TUGAS

EKOLOGI TUMBUHAN
RESUME JURNAL

OLEH :
VIRA YORISKA
18031117
PENDIDIKAN BIOLOGI C

DOSEN PENGAMPU :
Dr. AZWIR ANHAR. M. Si

JURUSAN BIOLOGI
FAKULTAS MATEMATIKA DAN ILMU PENGETAHUAN ALAM
UNIVERSITAS NEGERI PADANG
2020
PENGARUH FAKTOR ABIOTIK (LINGKUNGAN) TERHADAP
PERTUMBUHAN TANAMAN
 Efek Radiasi UV-B Terhadap Aspek Morfologi, Fisiologi, dan Biokimia Tanaman

Menipisnya lapisan ozon menyebabkan peningkatan radiasi ultraviolet (UV-B) yang

mencapai permukaan bumi (Madronich et al., 1998). Peningkatan radiasi UV-B akan
mengubah pertumbuhan dan metabolisme tanaman, sehingga radiasi UV-B bertindak sebagai
factor lingkungan / faktor abiotik pada tanaman, yang pada akhirnya menyebabkan
pertumbuhan tanaman terhambat, merusak pigmen fotosintesis, menurunkan asimilasi
karbon, mengubah alokasi biomassa pada akhirnya menghasilkan pengurangan biomassa dan
produktivitas (Tevini dan Teramura, 1989).

Semua tanaman menunjukkan berbagai respons terhadap UV-B, beberapa tanaman

dapat mentolerir ini dan beberapa menjadi sensitif dan tidak dapat mentolerir situasi seperti
itu. Tanaman ini akan memperoleh mekanisme pertahanan yang berbeda seperti peningkatan
ketebalan daun, produksi lebih banyak flavonoid, stimulasi pembentukan antioksidan;
aktivasi spesies reaktif untuk memadamkan radikal bebas, dll untuk melindungi tanaman dari
tekanan lingkungan semacam itu. (Caldwell et al., 2003; Agrawal dan Mishra, 2008).

Morfologi tanaman dianggap sebagai indikator kerusakan UV-B yang sangat efektif.
Pengukuran parameter lain seperti klorofil, karotenoid, fenol, peroksidasi lipid, dll. Juga telah
terbukti bermanfaat sebagai indikator dampak dan sensitivitas UV-B. Tanaman daun lebar
lebih sensitif dibandingkan dengan tanaman daun sempit. Selain itu, anggota family
Cucurbitaceae dan Brassicaceae lebih sensitif. Peningkatan kadar UV-B juga menginduksi
beberapa perubahan morfologi yang umum seperti pengurangan luas daun, penebalan daun,
pengeritingan atau pengupasan daun, peningkatan percabangan, anakan dan jumlah daun,
berkurangnya jumlah buah dan bunga dan pembibitan.

Naiknya radiasi UV-B di lingkungan menghasilkan respons fisiologis yang berbeda

(Tevini dan Teramura, 1989). Perubahan yang diamati setelah radiasi UV-B berlebihan
adalah deformasi epidermal (Tevini dan Steinmuller, 1987), perubahan konduktansi stomata,
perubahan struktur daun ultra, peningkatan tingkat flavonoid (Tevini et al. 1981, 1991, Beggs
dan Wellman, 1985) , pengurangan persentase perkecambahan serbuk sari (Flint dan
Cladwell, 1984), pengurangan biomassa (Tevini et al., 1981; Lydon et al., 1986; Sullivan dan
Teramura, 1988).

Naiknya radiasi UV-B di lingkungan juga berdampak pada hasil panen dan partisi
biomassa. Berkurangnya laju fotosintesis mengubah proses asimilasi karbon di berbagai
bagian mesofil daun. Paparan UV-B ke dedaunan menyebabkan akumulasi karbohidrat dalam
daun. Pembuatan floem adalah proses aktif yang membutuhkan energi dan peningkatan
konsentrasi UV-B mengurangi proses ini.
Journal of Scientific Research Vol. 61, 2017 : 87-113
Banaras Hindu University, Varanasi ISSN : 0447-9483

EFFECTS OF UV-B RADIATION ON MORPHOLOGICAL,

PHYSIOLOGICAL AND BIOCHEMICAL ASPECTS
OF PLANTS : AN OVERVIEW

Kshama Rai1 and S.B. Agrawal1*

1
Laboratory of Air Pollution and Global Climate Change
Department of Botany, Institute of Science,
Banaras Hindu University, Varanasi- 221005
Email id- kshamarai9@gmail.com
*Corresponding author
Email id- sbagrawal56@gmail.com
Phone no. : +91 542 2368156, Fax no. : +91 542 2368174

