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Phil. Trans. R. Soc. B (2012) 367, 3100–3114
doi:10.1098/rstb.2012.0074
Research
A demographic approach to study effects of
climate change in desert plants
Roberto Salguero-Gómez1, *, Wolfgang Siewert2, Brenda B. Casper3
and Katja Tielbörger2
1
Evolutionary Biodemography Laboratory, Max Planck Institute for Demographic Research,
Konrad-Zuse Strabe 1, Rostock 18057, Germany
2
Department of Evolution and Ecology, Plant Ecology Group, University of Tübingen,
Tübingen 72076, Germany
3
Department of Biology, University of Pennsylvania, Philadelphia, PA 19104-6018, USA
Desert species respond strongly to infrequent, intense pulses of precipitation. Consequently, indigenous flora has developed a rich repertoire of life-history strategies to deal with fluctuations in resource
availability. Examinations of how future climate change will affect the biota often forecast negative
impacts, but these—usually correlative—approaches overlook precipitation variation because they
are based on averages. Here, we provide an overview of how variable precipitation affects perennial
and annual desert plants, and then implement an innovative, mechanistic approach to examine the
effects of precipitation on populations of two desert plant species. This approach couples robust
climatic projections, including variable precipitation, with stochastic, stage-structured models constructed from long-term demographic datasets of the short-lived Cryptantha flava in the Colorado
Plateau Desert (USA) and the annual Carrichtera annua in the Negev Desert (Israel). Our results highlight these populations’ potential to buffer future stochastic precipitation. Population growth rates in both
species increased under future conditions: wetter, longer growing seasons for Cryptantha and drier years
for Carrichtera. We determined that such changes are primarily due to survival and size changes for
Cryptantha and the role of seed bank for Carrichtera. Our work suggests that desert plants, and thus
the resources they provide, might be more resilient to climate change than previously thought.
Keywords: demographic buffering; climate change; integral projection model; periodic population
matrix model; precipitation; stochastic population growth rate (lS)
1. INTRODUCTION
Drylands, the largest terrestrial ecosystem (figure 1a
[2,3]), are considered among the most sensitive to
projected global environmental change [4]. Global
circulation models project temperature increases, precipitation decreases and an increase in interannual
variability in precipitation for many deserts [4]. In
them, even small changes in precipitation are expected
to have large impacts on species composition and biodiversity [5]. However, a far-too-often overlooked fact is
that desert flora have evolved a set of unique structures
and mechanisms to withstand extensive periods of
drought. These include succulence [6], deep roots [7],
modified metabolic pathways [8], high modularity [9])
and bet hedging mechanisms such as seed dormancy
[10], or extreme longevity [11], among others. These
structures and mechanisms are thought to enable
* Author for correspondence ([email protected]).
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rstb.2012.0074 or via http://rstb.royalsocietypublishing.org.
One contribution of 10 to a Theme Issue ‘Impacts of global
environmental change on drylands: from ecosystem structure and
functioning to poverty alleviation’.
plants to buffer the enormous variability found in
deserts. Owing to such adaptations, projected changes
in abiotic conditions may still fall within the range of
variation that desert plants are accustomed to without
large consequences for long-term population viability.
Deserts are a particularly suitable ecosystem for
testing causal hypotheses of climate change. This is
so because their biological responses are strongly
controlled by water availability [12]. Climate change
models applied to deserts have mostly used average
temperature [13– 15] and—less commonly—average
precipitation [16,17] to explore future distributions
of species. This approach is problematic because the
frequency of climatic extremes is also projected to
change [4], and because deserts’ inherent variability
in precipitation render average values uninformative
of actual patterns [18,19]. Consequently, actual
responses of desert species to global environmental
change might differ from those generated by averagebased approaches such as climatic envelopes. In
addition, previous modelling approaches to determine
responses of desert species to climate change have
been highly correlative [20 – 22], and so our understanding of the causal mechanisms governing their
responses is very limited.
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This journal is q 2012 The Royal Society
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Climate change and plant demography R. Salguero-Gómez et al.
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(a)
Basin
Mojave
Sonoran
Colorado Plateau
Chihuahuan
Guajira
Taklamakan
Kavir
Gobi
Negev
Thar
Lybian
Arabian
Sahara
Nubian
Denakil
Caatinga
Sechura
Simpson
Atacama
Kalahari
Patagonian
1
2
Great Sandy
Gibson
Great Victoria
Namib
3
4
5
10
30
20
no. desert plant species studied with structured demographic models per country
yo
102
deciduous
forest
50
desert
Euph Fabaceae
orbia
cea
Crassulaceae e
e e
Cleomacea
a
idoide
r
o
l
h
C
e
Solanaceae
Zygophyllaceae
acea
M
alpine
58
e
acea
ncul ae
Ranu
ace ae
Po ace
r
po
marine
ranth
(c)
tropical
forest
shrubland
38 7
52
savannah
32
marsh 25
Ama
(b)
Asteraceae
eae
Boraginac
Brassicaceae
25
174
dune
grassland
131
Cactaceae
evergreen
forest
Figure 1. (a) Global distribution of desert plant demographic studies using structured population models. Red lines contain
dryland regions defined by the UNEP [1]. (b) Number of plant species for which these models have been applied as a function
of ecosystem. (c) Taxonomic family diversity of the aforementioned studies in deserts. Data in a,b from a database with ca 700
plant species (R. Salguero-Gómez 2012, unpublished data).
A useful but largely unexplored approach towards
a more mechanistic understanding of desert plants’
responses to climate change couples long-term
demographic models and high-resolution climatic projections. Size-/stage-structured demographic models
explore population dynamics not as a function of their
superficial characteristics (e.g. population size and
population growth rate), but by directly examining the
effects of a/biotic factors on underlying vital rates (e.g.
survival, reproduction [23,24]). Furthermore, this
demographic approach provides indirect information
about past and current selection on crucial life-history
traits [25]. Until recently, global climatic projections
have been too coarse to predict precipitation at a
specific population/site [4,26]. This is particularly
relevant in deserts, where precipitation is highly spatially
heterogeneous too [18]. A recent advance, a superhigh-resolution global model [27], provides reliable
monthly precipitation projections for any region
around the globe down to a 20-km2-grid resolution.
Phil. Trans. R. Soc. B (2012)
This model can be used in comparative demographic
studies even on different continents. The remaining
limitation for coupling demographic models and
climatological data is long-term, individual-based
demographic information from natural populations.
Unfortunately, such datasets are extremely rare in
drylands (but see [28]).
Coupling demographic and climatic data is particularly valuable when evaluating the response of
short-lived, desert species, with relatively quick population turnover, to climate change. A meta-analysis
using size-/stage-based demographic models concluded
that species with short lifespans are more vulnerable to
increased stochasticity than long-lived species [26].
