, 640 (2007); 315
K. B. Suttle,
to Changing Climate
Species Interactions Reverse Grassland Responses
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Species Interactions Reverse
Grassland Responses to
K. B. Suttle,1*† Meredith A. Thomsen,2Mary E. Power1
Predictions of ecological response to climate change are based largely on direct climatic effects on
species. We show that, in a California grassland, species interactions strongly influence responses
to changing climate, overturning direct climatic effects within 5 years. We manipulated the
seasonality and intensity of rainfall over large, replicate plots in accordance with projections of
leading climate models and examined responses across several trophic levels. Changes in seasonal
water availability had pronounced effects on individual species, but as precipitation regimes were
sustained across years, feedbacks and species interactions overrode autecological responses to
water and reversed community trajectories. Conditions that sharply increased production and
diversity through 2 years caused simplification of the food web and deep reductions in consumer
abundance after 5 years. Changes in these natural grassland communities suggest a prominent role
for species interactions in ecosystem response to climate change.
toward higher elevations (3, 4), phenological
events advance in time (5–7), and some species
disappear altogether (8). With further climate
change still expected, prediction of future im-
pacts has become critical to conservation plan-
ning and management. To forecast ecological
change under continued climate warming, how-
mpacts of recent climate change on plants
ic distributions shift poleward (1, 2) and
ever, we need a better understanding of the
relative importance of direct responses by indi-
vidual species to climate versus responses medi-
ated by changing interactions with resources,
competitors, pathogens, or consumers (9–14). We
imposed projected future precipitation regimes
over grassland in northern California to evaluate
the importance to ecosystem response of direct
effects on grassland species versus indirect ef-
fects arising from species interactions.
Much of the California coastal region ex-
periences a Mediterranean climate, characterized
by wet winters and long summer droughts. Eco-
logical responses to climate change in regions
with Mediterranean climate regimes may be
strongly driven by the redistribution of water in
time and space (15). Changes in seasonal water
availability that affect plant phenology, for ex-
ample, could lead to temporal mismatch between
resource availability and consumer demand (16),
which can have important effects on resource
flow and ecosystem function (17). General cir-
culation models developed at the Hadley Centre
for Climate Prediction and Research (HadCM2)
and the Canadian Centre for Climate Modeling
and Analysis (CCM1) (18) predict substantial
increases in precipitation over most of California
but differ in the projected seasonality of these
increases. The Hadley model calls for all addi-
tional rain to fall during the current winter rainy
season, whereas the Canadian model projects
increased rainfall extending into the current sum-
mer drought. The discrepancy between the two
scenarios may be critical to the fate of grass-
land ecosystems in California, where summer
drought severely constrains plant growth and
the timing of rainfall is more important to an-
nual production and species composition than
the amount (19–22).
In 2001, we began a large-scale rainfall ma-
nipulation in a northern California grassland to
regimes for production and diversity ofgrassland
plants and invertebrates. In a grassland at the
California (39° 44' 17.7″ N, 123° 37' 48.4″ W),
18 circular 70-m2plots were subjected to one of
three watering treatments: a winter addition of
water (January through March), a spring addi-
tion of water (April through June), and an
unmanipulated ambient control (Fig. 1). Each
watered plot received about 44 cm of sup-
plementary water over ambient rainfall per year,
roughly a 20% increase over mean annual pre-
cipitation but within natural variability in both
amount and timing at the study site (fig. S1). We
1Department of Integrative Biology, University of Califor-
nia, Berkeley, CA 94720, USA.
University of Wisconsin, La Crosse, WI 54601, USA.
*Present address: Earth and Planetary Science, University
of California, Berkeley, CA 94720, USA.