Abstract
Origin of life was never be thought without considering the role of UV radiation but
once the “boon”, is slowly becoming “curse” for life. Plants are exposed to many
factors but the problem of enhanced UV-B is created by the anthropogenic activities
resulted in ozone layer depletion. However, plants are performing well to cope up with
such problems, but the changing climatic conditions and their interactive effects needs
attention. Focusing on this, the main objective of this study is to summarize the plant
responses observed under various studies against enhanced UV-B. Depletion of
stratospheric ozone layer has created the threat of enhanced UV-B which causes the
reduction of productivity by reducing the rate of photosynthesis, plant growth, and
overall yield in most of the species. So, the scope of further research should be focused
on the selection of tolerant species for improving knowledge, scope of genetic
improvement and other responses against combination of stresses for better
understanding and management of plants with changing climate.
Keywords: Photosynthesis, Lipid peroxidation, Ozone layer, UV-B, Climatic.
Abbreviations: APX - ascorbate peroxidase; CAT - catalase; ˙OH - hydroxyl radical;
LPO - lipid peroxidation; MDA - malondialdehyde; ROS - reactive oxygen species;
SOD - superoxide dismutase; UV-B - ultraviolet B radiation; UV-B BE - biologically
effective UV-B.

Introduction
Although the Earth is now survivable but origin of life was dated back only few
billion years ago and was recorded with the help of some microbial evidences. This
origin of life is mainly supported by the solar spectrum which is the driving force for
entire ecosystems of Earth and is comprised of electromagnetic spectrum including
different wavelengths ranging from radio waves to gamma waves. These
 EFFECT OF UV-B RADIATION ON MORPHOLOGICAL, PHYSIOLOGICAL ... 88