Lewontin & Cohen [29] derived an approximation for
the stochastic population growth rate (a ¼ log(lS))
that points to the negative effect of variation in the
long run. This long-term population measure, a, is
directly proportional to the deterministic population
growth rate (l for a particular year, averaged over
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Climate change and plant demography
), but it decreases with interannual
multiple years as l
variation in l:
lÞ
Þ varð
pffiffiffiffiffiffi :
a ¼ logðls Þ logðl
2l
ð1:1Þ
It is commonly assumed that increased variation in
an abiotic factor (e.g. precipitation) will inevitably
decrease a in natural populations. However, for this prediction to hold true, changes in l must be strongly and
positively coupled with variation in the abiotic factor.
A few examples exist in the literature where this is not
the case [30,31]. These studies highlight the importance
of demographic buffering [32,33], that is, a population’s
ability to retain a more or less constant a despite varying
climate by virtue of re-adjusting its vital rates. This
can happen when, for instance, low fecundity is coupled
with high survival, or when bet-hedging strategies
reduce variance in fitness despite variance in abiotic factors across years. Therefore, whether or not short-lived
desert plant species are vulnerable to climate change will
depend not only on the climate change scenarios, but
also on the life histories and potential for demographic
buffering of the species [34].
The motivation for this manuscript is twofold. First,
we provide an overview of how variation in precipitation might affect population dynamics of perennial
and annual species and highlight promising avenues
of climate change research. Secondly, we illustrate our
suggested demographic approach for investigating
the effect of high-resolution climatic projections on
long-term population growth. We use unique long-term
datasets from two different short-lived species from two
contrasting deserts: the short-lived subshrub Cryptantha
flava from Utah, USA and the annual herb Carrichtera
annua from Israel. In Utah, USA, increases in precipitation are projected, and we hypothesized a consequent
increase in demographic performance, mostly mediated
by survival and growth. In Israel, more droughts are
projected, and we hypothesized negative effects but
demographic buffering via dormant seeds.
2. PRECIPITATION, GLOBAL
ENVIRONMENTAL CHANGE AND DESERT PLANT
POPULATION DYNAMICS
The consequences of global environmental change on
desert plant populations are largely unknown, particularly with respect to precipitation. This is most likely
due to the scarcity of long-term demographic data—a
problem with many species but particularly pronounced
for desert plants (figure 1b; but see [35]). Additionally,
other factors such as biased taxonomic interest, geographical representation or selection of a particular
methodology also play an important role in our limited
knowledge. We present an overview of how variable precipitation affects the population dynamics of desert
perennials and annuals, and offer suggestions for
future avenues of research.
(a) Precipitation effects on perennial desert
plant species
Demographic changes in aridland perennials are often
viewed as episodic. Most recruitment and high survival
Phil. Trans. R. Soc. B (2012)
occur in exceptionally favourable weather years
[36,37]. This view is supported primarily by studies
of woody shrubs and succulents, where populations’
densities may be relatively static or slightly declining
for decades [38– 40] and plant longevity well exceeds
the career—or even the lifespan—of the investigator.
Achieving a mechanistic understanding of the
demography for any long-lived species is challenging.
In arid systems, data often come from decadal or
longer census intervals for mapped or historically
photographed vegetation [39,41,42] or from estimating current population age structure based on yearly
incremental growth of individuals, even those without
distinct growth rings [36,40,43,44]. For some desert
species, these approaches have led to estimates of
remarkable longevity: ca 5000 years for Pinus longaeva
(Pinaceae) [45], and over 10 000 years for Larrea
tridentata (Zygophyllaceae) [46] (see [42] for more
examples). Such estimates, as pointed out by Miriti
et al. [37], may be woefully inaccurate if based on
census intervals that do not bracket the rare drought
events that trigger high mortality episodes.
Recent severe droughts in the southwestern US have
provided rare opportunities to capture population
responses [47]. In such cases, the link between lack of
precipitation and mortality does appear strong. In a
study of seven common shrub species in Joshua Tree
National Park in the Colorado Desert, USA [37], six
showed mortality rates ranging from 55 to 100 per cent,
with negligible mortality only in L. tridentata. In Ambrosia
dumosa (Asteraceae), Eriogonum fasciculatum (Polygonaceae), Simmondsia chinensis (Simmondsiaceae) and
Tetracoccus hallii (Picrodendraceae), individuals weakened by an earlier drought, as judged from their
growth rates, were more likely to die during a later one.
Likewise, a regional study showed L. tridentata to have
much higher survival at most locations than smaller
drought-deciduous species and provided evidence for
cumulative effects of multiple drought years [48].
Recruitment in desert perennials can, likewise, occur
in episodes of variable duration [44]. Nonetheless, a
causal link between precipitation and recruitment is not
often clear [40], probably because seedling establishment may depend on multiple, carefully timed
precipitation events [11,41], and be sensitive to numerous other factors [38]. Seed germination and seedling
emergence are separated from seed production at least
seasonally and potentially annually, especially if the
seeds require stratification or otherwise form a seed
bank [49]. It stands to reason that favourable precipitation conditions are then required for both events.
There may be a range of impinging biotic factors, including the seedling’s reliance on nurse plants [43],
competition from established individuals [37] and predation on seed and seedlings [50]. High predation rates
have led to the suggestion that mast fruiting may underlie
episodic recruitment events in aridland perennial species
[50,51]. Comprehensive investigations into rates of seed
production, predation and seedling establishment as a
function of both interannual and interseasonal variation
in precipitation would be worthwhile.
Precipitation deficits may additionally imprint the
demography of perennials by negatively impacting
individual plant size. A recent comparative study has
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Climate change and plant demography R. Salguero-Gómez et al.
shown a positive correlation between individual plant
shrinkage and survival [52], but the importance of this
phenomenon for population dynamics has often been
overlooked. Plant shrinkage or dieback of shrub canopies is common during drought events [37,53,54], and
negative size changes may occur over time even when
severe drought is not apparent [31,39,55]. Sometimes
the entire plant canopy dies, so dormant and dead
plants are not immediately distinguishable [37]. The
morphology of some desert shrubs [9], and at least
one subshrub [56], where the stem fragments into separate hydraulic sectors as the plant ages, lends itself
particularly to shrinkage, expressed through the death
of any fragment(s). Thus, hydraulic fragmentation
may enable the plant to slough off a part damaged or
cavitated due to drought without resulting in the death
of the entire individual [57]. The incidence of hydraulic
fragmentation among [9] and within (R. SalgueroGómez 2012, unpublished data) species is positively
correlated with aridity, the most pronounced form
being the splitting of the stem as in L. tridentata [58].
