Research

Diverse functional responses to drought in a Mediterranean-type

shrubland in South Africa
A. G. West1,2, T. E. Dawson2, E. C. February1, G. F. Midgley3, W. J. Bond1 and T. L. Aston1
1
Botany Department, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa; 2Department of Integrative Biology, University of California, Berkeley, Berkeley, CA 94720,
USA; 3Climate Change and Bioadaptation, South African National Biodiversity Institute, Rhodes Drive, P ⁄ bag x7, Kirstenbosch 7735, South Africa

Summary
Author for correspondence: • Mediterranean-type ecosystems contain 20% of all vascular plant diversity on Earth and
Adam G. West have been identified as being particularly threatened by future increases in drought. Of partic-
Tel: +27 21 6503628 ular concern is the Cape Floral Region of South Africa, a global biodiversity hotspot, yet there
Email: adam.west@uct.ac.za
are limited experimental data to validate predicted impacts on the flora. In a field rainout
Received: 19 January 2012 experiment, we tested whether rooting depth and degree of isohydry or anisohydry could aid
Accepted: 5 April 2012 in the functional classification of drought responses across diverse growth forms.
• We imposed a 6-month summer drought, for 2 yr, in a mountain fynbos shrubland. We
New Phytologist (2012) 195: 396–407 monitored a suite of parameters, from physiological traits to morphological outcomes, in
doi: 10.1111/j.1469-8137.2012.04170.x seven species comprising the three dominant growth forms (deep-rooted proteoid shrubs,
shallow-rooted ericoid shrubs and graminoid restioids).
• There was considerable variation in drought response both between and within the growth
Key words: biodiversity, drought, functional
types, fynbos, hydraulic strategies,
forms. The shallow-rooted, anisohydric ericoid shrubs all suffered considerable reductions in
isohydry ⁄ anisohydry, rainfall manipulation, growth and flowering and increased mortality. By contrast, the shallow-rooted, isohydric
rooting depth. restioids and deep-rooted, isohydric proteoid shrubs were largely unaffected by the drought.
• Rooting depth and degree of iso ⁄ anisohydry allow a first-order functional classification of
drought response pathways in this flora. Consideration of additional traits would further refine
this approach.

has been maintained by low extinction rates afforded by the mild

Introduction
Mediterranean-type ecosystems are home to a substantial frac-
tion of the world’s plant biodiversity. Located on five conti-
nents, yet covering only 2% of global land area, they contain
20% of all vascular plant diversity on Earth (Cowling et al.,
1996; Klausmeyer & Shaw, 2009). These winter-wet, sum-
mer-dry ecosystems have been identified as being particularly
threatened by future climate change, primarily due to a predic-
tion of increased and regionally acute drought (IPCC, 2007).
Of particular concern is the winter rainfall region of South
Africa, home to the highly diverse and endemic Cape Floral
Region (CFR; Goldblatt & Manning, 2002; Hannah et al.,
2005). The CFR, comprising primarily the fynbos and
succulent karoo biomes, contains over 9000 species of vascular
plants of which c. 68% are endemic to the region (Goldblatt &
Manning, 2002). Vascular plant diversity in this region is high
as a result of recent taxonomic radiations, resulting in high
species richness in relatively few clades (Linder, 2003; Klak
et al., 2004). The large number of such radiations are thought
to have coincided with the development of a winter-rainfall,
summer-drought Mediterranean-type climate brought on by the
establishment of the Benguela Upwelling System c. 10 Myr BP
(Dupont et al., 2011). Subsequently, plant diversity in the CFR
climate during the glacial maximum (Dynesius & Jansson,
2000), reliable winter rains (Cowling et al., 2005) and many cli-
mate refugia that coincide with a topographically and geologi-
cally complex region (Verboom et al., 2009).
Future climate projections for the CFR indicate that the region
will become warmer and drier, with more extreme events, leading
to increased frequency and intensity of drought (Hewitson et al.,
2005; Midgley et al., 2005; Hewitson & Crane, 2006; IPCC,
2007). This is of particular concern as the absence of extreme
and prolonged drought in the CFR may have aided in maintain-
ing its plant diversity. The temperature projections are largely
supported by climate data for the region indicating that temper-
atures are on the increase (Midgley et al., 2005; Hoffman et al.,
2009). There is, however, considerably more uncertainty in the
simulations of future rainfall (IPCC, 2007) that make predictions
of future climate in the CFR, and the consequences for biodiver-
sity, problematic. Examinations of historical data for the Western
Cape have yielded variable trends in rainfall across the region
(Midgley et al., 2005; Hoffman et al., 2009, 2011). Nevertheless,
a clearer understanding of the impact of drought in this
summer-dry region is necessary.
The majority of work studying the effect of climate change on
the CFR has taken the form of climate envelope modelling, both

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at the level of the biome (Midgley et al., 2002) as well as that of
individual species (Midgley et al., 2003; Schurr et al., 2007).
These studies have indicated the potential of severe consequences
for the flora including local extinctions and range shifts of many
of the dominant species (Hannah et al., 2005). As has been well
documented in the literature, their many assumptions and simpli-
fications compromise bioclimatic model assessments (Heikkinen
et al., 2006), particularly in the mega-diverse CFR (Yates et al.,
2010), indicating that current models are far from being able to
provide robust predictions, rather serving as first-cut assessments
that require testing using a variety of approaches (Yates et al.,
2010). Considering the uncertainty in climate projections,
together with the high levels of biodiversity, our limited under-
standing of species tolerance levels (Midgley et al., 2005) and the
topographic and geological complexity of the region with the
micro-refugia these might create (Dobrowski, 2011), the reality is
likely to be far more complex.
How well can we predict plant response to drought in a bio-
diverse region such as the fynbos biome? While there is a long
history of ecological work in the fynbos (Cowling, 1992; Stock
et al., 1992; Rebelo et al., 2006), there has been relatively little
work directly examining the response of species, in situ, to
drought. Previous work has mainly focused on observations of
seasonal water relationships (Miller et al., 1983, 1984; Moll &
Sommerville, 1985; Jeffery et al., 1987; van der Heyden &
Lewis, 1989, 1990; Richardson & Kruger, 1990), rooting depths
(Higgins et al., 1987), or proxy studies of drought tolerance
through examination of xylem anatomy and resistance to cavita-
tion (February & Manders, 1999; Jacobsen et al., 2007, 2009).
This body of work has pointed to the existence of distinct func-
tional groups in the fynbos that are represented by large,
taxon-specific groups. (e.g. tall, deep-rooted proteoid shrubs;
fine-leaved, shallow-rooted, ericoid shrubs; and graminoid resti-
oids) (see Stock et al., 1992) that are likely to respond differently
to drought. However, experimental studies manipulating water
availability in the field have been rare (Herppich et al., 1994;
Agenbag, 2006), and there have been no direct tests of the mech-
anistic basis for using these functional groups to categorize
drought response in this flora.