electromagnetic waves helped in the formation of early atmosphere on the Earth and
ultimately lead to the origin of early life.
The more energetic regions of the spectrum are at shorter wavelengths, but the
region of our interest in the spectrum is “Ultraviolet Radiation” which lies at the short
wavelength end. Ultraviolet, visible and infra red rays are critically very important for
life on the Earth. Infra red light and visible light are the part of solar spectrum, which
are responsible for increasing the temperature of the Earth up to the survival range.
Ultraviolet radiation (UV) is a part of the non ionizing region of the
electromagnetic spectrum which comprises approximately 8-9% of the total solar
radiation. UV is traditionally divided into three wavelength ranges: UV-A (320-400
nm) represents approximately 6.3% of the incoming solar radiation and is
comparatively less harmful part of UV- radiation (Table.1). UV-B (280-320 nm) is of
particular interest because this wavelength represents only 1.5% of the total spectrum,
but can induce a damaging effect in plants, animals as well as at ecosystem level
(Table.1). UV-C (200-280 nm) is extremely harmful to organisms (Table.1).
History of Ultra violet radiation
Ancient civilization thought that sun is the ultimate source of visibility, warmth,
health and vitality and their understanding about sun was immersed in the mythology
and cultural traditions. But their newer generations were not satisfied by the
explanations, so they lead to the beginning for search of new thoughts, believes and
understanding. By the start of 9th century, the newer knowledge and principles led to
the realization that sunlight is not a single stimulus of single wavelength but it is a
collection of stimuli of different wavelengths. In that series the discovery of UV
radiation prior to 1920 took place. First of all Sala (1614) made an observation in
which he found that silver nitrate crystal turned black when exposed to sunlight.
Scheele (1777) also found the same phenomenon, when he directed sunlight through a
prism onto a paper, a coloured spectrum was also observed by him. Ritter (1801)
noticed invisible rays beyond violet end of the spectrum and called it deoxidizing rays,
later it was termed chemical rays. Becquerel and Draper (1842) independently
observed that wavelength between 240 to 400 nm induce in or photochemical reaction.
This was the first indication of spectral extent of UV radiation.
Maxwell (1865) proposed the theory of electromagnetic waves. After that a
revolution in the field of solar spectrum studies occurred and by 1920, the existence of
UV radiation, its properties and relationship to sunlight were well established.
UV-B and life of terrestrial plants
Evolution of plants from the early Archean era began as single photosynthetic
cell (Cockell and Horneck, 2001). The effect of ultraviolet radiation is detrimental to
the terrestrial plants. It has been demonstrated with some most important biochemical
machinery i.e. DNA and PS-II (Singh et al., 2008).
 During the course of evolution, when stratospheric ozone was not formed; life
was not possible on land so the first life was originated under water but with the help of
UV-C and other solar radiations stratospheric ozone layer was formed. After that, all of
the UV-A and minor part of UV-B were allowed to reach the Earth’s environment and
UV-C was fully absorbed and scattered. Therefore, it can be said that UV radiation has
regulatory properties and hence, it altered the Earth’s environment over geological time
periods and it is essential to understand the evolutionary history of the Earth and also
the selection pressure developed by UV-B on terrestrial plants. In fact, Sagan (1973)
first considered the UV radiation as a selection pressure on the early photosynthetic
organisms.
The terrestrial plants coevolved under different solar UV-B levels and may have
experienced significantly higher UV-B irradiance during course of evolution than
current surface UV-B level (Cockell and Horneck, 2001; Rozema et al., 2002). So, the
UV-B tolerance acquired earlier; probably helps to explain why plants are distributed at
lower latitudes or higher elevations, where UV-B irradiance is greater, are less
sensitive to high levels of the UV-B radiations than those at higher latitudes and/or
lower elevations (Turunen and Latola, 2005).
UV-B environment of terrestrial plants is quite variable in both time and space
and thus, organisms experiences different UV-B doses and adapt to UV-B radiation at
different levels (Rozema, 2000). In this context, it is expected that terrestrial plants
responds differently to increasing solar UV-B. And because of the increasing
consequences of ozone layer depletion and UV-B irradiances, focus from the point that
UV-B radiation is a component of sunlight which is involved in the evolution of life on
Earth, may have distracted (Cockell and Horneck, 2001).
Ozone and UV-B irradiance
UV radiations are measured in two terms i.e. irradiance and fluence rate.
Irradiance is the radiation falling on a flat surface per unit area per second and when it
is multiplied by time then is called as dose. Fluence rate is the radiation falling on
sphere per unit cross section per second and when fluence rate is multiplied with time,
it is called as fluence. Ozone is a form of oxygen which plays a vital role in the
atmosphere. It is known that the protection of life on the Earth from UV-B and UV-C
radiations is a result of the absorbance of these radiations by stratospheric ozone layer.
While some ozone is also found in the tropospheric region, but its concentration is very
low as compared to stratospheric ozone concentration. In troposphere, ozone is an air
pollutant and is a green house gas which causes harmful effects on both living system
and environment. But in stratosphere, it forms a thick covering around the Earth which
protects the living organisms from the harmful rays of solar spectra. However, due to
anthropogenic activities this protective layer is depleting and it is termed as Ozone
Hole. The thinning of ozone layer less than 220 DU caused by ozone depleting
substances such as halocarbons is called as Ozone hole.
 The stratospheric ozone layer efficiently filters out most of the detrimental
shortwave UV radiation shorter than 280 nm. The absorbance coefficient of ozone
decreases rapidly at wavelengths longer than 280 nm and approaches zero at about 330
nm. This is referred to as “Column Ozone” since it is the total amount of ozone in a
column between the Earth’s surface and the top of the stratosphere; normally expressed
as “Dobson Unit” and abbreviated as “DU”. Therefore, UV-A radiation is virtually
unaffected by changes in ozone concentration. At the Earth’s surface, radiation
becomes significant between wavelengths 290-315 nm, increasing rapidly within this
range by about three orders of magnitude. A small decrease in ozone levels may cause
a large relative increase in biologically effective UV-radiation. In general, each 1%
decreases in ozone concentration causes an increase of 1.3 to 1.8% in UV-B radiation
reaching the biosphere.
The amount of radiation passing through the ozone column is dependent not only
on its concentration in the atmosphere, but also dependent on the elevation above the
sea level and angle of the Earth’s surface. The higher the elevation above the sea
surface the shorter the path through the atmosphere that the radiation has to travel;
which ultimately results in increase in irradiance.
Ozone Layer Formation
Formation of stratospheric ozone is a natural process, whereas formation of
tropospheric ozone is due to anthropogenic activities and tropospheric ozone acts as air
pollutant (secondary pollutant) and also as one of the green house gases.
Main sources of tropospheric ozone are automobiles, xerox machines, biomass
burning etc. In automobiles emissions, nitrogen dioxide breaks in presence of light into
nitric oxide and nascent oxygen which combines, with molecular oxygen to form
ozone.