It may not be coincidental that this species often exhibits
low mortality [59], even during severe droughts
[37,39,48]. The demography of desert plants with multiple stems are normally treated as single individuals (i.e.
genet), but the possible adaptive significance of stem
splitting provides a good reason for individual stem/
ramet demography as well [59,60].
While some desert perennials are famous for their
longevity, we need more information about the
demography of less charismatic species, including
short-lived shrubs, subshrubs or herbaceous perennials
whose populations may turn over in a shorter time than
the return frequency of extreme climatic events. Practically, the demography of these species would be more
amenable to modelling with annual or periodic projection matrix approaches [23,61]. To date, such models
are most commonly applied to species in the Cactaceae
(figure 1c), where emphasis is often placed on the relative importance of clonal versus sexual reproduction
[49]. In general, we need to evaluate the importance
of recruitment, mortality and growth responses to
extreme weather patterns compared with background
levels in more typical years [62].
We offer suggestions for building the most useful
database of demographic studies to accomplish this
goal. First, we need to choose study species more carefully, including sufficient numbers of common species
that are neither invasive nor threatened/endangered.
Several recent studies of cacti, for example, were motivated by the threatened status of the species [49].
Second, data are needed for a wider variety of perennial
life forms and taxonomic groups, including other desert
dominant families about which little is known (e.g. Agavaceae, Aizoaceae, Asclepiadaceae, Chenopodiaceae,
Cupressaceae, Cyperaceae, Liliaceae, Mimosoidaceae,
Rhamnaceae and Tamaricaceae). And finally, particularly because precipitation in arid systems is
temporally variable, studies need to be (i) of sufficient
duration to capture considerable natural variability,
even if they cannot always encompass the extreme
events of low recurrence interval, and/or (ii) to incorporate experimental manipulations of precipitation
following climatic projections.
Phil. Trans. R. Soc. B (2012)
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(b) Precipitation effects on annual desert
plant species
Studies explicitly addressing demographic responses of
dryland annual plants, a dominant component of
warm deserts [6], to precipitation patterns are rare
too. However, within the existing empirical body of evidence, three categories of studies can be distinguished:
(i) comparison of plant population dynamics over a
range of sites differing in mean precipitation (i.e. a
‘space-for-time’ approach), (ii) experimental manipulation of water availability, and (iii) observation of
plant populations in the field over a range of years differing in precipitation, as is typically done also with
perennials (see §2a above).
Comparing plant population dynamics over a range
of sites differing in mean precipitation provides an
evolutionary view of precipitation effects on plants
because it shows the result of long-term selection
regimes (i.e. precipitation). Consistent with theory,
annual plant populations from drier habitats have
been found to exhibit higher seed dormancy [63]
and a stronger response to precipitation as a trigger
of germination [64], compared with conspecifics
from wetter, less variable habitats. In addition, they
exhibit a faster life cycle [65] and larger reproductive
effort when resources are abundant [30].
Experimental manipulation of water availability gives
insight into the immediate (transient) effects of precipitation. Experiments of this nature are carried out either
in the field or under common garden or greenhouse
conditions, where water availability has been shown to
affect integral elements of population dynamics. In particular, additional precipitation increases germination
[63,64], biomass [10] and fecundity [64], while precipitation deficit leads to a shortened life cycle, expedited
flowering [65] and higher reproductive effort [30].
However, multi-species experiments have shown that
these responses are not ubiquitous and, often, coexisting species do not respond at all to changes in water
availability [10,30].
Studies in which plant populations were observed
over a longer time period, and therefore under different
natural precipitation conditions show that responses are
strongly species-specific. Still, two general patterns
seem to emerge. First, fecundity is positively correlated
with precipitation [66–68]. Second, drought years are
associated with low population sizes and frequently
result in complete reproductive failure. However, in
wet years, plant populations can be remarkably insensitive to rainfall [66,68], suggesting a saturation-type
response to precipitation. Levine et al. [68] found that
in such years, the temperature associated with the first
major precipitation event rather than total annual precipitation was the best predictor for plant density. The
amount and timing of the first rains after the dry
season serve as a germination cue for annual plants,
and a number of studies have found them to be of
high importance [69–71].
Another predictor of annual plants population
performance in response to precipitation is species
abundance. In a 4-year community study, Boeken &
Shachak [72] found abundant species showing no
response to variation in precipitation while rare species
varied strongly with rainfall. Levine & Rees [73]
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(a)
Lebanon
Syria
Wyoming
Utah
Golan
heights
West
bank
Gaza
Colorado
Israel
Jordan
Egypt
Arizona
New Mexico
400 km
Cryptantha flava
(b) 90
Carrichtera annua
current (1979–2009)
projected (2075–2099)
current (1981–2011)
projected (2075–2099)
80
70
precipitation (mm)
100 km
60
50
40
30
20
10
Nov
**Dec
Oct
Sep
Aug
July
June
Apr
* May
Mar
**Jan
**Feb
Dec
Nov
Oct
Sep
July
*Aug
June
Apr
May
Feb
**Mar
Jan
0
Figure 2. (a) Natural distribution of the herbaceous perennial C. flava (Boraginaceae; left) and distribution of the annual
C. annua (Brassicaceae; here only shown for Israel; right) represented by dark grey area. Stars indicate location of the populations studied for 15 and 8 years, respectively. (b) Mean monthly precipitation +95% CI at each population based on current
precipitation patterns (last 30 years) and projections from the super-high-resolution model used in this paper [76]. Single (*)
and double asterisks (**) represent monthly precipitation significant differences at p , 0.05 and p , 0.005, respectively, for
current versus projected scenarios.
reported a similar pattern when modelling the
dynamics of an abundant grass and a rare forb. The
latter did best in rainy years that were preceded by
dry years. Only then was this species able to germinate
from the seed bank while experiencing little competition from the grass competitor. Their study
suggests that the interannual variation in precipitation
may facilitate species coexistence because different
species specialize on different types of years and thus
avoid competition, similar to the storage effect
described earlier [10].
A study by Fox et al. [67] found that germination of
one species, Gilia tenuiflora arenaria (Polemoniaceae)
was favoured by rainy, warm conditions of El Niño
years. In such years, the species replenished its persistent seed bank, where the majority of seeds stayed
dormant until the next, infrequent, rainy year. Another
Phil. Trans. R. Soc. B (2012)
co-occurring species, Chorizanthe pungens pungens
(Polygonaceae), germinated more in drier conditions
and its population size was rather independent of
weather conditions, suggesting demographic buffering
[32]. The importance of rare, rainy years to restock the
seedbank has also been reported for Lepidium pailliferum
(Brassicaceae) [74]. This species apparently needs
extreme variation in precipitation to persist because
a long series of average precipitation years led to a
monotonic decline and ultimately local extinction.