†To whom correspondence should be addressed. E-mail:
2Department of Biology,
Fig. 1. (A) Bird’s-eye view of experimental communities in July 2002. A
nearby road is visible as a gray strip, top right. Research described here
is from 18 open-grassland plots (18 additional plots were used in sep-
arate research). (B) Schematic representation of an experimental plot,
shown as partitioned for measurement of plant biomass (30 900-cm2
subplots, small squares), plant species richness (two 2500-cm2subplots,
large squares), foliar and flying invertebrates (two perpendicular
sweep-net transects, dashed arrows), and ground-dwelling invertebrates
(two pitfall traps, circles) (not to scale). Detailed methods are available
2 FEBRUARY 2007VOL 315
on February 10, 2007
examined treatment effects on plant produc-
tion and species composition over 5 consecutive
years and quantified responses of invertebrate
herbivores and their natural enemies over 3
Effects of increased rainfall depended criti-
cally on the seasonality of the increase. Supple-
mental water addition during the wet winter
period produced moderate increases in plant
production in some years of the study (Fig. 2),
but effects did not extend to higher trophic
levels (Figs. 3 and 4). In general, communities
in winter-addition and ambient rainfall plots re-
sponded similarly across years to annual vari-
ation in rainfall.
Extending the rainy season via spring water
addition produced much more dramatic changes
in the grassland community. Plant production
more than tripled in the first year and more than
doubled in the second compared with the control
(Fig. 2A). The strongest initial response was by
nitrogen-fixing forbs, whose production in-
creased by nearly two orders of magnitude with
extended spring rainfall (Fig. 2B). Exotic annual
grasses showed a weaker response to the first
year of spring water addition, but after the
proliferation of nitrogen-fixing forbs that year,
annual grass production rose dramatically (Fig.
2C). These grasses, so-called winter annuals
because they are the first plants to germinate
each year and are among the earliest to complete
their life cycle and senesce, generally do not
respond to extensions of the rainy season be-
yond April (22, 24). Early phenology thus lim-
ited the direct response of annual grasses to
extended rainfall but allowed these plants to
benefit in the subsequent growing season from
a fertilization effect after decomposition of abun-
dant N-fixer litter (25–27). As this process
was repeated year after year, the accumulation
of annual grass litter suppressed germination
and regrowth of leafy forbs (Fig. 2D), as has
often been seen in California annual grasslands
(26, 28–30), and drove steep declines in plant
species richness (Fig. 3A).
Shifts in plant composition in spring-addition
plots had important consequences for bio-
diversity and food web structure. Initially, ex-
tended rainfall promoted increased plant species
richness (Fig. 3A), and this increase, coupled
with greater primary production and water avail-
ability, supported greater diversity and abun-
dance of invertebrate herbivores, predators, and
parasitoids (Figs. 3B and 4). As forbs were
eliminated from spring-addition plots by annual
grasses, however, plant species richness col-
lapsed to nearly half that in control plots. With
inating the resource base, food availability and
habitat quality for higher trophic levels dimin-
ished. This was especially true during summer,
when late-blooming forbs provide a critical food
resource for invertebrate herbivores (fig. S2). In
contrast, annual grass litter has low nutritional
value, and monocultures of these plants offer
less structural complexity than mixed grass-
By the fifth year of the study, when heavy
rains continued into summer in a naturally ex-
tended rainy season throughout northern Califor-
nia, spring-additionplots stood out as islands of
low biodiversity and reduced consumer abun-
50% reduction in plant species richness in
spring-addition relative to control plots, in-
vertebrate richness was 20% lower, and herbi-
vore and predator abundanceswere each nearly
50% lower than ambient values measured in
control plots. This simplification of the grass-
land community did not result from climatic
conditions that were inherently unfavorable to
level benefited strongly from experimental ex-
tension of the rainy season in spring-addition
plots early in the study, just as they did from a
natural extension of the rainy season in winter-
altered environmental conditions persisted across
years, individualistic responses by species to
climate were overshadowedby the lagged effects
gruence between initial responses to artificial
extension in spring-addition plots and responses
in the grassland as a whole to naturally late rain-
fall in year 5 provides compelling evidence that
these mechanisms are real rather than experi-
al climate models; indeed, the next-generation
Hadley model (HadCM3) forecasts decreased
rainfall over much of California (31). Yet under
any scenario of future climate change, prediction
web of interactions that mediate species- through
ecosystem-level responses (14). To date, forecasts
of range shifts and extinction probabilities are
based largely on species-climate envelope models
(32–34). These models are powerful initial tools
Fig. 2. Watering treatment effects on (A) total plant biomass and (B to D) biomass of individual plant groups (note difference in scales). Data represent
treatment means ± 1 SE. An asterisk denotesa statisticallysignificant treatment differenceafterBonferroni correction formultiple comparisons. See tableS1
for factor significance.
