Download resurveying Robert H. Whittaker`s Siskiyou sites (Oregon, USA)

Ecology, 91(12), 2010, pp. 3609–3619
Ó 2010 by the Ecological Society of America
Climate change effects on an endemic-rich edaphic flora:
resurveying Robert H. Whittaker’s Siskiyou sites (Oregon, USA)
ELLEN I. DAMSCHEN,1,4 SUSAN HARRISON,2
AND
JAMES B. GRACE3
1
Department of Biology, Washington University, St. Louis, Missouri 63130 USA
Department of Environmental Science and Policy, University of California, Davis, California 95616 USA
3
U.S. Geological Survey, National Wetlands Research Center, 700 Cajundome Boulevard, Lafayette, Louisiana 70506 USA
2
Abstract. Species with relatively narrow niches, such as plants restricted (endemic) to
particular soils, may be especially vulnerable to extinction under a changing climate due to the
enhanced difficulty they face in migrating to suitable new sites. To test for community-level
effects of climate change, and to compare such effects in a highly endemic-rich flora on
unproductive serpentine soils vs. the flora of normal (diorite) soils, in 2007 we resampled as
closely as possible 108 sites originally studied by ecologist Robert H. Whittaker from 1949 to
1951 in the Siskiyou Mountains of southern Oregon, USA. We found sharp declines in herb
cover and richness on both serpentine and diorite soils. Declines were strongest in species of
northern biogeographic affinity, species endemic to the region (in serpentine communities
only), and species endemic to serpentine soils. Consistent with climatic warming, herb
communities have shifted from 1949–1951 to 2007 to more closely resemble communities
found on xeric (warm, dry) south-facing slopes. The changes found in the Siskiyou herb flora
suggest that biotas rich in narrowly distributed endemics may be particularly susceptible to the
effects of a warming climate.
Key words: biodiversity; biogeographic affinity; climate change; edaphic; endemism; gradients; plant
community; Robert H. Whittaker; serpentine; soil type; species distribution; topography.
INTRODUCTION
Earlier budburst and flowering (Menzel et al. 2006),
upward shifts of montane floras (Beckage et al. 2008,
Kelly and Goulden 2008, Lenoir et al. 2008) and faunas
(Moritz et al. 2008), and local extinctions of populations
at low elevations and latitudes (Parmesan et al. 1999,
Parmesan and Yohe 2003) testify to the ever-growing
evidence for biotic impacts of global warming. Forecasts
of biotic change over the coming decades, derived by
modeling current vs. future climatic envelopes of species,
predict many global extinctions and dramatic reorganizations of natural communities (Thomas et al. 2004,
Schwartz et al. 2006, Loarie et al. 2008). Yet one aspect
of these forecasts may make them too optimistic: they
assume that even without any dispersal species will at
least survive in the geographic areas of overlap between
their present and future climatic envelopes. However,
this ignores other niche requirements that must be met in
addition to climatic suitability. For example, plants
confined to patchy outcrops of special soils such as
serpentine or limestone might be expected to have far
lower chances of successful migration to suitable sites
than plants that are soil generalists (Van de Ven et al.
Manuscript received 12 June 2009; revised 17 March 2010;
accepted 7 April 2010. Corresponding Editor: K. D. Woods.
4 Present address: Department of Zoology, Birge Hall,
University of Wisconsin, Madison, Wisconsin 53706 USA.
E-mail: [email protected]
2007). Extinction risks may be just as high in these
‘‘edaphic island’’ endemics as in the better-known case
of species confined to mountaintop ‘‘islands’’ (e.g.,
Pounds et al. 1999, Raxworthy et al. 2008).
Few studies have examined the sensitivity of specialsoil floras to human-induced climate change or other
widespread environmental alterations (but see Grime et
al. 2000, 2008). Yet global biological diversity is greatly
enhanced by edaphic endemics, such as the rich floras of
limestone grasslands in southern Europe, dolomite
glades in the Ozarks, shale barrens in Appalachia, or
serpentine outcrops in the Mediterranean, Cuba, New
Caledonia, and California (Anderson et al. 1999,
Kruckeberg 2005). In California, one of the world’s
botanical diversity hotspots (Myers et al. 2000, Stein et
al. 2000), 612 of 1742 rare plants are associated with
serpentine, limestone, volcanic outcrops, vernal pools,
or other special substrates (Skinner and Pavlik 1994),
and plants restricted to serpentine comprise .10% of
species unique to the state even though serpentine is
,2% of its area (Kruckeberg 2005, Safford et al. 2005).
Edaphic endemic plants have also been important
subjects for evolutionary studies (Brady et al. 2005).
Despite their naturally fragmented distributions, there
are several possible reasons for optimism about the
future of special-soil floras. One is that many of them are
found in zones of mountain uplift (Anderson et al. 1999,
Kruckeberg 2005), offering the hope of survival through
local shifts in elevation or from south- to north-facing
slopes (Loarie et al. 2009). Also, edaphic endemic species
3609
3610
ELLEN I. DAMSCHEN ET AL.
may have suites of traits that render them relatively
resistant to climate change (Grime et al. 2000, 2008,
Theurillat and Guisan 2001). For example, greater
drought tolerance in serpentine endemics is suggested
by their often xeromorphic (small, thick, hairy) leaves,
as well as some experimental evidence (Brady et al.
2005). In general, it may be that edaphic endemics
tolerate nutrient-poor or excessively cation-rich (‘‘toxic’’) soils at the expense of having low maximal growth
rates even when resources are abundant. Thus, some
studies have suggested that floras on special soils will be
less sensitive to altered temperature and water availability than those of more fertile soils (Grime et al. 2000,
2008, Theurillat and Guisan 2001). Also, other studies
suggest that climate change may cause species to alter
their habitat specificity through either ecological or
evolutionary processes (Thomas et al. 2001, Davies et al.
2006); for example, species may become less restricted to
serpentine in harsher, less-productive climates (Harrison
et al. 2009).
We tested the relative sensitivity of an edaphic
endemic flora to climate change by resampling vegetation in the Siskiyou Mountains of southern Oregon and
northern California at sites studied by ecologist Robert
Whittaker from 1949 to 1951 (Whittaker 1960). Within
a region of extraordinary plant diversity and endemism,
Whittaker measured the effects of topography and soil
parent material on plant community composition.