Recent progress in unifying the theory of plant response to
drought argues for the central role of a plant’s ‘hydraulic strategy’
in determining the mechanisms of plant mortality under drought
(McDowell et al., 2008, McDowell, 2011). The majority of this
work has considered co-occurring species of a similar growth
form (e.g. trees). In this context, hydraulic strategies can be
viewed as a continuum between isohydry (regulation of plant
water potential at the cost of gas exchange) and anisohydry
(maintenance of gas exchange at the cost of declining plant water
potential) (e.g. West et al., 2008). However, when considering
the diversity of growth forms in any particular region, an evalua-
tion of a plant’s hydraulic strategy would be incomplete without
additional traits. At a first approximation, a crucial trait for com-
parison across growth forms is rooting depth. Rooting depth
should determine the degree to which a plant experiences a given
meteorological drought, with deep-rooted species being buffered
from drought to a greater extent than shallow-rooted species
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(Nepstad et al., 1994, 2007). Can an evaluation of rooting depth
and degree of iso ⁄ anisohydry help to predict drought responses
across diverse growth forms? This is a central question of our
study.
Here we describe the results from a multi-year experimental
drought manipulation in a mountain fynbos shrubland, located
on the Cape Peninsula, South Africa. Drought was experimen-
tally imposed over the course of two summers, and a suite of
physiological parameters monitored in seven species representing
the three dominant growth forms. Our central hypothesis stated
that drought impacts would be largely determined by rooting
depth, augmented by water potential regulation strategy, and
would cluster by growth form. We predicted that the greatest
impacts would be seen in the shallow-rooted restioids and ericoid
shrubs with the least impact occurring in the large, deep-rooted
proteoid shrubs. We discuss how the evaluation of hydraulic
strategy can inform, and improve, our categorization of plant
functional responses to drought, ultimately helping to make
more accurate predictions regarding plant response to future
climate change.
Materials and Methods
Study sites
Study sites were located in the Silvermine Section of Table
Mountain National Park, South Africa (S34.105, E18.444).
Mean annual rainfall is 1187 mm with 75% occurring during the
winter months (MJJASO). Two sites were selected – an 8-yr
post-fire site with reproductively and structurally mature vegeta-
tion (labelled ‘Mature’ in figures) and a 2-yr post-fire site with
mostly reproductively and structurally immature vegetation
(labelled ‘Young’ in figures). The sites were located within 1.2
km of each other at a similar aspect and elevation (400 m asl).
Soils at both sites were sands formed from the underlying quartz
arenite (Table Mountain Sandstone) with a poorly developed
organic horizon. Soil depth was uniformly > 1.5 m at the young
site but was more variable at the mature site, with fractured sand-
stone rock being encountered between 0.5 and 1.5 m depth. The
vegetation on both sites was classed as mountain sandstone fynbos
(Rebelo et al., 2006). Vegetation height was c. 1.5 and 0.5 m at
the mature and young sites, respectively. A plant survey recorded
37 and 68 species in 144 m2 at the mature and young sites,
respectively. The mature site was dominated by the proteoid
Leucadendron laureolum (Lam.) Fourc. and Erica subcapitata
(N.E.Br.) E.G.H.Oliv. and Erica ericoides (L.) E.G.H.Oliv.. The
most common restioid on the site was Staberoha cernua (L.f.)
T.Durand & Schinz. The young site was dominated by the prote-
oids L. laureolum and Diastella divaricata (P.J.Bergius) Rourke.,
the restioid Hypodiscus aristatus (Thunb.) Krauss.. The most com-
mon Erica species were Erica pyxidiflora Salisb. and E. ericoides.
Experimental design
Nine 4 m · 4 m experimental plots were selected at each site so
as to include sufficient individuals of the focal species (Table 1).
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Table 1 Details of the focus species in this study
Site Species Code Functional type
Young Diastella divaricata Diadiv Proteoid
Leucadendron laureolum Leulau(s) Proteoid
Erica pyxidiflora Eripyx Ericoid
Erica ericoides Erieri Ericoid
Hypodiscus aristatus Hypari Restioid
Mature Leucadendron laureolum Leulau(a) Proteoid
Erica subcapitata Erisub Ericoid
Erica ericoides Erieri Ericoid
Staberoha cernua Stacer Restioid
Plots were clustered in groups of three, with each cluster consist-
ing of two treatment plots and one control plot. Distance
between plots within a cluster was c. 4 m and distance between
clusters was c. 15 m. Over each of the experimental plots, a rain
exclusion structure was constructed consisting of a steel frame-
work with six overlapping, clear polycarbonate roof panels that
could be tilted flat or at a 30 angle (Supporting Information
Fig. S1). When the panels were flat, rain falling on the surface
would run off into the gutter and be piped off site, resulting in
100% rain exclusion. When the panels were at 30, rain falling
on the panels would run onto the plot, resulting in 0% rain
exclusion while still casting the same shade as for the flat configu-
ration. The roofs were positioned slightly above the height of the
tallest vegetation at the site. The perimeters of the plots were
trenched to a depth of 50 cm and lined with thick plastic before
being backfilled. Plants were not measured within 75 cm of the
perimeter, providing a buffer zone from the effects of trenching
and precipitation entering from the sides of the structures.
Considerable effort was made to prevent trampling in the plots.
Stepping-stones were placed in each plot to provide access to
specific instrumentation. Plant measurements were conducted
from a 5-m horizontal ladder supported on either side of the plot.
Micrometeorological and soil moisture measurements
A fixed weather station was deployed at the young site, measuring
temperature and relative humidity (Vaisala HMP-45C), rainfall
(Texas Electronics TE-525 mm), windspeed and direction
(03001 Young Wind Sentry Set; Campbell Scientific, Logan, UT,
USA) and photosynthetically active radiation (QSO-S; Apogee
Instruments, Logan, UT, USA). Sensors were connected to a
CR10· data logger (Campbell Scientific). Photosynthetically
active radiation was also measured under a rain exclusion struc-
ture. Standalone rainfall gauges (RG3-M; Onset Computer
Corporation, Bourne, MA, USA) were deployed at both sites to
confirm there were no significant differences in microclimate
between the two sites. Temperature and relative humidity
(EL-USB-2; Lascar Electronics, USA) were also monitored at both
sites in the open, under treatment and under control rain-out-
shelters. The rainout shelters caused slightly altered micro-climate
(warmer, lower PAR) relative to ambient conditions (Fig. S2).
Soil moisture access tubes (5 cm B) were installed in each
experimental plot 2 months before the commencement of the
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Growth form Plant height (m) Regeneration strategy
Sprawling 0.15 Re-seeder
Tall shrub 0.35 Re-seeder
Shrub 0.25 Re-seeder
Shrub 0.15 Re-seeder
Restioid 0.65 Sprouter
Tall shrub 1.2 Re-seeder
Shrub 0.7 Re-seeder
Shrub 0.3 Re-seeder
Restioid 0.45 Re-seeder
experiment. Using these access tubes soil moisture was measured
every 0.1 m, for 1 m, using a Frequency Domain Reflectometry
(FDR) soil water profile sensor (Diviner 2000; Sentek Sensor
Technologies, Stepney, SA, Australia). These measurements were
taken every 2 wk. In addition to the Diviner profiles, a continu-
ously logging FDR soil moisture profile (Envirosmart SOLO;
Sentek Sensor Technologies) was established at each site. Data
were logged every 30 min at depths of 0.1, 0.2, 0.4, 0.6 and
1.0 m. The percentages of soil moisture measured with the FDR
sensors were compared with gravimetric measurements of soil
water for field calibration.