Stratospheric ozone is formed by the photolysis of molecular oxygen in

thermosphere and formation of ozone takes place in stratosphere because of the
favorable conditions like sufficient oxygen densities.
O2 O + O (in thermosphere)
O2 + O O3 (in stratosphere)
Ozone layer formation and degradation in stratosphere is a natural phenomenon
and a balance is maintained between molecular oxygen (O 2), hydroxyl ion (.OH) and
peroxy radical (HO2.), which maintains the thickness of ozone in stratosphere. But any
disturbance in the surrounding atmosphere like entry of ozone depleting substances
causes disturbance in these natural processes and depletion of ozone layer starts.
Through various studies it was found that 5% decrease in ozone layer thickness causes
10% increase in UV-B radiation penetration.
Ozone Layer Depletion
The process of ozone layer depletion was first reported by Farman and his team
at South Pole especially in spring season in 1982 and was later confirmed by NASA in
1987. The ozone layer depletion process begins when CFCs, NO X and other ozone
depleting substances (ODS) are emitted into the atmosphere. When this ODS reaches
up to stratospheric region, ozone depletion results. In the presence of strong UV-
radiation, ODS molecules break apart into chlorine atoms and other halogens and these
atoms are actually involved in destruction of ozone. Ozone is continuously produced
and destroyed in a natural cycle and the overall amount of ozone is essentially stable.
This ozone production and destruction are balanced and ozone levels remain stable. But
increase in stratospheric chlorine and bromine upsets that balance leading to decrease
in ozone production and creating ozone levels fall.
Ozone depletion represents two distinct but related phenomena observed in late
1970s i.e. a steady decline of about 4% per decade in the total volume of ozone in
Earth’s stratosphere (the ozone layer) and much larger decrease in stratospheric ozone
layer over Earth’s polar regions. The latter phenomenon results into Ozone Hole. CFCs
and other contributing substances are referred as ozone depleting substances (ODS).
The ozone layer inhibits the penetration of most harmful UV-B (280-320 nm) of UV-
radiation from passing through the atmosphere. The observed decrease in ozone
concentration have generated a worldwide concern, leading to the adoption of the
Montreal Protocol that bans the production of CFCs, halogens and other ozone
depleting substances such as carbon tetrachloride and trichloroethane.
Ozone can be destroyed by a number of free radicals such as hydroxyl free
radical (OH.), nitric oxide free radical (NO.), chlorine free radical (Cl .), peroxy radical
(HO2.) superoxide radical (.O2-) and these are found in certain organic compounds
especially CFCs. The Cl and Br atoms are liberated from the parent compounds by the
action of ultraviolet radiation.
CFCl3 + electromagnetic radiation → CFCl2 + Cl
These free radicals can then destroy ozone molecules through variety of
reactions. The simplest example of such reactions is, a chlorine atom reacts with ozone
molecules to form ClO and leaving a normal oxygen molecule. The chlorine monoxide
(ClO) reacts with second molecule of ozone to form another chlorine atom and two
molecules of oxygen.
Cl + O3 → ClO + O2
ClO + O3 → Cl + 2O2
Other reactions involving ozone destruction are:
 O3 + C2H4 → CH2O2. + HCHO
CH2O2. +SO2 → SO3 + HCHO
O3 + NO → NO2 + O2
NO2 + O3 → NO3 + O2
Consequences of Ozone layer depletion
In the last few decades, there has been an average of 7% increase in biologically
active UV-B radiation in northern mid latitude due to depletion in stratospheric ozone
layer (Yang et al., 2007).
The amount of UV-B radiation that penetrates through the ozone layer decreases
exponentially with the slant path thickness/density of the layer. Correspondingly, a
decrease in atmospheric ozone is expected to give rise to significantly increased levels
of UV-B near the surface.
According to IPCC 2007 report, it has been predicted that if the current rate of
anthropogenic pollution and green house gases emission continues, it will result into
tremendous stress on living system by increasing the concentration of heat trapping
gases which will lead to rise in global temperature from 0.4 oC to 1.1 oC by 2025 and up
to 5.8 oC by 2100. However, the proposed CO2 concentration is 720 to 1020 ppm up to
2100. These climate change models revealed that this climate change will have more
adverse effect than beneficial on ecosystem.
Clouds, Aerosols, Air Pollutants and UV-B irradiance
Stratospheric ozone determines the amount of UV-B radiation that reaches the
surface of the Earth, its level is significantly affected by variations in latitude and
altitude. Level of UV-B over tropical latitude is higher than in temperate region.
Atmospheric UV-B absorption is determined by the solar angle and ozone itself
(thinner in equatorial region). UV-B radiation is relatively high in tropical area and low
in polar area. Other than geographical factors, atmospheric pollutants like Smoke,
aerosols and weather factors like cloud, haze; greatly decreases the level of UV-B
reaching the Earth’s surface. Clouds have a large effect on irradiance on the Earth’s
surface.
Clouds and aerosols scatter radiation, but other air pollutants like sulphur dioxide
absorbs and scatters UV. However, the absorbance of UV radiation by gases other than
ozone is generally a small factor except in highly polluted areas. Thin cloud layers