Climatic warming has since been documented throughout the Pacific Northwest (Mote et al. 2003), including
in Whittaker’s study region (;28C increase in mean
summer temperatures from 1948 to 2007 in Medford,
Oregon; NOAA 2009; see Appendix A). By resampling
his sites 57 years later we can ask, first, whether
community composition has shifted in the direction
expected under a warming climate, second, whether the
rich endemic flora on serpentine soil has been more or
less susceptible to such a shift than the flora of normal
soils; and third, whether local topography has provided
a refuge for plant species in the face of climate change.
METHODS
Study system
The Klamath-Siskiyou Mountains (California and
Oregon, USA) are one of North America’s most
significant hotspots of plant diversity and endemism,
whose 3500 plant species include 131 species endemic to
the region and ;700 close to their northern or southern
range limits (Ricketts et al. 1999, Myers et al. 2000).
Exceptional botanical richness in this region has been
attributed to several factors: high topographic and
geologic complexity; a central location between the
Pacific Northwestern, Californian, and interior floras;
and a consistently favorable climate that has permitted
survival of plants from the mild and wet Tertiary
(Axelrod 1958, Whittaker 1960, Coleman and Kruckeberg 1999).
Ecology, Vol. 91, No. 12
The region includes North America’s largest exposure of serpentine or ultramafic (extremely high Mg
and Fe) rock. The large area, great age (.50 million
years), high rainfall, and topographic complexity of its
ultramafic rocks combine to make it the continent’s
leading location for edaphic endemism; of 246 plant
taxa confined to serpentine in California, 97 are found
here (Coleman and Kruckeberg 1999, Safford et al.
2005, Alexander et al. 2006, Harrison et al. 2006).
From 400 to 700 m, serpentine soils support open
woodland with Jeffrey pine (Pinus jeffreyi ), incense
cedar (Calocedrus decurrens), and a rich herb understory. From 700 to 1200 m, there is a denser coniferous
overstory (e.g., Douglas-fir, Pseudotsuga menziesii,
western white pine, Pinus monticola) and a shrubby
understory (e.g., huckleberry oak, Quercus vaccinifolia;
shrub tanoak, Lithocarpus densiflorus var. echioides)
(Whittaker 1960).
Other substrates represented in Whittaker’s study
included diorite, a sialic (high Si ) igneous rock similar to
granite, and gabbro, a mafic (moderately high Mg and
Fe) igneous rock with chemistry intermediate between
diorite and serpentine. From 500 to 1200 m, diorite soils
support typical vegetation for the region: closed forest
dominated by Douglas-fir with scattered ponderosa pine
(Pinus ponderosa), sugar pine (Pinus lambertiana), and
broadleaved evergreens (tanoak; madrone, Arbutus
menziesii; canyon live oak, Quercus chrysolepis); white
fir (Abies concolor) increases in abundance with elevation (Whittaker 1960).
Much of Whittaker’s study area was logged in the
1960s–1980s (Jules et al. 2008), but in our study we
avoided logged sites. Other recent human impacts on the
region’s vegetation include fire suppression since the
early 20th century (Agee 1991, Skinner 1995). None of
our sites were grazed by livestock, and exotic species
were infrequent (see Results).
Historic data collection
Whittaker quantified plant communities along three
gradients: elevation, soil type, and the local variation
from cool north-facing to warm south-facing slopes
that he called the ‘‘topographic moisture gradient’’
(TMG): a semi-quantitative spectrum from 1 to 10,
where low values indicate communities on cool or
‘‘mesic’’ sites (e.g., mild to moderate north-facing
slopes), and high values indicate communities on warm
or ‘‘xeric’’ sites (e.g., steep south-facing slopes). He
considered the TMG to be a product of multiple
factors, including wind exposure, soil depth and
chemistry, temperature, and moisture, and believed it
could best be quantified using vegetation data. In the
absence of computers, he sought simple methods to
ordinate community samples along this gradient. His
did this by subjectively choosing plots and assigning
them to positions on the 10-point TMG scale, sampling
their vegetation, and then using the frequencies of
indicator species to refine the assignment of plots to
December 2010
ENDEMIC-RICH FLORA AND CLIMATE CHANGE
positions on the 10-point scale (Whittaker 1960).
Sometimes, for unknown reasons, he used gradient
lengths other than 10 (range 6–11). Also, he sometimes
assigned multiple gradient scores to a single site. We
standardized his topographic moisture scores to a
gradient of 0–1 and averaged these to arrive at a single
TMG score for each site. We found that these scores
were correlated (r ¼ 0.51, P , 0.001) with estimated
January insolation for each site, a function of slope and
aspect (McCune 2007). As sites range from TMG
scores of 0 to 1, some species (Whittaker’s ‘‘mesic
indicators’’) consistently decrease and others (his ‘‘xeric
indicators’’) consistently increase in abundance (Appendix B).
Whittaker collected data from 290 plots on diorite
soils, 55 plots on serpentine, and 51 plots on gabbro soils
from June–August 1949–1951 (hereafter, 1950). Within
each soil, he chose at least five plots representing each
point on his 10-point scale, where a score of 1 was very
mesic (usually along a ravine with flowing water), scores
of 2–4 were progressively less mesic (usually north and
northeast-facing or not very steep), 5–6 were intermediate (e.g., northwest or southeast slopes), and 7–10
were more xeric (e.g., a 10 being a steep south or
southwest slope). On diorite, he repeated this arrangement for each of several elevational bands between 500
and 2000 m. He chose relatively homogeneous tree
stands, avoided obvious disturbances and openings, and
sampled near roads and trails for efficiency (Whittaker
1960, Westman and Peet 1982).
At each plot, Whittaker laid out a 50-m tape, usually
in the upslope direction, along which he established 25
1 3 1 m quadrats on at alternate 1-m intervals. In each
quadrat, he counted stems of each species and recorded
the species intercepted by each quadrat corner. By
summing for each species how many of the 25 quadrat
corners it intercepted, he obtained an estimate of percent
cover for that species in that plot (25 quadrats 3 4
corners ¼ 100). Within the whole 50 3 20 m plot centered
on the tape, he counted tree individuals by diameter at
breast height (dbh) classes and species, and shrub
individuals by species. He does not appear to have
marked, mapped, or returned to these plots (Whittaker
1960; R. H. Whittaker, unpublished data).