Gas exchange measurements
Assimilation (A) and stomatal conductance (gs) were measured
using a LI-6400 infrared gas analyzer (Li-Cor, Lincoln, NE,
USA). Measurements were made on clear, sunny days between
the hours of 10:00 h and 15:00 h. From 12:00 h to 13:00 h,
midday stem water potential measurements (WMD) were made
on the same plants that were used for gas exchange using a
Scholander Pressure Chamber (PMS Instruments, Corvallis, OR,
USA). All plants within a site were measured on the same day to
eliminate the effects of variable weather. Gas exchange measure-
ments were usually completed within 120 s of clamping on to
the leaf so as to minimize chamber acclimation. The CO2 con-
centration was maintained at 380 ppm, flow rate was 400 lmol
s)1, PAR inside the chamber was 1500 lmol (LI-6400 LED light
source) and chamber humidity was maintained slightly below
ambient. Sample and reference cells were matched before every
measurement and empty chamber measurements were taken
regularly to correct for drift in the CO2 and H2O sample cell
values. Measurements were made on the most healthy sunlit
foliage on the north side of each plant. Immediately following
the measurement, the measured leaf material was photographed
underneath a LI-6400 gasket in the exact configuration that it
had been in the chamber. Projected leaf area was calculated using
ImageJ (http://rsbweb.nih.gov/ij/). This photographic method
prevented excessive defoliation over the course of the experiment.
Isotopes and rooting depths
We measured hydrogen and oxygen stable isotope ratios of water
as a proxy of rooting depths for the focus species in our study
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(Dawson, 1993). Suberized stems (proteoids and ericas),
rhizomes (restioids) and soil cores were collected in the experi-
mental plots during a summer sampling campaign (February,
2008 ⁄ 9) coincident with our gas exchange and water potential
measurements. Samples were immediately placed in screw-topped
glass vials and sealed with Parafilm (Pechiney Plastic Packaging,
Chicago, IL, USA) to prevent any evaporation. Once in the labo-
ratory, samples were kept frozen at ) 20C until extraction.
Water was cryogenically extracted from the samples at the Uni-
versity of Cape Town following the methodology of West et al.
(2006). Hydrogen isotope ratios (d2H) were measured by inject-
ing microlitre quantities of water into an H ⁄ Device coupled to a
Delta Plus mass spectrometer (ThermoFinnigan, Bremen,
Germany). Injected H2O was reduced to H2 gas in a hot chromium
reactor and the 2H ⁄ H ratio of this gas was then analysed by mass
spectrometry (Brand et al., 1996; Gehre et al., 1996). Oxygen
isotope ratios (d18O) were measured by CO2 equilibration (Socki
et al., 1992). Water samples were left to equilibrate with a 0.2%
CO2 headspace for 48 h at 21–23C. Following equilibration,
the vials were inserted into a GasBench II connected to a Delta
Plus XL mass spectrometer (ThermoFinnigan). The GasBench II
was modified with a 10-port injection valve, allowing a 0.2%
CO2 reference injection to follow each sample CO2 injection. All
isotope analyses were conducted at the Center of Isotope Biogeo-
chemistry, University of California, Berkeley and are expressed in
per mil notation (&) relative to the standard V-SMOW, follow-
ing the equation (Brand et al., 2009):
 
Rsample
dn E ¼ 1 Eqn 1
Rstandard
(n is the heavy isotope of element E, R is the ratio of the heavy to
light isotope (2H ⁄ 1H or 18O ⁄ 16O)). Analytical precision on
internal quality control standards was at least 1.5& (d2H) and
0.15& (d18O).
Growth, phenology and mortality measurements
In order to assess the impact of our drought treatment on the
seven focal species, we made monthly measurements of growth,
phenology and mortality. All measurements were made on six
individuals per species, per treatment, per site. At each measure-
ment period, phenological data were recorded as pres-
ence ⁄ absence of new growth, flowers, seeds or cones. Mortality
data were scored as % mortality of the whole plant. Monthly
shoot or culm growth was measured on four shoots ⁄ culms per
individual that were tagged with coloured wire. For the Restiona-
ceae (S. cernua and H. aristatus), culm growth was measured on
healthy, newly emerged culms > 10 cm long. Tags were switched
to new culms before they approached maximum length. For the
Proteaceae and Ericaceae, distal tips of healthy shoots were
targeted for measurement. In the case of shoot damage through
herbivory or mechanical damage, the shoot was excluded from
that month’s data and the tag was repositioned on another shoot.
In the case of shoot death from drought, the shoot was measured
and the data included. Following this the tag was repositioned on
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another healthy shoot on the plant. In this manner, measure-
ments were biased towards actively growing parts of the plant. To
account for canopy dieback, monthly shoot growth was scaled by
the live canopy fraction. Growth data are presented as relative
canopy growth rate (RCGR, mm mm)1 d)1):
Lt
RCGR ¼
Lt 1  Dt ðt 1Þ
 CL Eqn 2
(Lt is total shoot length measured at time t, Lt)1 is the total length
of the shoot at the previous monthly measurement, D is the num-
ber of days between t and t)1, and CL is the live canopy fraction.
Effect size
In order to examine the significance of differences between treat-
ment and control measurements (for soil moisture, growth and
mortality), data were plotted as effect size (ES):
MT  MC
ES ¼ pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi Eqn 3
e2T þ e2C
(MT and MC represent the mean values for treatment and control
plots, respectively, and eT and eC are the standard errors of the
mean for treatment and control plots, respectively.) Thus, ES is
in units of standard errors. We considered times where )2 > ES
> 2 to represent significant differences between treatment and
control.
Response pathways
We used our analyses of traits and outcomes (described in the
Results section) as evidence for describing the ‘response path-
ways’ species took in relation to the rainfall manipulation
(Fig. 6). The relative position of each species at each tier (trait or
outcome) was assigned qualitatively, based on data collected in
this study, to compare responses and detect common pathways of
response. The tiers are organized as a hierarchy from the traits
measured to the outcomes of how the plants responded to our
treatments in terms of mortality and flowering (fitness). For some
of the species we were unable to obtain all of the data for every
tier and in these cases the symbol and lines are simply missing
from that tier.
Results
Climate and soil moisture during the course of the
experiment
Seasonal variations in temperature, vapour pressure deficit and
rainfall at our sites reveal a cool, wet winter and warm, dry sum-
mer climate typical of the region (Fig. S3). Our rain exclusion
structures significantly reduced soil moisture in the top 40 cm of
soil in the treatment plots during the two summer drought peri-
ods, resulting in an intense, shallow soil drought (Fig. 1). The
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treatment effect was considerably greater in the first summer as
rainfall was higher (Table S1) and more frequent (Table S2);
thus, surface soil moisture in the control plots was regularly
increased relative to the treatment plots. During the second
summer, limited summer rainfall resulted in little difference
between treatment and control plots, both being relatively dry.
Effect of drought on gas exchange and water status
Changes in leaf level gas exchange with shoot WMD reveal differ-
ent water potential regulation strategies for the species examined
(Fig. 2). The patterns were consistent within a species for species
present in both young and mature sites despite different plant
age. The three Erica species – E. subcapitata, E. ericoides and
E. pyxidiflora – exhibited a strongly anisohydric strategy, allowing
WMD to fall to very negative values while still maintaining gas
exchange, albeit at a very reduced rate. By contrast, the proteoids
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Fig. 1 Soil moisture dynamics and treatment effect over
the course of the study on functional responses to
drought in a Mediterranean-type shrubland in South
Africa. Left-hand panels: average gravimetric soil mois-
ture (%, ± 1 SE) at multiple depths for treatment (closed
symbols) and control (open symbols) plots at both sites.