actually scatter a significant portion of the UV-B towards the Earth, while thick cloud
layers scatter most of the UV-radiation back to the space. Thus, it can be said that
clouds are not necessarily good protector from sun burn. Depending upon the type and
height of clouds, light water content and particle distribution, cloud cover can attenuate
over 70% of the incident UV-B radiation (McKenzie et al., 2007).
Steps for recovery of ozone layer
In 1972, it was warned that nitrous oxide and CFCs (Chlorine containing
compounds) causes the breakdown of large amount of ozone in the stratosphere
(Molina and Rowland, 1974; Velders et al., 2007). This fact causes the depletion of
stratospheric ozone layer, increasing the UV-B radiation at the ground level, especially
in Antarctica and Arctic region as well as at high altitude area. After which the British-
Antarctica Survey was done by Farman et al. (1985) and the result of the survey
showed a springtime ozone hole in Antarctic ozone layer. In the same year, 20 nations
signed the Vienna Convention, which established a frame work for negotiating an
international regulation on ozone depleting substances.
On September 16, 1987, the Montreal Protocol on “Substances that deplete the
Ozone layer” was signed and applied on January 01, 1989 (Veldars et al., 2007). The
ozone depletion is a global phenomenon and according to European Ozone Research
Coordinating Unit (EORCU) its amount reaches approximately 0.6% per year. Despite
reductions in production and use of ozone depleting chemicals, the potential of ozone
depletion by anthropogenic emissions or natural causes (e.g. Volcanoes) still remains.
Recently, in 2016, a springtime recovery in ozone layer is reported by Solomon et al.
(2016) over 1.5 million sq. miles.
Effects of UV-B on Plants
Depletion of ozone layer leads to the increase in ultraviolet radiation (UV-B)
reaching to the Earth surface (Madronich et al.,1998). Increase of UV-B radiation will
alter the growth and metabolism of plants, thus UV-B radiation acts as an
environmental stress/ abiotic factor on plants, which ultimately causes the slowing of
plant growth, damages the photosynthetic pigments, lowers the carbon assimilation,
altering the biomass allocation ultimately results in reduction of biomass and
productivity (Tevini and Teramura, 1989).
All the plants show various responses to UV-B, some plants can tolerate this
stress and some becomes sensitive and cannot tolerate such situation. These plants will
acquire different defense mechanisms like increased thickness of leaves, production of
more flavonoids, stimulation of the antioxidant formation; activation of the reactive
species to quench free radicals, etc to protect the plants from such kind of
environmental stresses. (Caldwell et al., 2003; Agrawal and Mishra, 2008). Rise in UV-
B radiation in the environment results into different physiological responses (Tevini
and Teramura, 1989). Changes observed after supplemental UV-B radiation includes
epidermal deformation (Tevini and Steinmuller, 1987), changes in stomatal
conductance, changes in ultra structure of leaves, increased level of flavonoids (Tevini
et al. 1981,1991; Beggs and Wellman, 1985), reduction in percentage of pollen
germination (Flint and Cladwell, 1984), biomass reduction (Tevini et al.,1981;Lydon et
al., 1986; Sullivan and Teramura,1988). These changes could be the result of DNA
damage, photosynthetic damage, alteration in membrane, destruction of protein,
hormone inactivation (Tevini et al. 1989, 1991b), and signal transduction through
phytochrome (which photoconverts in response to UV-B)(Pratt and Butler, 1970), or
signal transduction via a UV-B photo receptor.
Morphological changes induced by UV-B
Morphology of plants is considered to be a very effective indicator of UV-B
damage. Measurements of other parameters like chlorophyll, carotenoids, phenols, lipid
peroxidation, etc. have also proved to be useful indicators of UV-B tolerance and
sensitivity.
Solar radiation comprised of various radiation, among which the percentage of
UV-B is very less but the range of its morphological effects on plants is very diverse.
And these changes includes from increase in leaf thickness, discoloration of leaves,
increase in leave serration to changes in root-shoot ratio (Jansen et al., 2002).
As a result of UV-B stress, initially bronzing, cupping, glazing of leaves are
observed which is followed by development of irregular patches and with prolonged
exposure, these patches gets converted into brown spot and dies (Singh et al., 2008).
Zhao et al. (2003) has reported that these chlorotic and necrotic spots are formed due to
decrease in chlorophyll content. It was also reported that leaf size decreases, leading to
less leaf area and lesser branches, extension rate of stem also declines (Kakani et al.,
2003; Reddy et al., 2003; Zhao et al., 2003) but sometimes opposite trends was
observed like intense branching, more number of internodes, increased plant height and
dense canopy. Exposure to UV radiation also leads to increase in cuticular wax
deposition.
Kakani et al. (2003) had reported that prolonged exposure of UV-radiation leads
to delayed flowering in different crops; opposite to that Sinclair et al. (1990) has told
that early bud or flower development or time of first flower is not affected by UV-B.
Broad leaf plants are more sensitive in comparison to narrow leaf plants.
Moreover, the members of family Cucurbitaceae and Brassicaceae are more sensitive.
Increased level of UV-B also induces some common morphological changes such as