In summary, results from empirical studies indicate
that interannual variation in precipitation is the major
driver of annual plant population dynamics in arid
ecosystems. Though annuals share the same overall
dependence on precipitation with perennials (see
§2a), the former may differ largely from the latter in
their responses to rain via distinctive life-history
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Climate change and plant demography R. Salguero-Gómez et al.
(a)
3105
Cryptantha flava
1
dormant season
e
j
c
sg
(b) Carrichtera annua
3
1
ygerm
s
2
dormant season
dgerm
egerm
ybank
Dec
Nov
Oct
Sep
Aug
July
June
dbank1
May
Apr
dbank3
Mar
Feb
Jan
dbank2
Figure 3. Life cycles of (a) the perennial C. flava and (b) the annual C. annua. Light grey and dark grey areas in the rectangles
represent periods of photosynthetic activity and vegetative dormancy, respectively. White circles represent timing and frequency of field censuses. (a) In Cryptantha, established individuals can survive (s) to the next year and change in size (g),
become reproductive (w), producing a given number of flowering stalks (x) whose seeds may then establish (1) and achieve
a specific size the next year (q). (b) In Carrichtera, reproductive individuals may produce seeds (cgerm) that will germinate
after the dry season if they survive (dgerm). Seedlings may then survive (s) to become reproductive the next year. Reproductive
individuals can also contribute to the seedbank (cbank). Seeds in the seedbank may stay dormant during each period (dbank1,2,3)
and emerge as germinable seeds in April (1germ). Black arrows in both life cycles represent demographic events of established
individuals, while grey arrows represent events during sexual reproduction.
strategies. Rather than leading to synchronized
responses, the high variation in precipitation allows
for multiple strategies and may be a requisite for population persistence [74] and species coexistence [73].
Seed germination has been identified as a key life
stage for desert annual demography [75]. Even
though seed dormancy has been studied relatively frequently, demographic records of annual plant
populations still lack fine estimates of seed banks,
probably owing to the difficulty of observing or estimating below-ground demographic stages. One
possible solution could be a combination of longterm field surveys of annual plant populations with
seed-bank experiments in the greenhouse or in situ.
Similar to perennials, there is a need for long-term surveys that examine in-depth demographic processes to
identify the mechanisms that control annual plant
population responses to precipitation. Measuring
single traits of single species under controlled conditions instead of all crucial vital rates seems
insufficient. Finally, the study bias (figure 1) may be
even more at the expense of annuals than perennials,
because they are often an invisible component of
desert plant communities, especially in drought years.
3. PRECIPITATION SHIFTS IN TWO COMMON
DESERT SHORT-LIVED SPECIES
In the following section, we address some of the
above research gaps by evaluating demographic
Phil. Trans. R. Soc. B (2012)
performance for two short-lived species in the light of
projected shifts in precipitation. We do this by
coupling long-term individual-based demographic
information in the form of size-/stage-structured
models with super-high-resolution climatic models for
precipitation. The two native study species are the subshrub C. flava (Boraginaceae) from the Colorado
Plateau in North America (Cryptantha hereafter), and
the native, annual C. annua (Brassicaceae) from the
Negev Desert in the Middle East (Carrichtera hereafter).
(a) Study species
Cryptantha grows along the Colorado Plateau, USA
(figure 2a; [77]). Its mean lifespan is 4.3 + 2.1 (s.d.)
years (R. Salguero-Gómez 2012, unpublished data).
Individuals consist of one to approximately 200 leaf
rosettes [77], organized into branches that emerge
from a woody underground stem. The root system
consists of a single, deep taproot and 5– 15 lateral
roots [78]. Leaf rosettes first appear in mid April
(figure 3a), and new rosettes may develop throughout
the growing season from axillary meristems of existing
rosettes. Once induced to reproduce, a rosette bolts to
approximately 25 cm and produces 20 – 70 flowers
[79]. Flowering rosettes die as seeds ripen in late
July. Seedlings may emerge in September – October
or at the beginning of the next growing season, and
there appears to be no permanent seed bank [79].
Individuals typically enter vegetative dormancy in
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early August. However, late growing season monsoons and experimental precipitation have been
shown to prolong the growing season into September
[80,81]. Individuals of Cryptantha possess great size
plasticity, sometimes displaying extreme changes in
size within 1 year, either positive (growth) or negative
(shrinkage), as a function of the amount of precipitation [77]. Because individuals of Cryptantha become
internally fragmented with development [56], some
can decrease in size more than 80 per cent through
the mortality of entire fragments.
Carrichtera is an annual herb native to shrub-steppe
and desert habitats in most Mediterranean countries
[82], but an invasive in semi-arid southern Australia
[83]. In Israel, Carrichtera grows in Mediterranean
and semi-arid shrublands and in deserts (figure 2a;
[84]). Individuals germinate at the beginning of the
rain season (October – December). Seedlings may
become reproducers and create new seeds before
dying towards the end of the rain season (March–
May). Throughout the dry season (May – October),
the population is ‘dormant’, being exclusively represented by seeds (figures 2b and 3b). Newly
produced seeds are enclosed in lignified structures
on the dried-out plant and thus are maintained as
aerial seed banks until they are rain-dispersed [85].
Most seed loss is due to granivores during the dormant
season, mainly harvester ants and rodents [83].
Carrichtera maintains a persistent seed bank, which
means that a certain fraction of viable seeds do not germinate the first year, even if conditions are suitable.
Seeds typically remain dormant until the second or
later germination season.
(b) Experimental design
We studied the dynamics of a natural population of
Cryptantha near its distribution centre over 14 years
(1997 – 2011). The fieldsite located by the Redfleet
State Park in Uintah County in northeastern Utah,
USA (408300 N, 1098220 3000 W, 1730 m a.s.l.) is dominated by perennial woody species, such as Artemisia
tridentata Nutt. (Asteraceae), Chrysothamnus nauseosus
(Pallas) Britt. (Asteraceae) and Juniperus osteosperma
(Torr.) Little (Cupressaceae). Cryptantha is the dominant subshrub species. Detailed descriptions of the
experimental design are provided elsewhere [86].
Briefly, we established six 5 5 m2 permanent plots
in early spring 1997, ensuring at least 20 m distance to
encompass spatial heterogeneity. Each plot contained
13 – 1 1 m2 quadrats arranged in a chequerboard pattern. We conducted censuses each end of May,
coinciding with the peak of the flowering for the study
species (figure 2a). For each individual, we measured
its Cartesian coordinates with reference to the plot to
enable relocation each year and counted total number
of living rosettes and number of reproductive rosettes.