His data are in the Cornell University Library,
Division of Rare and Manuscript Collections. Each plot
is described by a plot number, substrate, road or trail,
elevation, slope and aspect (e.g., 268, serpentine, Wimer
Rd., 2400 0 , E 258). The precision was 308 of aspect (i.e.,
ENE, WSW) and 30.5 m (100 feet) of elevation. Data
for each plot include: numbers of herb individuals by
species, percent cover of herbs by species (both of these
from summing across the 25 1-m2 quadrats), and
numbers of shrub and tree individuals in the 50 3 20
m plot by species. Data on individual quadrats are
absent. He deposited voucher specimens in the Ownbey
Herbarium at Washington State University, Pullman,
Washington, USA.
3611
Present-day data collection
We entered Whittaker’s data into a database with
herb count, herb cover, and shrub and tree counts, each
by species and plot number. We updated species names
using the Jepson Interchange (available online).5
The severe Biscuit Fire of 2002 burned Whittaker’s
entire gabbro study area at York Butte in the
Kalmiopsis Wilderness, but very little of his serpentine
study areas at Eight Dollar Mountain, Josephine
Mountain, Tennessee Pass, Rough and Ready Creek,
and Wimer Road, and none of his diorite sites.
However, most of his diorite sites on the Siskiyou
National Forest were logged beginning in 1952. In the
vicinities of Grayback Campground, Caves Creek
Campground, Caves Highway, and Oregon Caves
National Monument, we were able to find 53 unlogged
Whittaker diorite sites at elevations comparable to those
of his 55 serpentine sites (i.e., 400–1200 m).
To locate sample plots as close as possible to
Whittaker’s (e.g., his plot number 268), we followed
the same road or trail on the same substrate (e.g., Wimer
Road, serpentine), stopped at the same elevation (e.g.,
2400 0 or 702 m), and found the nearest place with the
same slope and aspect (e.g., 258 E), using a global
positioning system (GPS), topographic maps, and
clinometer. Like Whittaker, we avoided disturbances
and openings. While the lack of exact plot locations
undoubtably adds some random error/uncertainty to
data comparisons, we feel our method for establishing
resampling plots is free of bias.
In May–June 2007, we sampled 55 plots representing
all of Whittaker’s serpentine plots, from 410–1140 m
elevation. In June–August 2007, we sampled 53 plots
representing a subset of Whittaker’s diorite plots that
were chosen because they were not logged and matched
the serpentine plots in elevation (500–1200 m), so that
elevational differences would not confound the substrate
difference. We followed Whittaker’s sampling methods
exactly, except that we revisited our sites approximately
one month later to look for new herb species. For the
purposes of this paper, we use the herb percent cover
data obtained from the corners of the 25 quadrats and
the shrub and tree counts from the 20 3 50 m plot
(described above) because these methods are all repeatable by multiple observers.
To reconcile identity questions, we examined Whittaker’s voucher specimens at the Ownbey Herbarium in
November 2007. For additional conservatism, we used
only those species found by both Whittaker and us and
eliminated unidentified morphospecies. Because Whittaker recorded grass cover as ‘‘unknown grass,’’ but later
identified the grass species present in each plot, we
eliminated grass species from analyses dependent on
species identity, but retained them for analyses comparing responses of groups (i.e., life forms).
5
hucjeps.berkeley.edu/interchange.htmli
3612
ELLEN I. DAMSCHEN ET AL.
Species traits
To compare changes in different groups of species, we
classified species as belonging to families or genera of
northern (Arcto-Tertiary) or southern (Madro-Tertiary,
California Floristic Province, or desert) biogeographic
affinities, using Raven and Axelrod (1978); see Harrison
and Grace [2007] and Ackerly [2003, 2009] for a full
discussion of these categories). We also classified species
as being either at or not at their northern and southern
range limits in the Klamath-Siskiyou region using the
USDA Plants Database (USDA 2008). (For this
purpose, we defined the Klamath-Siskiyou region as
Josephine, Jackson, and Curry Counties, Oregon, and
Del Norte, Siskiyou, Humboldt, Trinity, and Shasta
Counties, California.) Serpentine endemism was evaluated using the criteria of Safford et al. (2005); based on a
literature review, endemics were defined as species with
scores of 4.5 on a 6-point scale. Change in widespread
species (those without southern or northern range limits
in our study region) was compared to changes in species
near their latitudinal range limits on both soil types. On
serpentine soils, we compared the change in serpentine
endemics (species with serpentine scores 4.5) to soil
generalists (species with serpentine scores ,4.5). Note
that we were unable to classify grasses because
Whittaker lumped all grass species into a single group.
A list of all study species and their traits can be found in
Appendix C.
Analyses
In order to test our predictions by comparing groups
of species with particular traits, we performed two sets
of analyses for each comparison of interest. First, we
used a nonparametric PERMANOVA (Anderson 2001)
with the summed relative cover values of species in the
different trait groups as multiple response variables.
Year, soil type, and their interactions were included as
fixed effects and plot identity as a random effect. We
used Euclidean distance measures on log-transformed
data. Other transformations and distance measures
yielded similar results. We followed significant multivariate non-parametric analyses with univariate models
in order to evaluate directionality of responses and
differences in the degree of change among species groups
and soil types. In this case, species trait categories were
used as a predictor variable in addition to year, soil type
(fixed effects), and plot identity (random effect).
PERMANOVAs were performed with Primer v. 6 with
PERMANOVAþ (Clarke and Gorley 2006). SAS
version 9.1.3 (SAS Institute 2007) was used for the
univariate models. Detailed descriptions of statistical
models and their results are presented in Appendix D.
For comparisons of forbs and grasses, raw percent
cover per plot was used as the response variable of
interest. For the univariate model, we used a generalized
linear mixed model with a Poisson distribution and log
link function. For comparisons of species with northern
vs. southern biogeographic affinties, species with their
Ecology, Vol. 91, No. 12
range limits in our study region vs. widespread species,
and serpentine endemics vs. generalist species, we used
relative percent cover as our response variable of
interest. In these cases, our univariate models were
generalized linear mixed models with binomial distributions and logit link functions.