reduction in leaf area, thickening of the leaves, curling or cupping of the leaves,
increases in branching, tillering and number of leaves, decreases in number of fruits
and flowers and seedling.
Reduction in leaf area occurs due to destruction of photosynthetic pigments but
to cope up with the situation and to increase photosynthesis, number of leaves increases
into the affected plants, which ultimately leads to increased number of branching in
dicots and increased number of tillers in monocots. Most of the energy is lost in repair
mechanisms, leading to the reduction in flowering and fruiting. Moreover, thickening
of leaves are a defense mechanism acquired by the plants in order to increase the path
length of UV radiation.
Due to conversion of Indole-acetic-acid into 3-methylene oxindole curling of
leaves takes place.
 By this conversion, less growth of the upper side and normal growth of the lower
side of the leaves take place, this ultimately causes the cupping of leaves (Kakani et al.,
2003).
Physiological changes induced by UV-B
The process of conversion of CO2 and water into carbohydrate in the presence of
sunlight is termed as “Photosynthesis”. Photosynthetic apparatus is comprised of two
photosystems: PS-I and PS-II. Although UV-B encroaches most of the aspects of
photosynthesis such as damages to ultra structure of chloroplast and light harvesting
complex, decrease in the activity of Rubisco, decline in the oxygen evolving and CO 2
fixation, reduction in the chlorophyll and starch content. And the photosynthetic
responses of plants towards UV-B radiation depend on plant species, cultivars,
experimental conditions, UV-B dosage, and the ratio of PAR to UV-B radiation.
But the main target of UV-B is PS-II (Fiscus and Booker, 1995). PS-II is a
complex of protein and pigment which transports the flow of electron(s) from splitting
of water to plastoquinones (Barber et al., 1997; Mattoo et al., 1999). PS-II is
comprised of two proteins, namely D1 and D2, which forms the core of PS-II. These
two proteins are very sensitive against UV-B and UV-B driven degradation of D1 and
D2 protein leads to impairment of PS-II, which can be measured in terms of decreased
oxygen evolution or variable chlorophyll florescence. This variable chlorophyll
florescence is often intended as a measure of radiation-damage to PS-II.
According to previous reports, almost all components from Mn binding sites to
plastoquinone acceptor sites within PS-II on thylakoid membrane are sensitive against
UV-B. In addition, some indirect effects of UV-B are also observed which alters the
rate of photosynthesis, such as, stomatal closure, changes in leaf thickness and
anatomy, decrease in individual leaf area and total canopy leaf area. According to Van
Rensen et al. (2007) damage caused by UV-B radiation occurs first on the acceptor side
of photosystem II and only later on the donor side.
Due to elevated UV-B, changes in ultra structure of leaves takes place, which
modifies the light attenuation by leaf and the total UV-B radiation in turn, affect
photosynthesis. Leaf reflects 3-6% (Gao et al., 1996, Yang et al., 1995) to 10-40%
from pubescent or glaucous surface (Robberecht and Caldwell, 1980). An increase in
incident UV-B radiation would increase the amount transmitted if no additional
reflection occurs at leaf surface. Plant species differed in their anatomical responses to
UV-B radiation, while increase in leaf thickness due to UV-B was common (Nagel et
al., 1998; Bornman and Vogelman, 1991). The palisade cells from UV-B irradiated
leaves of species were wider. The increase in cell number would increase the cell wall
surface area, which blocks and prevents the harmful UV-B radiation from reaching the
abaxial photosynthetically active mesophyll. The increased palisade cell number would
also increase the amount of air cell wall interfaces, an important parameter that affects
reflectance (Knipling, 1970) and transmission of the incident radiation through the leaf
surface (Bornman and Vogelman, 1991).
 Other changes produced by elevated UV-B include more trichomes on the
abaxial leaf surface (Barnes et al., 1996), a reduction in number and diameter of xylem
tubes, decreased stomatal frequency and distorted leaf area (Lingakumar and
Kalandaivelu, 1993). These adverse effects of UV-B on leaf anatomy would inhibit the
uptake of CO2 and in turn more assimilate production. UV-B exposure also reduces the
CO2 fixation by decreasing the activity and concentration of Rubisco. This decline in
the activity of Rubisco is due to the decrease in soluble protein.
Moreover, stomatal conductance is the single and most variable factor which
governs the responses of plants to UV-B. Therefore, intra- and inter specific variations
in the impacts of UV-B often correlate with the intrinsic capacity of stomatal
conductance; plants with higher rates of stomatal uptake exhibiting greater effects
(Mansfield and Freer-Smith, 1984). Furthermore, since exposure generally results in
the decline in stomatal apertures, plants that display most rapid stomatal closure in
response to UV-B are often reported to be resistant. However, stomatal closure leads to
reduction of evapotranspirational loss of water and water use efficiency gets increased,
which ultimately leads to increased plant growth.
Factors such as volume of leaves, intercellular air spaces and exposed mesophyll
cell surface area play an important role in determining the variable UV responses.