In addition, we carefully checked for the establishment
of new recruits. During the length of this study, we
followed 1232 individuals over 60 m2. The 2002
census was not carried out, and here we report the
dynamics of the 2001 – 2003 annual period instead
of 2001– 2002 and 2002 –2003 (see the electronic
supplementary material, appendix SA).
Phil. Trans. R. Soc. B (2012)
We also studied the dynamics of a natural population of Carrichtera for 8 years (2001 –2009). The
perennial vegetation at the fieldsite located in the
Northern Negev desert (318230 N, 348540 E, 590 m
a.s.l.) consists of dwarf shrubs, mainly Sarcopoterium
spinosum (L.) Spach (Rosaceae), associated with herbaceous, mainly annual, plant species [87]. Among
the annual species, Carrichtera is one of the most
abundant. Five 10 25 m2 permanent plots were established in the 2001 dry season. Each plot contained ten
20 20 cm2 permanent quadrats. We monitored them
twice annually to quantify population size of seedlings
(November–December) and adults (March) (figure
3b; see [88]). At the end of each growing season in all
years except 2005, per capita biomass was measured by
harvesting individuals in randomly chosen quadrats.
In 2008, 29 randomly chosen individuals were harvested
to examine the seed number–biomass relationship.
The seed bank was inspected using 10 random
5 5 5 cm3 units per plot annually at the end of the
dormant season, before the onset of autumn rains. Soil
samples were spread in plastic trays and irrigated
during winter in a net-house at the Botanical Gardens
of Tel Aviv University (Israel). Soil collection was done
each year and each year’s collection was germinated in
three consecutive years. Emerging seedlings were
counted and continuously removed until no further
emergence was observed (more details in [89]). Biomass
and seed bank sampling, both invasive methods, were
carried out in restricted areas within the permanent
plots to avoid disturbance of natural population
dynamics in the permanent quadrats.
(c) Size-/stage-structured demographic models
To explore the effects of projected shifts in precipitation
regime (figure 2b) on the population of Cryptantha and
Carrichtera, we used two well-established demographic
approaches: integral projection models (IPMs hereafter;
[24]) for Cryptantha and periodic matrix models
(PMMs hereafter; [90]) for Carrichtera. The usage of
each model was tailored to the biology and life history
of each study species.
We applied an IPM framework to the long-term
demographic data of Cryptantha. Briefly, an IPM links
the size distributions of individuals in a population
one year to the distribution the next year by explicitly
incorporating the effect of individual size on the vital
rates that affect survival and reproduction, and thus ultimately population growth rate (l) [24]. The vital rates
incorporated in our IPM to describe the life cycle of
Cryptantha are described in figure 3a. We chose
an IPM approach for the demographic dataset of
Cryptantha, instead of classical matrix models where
individuals are categorized into a small number of
stages [23], because Cryptantha’s vital rates of survival
(s), change in size (g), reproduction (w) or recruitment
(x ; figure 3) were more adequately described by continuous functions of size than by the discrete step
functions (not shown). In addition, IPMs represent a
preferable approach over discrete projection matrices
because the former (i) describe better large-size variations exhibited by individuals in the population [91],
as in Cryptantha; (ii) are more robust when data are
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Climate change and plant demography R. Salguero-Gómez et al.
limiting [92,93], as it was here the case in some
annual periods (x ¼ 254.86 + 44.78 (s.e.) individuals
per annual period; range ¼ 92–582); and (iii) are also
applicable to data that are not truly continuous, as
here (i.e. rosette numbers [94]).
We applied a PMM approach to Carrichtera. PPMs
describe cyclic temporal variation and account for the
effects of multiple demographic processes [90,95] that
typically govern annual species population dynamics.
In this case, data were collected for four discrete
plant stages and not as a function of plant size, as for
Cryptantha. Namely, these are: reproductive individual, dormant seed, germinable seed and seedling;
and during three time points, which defined three
seasons: dormant, post-dormant and pre-dormant seasons. In the constructed demographic model, the life
cycle of Carrichtera can be thought of as having two
pathways: a vegetative pathway, where adults produce
seeds that germinate the same year of their production,
and a dormant pathway, where seeds remain in the seed
bank (figure 3b). A description of the vital rates used
in this model is provided in figure 3b. Details of
both the IPMs and PMMs are described in electronic
supplementary material, appendix SB.
(d) Projecting demographic effects of changes
in precipitation
We explored how the population dynamics of
Cryptantha and Carrichtera are likely to change from
current to projected precipitation conditions. We first
classified each annual period for which we had demographic information as an extreme precipitation or
average precipitation period. We obtained annual precipitation records from the closest permanent weather
station to both field sites for the 30 years previous to
the last census: 1981 – 2011 for Cryptantha [86] and
1979– 2009 for Carrichtera [87]. Then, we calculated
annual precipitation as the sum of monthly precipitations from May of year t to April of t þ 1. In this
way, annual precipitation was temporally matched for
later analyses with population growth rates, based on
the timing of the field censuses (figure 3; see the electronic supplementary material, appendix SA). We used
the 75th and 25th percentiles of these precipitation
records as the thresholds to classify annual periods as
wet, normal or dry. These percentiles were 399.35
and 288.16 mm for Cryptantha and 321.31 and
212.46 mm for Carrichtera (see the electronic supplementary material, appendix SD). Consequently,
under current precipitation conditions, the probability
of occurrence of a wet, normal or dry annual period
was 0.25, 0.5 or 0.25, respectively, in both field sites
(table 1). This discrete classification of annual periods
in demographic models, instead of using continuous
classifications of precipitation [96], is based on the
deserts’ wide variation in precipitation (precipitation
coefficients of variation: 25.47% near Utah, USA
field site, and 32.25% near Israel field site, based on
permanent weather station records).
Next, we calculated the probability of occurrence of a
wet, normal or dry annual precipitation period in
the future. We obtained high-resolution precipitation
data for both field sites from the MRI-AGCM3.2S
Phil. Trans. R. Soc. B (2012)
3107
Table 1. Probability of occurrence of wet, normal and dry
annual periods at both field sites based on current (1981 –
2011) in situ precipitation records, and projected (2075–
2099) scenario under the super-high-resolution climate
change model used in this manuscript [76]. Superscript
‘m.s.’ denotes marginally significant at 0.05 , p , 0.10.
wet
normal
dry
Cryptantha flava
(UT, USA)
Carrichtera annua
(Israel)
current
projected
current
projected
0.25
0.50
0.25
0.33
0.50
0.17
0.25
0.50
0.25
0.21
0.25m.s.