To assess whether species richness changed over time
and if soil type altered the degree of change, we used a
generalized linear mixed model with a Poisson distribution and log link function. Because Whittaker did not
identify grasses to species, we analyzed only the species
richness of forbs with year, soil type, and their
interaction (fixed effects) and plot location (random
effect) as predictor variables.
To test whether species composition had changed over
time to more strongly resemble the species composition
of warm south-facing sites we performed ordinations
using PC-ORD v. 4.14 (McCune and Mefford 1999). We
ordinated the herb and tree communities separately. We
did not ordinate the shrub data because Whittaker did
not count individuals of three shrubs he described as
being among the most common on serpentine (Garrya
buxifolia, Lithocarpus densiflorus var. echioides, and
Quercus vaccinifolia), recording them only as present
or absent. We also used separate ordinations for the
strongly differing communities on serpentine and diorite
soils, but we combined the 1950 and 2007 data in each
ordination.
We ordinated sites with non-metric multidimensional
(NMS) ordination (McCune and Grace 2002), excluding
those species found in less than 5% of samples. NMS is a
computationally intensive technique that searches iteratively for the best position of n entities with p attributes
on k axes that minimizes ‘‘stress,’’ defined as deviation
from monotonicity in the relationship between dissimilarity of entities in the original p-dimensional space and
in the reduced k-dimensional space. We used the
autopilot mode in PCOrd to search for the optimal
dimension reduction (two to six dimensions) using 200
iterations of the analysis. Autopilot mode is an
algorithm in PC-ORD that assists in choosing the best
solution in each dimensionality and testing for significance; all options are set automatically (maximum
number of iterations, instability criterion, starting
number of axes, number of real runs, number of
randomized runs), except for the distance metric, which
must be selected by the user (McCune and Mefford
1999, McCune and Grace 2002). Significance was
evaluated by comparing stress reduction to that found
in a random matrix using Monte Carlo permutation
tests.
We rotated Axis 1 of each ordination to maximize its
correlation with Whittaker’s topographic moisture
gradient, and tested for significant differences in mean
Axis 1 scores between sites in 1950 and sites in 2007
using both conventional test procedures and Markov
chain Monte Carlo methods (Gelman and Hill 2007). A
positive change in Axis 1 score would indicate that
December 2010
ENDEMIC-RICH FLORA AND CLIMATE CHANGE
3613
FIG. 1. Changes in cover of forbs and grasses. Total percent forb and grass cover per plot decreased over time. Error bars
represent 95% confidence limits. Lowercase letters indicate significant differences (P 0.05) among groups across both panels (A
and B). See Methods and Appendix D for full statistical methods and results.
community composition has changed over time in the
same direction that composition changes over space
from mesic (cooler, moister) to xeric (warmer, drier)
slopes.
To evaluate corresponding changes in shrubs and
trees, we used generalized linear mixed models with a
Poisson distribution and log link function. Soil type and
year were used as fixed effects and plot location as a
random effect. Separate models were run for the number
of shrubs, number of trees, number of hardwood trees,
and number of coniferous trees per plot. For analyses of
hardwood trees, only plots that had hardwood trees
present in one or both time periods were included.
species near their northern latitudinal limits in the study
region on diorite soils and of regional endemics on
serpentine soils also declined (Fig. 5). In contrast, widely
distributed species whose range limits are not in the
Klamath-Siskiyous and species with their southern
latitudinal range limits in the study region showed no
change in relative cover on either soil type (Fig. 5).
Few exotic herb species were found in either time
period (1 in 1950, 7 in 2007), and annual herb species
were also relatively uncommon (12 in 1950 and 17 in
2007). No exotic herbs had cover values of .0% (i.e.,
RESULTS
Changes in species abundance and richness
Total herb cover was sharply lower in 2007 than in
1950 on both diorite and serpentine (Fig. 1). This decline
in herb cover was greater on serpentine than on diorite.
On both soils, the decline in cover was much greater for
forbs than grasses. Mean numbers of herb species at
each site (alpha diversity) likewise declined (Fig. 2),
although the total numbers of herb species at all sites
combined (gamma diversity) did not decline (117 vs. 122
species in 1950 and 2007, respectively). The decline in
species richness was greater on serpentine than diorite
soils.
Relative cover (i.e., the cover by a group divided by
total cover in a plot) of species belonging to taxa of
northern biogeographic affinity declined on both soil
types, while the relative cover of species with southern
biogeographic affinity increased on diorite and showed
no change on serpentine (Fig. 3). Relative cover of
edaphic endemic forbs declined more than generalist
forbs on serpentine soils (Fig. 4). The relative cover of
FIG. 2. Forb species richness per plot decreased over time,
and this decline was smaller on diorite than on serpentine soils.
Lowercase letters indicate significant differences (P 0.05)
among groups. Error bars represent 95% confidence limits. See
Methods and Appendix D for full statistical methods and
results.
3614
ELLEN I. DAMSCHEN ET AL.
Ecology, Vol. 91, No. 12
FIG. 3. Changes in species with northern and southern biogeographic affinities. The relative percent cover out of the total herb
cover per plot for species belonging to taxa of northern biogeographic affinities declined over time on (A) diorite and (B) serpentine
soils, while the relative percent cover of species belonging to higher taxa with southern biogeographic affinities increased on diorite
and did not change on serpentine. Error bars represent 95% confidence limits. Lowercase letters indicate significant differences (P 0.05) among groups across both panels (A) and (B). See Methods and Appendix D for full statistical methods and results.
they were present but never intercepted a quadrat
corner).
On serpentine, the number of shrubs increased and
the number of tree individuals did not change. On
diorite, the numbers of shrub and tree individuals
decreased over time; declines were most evident in
hardwood trees, while coniferous trees increased (Fig.
6). Detailed statistical results for all of these analyses
can be found in Appendix D.
Changes in community composition
All four ordinations (diorite herbs, serpentine herbs,
diorite trees, and serpentine trees) caused significant
reductions in stress within the dissimilarity matrices
compared to randomized data based on Monte Carlo
tests. Minimum stress values obtained were 19.1%,
21.3%, 9.8%, and 12.7%, respectively.