Furthermore, thinner leaves are generally found to be more sensitive to UV-B than
thicker leaves.
Chlorophyll fluorescence is an effective physiological indicator of plant response
to stress. A decrease in Fv/Fm ratio under UV-B; reflects photo inhibition. Light-
dependent inactivation of the photosystem II (PSII) reaction centre is associated with a
decline in Fm and Fv/Fm and with an increase in initial fluorescence as is observed in
UV-B-exposed plants (Long and Humphries, 1994). A diminished electron flow from
the water-splitting complex could cause impairment on the donor side, probably
lowering Fm in UV-B-exposed plants (Demmig-Adams et al., 1989). Fv, which
characterizes the photosynthetic competence of a leaf or chloroplast, reduced under
ambient and UV-B levels to a similar extent. The impact of UV-B radiation on PSII
activity is commonly measured as a decrease in oxygen evolution or variable
fluorescence (Vass et al., 1996). The decrease in Fv/Fm ratio was reported to be
accompanied by an elevated production of superoxide radicals (Jin and Tao, 2000)
which corresponded directly with higher MDA content under UV-B stress. UV-B
caused more membrane damage measured in terms of MDA content with a higher
magnitude of damage under UV-B.
Although, photosynthesis is directly related to the biomass accumulation in
plants but reduction in biomass is not necessarily related with the UV induced
reduction in photosynthesis. To cope up with prevailing climatic conditions, light and
UV-B stress, plant induces the synthesis of various secondary metabolites, which also
alters the physiological processes and might be a reason for reduction of biomass.
Biochemical responses against UV-B and defense mechanisms adapted by the
plants
UV-B is well known for its deleterious effects and severe consequences on
various physiological and biochemical characteristics of economically important plants
(Miller et al., 1994; Rao et al., 1996; Ambhast and Agrawal, 2003). UV-B penetrates
through leaves and is absorbed by chromophores associated with the photosynthetic
apparatus. Leaves absorb over 90% of incident UV-B. Leaf surface reflectance in the
wavelength is generally below 10% and there is negligible transmission of UV-B
through leaves (Robberecht and Caldwell, 1980; Cen and Bornman, 1993; Gonzalez et
al., 1996). Cell components which absorb UV-B directly include nucleic acids,
proteins, lipids and quinones (Jordan, 1996). Water soluble phenolic pigments such as
flavonoids are also found in leaves, which strongly absorb UV-B radiations and protect
the plants. UV-B stress leads to the production of reactive oxygen species. Rao et al.
(1996) proposed that UV-B activates membrane localized NADPH oxidase, which then
leads to the generation of ROS. Plants comprised of several strategies to acclimatize
and metabolise ROS. These includes active defence systems using low molecular
weight antioxidants such as ascorbic acid, phenols, flavonoids, glutathione,
carotenoids, etc and high molecular weight enzymes such as superoxide dismutase
(SOD), ascorbate peroxidase (APX), peroxidase (POD), catalase (CAT), etc (Miller,
2002; Cervilla et al., 2007).
Increased levels of UV-B radiations are responsible for the increased reflectivity
of the plants surface i.e. the leaves becomes more shiny and glabrous because of the
increased deposition of waxy material. It is a common type of defense mechanism
acquired by the plants to protect them from harmful UV-B radiation. Excess UV-B
exposure also induces the bronzing and reddening of leaves, due to more production of
polyphenolic compounds like flavonoids.
UV-B and photosynthetic pigments
Chlorophyll a and b are the main photosynthetic pigments in all higher plants
whereas carotenoids are the main UV-protecting pigments. Carotenoids act as quencher
in plants during stress. Carotenoids are effective scavengers of ROS and thus protect
chlorophylls against photo oxidative damage caused by UV-B irradiation by dissipating
excess excitation energy (Yamamoto and Bassi, 1996). Along with carotenoids other
pigments like xanthophylls, anthocyanin etc are also found in plants and they also
protect the plants during stress.
Elevated UV-B radiation reduces the chlorophyll content in many plant species,
this occurs due to lipid peroxidation in chloroplast membrane. The photo reduction of
protochlorophyllide to chlorophyllide by protochlorophyllide oxidoreductase is one of
the possible targets of UV-B (Marwood and Greenberg, 1996). Because this reaction is
light driven, it is possible that UV-B can damage this enzyme resulting in lowering rate
of chlorophyll accumulation. UV-B down regulates the expression of genes, which
encodes for chlorophyll a/b binding proteins (Casti and Walbot, 2003).
 Chlorophylls are relatively photostable except at very high white light
illumination. Chlorophyll destruction was a function of UV-B fluence rate; carotenoids
are similarly affected in sensitive species. Decrease in chlorophyll content was evident
on exposure to elevated UV-B radiation in most of the crop species reviewed,
ultrastructural damage to chloroplast and changes in photosynthetic pigments results in
the reduction of photosynthesis (Sullivan and Rozema, 1999). Chlorophyll reduction on
exposure to UV-B in major crops species ranged from as low as 10% (Mirecki and
Teramura, 1984; Tevini et al., 1981; Pal et al., 1999) to as high as 70% (Tevini et al.,
1981; He et al., 1993) and reduction being higher among the dicots species (10-78%)
compared to that in monocot species (0-33%).