Right-hand panels: soil moisture treatment effect at vari-
ous depths for each site, plotted as effect size (number of
standard errors). Differences < ± 2 SEs from 0 are
regarded as insignificant (open symbols). Differ-
ences > ± 2 SEs from 0 are regarded as significant (closed
symbols). Differences that exceeded the scale are
truncated and plotted as diamonds. For all panels, grey
shaded bars represent the summer drought exclusion
treatments (2008 ⁄ 9), and subsequent monitoring period
(dashed lines) when no experimental drought was
imposed (2010).
L. laureolum and D. divaricata maintained constant WMD
despite decreasing gs and A to zero during the summer drought
period. This is indicative of an isohydric regulation of W at the
cost of gas exchange. A similar isohydric strategy was observed for
the restioid, S. cernua. The data from the restioid H. aristatus
were suggestive of isohydry, but inconclusive. Gas exchange did
not reach zero in this species and the water potential did not
decline beyond the range seen for other isohydric species. How-
ever, it was clear that the experimental drought was insufficient
to induce complete stomatal closure or highly negative water
potentials in this species.
Isotopic evidence for rooting depths
In order to infer the relative dependence of plants on shallow or
deeper water sources during summer, we measured the d2H and
d18O of water from plant stems (proteoids and ericoids) and
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Fig. 2 Light-saturated photosynthetic assimilation (Amax) and stomatal
conductance (gs max) vs midday shoot water potential (WMD) for seven
fynbos species of varying growth form. Open symbols, control plants;
closed symbols, treatment plants; circles, plants from the mature site;
squares, plants from the young site. Species codes are listed in Table 1.
rhizomes (restioids) in February over 2 years (2008 ⁄ 9). From
monthly measurements of rainwater over the course of the study,
we constructed a local meteoric water line (LMWL; Fig. 3). This
line was similar to that from a nearby long-term dataset (Harris
et al., 2010). As expected, summer rainfall and cloud moisture
collected over the month preceding our sampling effort fell on
the LMWL. The amount-weighted rainfall (averaged over the
study) was more negative than the summer precipitation owing
to the predominance of winter rainfall inputs. We intended to
use soil water isotope profiles to establish plant rooting depths.
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Fig. 3 d2H and d18O isotopic composition of plant xylem water and
precipitation in a Mediterranean-type shrubland in South Africa. GMWL,
the Global Meteoric Water Line (y = 8x + 10); LMWL, the local meteoric
water line (y = 5.7x + 6.9) defined from local precipitation over the course
of the study. Summer rain and cloud are from samples collected a month
before the plant sampling. Weighted rain is the amount weighted isotope
composition of precipitation over the course of the study. Species codes
are listed in Table 1. Plants inferred to be deep-rooted and shallow-rooted
are circled.
However, analytical problems with extracting water from the dry
soils rendered these data unreliable. Despite this we were able to
infer relative rooting depth (deep or shallow) by comparing the
plant water data to the LMWL. Plant water plotted away from
the amount-weighted annual rainfall along a line with a shallower
slope than the LMWL (Fig. 3), known to represent evaporation
(Sharp, 2007; Dawson & Simonin, 2011). An extensive literature
on plant and water source isotope data (reviewed by Dawson
et al., 2002) supports the interpretation that the greater the
distance a sample occurs along an evaporation line from the
amount-weighted annual rainfall, the shallower the soil the
sample was derived from. Based on this interpretation, the most
deep-rooted plants are the proteoids L. laureolum and
D. divaricata. The Erica species and the restioids appeared to be
more shallow-rooted. These general rooting patterns were
confirmed with qualitative plant excavations on site.
Effect of drought on growth, canopy mortality and
flowering
Ericas The Erica species were the most severely impacted by the
experimental drought, with droughted plants showing reduced
growth, increased levels of mortality and reduced reproductive
effort relative to the controls.
Our first rain exclusion induced very negative shoot water
potentials in all three Erica species (Fig. 2) resulting in little to
no shoot growth in the droughted plants (Fig. 4). At the same
time, the relatively wet summer (Tables S1,S2) allowed consider-
able growth in the control plants. The result was a marked treat-
ment effect, with significantly less growth occurring in the
treatment plants for these species (Fig. 4). During this treatment,
there was high mortality amongst the droughted E. pyxidiflora
seedlings, with no mortality occurring amongst the control plants
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(Fig. 5). While there was no whole plant mortality for the adult
Erica species, E. subcapitata suffered considerable leaf loss and
canopy dieback following this period (Fig. 5). By contrast,
E. ericoides managed to avoid extensive canopy dieback. When
the drought period was relieved in May, previously droughted
E. ericoides plants had increased growth relative to the control
plants. Erica subcapitata also showed considerable shoot growth
in the surviving shoots during this time; however, the high levels
of canopy mortality meant that whole plant growth was indistin-
guishable from the control (Fig. 4). For E. pyxidiflora, there was
no difference in shoot growth between previously droughted and
control plants following the first drought period (Fig. 4).
The second experimental drought occurred during a much
drier summer (Tables S1,S2), with control plants at the mature
site having much lower growth than in the previous summer
(Fig. 4). This resulted in a much smaller treatment effect over
this drought period for E. subcapitata and E. ericoides. Neverthe-
less, the pattern of reduced growth in the droughted plants was
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Fig. 4 Shoot and culm growth rates as relative shoot
growth (left-hand side panels) and effect size (right-hand
panels) over the course of the study on functional
responses to drought in a Mediterranean-type shrubland
in South Africa. For relative shoot growth: closed symbols,
treatment plants; open symbols, control plants. For effect
size (plotted as number of standard errors), differ-
ences < ± 2 SEs from 0 are regarded as insignificant
(open symbols). Differences > ± 2 SEs from 0 are
regarded as significant (closed symbols). Shaded panels
represent drought periods, as for Fig. 1.
repeated (Fig. 4). This second drought period resulted in some
whole plant mortality for E. subcapitata (Fig. 5), as previously
stressed plants with reduced live canopy area were unable to
survive a second drought period. No control E. subcapitata plants
died during this time. Plant mortality in E. ericoides was too low
to interpret in terms of our experimental treatments (Fig. 5). At
the young site, growth in control E. pyxidiflora plants was
unaffected by the lower summer rainfall, most likely due to the
wetter nature of this site (Fig. 1), and the same pattern of
reduced growth in droughted plants was documented as for the
first experimental drought. Interestingly, there was no
E. pyxidiflora mortality associated with this second drought
period, possibly as these plants had survived the first drought
period presumably through being better established, and were
thus able to survive this drought period too.
The experimental droughts had considerable impact on flowering
in the Erica species. Following the first experimental treatment,
none of the droughted E. subcapitata plants produced flowers,
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Phytologist Research 403

Fig. 5 Mortality trends for all species over the course of

the study on functional responses to drought in a
Mediterranean-type shrubland in South Africa. Mortality
is presented as % canopy mortality (closed symbols,
treatment plants; open symbols, control plants) and
cumulative plant mortality (black lines, treatment plants;
white lines, control plants). Species codes are listed in
Table 1. Shaded panels represent drought periods, as for
Fig. 1.