Herb community composition at both diorite and
serpentine sites shifted toward significantly higher Axis 1
scores in 2007 compared to 1950 (Fig. 7A), meaning that
communities in 2007 included greater relative cover by
species characteristic of warm south-facing locations,
and lower relative cover by species characteristic of cool
north-facing locations, than the communities at the
corresponding locations in 1950. This was not true for
trees (Fig. 7B). These results were consistent based on
both conventional frequentist tests and credible intervals
produced using Markov chain Monte Carlo methods
(Gelman and Hill 2007). Ordination plots can be found
in Appendix E.
Such community-level shifts in herbs could arise
because species peak abundances are now found on
cooler slopes than in the past (i.e., sites that are cooler
within any one time period, such as more northerly
slopes), and thus sites are left with arrays of species more
characteristic of warm sites (i.e., sites that are warmer
within any one time period, such as more southerly
slopes). We found evidence for this in diorite herbs, for
which peak abundances (abundance-weighted mean
TMG positions) significantly shifted toward cooler
microsites (TMG score change ¼ 0.10 6 0.04 [mean
6 SE], t1,26 ¼ 2.34, P ¼ 0.027). This shift was generated
predominantly by differential losses of species across
cool and warm sites, as opposed to increases in
abundance on cool sites; overall, 85% of species on
diorite soils decreased in total abundance. On serpentine, the peak distributions for individual species did not
shift along the topographic moisture gradient (abundance-weighted TMG score change ¼0.02 6 0.04, t1,43
¼ 0.52, P ¼ 0.603). Instead, the shift toward ‘‘warmer’’
community composition appears to be associated with
the disproportionate loss of the abundance of forbs
relative to grasses (Fig. 1).
FIG. 4. Changes in serpentine endemics and generalists. The
relative percent cover of species in each plot that are endemic to
serpentine declined over time while generalists did not change
over time. Lowercase letters represent statistically significant
differences (P 0.05) among groups. Error bars represent 95%
confidence limits. See Methods and Appendix D for full
statistical methods and results.
December 2010
ENDEMIC-RICH FLORA AND CLIMATE CHANGE
FIG. 5. Changes in species with range limits in the study
region vs. widespread species. The relative percent cover per
plot of widespread herbs on (A) diorite and (E) serpentine soils
did not change over time. Species with northern range limits in
the study region on (B) diorite soils declined over time but
showed no change on (F) serpentine. Species with their
southern range limits in the study region showed no change
on either (C) diorite or (G) serpentine soils. Regional endemics
did not change on (D) diorite but significantly declined on (H)
serpentine over time. Error bars represent 95% confidence
limits; n.s., not significant. See Methods and Appendix D for
full statistical methods and results.
3615
FIG. 6. Shrub and tree change over time. The number of
shrubs per plot has declined on (A) diorite but has increased on
(E) serpentine. The number of trees per plot on (B) diorite has
decreased over time but has not changed on (F) serpentine.
Hardwood trees have (C) decreased on diorite and (G)
serpentine. Coniferous trees have increased on (D) diorite but
have decreased on (H) serpentine. Error bars represent 95%
confidence limits. See Methods and Appendix D for full
statistical methods and results.
DISCUSSION
Our results indicate that herb communities in the
Klamath-Siskiyous have dramatically declined in overall
abundance and changed in species composition over the
past 57 years. Declines have been strongest in the most
unusual elements of this flora, including species that are
found on serpentine soil and are endemic to the region,
and species that are endemic to serpentine soils.
3616
ELLEN I. DAMSCHEN ET AL.
FIG. 7. Changes in community composition. For the (A)
herb community, differences in Axis 1 ordination scores (i.e.,
the topographic moisture gradient) were calculated by subtracting the 1950 score from the 2007 score. Positive differences
were significantly different from zero on both diorite and
serpentine soils, indicating that communities today are composed of more xeric-associated species than they were in 1950.
For the (B) tree community, there were no significant shifts,
indicating that tree communities have neither become more
mesic nor more xeric over time on either soil type. Medians and
95% percentiles are shown for each soil type.
Climatic warming
Vegetation change in response to climatic warming is
implicated by two aspects of our results. First, as we
expected, declines in herb cover were strong in species
belonging to families and genera of northern (ArctoTertiary) biogeographic origins, and much weaker in
those belonging to families and genera of southern
(Madro-Tertiary) biogeographic origins (Raven and
Axelrod 1978). These two groups have been shown to
have opposing responses to climatic variation over both
time (Valiente-Banuet et al. 2006) and space (Harrison
and Grace 2007, Ackerly 2009). In woody species, it has
been shown that northern-origin taxa are characterized
by broad, thin leaves and other adaptations to cooler
and moister habitats, while southern-origin taxa tend to
show the opposite sets of traits (Ackerly 2003, 2009).
The second source of evidence for climatic warming is
that, again as predicted, the overall shifts in herb
community composition on both serpentine and diorite
Ecology, Vol. 91, No. 12
soils were in the warmer direction along Whittaker’s
topographic moisture gradient. In other words, the herb
species composition of sites in 2007, compared with that
of the corresponding sites in 1950, has changed to more
strongly resemble the species composition of a warm
south-facing slope. Such a shift can arise both from the
differential declines of species characteristic of cool
north-facing slopes (such as the Raven-Axelrod ‘‘northern’’ species), and from losses of populations toward the
warmer ends of species’ local topographic distributions.
The lack of such shifts in trees is not surprising, given
their slower population dynamics, and this lack of
change in trees also suggests that our herb community
results were not caused by biased site selection.
We found declines in species with their northern range
limits in the Klamath-Siskiyou region, and no relative
change in those with southern limits in this region,
contrasting with the expected pattern under a warming
scenario. While we cannot fully explain this result, we
suspect that one contributing factor is the extreme
topography and complex biogeographic history of this
region. When species reach their range limits in this
region, it may be more because of physical barriers or
for other historical reasons than because they reach their
climatic limits within a smoothly varying north-to-south
gradient of temperature and moisture. If this is true, or if
locally adapted climatic ecotypes are prevalent, then
regional range limits will not be good predictors of
climatic tolerances.