0.54*
*Significant differences at p , 0.05.
super-high-resolution climate model ([76]; R. Mizuta
2012, personal communication). The models were
run for the four 20 km2 grids around the GPS coordinates of the centre of both populations. The model
output consists of monthly precipitation into the past
(1979–2003) using the AMIP scenario (back-projected
precipitation, hereafter; see the electronic supplementary
material, appendix SC) and into the future (2075–
2099; projected precipitation, hereafter) using the A1B
scenario of the IPCC [4]. We classified wet, normal
and dry annual periods using the 75th and 25th percentiles from the back-projected precipitation. We then
applied the percentile values from the back-projected
to the projected model to get the probabilities for wet,
normal and dry annual periods in the future. We used
back-projected model values, instead of the permanent
weather stations, because precipitation means were
lower for the back-projected precipitation values
(Cryptantha: xcurrent ¼ 350.75 + 16.31 mm (s.e.),
xback-projected ¼ 267.67 + 10.09 mm, t46.79 ¼ 4.33, p ,
0.001; Carrichtera: xcurrent ¼ 264.43 + 15.57 mm,
xback-projected ¼ 238.09 + 13.00 mm, t51.78 ¼ 1.30, p ¼
0.20). Thus, imposing the percentiles of the current
weather would have resulted in future projections for a
higher frequency of dry periods in Utah, USA, when
in fact a significant increase in precipitation has
been recorded during the last 75 years at the field site
(R. Salguero-Gómez 2012, unpublished data). With
this approach, we also secured that the percentile
thresholds would result in 0.25, 0.50 and 0.25 probabilities for wet, normal and dry annual periods under backprojected precipitation conditions (see the electronic
supplementary material, appendix SC). Finally, we
compared whether the frequency of wet, normal and
dry annual periods changed significantly between current and projected scenarios using z-tests for two
proportions of independent groups [97].
To explore short-term effects of precipitation on the
population of both species, we quantified the overall
demographic performance for each annual period of
our studies. We calculated the deterministic population
growth rates (l) as the eigenvalue of each discretized
kernel K resulting from the IPMs of Cryptantha, and
annual projection matrix A resulting from the back-multiplication of the periodic matrices of Carrichtera.
Briefly, the kernel K and the annual projection matrix
A describe the population dynamics in each population.
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3108
R. Salguero-Gómez et al.
Climate change and plant demography
A detailed description of their construction and analyses is available in the electronic supplementary
material, appendix SD. The deterministic population
growth rate describes the asymptotic growth of a population under constant environmental conditions without
density-dependence [23]. We jack-knifed the individual
data for both species 999 times and re-calculated the K
kernel and A matrix for each annual period. Next, we
used Spearman’s rank correlation coefficient (r)
to correlate annual period precipitation with the
jack-knifed population growth rate values.
We accounted for the large variation in precipitation
at the Colorado Plateau and Negev deserts by quantifying stochastic population growth rates (a ¼ log(lS))
of both populations. A set of discretized, annual kernels K for Cryptantha, and a set of PMMs Bi (the
matrix that describes the population dynamics within
each season in the life cycle; see the electronic supplementary material, appendix SD) for Carrichtera
were then randomly chosen, after having been classified into dry, normal or wet annual periods under the
aforementioned current and projected precipitation
scenarios. This approach treats the variability within
each period as crude estimates of the variation in the
vital rates [98]. The model abstracts a continuous
environmental factor into a finite set of discrete environmental states [23]. The sampling frequency of each type
of kernel/matrix depends on the frequency of wet,
normal and dry annual periods described in the electronic supplementary material, appendix SA. We
estimated lS using the mean population size over T ¼
4000 iterations, but discarding the first 250 projections
in order to avoid transient dynamics [98]. This simulation was replicated 100 times to quantify variation.
The population growth rate was calculated as
a ¼ logðls Þ ¼
ðlog NðT Þ log Nð0ÞÞ
;
T
ð3:1Þ
where N(0) is the mean population size at time t ¼ 0 and
N(T ) the mean population size 3750 iterations later.
We obtained a more mechanistic understanding of
potential differences in the stochastic population
growth rates during current versus projected scenarios
by calculating their stochastic elasticities. In its simplest form, deterministic elasticities inform about the
relative importance of a given demographic process
(e.g. reproduction) on the deterministic population
growth rate, l [23,99]. A stochastic elasticity (E S)
takes into account the variation in vital rate values
through time [100]. However, E S can be difficult to
interpret because it includes the effect of mean and
variation in values of the vital rates on a. Consequently, we also calculated the stochastic elasticity
E Sm for perturbations onto mean vital rate values and
the stochastic elasticity E Ss for perturbations onto
vital rate variances. We performed these calculations
in R [101] modifying available programming [100].
We implemented stochastic elasticities analyses tailored to the two demographic models employed. For
the IPMs in Cryptantha, we perturbed (i.e. increased
by an infinitesimal amount, 0.0001) the intercept of
the vital rates of its life cycle (figure 3a; see the electronic supplementary material, appendix SC). Our
Phil. Trans. R. Soc. B (2012)
approach affected all individuals equally, as opposed
to individually as a function of their sizes, which
would be difficult to justify from a biological point of
view. For instance, this infinitesimal increase in the
intercept of the regression for changes in size g
resulted in bigger individuals, regardless of initial size
[96]. For the PMPs in Carrichtera, instead of perturbing the elements of the annual matrix A (see the
electronic supplementary material, appendix SB),
which would blur different biological processes, we
carried out vital rate perturbations in the periodic
matrices following methods described elsewhere [95].
(e) Results
Precipitation monthly regimes and annual amounts are
projected to change in opposite directions in the two
regions. In the case of Cryptantha in northeast Utah,
USA, the super-high-resolution climatic model projects an increase in frequency of wet periods in
comparison to the actual historical records, which
results in fewer dry periods while normal precipitation
periods will remain the same (table 1). However, we
must note that these shifts are not statistically significant. Projections also report a lengthening of the
growing season of Cryptantha, with more precipitation
in March and August (figure 2b). In contrast, in the
case of Carrichtera in Israel, the climatic model projects more frequent dry periods (z ¼ 22.20, p ¼
0.03), halving the frequency of normal precipitation
annual periods (z ¼ 1.90, p ¼ 0.058), and slightly
decreasing the frequency of dry periods (table 1). In
this region, winters (December, January and February) are expected to become drier with an increase in
precipitation in May, that is, after desert annuals
have shed their seeds (figure 2b)
The deterministic population growth rates (l) of
both species were strongly affected by annual current
precipitation. In Cryptantha, the effect of precipitation
on l was positive (Spearman’s rank correlation coefficient r ¼ 0.17, p , 0.001). For Carrichtera, when all
annual sampled periods were included, there was a
negative correlation between precipitation and l
(r ¼ 20.11, p , 0.001). However, this correlation
was mostly driven by the high l jack-knifed values
during 2008 –2009 (see the electronic supplementary
material, appendix SA). Treating this annual period
as an outlier resulted in a positive correlation between
l and annual precipitation (r ¼ 0.77, p , 0.001).