whereas 80% of control plants had considerable reproductive significant differences for adult plants occurred in the first experi-
effort. Flowering over the second summer drought was more vari- mental drought when growth declined slightly earlier for drough-
able, but droughted plants had significantly less flowering effort ted plants than control plants (Fig. 4). Interestingly, for the
than control plants (Table 2). For E. ericoides, flowering was less juvenile L. laureolum plants there were no significant differences
affected by the experimental treatments, and there was no signifi- between treatment and control plants during our experimental
cant difference between control and treatment over the course of droughts (Fig. 4), suggesting that these plants were already able
the study (Table 2). However, what was evident was the to access a stable water source from the shallow water table at this
month-long delay in onset of flowering in droughted E. ericoides site. There was also very little canopy dieback and plant mortality
following the first drought treatment (Fig. S4). Flowering was for this species over the duration of the experiment (Fig. 5), and
also somewhat reduced in droughted plants following the second no difference in female cone production between treatment and
experimental treatment. The effect of our experimental drought control groups (Table 2).
on flowering in E. pyxidiflora was the most striking. No drough- In contrast to L. laureolum, D. divaricata was highly sensitive
ted plants flowered over the course of the entire experiment to the experimental drought. During both experimental
(Fig. S4). By contrast, many of the control plants did flower, in drought periods, growth was significantly reduced in droughted
increasing amounts as the young plants reached maturity. D. divaricata plants (Fig. 4). There was also considerable plant
mortality during the second experimental drought, with eight
Proteoids For both the adult and juvenile L. laureolum plants, plants dying in treatment plots compared with only two in
there was very little treatment effect on growth (Fig. 4). The only control plots (Fig. 5). Additionally, droughted D. divaricata
plants flowered significantly less than control plants (Table 2),
with this being most obvious during the late summer of our
Table 2 Differences in flowering between treatment and control plants experimental treatments (Fig. S4). In the third summer, when
over the course of the study, as tested by paired t-test there was no experimental drought, surviving D. divaricata
plants had identical growth patterns in treatment and control
Control Treatment
plots, with no further mortality (Fig. 5). However, previously
mean mean
Species (% flowering) (% flowering) t df P droughted plants had less of a reproductive effort than control
plants, possibly a consequence of the previous two drought
Diastella divaricata 53.0 22.2 )7.5 27 < 0.0001 periods.
Erica ericoides 16.1 12.1 )1.1 27 0.290
Erica pyxidiflora 6.1 0.0 )2.2 27 0.039
Erica subcapitata 25.4 12.1 )2.3 27 0.030 Restioids There appeared to be little treatment effect on growth,
Hypodiscus aristatus 97.5 97.6 0.06 27 0.952 mortality and flowering for the two restioid species studied
Staberoha cernua 98.2 98.3 0.07 27 0.943 (H. aristatus and S. cernua), with growth differing significantly
Leucadendron 95.2 95.2 0.02 27 0.981 between treatment and control plants only in a few instances
laureolum1
(Fig. 4), and no significant differences occurring in the mortality
1
Presence of live female cones. Values in bold are significant at P < 0.05. (Fig. 5) or flowering (Table 2) data.

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404 Research
Discussion
Our study has shown fynbos plants to have both considerable
resilience and sensitivity to drought in this unique biodiversity
hotspot. Far from being uniformly sensitive to our experimental
6-month droughts, we observed substantial variation in drought
impacts for the study species. We had predicted that deep-rooted
species would be buffered from our drought treatment and would
show little impact, whereas shallow-rooted species would be
negatively affected by the shallow soil drought. While this was
the case for the deep-rooted L. laureolum (no impact) and
shallow-rooted Erica species (moderate to high impact), it was
not the case for the shallow-rooted restioids (no impact) and the
deep-rooted D. divaricata (high impact). The variation in
response to shallow soil drought highlights the complexity of
predicting drought impacts in such a biodiverse system, and
emphasizes the need for improved mechanistic understanding of
plant susceptibility to drought (McDowell et al., 2011).
Hydraulic theory predicts that shallow-rooted, anisohydric
species would be most severely impacted by our intense, shallow
experimental drought as they would experience rapidly declining
water potential, possibly to the point of hydraulic failure
(McDowell et al., 2008). Hydraulic safety margins tend to
increase with increasing degree of anisohydry (Meinzer et al.,
2009), and thus anisohydric plants can continue to transpire into
a drought, albeit with increased costs of xylem dysfunction (West
et al., 2008). Survival of droughted anisohydric plants is thus
tightly coupled to xylem vulnerability to cavitation (McDowell
et al., 2008). All Erica species – adult or seedling – showed a
strongly anisohydric response, with considerable declines in stem
water potential being measured during the experimental
droughts. Water potentials as low as ) 10 MPa were measured,
which is considerably lower than previously reported (e.g. Miller
et al., 1983; Jacobsen et al., 2007). These low water potentials
resulted in canopy dieback of up to 80% for E. subcapitata and
considerable whole plant mortality for the E. pyxidiflora
seedlings. Remarkably, there was little mortality or canopy
dieback in E. ericoides, despite very low water potentials being
measured. An independent survey of naturally droughted plants
near our experimental plots (data not shown) showed that
E. ericoides was able to withstand WMD of ) 8 MPa over the sum-
mer and still retain a full canopy and subsequently flower in the
wet season. However, plants that experienced more negative WMD
were dead the following spring. As in other genera of the Ericaceae
(e.g. Arctostaphylos in California), this high cavitation resistance
may be related to xylem architecture (i.e. vasicentric tracheids;
Carlquist, 1985). However, given a drought of sufficient intensity,
such as those predicted to occur under climate change, Erica
species are likely to suffer hydraulic failure and mortality.
In contrast to the anisohydric response described above,
shallow-rooted isohydric species should have been less severely
impacted by our experimental drought, as drought mortality in
isohydric plants is only likely to manifest itself after prolonged
drought (McDowell et al., 2008). While our rain exclusion was
maintained for nearly 6 months, the period of drought experi-
enced by plants was considerably shorter than this for two
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reasons. First, soil moisture took several months to decline fol-
lowing the imposition of our drought treatment (Fig. 1). Second,
our rain-exclusion structures did not exclude regular periods of
cloud moisture during the summer (Table S2), which may have
periodically alleviated water stress for those species able to utilize
it. Isohydric plants typically maintain high hydraulic conductivity
through the regulation of water potential, allowing a greater abil-
ity to respond to pulses of soil moisture (West et al., 2007a,b). In
our study, the shallow-rooted, isohydric restioids possibly
avoided significant drought impacts through the avoidance of
cavitation and the use of regular cloud moisture events. The
potential for the restioid growth form to collect cloud moisture
to alleviate drought has been recognized since the early 20th cen-
tury (Marloth, 1903). Cloud moisture can improve plant water
status by direct foliar uptake (Burgess & Dawson, 2004;
Breshears et al., 2008; Limm et al., 2009; Simonin et al., 2009)
or through uptake of cloud or fog drip from plant canopies into
the shallow soil (Dawson, 1998). During our experiment, there
was considerable evidence of cloud moisture collecting on resti-
oid culms and being channeled to the base of these plants
(Fig. S5). It is likely that the shallow-rooted, isohydric, restioids
were exploiting regular cloud moisture events for brief periods of
gas exchange during the summer drought, possibly alleviating a
negative carbon balance in droughted plants. However, cloud
moisture is a highly site-specific phenomenon in the Cape moun-
tains, and restioids are not restricted to the cloud belt. Future
research should explore the drought sensitivity of restioids with-
out a cloud water subsidy to test the generality of our findings in
this experiment.