Susceptibility of the endemic-rich serpentine flora
vs. normal soils
The community-level shift to a warmer species
composition was just as strong in the herb flora of
serpentine soils as in that of diorite soils. Furthermore,
within the serpentine herb flora, edaphic endemic species
declined more than more widespread species. The one
striking exception was that grasses, which provide a
substantial amount of herb cover on serpentine but not
on diorite, appeared relatively resistant to the changes
that affected other herbs (unfortunately we could not
examine grass responses in detail because we lacked
species-specific information from Whittaker).
Our results appear inconsistent with those of Grime et
al. (2000, 2008), who found lesser sensitivity to
experimental warming and drought in a nutrient-poor
‘ancient’ limestone grassland than a more disturbed and
fertile one, and who concluded that nutrient-poor
ecosystems are secure refuges for biodiversity in the
face of climate change unless they are also subjected to
land-use change. Moreover, our results also contrast
with those of a paleoecological study, in which Briles
(2008) found a lesser degree of centennial-to-millenial
fluctuation in the dominant woody vegetation on
serpentine than granite soils in the Klamath Mountains,
California, USA over the past 15 000 years.
One possible explanation for the discrepancy between
our results and these previous studies is that we
December 2010
ENDEMIC-RICH FLORA AND CLIMATE CHANGE
3617
examined herbaceous understories beneath woody canopies. While canopies are dense and continuous on
diorite soils, they are much more open and patchy on
serpentine, potentially leading to less buffering of
ground surface temperatures on serpentine (consistent
with this, we found greater north-south slope differences
in near-surface temperatures on serpentine than diorite;
E. Damschen and S. Harrison, unpublished data).
Whatever the explanation, our results suggest that
complacency is unwise when considering the future of
special-soil floras under climate change, especially those
that occur on isolated outcrops within narrow elevational ranges.
Topographic shifts are a possible means by which
species can be buffered against climate change and
perhaps survive without long-distance dispersal (e.g.,
Weiss and Weiss 1998, Loarie et al. 2009). However, we
found little evidence of this buffering effect in our study,
since the majority of herb species (38 of 42 on diorite
and 75 of 79 on serpentine) declined in cover on both the
cooler and warmer halves of the topographic gradient.
Our study stands as a warning that there may be a
substantial lag time in species responses, such that even
at the microsite level, declines in unfavorable locations
long precede increases in newly favorable ones.
Other factors contributing to change
Conclusions
Livestock grazing and exotic species do not appear to
be important influences in our study region, and we
avoided logged sites, but fire suppression is another
potential source of vegetation change. Fire has been
excluded from our study areas since the early 1900s,
while return intervals were previously 12–19 years (Agee
1991, Skinner 1995). Our diorite sites might be expected
to be in the canopy closure stage of succession,
characterized by conifer dominance, stable tree abundance, and shady understories (Taylor and Skinner
2003, Odion et al. 2004, Jules et al. 2008). Increased
shading is consistent with some of the changes we
observed, including the decline in hardwoods and
increase in conifers on diorite and the decline in herb
cover on both soils. However, increased shading does
not explain the relative decline in herbs of northern
biogeographic affinity, the community shifts to warmer
species composition, or the shifts of species peak
abundances to cooler topographic positions on diorite.
Thus, our results suggest that the effects of a warming
climate have been strong enough to overcome any
potential ameliorating effect of the shadier conditions
created by fire suppression.
In the woody community on serpentine, shrubs
increased and conifers decreased. We know little about
the possible causes of these changes, though we can
speculate on possible roles for fire suppression and
occasional small-scale harvesting of conifers for timber.
It is also interesting to note that Briles (2008) found
declines in trees (notably Pinus jeffreyi ) and increases in
shrubs (notably Quercus vaccinifolia) on serpentine
during early Holocene warming.
Random variation in rainfall is unlikely to explain the
declines in herb cover we observed. The years that
Whittaker sampled (1950) had 73%, 76%, and 63% of
the 105-year mean of growing-season (February–June)
rainfall, while 2007 had 97% of the mean amount (data
from the National Oceanic and Atmospheric Administration for Grants Pass, Oregon; available online).6
Our study demonstrates a paradox: regions that have
acted as climatic refugia in the past, in part because of
their rugged topography and variety of available
microclimates, may contain a disproportionate number
of narrowly distributed species (Ohlemuller et al. 2008).
Thus, such regions may also show elevated rates of
extinction under rapid modern climatic warming. It also
may be unrealistic to expect lesser changes in stresstolerant species such as our serpentine endemics, since
these species already occur in more abiotically stressful
locations. While managed relocation (i.e., assisted
colonization, assisted migration) remains controversial
(McLachlan et al. 2007, Davidson and Simkanin 2008,
Hoegh-Guldberg et al. 2008, Huang 2008), we suggest
that narrowly distributed edaphic endemics should be
considered high-priority candidates if and when such
intervention is contemplated.
6
hhttp://www.wrcc.dri.edui
The role of topography under global climate change
ACKNOWLEDGMENTS
L. L. Olsvig-Whittaker and the Cornell University Library’s
Division of Rare and Manuscript Collections provided access
to Robert Whittaker’s data. Field and data entry assistance
were provided by M. Brown, T. Elder, K. Fuccillo, C. Garnier,
J. Hansford, T. Hoang, F. Hrusa, M. Jules, A. King, K.
Kostelnik, R. Mack, K. Moore, T. Talty, and K. Torres.
Valuable discussions and manuscript comments were provided
by D. Ackerly, H. Cornell, N. Haddad, E. Jules, D. Levey, D.
Odion, J. Orrock, R. Peet, J. Roth, N. Sanders, M. Schwartz,
A. Storfer, J. Tewksbury, T. Wentworth, and the Damschen
and Harrison Labs. Logistical support was provided by the
Siskiyou Field Institute-Deer Creek Center, Siskiyou National
Forest, Oregon Caves National Monument, and the Marion
Ownbey Herbarium at Washington State University. Funding
was provided by the National Science Foundation DEB0542451, as well as by the USGS Global Climate Change
Program. The use of trade names is for descriptive purposes
only and does not imply endorsement by the U.S. Government.