Fig. 3. Watering treatment effects on (A) plant species richness and (B) invertebrate family
richness. Data represent treatment means ± 1 SE. Gray shading highlights the year that late
natural rainfall mirrored the spring-addition watering treatment. See tables S2 and S3 for
taxonomic listings of plant species and invertebrate families, respectively.
VOL 3152 FEBRUARY 2007
on February 10, 2007
with which to explore consequences of alter-
native climate scenarios, but they cannot fore-
cast lagged impacts of altered higher-order
interactions that will govern the trajectories of
ecosystems under sustained climatic change.
Nonlinearities are expected from the assembly
of new combinations of species brought to-
gether by climate-induced range shifts, but
these can also arise from environmental effects
on the strength and direction of interspecific
interactions without any change in species com-
position (35, 36). The nature and scales of these
effects are best revealed by long-term experi-
ments in natural field settings that improve un-
derstanding of how climate change impacts
propagate through ecological communities.
Indirect effects of climate on species will com-
monly lag behind direct effects, but their impor-
tance makes system-level interactions crucial to
climate change forecasting even at subdecadal
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Supporting Online Material
Materials and Methods
Figs. S1 and S2
Tables S1 to S3
17 October 2006; accepted 13 December 2006
An X Chromosome Gene, WTX,
Is Commonly Inactivated in
Miguel N. Rivera,1,2,3Woo Jae Kim,1Julie Wells,1David R. Driscoll,1Brian W. Brannigan,1
Moonjoo Han,2James C. Kim,2Andrew P. Feinberg,4William L. Gerald,5Sara O. Vargas,6
Lynda Chin,7A. John Iafrate,2Daphne W. Bell,1* Daniel A. Haber1†
Wilms tumor is a pediatric kidney cancer associated with inactivation of the WT1 tumor-suppressor
gene in 5 to 10% of cases. Using a high-resolution screen for DNA copy-number alterations in
Wilms tumor, we identified somatic deletions targeting a previously uncharacterized gene on the X
chromosome. This gene, which we call WTX, is inactivated in approximately one-third of Wilms
tumors (15 of 51 tumors). Tumors with mutations in WTX lack WT1 mutations, and both genes share
a restricted temporal and spatial expression pattern in normal renal precursors. In contrast to
biallelic inactivation of autosomal tumor-suppressor genes, WTX is inactivated by a monoallelic
“single-hit” event targeting the single X chromosome in tumors from males and the active X
chromosome in tumors from females.
precursors that produce undifferentiated blaste-
ilms tumor (nephroblastoma) is the
most common pediatric kidney cancer
and is derived from pluripotent renal
mal components [reviewed in (1)]. In 1972,
Knudson and Strong proposed that Wilms
tumor, like retinoblastoma, may develop as a
consequence of two independent rate-limiting
genetic events, subsequently defined as biallelic
Fig. 4. Watering treat-
ment effects on abun-
dances (mean ± SE) of
(A) invertebrate herbi-
vores, (B) predators, and
(C) parasitoids, as mea-
sured in sweep net and
pitfall trap collections.
Gray shading highlights
responses in the final
year of the study, when
late natural rainfall mir-
rored the spring-addition
2 FEBRUARY 2007VOL 315
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