The minimal impact of our experimental drought on both
adult and seedling L. laureolum resulted from a combination of
isohydric behavior and access to deeper water throughout the
summer. Furthermore, hydraulic lift (Hawkins et al., 2009) may
have mitigated the effects of shallow soil drought for this growth
form. The lack of drought stress in the 2–3-yr-old L. laureolum
supports the finding that taproot growth is rapid in this group
(Manders & Smith, 1992), and is crucial to their survival over
the summer drought. While established L. laureolum plants
appear well buffered from drought, this growth form may still be
vulnerable to intense summer drought in the post-fire establish-
ment phase. In contrast to the woody, emergent L. laureolum,
D. divaricata was more herbaceous, with a sprawling growth
form constraining the plant to within the boundary layer created
by surrounding vegetation. Why was this species so heavily
impacted by our experimental drought? The strongly isohydric
behavior of D. divaricata resulted in prolonged stomatal closure
over the summer drought. Air temperatures below our rainout
shelters, but above the vegetation boundary layer, reached 42C
over the summer drought. Stomatal closure, combined with the
low windspeed in the vegetation boundary layer, would have
resulted in limited opportunity for latent and sensible heat loss
from leaves potentially leading to a negative carbon balance
and ⁄ or lethal leaf temperatures in D. divaricata.
Despite 6 months of rain removal, there was little outright
mortality in our experiment (Fig. 5). The relevance of nonlethal
drought events in shaping vegetation structure is currently under
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Phytologist Research 405

debate (McDowell & Sevanto, 2010; McDowell et al., 2011).

Yet, in a fire-prone flora, such as the fynbos, nonlethal droughts
may be of great importance in determining the success of
post-fire recruitment. Seeder life histories (i.e. nonsprouters) are
common in the fynbos, possibly due to the reliable winter rainfall
in this region (Ojeda, 1998; Cowling et al., 2005; Ojeda et al.,
2005). While drought may not result in outright mortality of
plants, compromised reproductive output may result in local
extinction following fire. An example of this can be seen in
E. pyxidiflora, where the drought delayed maturation of the seed-
lings, resulting in no flowers being produced (Table 2, Fig. S4).
A fire in this system following the drought could result in local
extinction of this species. For resprouters, the impacts of drought
on post-fire recovery is less clear, but is likely to be tightly
coupled to the plants carbon reserves (Verdaguer & Ojeda,
2002). Drought-induced carbon starvation is a controversial
hypothesis (Sala et al., 2010); however, reduced photosynthesis
and increased water stress during drought would likely result in a
lower ability to store carbon, negatively impacting resprouting
ability post-fire. Thus, nonlethal drought may have considerable
impact on the vegetation of this frequently burnt flora, possibly
shifting the dominance between seeders and re-sprouters. We
suggest that in fire-prone systems, examination of the impacts of
nonlethal drought on post-fire regeneration, particularly the
interaction between hydraulics and carbon metabolism (Sala
et al., 2010; McDowell et al., 2011), is an important avenue for
future research. Fig. 6 A graphical synthesis of the data presented in this study on
The multiple lines of evidence collected during our experiment functional responses to drought in a Mediterranean-type shrubland in
(from physiological traits to fitness outcomes) illustrate three key South Africa. These ‘response pathways’ visually depict the variations in
trait combinations and consequent fitness outcomes (mortality and
findings. First, in a broad sense, species representing tall proteoid
flowering) for the species measured in this study. The position of each
shrubs (L. laureolum), small ericoid shrubs (Erica species) and species in each tier was based on data presented in previous figures and is
restioids (S. cernua and H. aristatus) appeared to have distinct designed to reflect relative, rather than absolute, differences. Where
‘response pathways’ (Fig. 6, inset) lending support to the use of symbols overlap, no difference in the value of the trait is inferred, and
these functional groups for predicting drought response. Of these separation of symbols is simply for clarity. Inset: a simplified and
conceptual view of the distinct pathways followed by the key functional
three major growth forms, we suggest that shallow-rooted, anis-
groups in this study (P, proteoid; E, ericoid; R, restioid).
ohydric seeder species (e.g. Erica) will be the most sensitive to
future increases in summer drought. Second, nested within these certain elements of the flora (e.g. deep-rooted proteoids and shal-
broad response groups is a considerable range of responses to low-rooted restioids, respectively) from increased summer
drought (Fig. 6). In several instances, common physiological drought. The extent to which drought may impact the flora in
traits resulted in very different fitness outcomes (e.g. E. ericoides areas without these moisture resources is as yet unknown. Impor-
vs E. subcapitata). These apparent contradictions most likely arise tantly, simple bioclimatic modelling approaches are unlikely to
from two main causes: (a) variables that appear as discrete are in be able to capture these subtleties, and this approach needs care-
fact a continuum, which we lack the power to resolve in this ful amendment if it is to be applied in future. While our study
study. For example, the degree of isohydry and anisohydry is rep- has indicated that hydraulic strategy is a useful approach for
resented here as a somewhat artificial dichotomy (Fig. 6), rather catagorizing drought responses in a biodiverse area, it remains a
than a continuum, mainly due to an inability to resolve the dif- significant challenge to scale-up from detailed physiological stud-
ferences between species more finely, and (b) consideration of ies to regional predictions to enable suitable risk assessment in
additional traits is necessary for determining species-specific future.
drought responses. In the case of D. divaricata and L. laureolum,
we hypothesize that growth form is a key trait influencing
Acknowledgements
drought tolerance. In the case of Erica species, it is likely that var-
iation in xylem vulnerability to cavitation is important in resolv- Funding was generously provided by the Andrew W. Mellon and
ing their range of drought response. Third, and lastly, we must National Research Foundation, South Africa. Site access was pro-
consider that microsite characteristics could strongly influence vided by SANParks and the South African Navy. We acknowl-
drought impacts in these major growth forms. Shallow water edge dedicated assistance from C. Moseley, E. Kleyhans, R.
tables or high-altitude sites with summer cloud inputs may buffer Skeleton, U. Mutzek and numerous field assistants.

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406 Research
References
Agenbag L. 2006. A study on an altitudinal gradient investigating the potential
effects of climate change on rynbos and the rynbos-succulent Karoo boundary.
Stellenbosch, South Africa: University of Stellenbosch.
Brand WA, Avak H, Seedorf R, Hofmann D, Conradi T. 1996. New methods
for fully automated isotope ratio determination from hydrogen at the natural
abundance level. Isotopes in Environmental and Health Studies 32: 263–273.
Brand WA, Coplen TB, Aerts-Bijma AT, Bohlke JK, Gehre M, Geilmann H,
Groning M, Jansen HG, Meijer HAJ, Mroczkowski SJ et al. 2009.
Comprehensive inter-laboratory calibration of reference materials for delta 18O
versus VSMOW using various on-line high-temperature conversion techniques.
Rapid Communications in Mass Spectrometry 23: 999–1019.
Breshears DD, McDowell NG, Goddard KL, Dayem KE, Martens SN, Meyer
CW, Brown KM. 2008. Foliar absorption of intercepted rainfall improves
woody plant water status most during drought. Ecology 89: 41–47.
Burgess SSO, Dawson TE. 2004. The contribution of fog to the water relations
of Sequoia sempervirens (D. Don): foliar uptake and prevention of dehydration.
Plant, Cell & Environment 27: 1023–1034.
Carlquist S. 1985. Vasicentric tracheids as a drought survival mechanism in the
woody flora of southern California and similar regions; review of vasicentric
tracheids. Aliso 11: 37–68.