The funders had no role in study design, data collection and
analysis, decision to publish, or preparation of the manuscript.
LITERATURE CITED
Ackerly, D. D. 2003. Community assembly, niche conservatism,
and adaptive evolution in changing environments. International Journal of Plant Sciences 164:S165–S184.
Ackerly, D. D. 2009. Evolution, origin and age of lineages in
the Californian and Mediterranean floras. Journal of
Biogeography 36:1221–1233.
3618
ELLEN I. DAMSCHEN ET AL.
Agee, J. K. 1991. Fire history along an elevational gradient in
the Siskiyou Mountains, Oregon. Northwest Science 65:188–
199.
Alexander, E. A., R. G. Coleman, T. Keeler-Wolf, and S.
Harrison. 2006. Serpentine geoecology of western North
America. Oxford University Press, Oxford, UK.
Anderson, M. J. 2001. A new method for non-parametric
multivariate analysis of variance. Austral Ecology 26:32–46.
Anderson, R. C., J. S. Fralish, and J. M. Baskin. 1999.
Savannas, barrens and rock outcrop communities of North
America. Cambridge University Press, Cambridge, UK.
Axelrod, D. 1958. Evolution of the Madro-Tertiary geoflora.
Botanical Review 24:433–509.
Beckage, B., B. Osborne, D. G. Gavin, C. Pucko, T. Siccama,
and T. Perkins. 2008. A rapid upward shift of a forest
ecotone during 40 years of warming in the Green Mountains
of Vermont. Proceedings of the National Academy of
Sciences USA 105:4197–4202.
Brady, K. U., A. R. Kruckeberg, and H. D. Bradshaw. 2005.
Evolutionary ecology of plant adaptation to serpentine soils.
Annual Review of Ecology, Evolution, and Systematics 36:
243–266.
Briles, C. E. 2008. Holocene vegetation and fire history from
the floristically diverse Klamath Mountains, northern California, USA. Dissertation. University of Oregon, Eugene,
Oregon, USA.
Clarke, K. R., and R. N. Gorley. 2006. Primer v6 Permanovaþ.
Primer-E Ltd., Plymouth, UK.
Coleman, R. G., and A. R. Kruckeberg. 1999. Geology and
plant life of the Klamath-Siskiyou mountain region. Natural
Areas Journal 19:320–340.
Davidson, I., and C. Simkanin. 2008. Skeptical of assisted
colonization. Science 322:1048–1049.
Davies, Z. G., R. J. Wilson, S. Coles, and C. D. Thomas. 2006.
Changing habitat associations of a thermally constrained
species, the silver-spotted skipper butterfly, in response to
climate warming. Journal of Animal Ecology 75:247–256.
Gelman, A., and J. Hill. 2007. Data analysis using regression
and multilevel/hierarchical models. Cambridge University
Press, New York, New York, USA.
Grime, J. P., V. K. Brown, K. Thompson, G. J. Masters, S. H.
Hillier, I. P. Clarke, A. P. Askew, D. Corker, and J. P. Kielty.
2000. The response of two contrasting limestone grasslands
to simulated climate change. Science 289:762–765.
Grime, J. P., J. D. Fridley, A. P. Askew, K. Thompson, J. G.
Hodgson, and C. R. Bennett. 2008. Long-term resistance to
simulated climate change in an infertile grassland. Proceedings of the National Academy of Sciences USA 105:10028–
10032.
Harrison, S., E. I. Damschen, and B. Going. 2009. Climate
gradients, climate change, and special edaphic floras.
Northeastern Naturalist 16:121–130.
Harrison, S., and J. B. Grace. 2007. Biogeographic affinity
helps explain productivity-richness relationships at regional
and local scales. American Naturalist 170:S5–S15.
Harrison, S., H. D. Safford, J. B. Grace, J. H. Viers, and K. F.
Davies. 2006. Regional and local species richness in an
insular environment: Serpentine plants in California. Ecological Monographs 76:45–56.
Hoegh-Guldberg, O., L. Hughes, S. McIntyre, D. B. Lindenmayer, C. Parmesan, H. P. Possingham, and C. D. Thomas.
2008. Assisted colonization and rapid climate change. Science
321:345–346.
Huang, D. W. 2008. Assisted colonization won’t help rare
species. Science 322:1049.
Jules, M. J., J. O. Sawyer, and E. S. Jules. 2008. Assessing the
relationships between stand development and understory
vegetation using a 420-year chronosequence. Forest Ecology
and Management 255:2384–2393.
Kelly, A. E., and M. L. Goulden. 2008. Rapid shifts in plant
distribution with recent climate change. Proceedings of the
National Academy of Sciences USA 105:11823–11826.
Ecology, Vol. 91, No. 12
Kruckeberg, A. R. 2005. Geology and plant life. University of
Washington Press, Seattle, Washington, USA.
Lenoir, J., J. C. Gegout, P. A. Marquet, P. de Ruffray, and H.
Brisse. 2008. A significant upward shift in plant species
optimum elevation during the 20th century. Science 320:
1768–1771.
Loarie, S. R., B. E. Carter, K. Hayhoe, S. McMahon, R. Moe,
C. A. Knight, and D. D. Ackerly. 2008. Climate change and
the future of California’s endemic flora. PLoS One 3:2502.
Loarie, S., P. B. Duffy, H. Hamilton, G. P. Asner, C. B. Field,
and D. D. Ackerly. 2009. The velocity of climate change.
Nature 462:1052–1055.
McCune, B. 2007. Improved estimates of incident radiation and
heat load using non-parametric regression against topographic variables. Journal of Vegetation Science 18:751–754.
McCune, B., and J. B. Grace. 2002. Analysis of ecological
communities. MjM Software Design, Gleneden Beach,
Oregon, USA.
McCune, B., and M. J. Mefford. 1999. PC-ORD: multivariate
analysis of ecological data. MjM Software Design, Gleneden
Beach, Oregon, USA.
McLachlan, J. S., J. J. Hellmann, and M. W. Schwartz. 2007. A
framework for debate of assisted migration in an era of
climate change. Conservation Biology 21:297–302.
Menzel, A., et al. 2006. European phenological response to
climate change matches the warming pattern. Global Change
Biology 12:1969–1976.