The projected precipitation scenarios increased
population growth rates of both species, even though
an increase in precipitation was projected for Cryptantha
and a decrease for Carrichtera. The stochastic population growth rate (a; equation (3.1)) of Cryptantha
under current precipitation conditions was significantly lower than zero (acurrent ¼ 20.1752 + 0.04
(95% CI)), implying demographic inviability under
the present precipitation regime. In contrast, its
aprojected ¼ 20.044 + 0.05 for the projected precipitation scenario was statistically greater than Acurrent
(t23896.59 ¼ 106.15, p , 0.001), and overlapped with
zero, implying demographic viability (figure 4). In
Carrichtera, the fitness values under current and
projected conditions indicated demographic viability
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Climate change and plant demography R. Salguero-Gómez et al.
stochastic population growth rate
0.3
0.2
***
0.1
0
***
–0.1
–0.2
–0.3
Cryptantha flava
Carrichtera annua
Figure 4. Stochastic population growth rates (a ¼ log(lS) +
95% CI; number of jack-knife iterations ¼ 999) under current
and projected changes in frequency of wet, normal and dry
annual periods (table 1) in the studied populations of the perennial C. flava and the annual C. annua. Three asterisks (***)
represents significant differences at p , 0.001. Filled bars
denote projected, unfilled bars, current.
(acurrent ¼ 0.015 + 0.03, aprojected ¼ 0.138 + 0.04), but
the projected demographic performance was also significantly greater under projected than under current
conditions (t15997.81 ¼ 7.58, p , 0.001; figure 4).
Neither for Cryptantha nor for Carrichtera were the
magnitudes of total stochastic elasticities (E S), mean
stochastic elasticities (E Sm) and variance stochastic
elasticities (E Ss) to vital rates drastically different
under current and projected precipitation conditions
(figure 5). For Cryptantha, population dynamics
under projected conditions relied more on survival
(s) and changes in individual size (g ; both growth
and shrinkage), as well as greater sizes of new seedlings
(q), and less on reproduction (c) and establishment
(1) probabilities. The effects of variation in all vital
rates on the stochastic population growth rate a were
negligible, with the exception of changes in individual
size (figure 5c); the ability to rapidly change in size had
a positive effect on the population growth rate. For
Carrichtera, differences in the relative impact of the
vital rates on a were negligible, despite the significant
differences in a values shown in figure 4 under current
and projected conditions. All its vital rates had an overall similar effect on a when considering effects of mean
and variance in vital rates simultaneously, as depicted
in E S values (note that for each season SE S ¼ 1).
However, the effect of mean values (E Sm) of emergence
of seeds from the seed bank (1germ) was one order of
magnitude greater than the effects of mean values for
all other vital rates. The impact of variation of 1germ
(E Ss) was greatly negative. The impacts of E Ss for
contributions of adults were positive if the seed went
into the seed bank (cbank), and negative when seeds
germinated the same year as that of production (cgerm).
4. CLIMATE CHANGE, PRECIPITATION AND
DESERT PLANT DEMOGRAPHY
We found a surprising pattern of increased population
growth for both study species when we compared
Phil. Trans. R. Soc. B (2012)
3109
population dynamics in the future to current conditions,
consistent with increasing precipitation in Utah, USA
and despite decreasing precipitation in Israel. Our findings support our hypotheses for C. flava’s improved
demographic performance in wetter years and highlight
the potential of the annual C. annua to buffer stochasticity of drier years via its seed bank (i.e. demographic
buffering [33,34]). This is the first usage of a comparative demographic approach studying desert plant
responses to climate change, and our conclusions
challenge the commonly held perception based on
correlative approaches (e.g. bioclimatic envelope
approaches) suggesting that desert organisms may be
particularly vulnerable to climate change [14,20–22].
The tools we have used here, size-/stage-structured
population models [23,24], provide a robust, quantitative link between the overall characteristics of the
population (e.g. population size and growth rate), their
underlying vital rates (e.g. survival, changes in size, germination, seed dormancy), and evolutionary pressures
[96,99]. In particular, our stochastic simulations based
on high-resolution projections of precipitation for
2075–2099, as well as on long-term, field-collected
demographic data, allowed us to discern the vital rates
underlying the demographic improvement. Interestingly, the significant increases in stochastic population
growth rates took place with relatively little change in
the relative impact of the vital rates. In the case of the
population of Cryptantha in Utah, USA, where more frequent rainy years and a resulting longer growing season
are projected, population growth rates are expected to
increase, mediated through more drastic changes in
size (growth and shrinkage), increases in survival and
in size of new recruits. The fact that such changes in
size, when examined in a stochastic, long-term perspective, currently and in the future have positive impact on
the stochastic population growth rate might provide
further support for the hypothesized adaptive value of
hydraulic fragmentation [9]. Internally fragmented individuals in desert species typically experience rapid
shrinkage under dry conditions [56,81]. We believe
that the linkage of this phenomenon to population
dynamics deserves further attention [52].
Our analyses highlight the crucial role of seed
dormancy in C. annua in Israel as a bet-hedging mechanism buffering extreme precipitation years. In both
current and future scenarios, the vital rate elasticity to
seed bank emergence was the most important one to
population growth. In this population, we were able to
discern a complex pattern behind the almost identical
vital rate stochastic elasticities under current versus projected conditions: reducing only the frequency of wet
years in our models led to a decrease in the relative
importance of the vegetative pathway, with seeds germinating the same year of their production (figure 3b). On
the other hand, increasing only the frequency of dry
annual periods had the opposite effect: the relative
impact of the dormant pathway, with seeds remaining
in the seed bank, decreased (W. Siewert 2012, unpublished data). Since wet periods will become less
frequent and dry periods more frequent in the climate
change projection, the effects cancel each other out,
resulting in negligible difference, but still producing a
higher growth rate than under current conditions.
