The rates of
population replacement were ,1.0 in both a good year
(2006–2007) when the natural Holocarpha population
grew, and a bad year (2007–2008) when the natural
population declined. This evidence for strong spatial
niche differences is reinforced by the lower rates of
survival, growth, and reproduction we found for
Holocarpha in Calycadenia and Hemizonia habitats
compared with its own habitat, and by the significant
differences in soils among the habitats occupied by the
three species.
Holocarpha appears to be excluded from its compet-
itors’ habitats primarily by abiotic factors because its
performance in these habitats was low even when
competitors were excluded, but also by diffuse compe-
FIG. 5. Interannual rate of population change (k, meanwith 95% CI) for Holocarpha in natural controls in Holocarphahabitat (N ¼ 80), vs. in experimental plots in Calycadenia orHemizonia habitat (N ¼ 40 for each): k2007 ¼ seedlings 2007/seedlings 2006, k2008 ¼ seedlings 2008/seedlings 2007; k2009 ¼seedlings 2009/seedlings 2008. Confidence intervals crossing thedashed line indicate changes not significantly different fromstasis (k¼ 1). Different letters above bars indicate significantlydifferent changes among habitats (P , 0.05).
SUSAN HARRISON ET AL.2148 Ecology, Vol. 91, No. 7
tition because its performance in these habitats was even
lower when competitors were present. The apparent
inability of Holocarpha to persist in the habitats
dominated by the other two species appears more
consistent with the traditional Hutchinsonian niche
concept than with any of the more recent theories we
examined. Competitive outcomes and community as-
sembly in this system appear to be largely deterministic
in space and time. Based on these results, we would
expect the distributions of the three tarweeds to remain
fairly constant, although with minor changes over time
due to random dispersal events and recurring distur-
bances such as gopher activity and grazing. These results
are consistent with reviews by Turnbull et al. (2000) and
Levine and Murrell (2003), suggesting that altering the
seed rain within realistic bounds often has little long-
term effect on community composition. Our results also
support the prediction by Chave (2004) that community
structure will be relatively predictable in cases where a
small number of abundant species interact in an
environment with strong spatial heterogeneity.
We conclude that there is a strong case for a
deterministic view of competitive coexistence in het-
erogeneous environments. Nonetheless, our results
also have some implications for the stochastic aspects
of community assembly. The experimental populations
of our annual study species will likely persist for a few
more years (generations), with this period of transient
persistence facilitated by their capacity for long-term
seed dormancy. In communities where disturbance and
propagule movement are frequent and established
individuals are long-lived, species richness may be
enhanced for long periods of time by transients such as
our experimental Holocarpha populations. This pre-
sents a possible explanation for the paradox of
community unsaturation (Tilman 2004, Harrison and
Cornell 2008, Stohlgren et al. 2008): why are native
species absent from communities and yet able to
persist when they are added? A species may be
excluded from a community by its long-term inability
to replace itself, but may still, if added, contribute to
that community’s diversity for an ecologically mean-
ingful length of time.
PLATE 1. Tarweed habitat at the Donald and Sylvia McLaughlin University of California Reserve. Calycadenia paucifloradominates the rocky hilltop, Holocarpha virgata the hillside, and Hemizonia congesta the bottomland in the foreground. Photocredit: S. Harrison.
July 2010 2149SPATIAL NICHES AND COEXISTENCE
ACKNOWLEDGMENTS
For helpful discussions and manuscript comments, we aregrateful to P. Amarasekare, B. Anacker, J. Baty, P. Chesson, K.Davies, S. Elmendorf, J. Levine, B. Melbourne, and S. Veloz.For use of the Grid data we thank B. Inouye and K. Davies.For logistical support we thank the Donald and SylviaMcLaughlin University of California Natural Reserve.
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