Moritz, C., J. L. Patton, C. J. Conroy, J. L. Parra, G. C. White,
and S. R. Beissinger. 2008. Impact of a century of climate
change on small-mammal communities in Yosemite National
Park, USA. Science 322:261.
Mote, P. W., E. Parson, A. F. Hamlet, W. S. Keeton, D.
Lettenmaier, N. Mantua, E. L. Miles, D. Peterson, D. L.
Peterson, R. Slaughter, and A. K. Snover. 2003. Preparing
for climatic change: the water, salmon, and forests of the
Pacific Northwest. Climatic Change 61:45–88.
Myers, N., R. A. Mittermeier, C. G. Mittermeier, G. A. B. da
Fonseca, and J. Kent. 2000. Biodiversity hotspots for
conservation priorities. Nature 403:853–858.
NOAA. 2009. National Environmental Satellite, Data, and
Information Service U.S. Climate Data. NOAA, Washington, D.C., USA.
Odion, D. C., E. J. Frost, J. R. Strittholt, H. Jiang, D. A.
Dellasala, and M. A. Moritz. 2004. Patterns of fire severity
and forest conditions in the western Klamath Mountains,
California. Conservation Biology 18:927–936.
Ohlemuller, R., B. J. Anderson, M. B. Araujo, S. H. M.
Butchart, O. Kudrna, R. S. Ridgely, and C. D. Thomas.
2008. The coincidence of climatic and species rarity: high risk
to small-range species from climate change. Biology Letters
4:568–572.
Parmesan, C., et al. 1999. Poleward shifts in geographical
ranges of butterfly species associated with regional warming.
Nature 399:579–583.
Parmesan, C., and G. Yohe. 2003. A globally coherent
fingerprint of climate change impacts across natural systems.
Nature 421:37–42.
Pounds, J. A., M. L. P. Fogden, and J. H. Campbell. 1999.
Biological response to climate change on a tropical mountain. Nature 398:611–615.
Raven, P. J., and D. Axelrod. 1978. Origin and relationships of
the California flora. University of California Publications in
Botany 72. University of California Press, Berkeley, California, USA.
Raxworthy, C. J., R. G. Pearson, N. Rabibisoa, A. M.
Rakotondrazafy, J.-B. Ramanamanjato, A. P. Raselimanana, S. Wu, R. A. Nussbaum, and D. A. Stone. 2008.
Extinction vulnerability of tropical montane endemism from
warming and upslope displacement: a preliminary appraisal
for the highest massif in Madagascar. Global Change
Biology 14:1703–1720.
December 2010
ENDEMIC-RICH FLORA AND CLIMATE CHANGE
Ricketts, T. H., E. Dinerstein, D. Olson, C. Loucks, and W.
Eichbaum. 1999. Terrestrial ecoregions of North America: a
conservation assessment. Island Press, Washington, D.C.,
USA.
Safford, H. D., J. H. Viers, and S. Harrison. 2005. Serpentine
endemism in the California flora: a database of serpentine
affinity. Madroño 52:222–257.
SAS Institute. 2007. SAS version 9.1.3. SAS Institute, Cary,
North Carolina, USA.
Schwartz, M. W., L. R. Iverson, A. M. Prasad, S. N. Matthews,
and R. J. O’Connor. 2006. Predicting extinctions as a result
of climate change. Ecology 87:1611–1615.
Skinner, C. N. 1995. Change in spatial characteristics of forest
openings in the Klamath Mountains of northwestern
California, USA. Landscape Ecology 10:219–228.
Skinner, M. W., and B. A. Pavlik. 1994. California Native Plant
Society’s inventory of rare and endangered plants in
California. Fifth edition. California Native Plant Society,
Sacramento, California, USA.
Stein, B. A., L. S. Kutner, and J. S. Adams. 2000. Precious
heritage: the status of biodiversity in the United States.
Oxford University Press, Oxford, UK.
Taylor, A. H., and C. N. Skinner. 2003. Spatial patterns and
controls on historical fire regimes and forest structure in the
Klamath Mountains. Ecological Applications 13:704–719.
3619
Theurillat, J. P., and A. Guisan. 2001. Potential impact of
climate change on vegetation in the European Alps: a review.
Climatic Change 50:77–109.
Thomas, C. D., E. J. Bodsworth, R. J. Wilson, A. D. Simmons,
Z. G. Davies, M. Musche, and L. Conradt. 2001. Ecological
and evolutionary processes at expanding range margins.
Nature 411:577–581.
Thomas, C. D., et al. 2004. Extinction risk from climate change.
Nature 427:145–148.
USDA. 2008. The PLANTS database, version 3.5. National
Plant Data Center, Baton Rouge, Louisiana, USA.
Valiente-Banuet, A., A. V. Rumebe, M. Verdú, and R. M.
Callaway. 2006. Modern Quaternary plant lineages promote
diversity through facilitation of ancient Tertiary lineages.
Proceedings of the National Academy of Sciences USA 103:
16812–16817.
Van de Ven, C. M., S. B. Weiss, and W. G. Ernst. 2007. Plant
species distributions under present conditions and forecasted
for warmer climates in an arid mountain range. Earth
Interactions 11:1–33.
Weiss, S. B., and A. D. Weiss. 1998. Landscape-level phenology
of a threatened butterfly: a GIS-based modeling approach.
Ecosystems 1:299–309.
Westman, W. E., and R. K. Peet. 1982. Whittaker, Robert, H.
(1920–1980): the man and his work. VegetatioC97–122.
Whittaker, R. H. 1960. Vegetation of the Siskiyou Mountains,
Oregon and California. Ecological Monographs 30:279–338.
APPENDIX A
A figure showing average summer temperatures over time near the study region (Ecological Archives E091-254-A1).
APPENDIX B
A figure demonstrating Whittaker’s topographic moisture gradient (TMG) (Ecological Archives E091-254-A2).
APPENDIX C
A table of species and traits used in the analyses (Ecological Archives E091-254-A3).
APPENDIX D
Tables presenting statistical results for data analyses (Ecological Archives E091-254-A4).
APPENDIX E
Figures of herb community ordination for diorite and serpentine soils (Ecological Archives E091-254-A5).