Cowling R, ed. 1992. The ecology of fynbos: nutrients, fire and diversity. Cape
Town, South Africa: Oxford University Press.
Cowling RM, Ojeda F, Lamont BB, Rundel PW, Lechmere-Oertel R. 2005.
Rainfall reliability, a neglected factor in explaining convergence and divergence
of plant traits in fire-prone mediterranean-climate ecosystems. Global Ecology
and Biogeography 14: 509–519.
Cowling RM, Rundel PW, Lamont BB, Kalin Arroyo M, Arianoutsou M. 1996.
Plant diversity in mediterranean-climate regions. Trends in Ecology & Evolution
11: 362–366.
Dawson TE. 1993. Water sources of plants as determined from xylem-water
isotopic composition: perspectives on plant competition, distribution, and
water relations. In: Ehleringer JR, Hall AE, Farquhar G, eds. Stable isotopes and
plant carbon–water relations. San Diego, CA, USA: Academic Press, 465–496.
Dawson TE. 1998. Fog in the California redwood forest: ecosystem inputs and
use by plants. Oecologia 117: 476–485.
Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP. 2002. Stable
isotopes in plant ecology. Annual Review of Ecology and Systematics 33:
507–559.
Dawson TE, Simonin K. 2011. The roles of stable isotopes in forest hydrology
and biogeochemistry. In: Levia DF, Carlyle-Moses D, Tanaka T, eds. Forest
hydrology and biogeochemistry. Synthesis of past research and future directions.
Heidelberg, Germany: Springer-Verlag, 137–161.
Dobrowski SZ. 2011. A climatic basis for microrefugia: the influence of terrain
on climate. Global Change Biology 17: 1022–1035.
Dupont LM, Linder HP, Rommerskirchen F, Schefuß E. 2011. Climate-driven
rampant speciation of the Cape flora. Journal of Biogeography 38: 1059–1068.
Dynesius M, Jansson R. 2000. Evolutionary consequences of changes in species’
geographical distributions driven by Milankovitch climate oscillations.
Proceedings of the National Academy of Sciences, USA 97: 9115–9120.
February E, Manders P. 1999. Effects of water supply and soil type on growth,
vessel diameter and vessel frequency in seedlings of three fynbos shrubs and two
forest trees. South African Journal of Botany 65: 382–387.
Gehre M, Hoefling R, Kowski P, Strauch G. 1996. Sample preparation device
for quantitative hydrogen isotope analysis using chromium metal. Analytical
Chemistry 68: 4414–4417.
Goldblatt P, Manning JC. 2002. Plant diversity of the Cape Region of southern
Africa. Annals of the Missouri Botanical Garden 89: 281–302.
Hannah L, Midgley G, Hughes G, Bomhard B. 2005. The view from the cape.
Extinction risk, protected areas, and climate change. BioScience 55: 231–242.
Harris C, Burgers C, Miller J, Rawoot F. 2010. O- and H-isotope record of
Cape Town rainfall from 1996 to 2008, and its application to recharge studies
of Table Mountain groundwater, South Africa. South African Journal of Geology
113: 33–56.
Hawkins H, Hettasch H, West AG, Cramer MD. 2009. Hydraulic
redistribution by Protea ‘Sylvia’ (Proteaceae) facilitates soil water replenishment
New Phytologist (2012) 195: 396–407
www.newphytologist.com
New
Phytologist
and water acquisition by an understorey grass and shrub. Functional Plant
Biology 36: 752–760.
Heikkinen RK, Luoto M, Araujo MB, Virkkala R, Thuiller W, Sykes MT.
2006. Methods and uncertainties in bioclimatic envelope modelling under
climate change. Progress in Physical Geography 30: 751–777.
Herppich M, Herppich WB, Vonwillert DJ. 1994. Influence of drought, rain
and artificial irrigation on photosynthesis, gas-exchange and water relations of
the fynbos plant Protea–acaulos (L) Reich at the end of the dry season. Botanica
Acta 107: 440–450.
Hewitson BC, Crane RG. 2006. Consensus between GCM climate change
projections with empirical downscaling: precipitation downscaling over South
Africa. International Journal of Climatology 26: 1315–1337.
Hewitson B, Tadross M, Jack C. 2005. Scenarios from the University of Cape
Town. In: Schulze RE, ed. Climate change and water resources in southern Africa:
studies on scenarios, impacts, vulnerabilities and adaptation. Pretoria, South
Africa: Water Research Commission, 39–56.
van der Heyden F, Lewis OAM. 1989. Seasonal variation in photosynthetic
capacity with respect to plant water status of five species of the
Mediterranean climate region of South Africa. South African Journal of
Botany 55: 509–515.
van der Heyden F, Lewis OAM. 1990. Environmental-control of photosynthetic
gas-exchange characteristics of fynbos species representing 3 growth forms.
South African Journal of Botany 56: 654–658.
Higgins KB, Lamb AJ, Van Wilgen BW. 1987. Root systems of selected plant
species in mesic mountain fynbos in the Jonkershoek Valley Southwestern
Cape Province South Africa. South African Journal of Botany 53: 249–258.
Hoffman MT, Carrick PJ, Gillson L, West AG. 2009. Drought, climate change
and vegetation response in the succulent karoo, South Africa. South African
Journal of Science 105: 54–60.
Hoffman MT, Cramer MD, Gillson L, Wallace M. 2011. Pan evaporation and
wind run decline in the Cape Floristic Region of South Africa (1974–2005):
implications for vegetation responses to climate change. Climatic Change 109:
437–452.
IPCC. 2007. Pachauri RK, Reisinger A, eds. Climate change 2007: synthesis report.
Geneva, Switzerland: IPCC.
Jacobsen AL, Agenbag L, Esler KJ, Pratt RB, Ewers FW, Davis SD. 2007.
Xylem density, biomechanics and anatomical traits correlate with water stress
in 17 evergreen shrub species of the Mediterranean-type climate region of
South Africa. Journal of Ecology 95: 171–183.
Jacobsen AL, Esler KJ, Pratt RB, Ewers FW. 2009. Water stress tolerance of
shrubs in Mediterranean-type climate regions: convergence of fynbos and
succulent karoo communities with California shrub communities. American
Journal of Botany 96: 1445–1453.
Jeffery D, Moll EJ, Vanderheyden F. 1987. Comparative water potentials of
4-month-old and 40-year-old Cape fynbos plants. South African Journal of
Botany 53: 32–34.
Klak C, Reeves G, Hedderson T. 2004. Unmatched tempo of evolution in
Southern African semi-desert ice plants. Nature 427: 63–65.
Klausmeyer KR, Shaw MR. 2009. Climate change, habitat loss, protected areas
and the climate adaptation potential of species in Mediterranean ecosystems
worldwide. PLoS ONE 4: 1–9.
Limm EB, Simonin KA, Bothman AG, Dawson TE. 2009. Foliar water uptake:
a common water acquisition strategy for plants of the redwood forest. Oecologia
161: 449–459.
Linder HP. 2003. The radiation of the Cape flora, southern Africa. Biological
Reviews 78: 597–638.
Manders PT, Smith RE. 1992. Effects of artificially established depth to water
table gradients and soil type on the growth of Cape fynbos and forest plants.
South African Journal of Botany 58: 195–201.
Marloth R. 1903. Results of experiments on Table Mountain for ascertaining the
amount of moisture deposited from the south-east clouds. Transactions of the
South African Philosophical Society 14: 403–408.