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3110
R. Salguero-Gómez et al.
Climate change and plant demography
1.2
stochastic elasticity
(E S)
Cryptantha flava
(a)
1.0
stochastic elasticity
to mean (ESm)
(b)
Carrichtera annua
current
projected
0.8
0.6
0.4
0.2
0
5
4
3
2
1
0
stochastic elasticity
to variance (ESs )
(c)
0
–2
–4
–6
y
s
g
e
c
dgerm
q
vital rates
s
dbank1
ygerm
egerm
dbank2 ybank dbank3
vital rates
Figure 5. (a) Stochastic elasticity of the stochastic growth rate (a ¼ log(lS)), and stochastic elasticity of a to (b) the mean and
(c) variance of each of the vital rates involved in the life cycle of the perennial C. flava and the annual C. annua (figure 3) under
current (open bar) and projected (filled bar) precipitation regimes. Negative values indicate that increasing variability of a vital
rate decreases a. Vital rates for Cryptantha: survival (s), change in size (g), probability of reproduction (w), production of flowering stalks (x), seedling establishment (1) and seedling size (q). Vital rates for Carrichtera: germination probability (dgerm),
seedlings survival (s), germinable seed production (cgerm), survival in seed bank (dbank1, dbank2 and dbank3), seed-bank contribution (cbank) and seed-bank emergence probability (1germ).
However, it must be noted that a single and rather
exceptional year is responsible for the increase in stochastic population growth rate. In the 2008– 2009
annual period, the driest one in our study, we measured
an extremely high population growth rate owing to very
high fecundity. If we excluded this year from our simulation, we found a decreasing growth rate with
increasing frequency of dry years. Still, the correctness
of the measured fecundity was confirmed by a record
number of individuals in the following 2009 –2010
growing season ( J. Kigel 2012, unpublished data).
Very high fecundity associated with a drought year is
unusual in desert annual demography and inconsistent
with general findings of reproductive failure (see §2b).
A possible explanation for this pattern may be reduced
competition from coexisting plant species. Indeed,
population size of Trisetaria macrochaeta (Poaceae), the
most abundant species at the site, was the lowest
during 2008–2009 (W. Siewert 2012, unpublished
data). Nonetheless, future work will re-visit the present demographic projections with higher temporal
replication in the estimates of seedbank dynamics.
Phil. Trans. R. Soc. B (2012)
Our study contributes two notable exceptions to
the accepted view that short-lived species, regardless
of habitat, are particularly vulnerable to climate
change [26]. We argue that for both species, the potential for demographic buffering is high, in the light of
the resulting higher stochastic population growth
rates. However, other plausible explanations, such as
interannual co-variance of vital rates [102], deserve
further exploration. The simplicity of our modelling
approach, whenever long-term demographic data is
available, together with the robustness of the climatic
projections, calls for its application to other species,
particularly when considering the urgent need to
understand responses to climate change of more
desert species that might prove important in alleviating
poverty. If our findings are applicable to other desert
plant species, the implications for carbon storage
[103,104], particularly below-ground, exploitation of
natural resources [105], and self-sustainability should
be re-evaluated in the context of the large amount of
dryland human inhabitants [2], a number that is
only expected to increase owing to desertification [3].
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Climate change and plant demography R. Salguero-Gómez et al.
(a) Future directions
Clearly, we are still far from achieving a detailed understanding of how climate change will affect desert plant
species in general, or whether it will at all, given their
potential for buffering abiotic stochasticity. More and
longer studies with more frequent censuses will help
in this task by encompassing a large range of probable
precipitation situations to which desert plants are
exposed. Demographic studies in which plots exposed
only to natural precipitation are revisited every decade
[39,40,44] may not offer enough resolution to examine
the underlying vital rates that govern the population
dynamics, especially if large positive and negative
changes in individual size may occur [77], or provide a
mechanistic understanding of the effects of precipitation. We see great value in simulating expected
precipitation pulses experimentally, as in physiological
studies [106–108], but at the whole-population level.
This approach can drastically decrease the amount of
years necessary to provide robust demographic projections (R. Salguero-Gómez 2012, unpublished data).
The coupling of field-based studies with greenhouse
experiments to explore more obscure demographic processes, such as seed bank and vegetative dormancy,
will also be beneficial here [49–51]. Along the same
lines, the conclusions of our field study where only
one population was studied per species must be carefully
evaluated. Demographic heterogeneity has been shown
in different populations within the same species [109] in
other ecosystems and is likely not an exception in
deserts. Better spatially replicated studies are needed
in deserts, perhaps including populations from recently
desertified versus historically desert regions.
Demographic studies that reach beyond charismatic
taxa (e.g. Cactaceae; figure 1c) and field sites close to
research groups (e.g. USA, Australia; figure 1a) need
to be carried out. As a suggestion, the demography of
dominant desert families, such as the Agavaceae, Aizoaceae, Cyperaceae and Rhamnaceae remain completely
unexplored. Likewise, despite the crucial role that biological soil crusts play in ecosystem functioning and
structure [110], no demographic model has studied
these lichen-moss-cyanobacterial symbiotic assemblies.
It is also puzzling that so much plant demography has
been done in other ecosystems (figure 1b), despite
deserts’ species richness and extension [2]. Geographically, it seems logical that research efforts should
prioritize demographically unexplored real deserts (less
than 100 mm yr21) such as the Patagonian, Sahara,
Namib, Kalahari, Karakum, Kavir, Taklamakan and
Gobi (figure 1a). Finally, we call for the importance of
comparing underlying vital rates of populations of the
same species under different aridity gradient values.
Work in this regard has shown drastic changes in seed
production and seedling establishment [111]. We
hope that a greater interest in deserts will generate
more long-term demographic datasets to which superhigh-resolution climatic models [76] can be applied.
Such efforts should result in a more comprehensive
understanding of how deserts will fare in the future.
The authors are most grateful to R. Mizuta, A. Kitoh and
M. Hosaka for providing the super-high-resolution
precipitation projections used in this manuscript. LongPhil. Trans. R. Soc. B (2012)
3111
term research on C. flava was supported by grant IBN95–
27833 (National Science Foundation) to B.B.C., and by
CTL Fellowship, Binns-Williams Funds, Forrest Shreve
Desert Ecology Award (Ecological Society of America),
Grant-In-Aid of Research (Sigma Xi), Lewis & Clark
Funds for Exploratory Field Research (American
Philosophical Society), and the Max Planck Institute for
Demographic Research to R.S.-G. Long-term research on
C. annua by W.S. and K.T. is part of the GLOWA Jordan
River project funded by the German Federal Ministry of
Education and Research (BMBF). R.S.-G. and B.B.C.
thank H. and P. Kempenich, C. Plunkett, J. Sinclear,
J. Salix and T. Faircloth from the US Forest Service and
Bureau of Land Management in Vernal, UT, for logistical
support. W.S and K.T. thank J. Metz for doing most
censuses, and J. Kigel and M. Sternberg for sharing data
on biomass and seed bank dynamics, as well as for
logistical support.
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