McDowell NG. 2011. Mechanisms linking drought, hydraulics, carbon
metabolism, and vegetation mortality. Plant Physiology 155: 1051–1059.
McDowell NG, Beerling DJ, Breshears DD, Fisher RA, Raffa KF, Stitt M.
2011. The interdependence of mechanisms underlying climate-driven
vegetation mortality. Trends in Ecology and Evolution 26: 523–532.
 2012 The Authors
New Phytologist  2012 New Phytologist Trust
New
Phytologist
McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut
J, Sperry J, West AG, Williams DG et al. 2008. Mechanisms of plant survival
and mortality during drought: why do some plants survive while others
succumb to drought? New Phytologist 178: 719–739.
McDowell NG, Sevanto S. 2010. The mechanisms of carbon starvation: how,
when, or does it even occur at all? New Phytologist 186: 264–266.
Meinzer FC, Johnson DM, Lachenbruch B, McCulloh KA, Woodruff DR.
2009. Xylem hydraulic safety margins in woody plants: coordination of
stomatal control of xylem tension with hydraulic capacitance. Functional
Ecology 23: 922–930.
Midgley GF, Chapman RA, Hewitson B, Johnston P, De Wit M, Ziervogel G,
Mukheibir P, Van Niekerk L, Tadross M, Van Wilgen BW et al. 2005. A
status quo, vulnerability and adaptation assessment of the physical and
socio-economic effects of climate change in the Western Cape. Stellenbosch, South
Africa: CSIR Environmentek.
Midgley GF, Hannah L, Millar D, Rutherford MC, Powrie LW. 2002.
Assessing the vulnerability of species richness to anthropogenic climate
change in a biodiversity hotspot. Global Ecology and Biogeography 11:
445–451.
Midgley GF, Hannah L, Millar D, Thuiller W, Booth A. 2003. Developing
regional and species-level assessments of climate change impacts on biodiversity
in the Cape Floristic Region. Biological Conservation 112: 87–97.
Miller PC, Miller JM, Miller PM. 1983. Seasonal progression of plant water
relations in fynbos in the Western-Cape-Province, South-Africa. Oecologia 56:
392–396.
Miller JM, Miller PC, Miller PM. 1984. Leaf conductances and xylem pressure
potentials in fynbos plant dpecies. South African Journal of Science 80:
381–385.
Moll EJ, Sommerville JEM. 1985. Seasonal xylem pressure potentials of two
South African coastal fynbos species in three soil types. South African Journal of
Botany 51: 187–193.
Nepstad DC, De CCR, Davidson EA, Jipp PH, Lefebvre PA, Negreiros GH,
Da SED, Stone TA, Trumbore SE, Vieira S. 1994. The role of deep roots in
the hydrological and carbon cycles of amazonian forests and pastures. Nature
372: 666–669.
Nepstad DC, Tohver IM, Ray D, Moutinho P, Cardinot G. 2007. Mortality of
large trees and lianas following experimental drought in an Amazon forest.
Ecology 88: 2259–2269.
Ojeda F. 1998. Biogeography of seeder and resprouter Erica species in the Cape
Floristic Region – where are the resprouters? Biological Journal of the Linnean
Society 63: 331–347.
Ojeda F, Brun FG, Vergara JJ. 2005. Fire, rain and the selection of seeder and
resprouter life-histories in fire-recruiting, woody plants. New Phytologist 168:
155–165.
Rebelo AG, Boucher C, Helme N, Mucina L, Rutherford MC. 2006. Fynbos
biome. In: Mucina L, Rutherford MC, eds. The vegetation of South Africa,
Lesotho and Swaziland. Pretoria, South Africa: South African National
Biodiversity Institute, 53–219.
Richardson DM, Kruger FJ. 1990. Water relations and photosynthetic
characteristics of selected trees and shrubs of riparian and hillslope habitats in
the South-Western Cape Province South Africa. South African Journal of Botany
56: 214–225.
Sala A, Piper F, Hoch G. 2010. Physiological mechanisms of
drought-induced tree mortality are far from being resolved. New Phytologist
186: 274–281.
Schurr FM, Midgley GF, Rebelo AG, Reeves G, Poschlod P, Higgins SI. 2007.
Colonization and persistence ability explain the extent to which plant species
fill their potential range. Global Ecology and Biogeography 16: 449–459.
Sharp ZD. 2007. Principles of stable isotope geochemisty. Upper Saddle River, NJ,
USA: Pearson Prentice Hall.
Simonin KA, Santiago LS, Dawson TE. 2009. Fog interception by Sequoia
sempervirens (D. Don) crowns decouples physiology from soil water deficit.
Plant, Cell & Environment 32: 882–892.
 2012 The Authors
New Phytologist  2012 New Phytologist Trust
Research 407
Socki RA, Karlsson HR, Gibson EK. 1992. Extraction technique for the
determination of 18O in water using preevacuated glass vials. Analytical
Chemistry 64: 829–831.
Stock WD, van der Heyden F, Lewis OAM. 1992. Plant structure and function.
In: Cowling RM, ed. The ecology of fynbos: nutrients, fire and diversity. Cape
Town, South Africa: Oxford University Press, 226–240.
Verboom GA, Archibald JK, Bakker FT, Bellstedt DU, Conrad F, Dreyer LL,
Forest F, Galley C, Goldblatt P, Henning JF et al. 2009. Origin and
diversification of the Greater Cape flora: ancient species repository, hot-bed of
recent radiation, or both? Molecular Phylogenetics and Evolution 51: 44–53.
Verdaguer D, Ojeda F. 2002. Root starch storage and allocation patterns in
seeder and resprouter seedlings of two Cape Erica (Ericaceae) species. American
Journal of Botany 89: 1189–1196.
West AG, Hultine KR, Burtch KG, Ehleringer JR. 2007a. Seasonal variations in
moisture use in a pinon–juniper woodland. Oecologia 153: 787–798.
West AG, Hultine KR, Jackson TL, Ehleringer JR. 2007b. Differential summer
water use by Pinus edulis and Juniperus osteosperma reflects contrasting
hydraulic characteristics. Tree Physiology 27: 1711–1720.
West AG, Hultine KR, Sperry JS, Bush SE, Ehleringer JR. 2008. Transpiration
and hydraulic strategies in a pinon-juniper woodland. Ecological Applications
18: 911–927.
West AG, Patrickson SJ, Ehleringer JR. 2006. Water extraction times for plant
and soil materials used in stable isotope analysis. Rapid Communications in
Mass Spectrometry 20: 1317–1321.
Yates CJ, Elith J, Latimer AM, Le Maitre D, Midgley GF, Schurr FM, West
AG. 2010. Projecting climate change impacts on species distributions in
megadiverse South African Cape and Southwest Australian Floristic Regions:
opportunities and challenges. Austral Ecology 35: 374–391.
Supporting Information
Additional supporting information may be found in the online
version of this article.
Fig. S1 Photograph of the rainout shelters used in this study.
Fig. S2 Microclimate beneath the rainout shelters.
Fig. S3 Ambient environmental variables measured over course
of the 3-yr experiment.
Fig. S4 Flowering trends, for those species with visible flowers,
over the course of the experiment.
Fig. S5 Soil moisture in bare soil and beneath restioids following
a cloud moisture event.
Table S1 Comparison of long-term rainfall averages (1956–2008)
with rainfall measured during this study
Table S2 Number of days between rain events and number of
cloud days
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