The chlorophyll components, thylakoids and grana were sensitive to the
incoming solar radiation (Tevini et al., 1991; He et al., 1994; Cassi-Lit et al., 1997). An
increase in UV-B radiation resulted in rupture of the thylakoid and grana due to
disintegration of the membrane. Photo bleaching was dependent on the length and
intensity of UV-B radiation (Huang et al., 1993). Most higher plants accumulate UV-
absorbing pigments in their leaves particularly phenylpropanoids after irradiation with
UV-B (Wellman, 1983; Tevini et al., 1983; Beggs et al., 1986), these compounds were
commonly located at upper epidermal layer of the leaves. These UV-absorbing
compounds are mainly phenylpropanoids such as cinnamoyl esters, flavones, flavonols,
etc.
UV-B and permeability
An early consequence of UV-B radiation is an increase in ion permeability of
thylakoid membranes, UV-B induced leakiness is also observed in the plasma
membrane which is explained by association with specific ion channels. UV-B induced
loss of K+ ions from guard cell may be responsible for the observed loss of stomatal
conductance in irradiated plants (Negash and Bjorn, 1986). UV-B induced damage of
membrane is mainly focussed on the transport phenomenon (Murphy et al., 1985).
UV-B and phenols
Increase in phenolic content is an adaptive response, acting as a screen that
provides protection against UV-B penetration in leaf tissues and as antioxidants
protecting cells from reactive oxygen species (Bornman et al., 1998; Rozema et al.,
2002). Phenolic compounds of plants have been generally reported to be responsible
for different biological properties. Hence, enhancement in the level of phenolics in UV-
B-exposed plants plays a significant role in plant functions. The activation of the genes
of phenyl propanoid pathway producing phenolic compounds is a common response to
UV-B stress in plants. These phenolic compounds are produced from aromatic amino
acids (phenylalanine and tyrosine) via the phenyl propanoid pathway. These
compounds can mitigate the UV-induced damage by protecting the photosynthetic
pathway and cellular components. Increase in concentrations of UV-B absorbing
compounds including phenolic acid and flavonoids are the most consistent response of
plants to UV-B supplementation. Many studies have shown that plant mutants with
elevated accumulation of UV-B absorbing phenolics compounds including flavonoids
display markable tolerance to UV-B (Bieza and Lois, 2001). Phenolics may have a
multifunctional role in UV-B defence. They screen out harmful UV-B radiation and
emit less-harmful longer-wavelength fluorescent radiation and also act as antioxidants
directly scavenging the active oxygen species induced by UV-B radiation (Rozema et
al., 2002).
UV-B and flavonoids
Flavonoids, the most common group of polyphenolic compounds that are found
ubiquitously in plants. Flavonoids are potential antioxidants and have aroused
considerable interest recently because of their potential beneficial effects on human
health in fighting diseases. The capacity of flavonoids to act as antioxidants depends
upon their molecular structure. The position of hydroxyl groups and other features in
the chemical structure of flavonoids are important for their antioxidant and free radical
scavenging activities. Quercetin, the most abundant dietary flavonol, is a potent
antioxidant because it has all the right structural features for free radical scavenging
activity. Flavonoids helps in reproduction by providing colours to the petals, helps in
signal transduction, help in nector guiding, provides allelopathy and also interacts with
microbes and helps in root nodule and mycorrhizal association formation. Flavonoids
are confined to the epidermal part of the plants and it remains bound inside the
vacuoles and is also found in root hairs, glandular hairs or trichomes of the plants.
There are two types of flavonoids that are found in plants: constitutive flavonoids
and induced flavonoids. Constituted flavonoids (e.g. Hydroxy cinnamic acid) are
normally present in plants; these are simple and are able to remove small amount of
UV radiation. But high amount of UV radiation induced flavonoids (e.g. Quercetin-
upper part of plant and Kaempferol- lower part of the leaf); these are specialized
flavonoids known as flavonoids glycosides.
Plants respond to UV B by balancing reactions that lead to damage, repair, and
acclimation. UV-B attenuation is mainly attributed to flavonoids and related phenolic
compounds that absorb UV-B radiation effectively while transmitting PAR to the
chloroplasts (Caldwell et al., 1983; Li et al., 1993; Reuber et al., 1996). Levels of these
complex phenolic compounds vary considerably between plant species, with
developmental stage, and with differing environmental conditions such as visible
radiation levels, water, and nutrient supply (Caldwell, 1971; Murali and Teramura,
1985). In addition, exposure to UV-B radiation may increase the concentration of UV-
B-absorbing compounds in the epidermis, rendering some plants less susceptible to
photosynthetic damage due to UV-B exposure. Oilseed rape plants when pre-adapted to
grow in UV-B, developed tolerance (Wilson and Greenberg, 1993). These plants have
elevated levels of flavonoids in their epidermal cells. Increased amounts of UV
protective compounds have been commonly shown in the literature (Tevini et al., 1991;
Ziska and Teramura, 1992; Santos et al., 1993), while stimulation in leaf respiration has
previously been observed (Sisson and Caldwell, 1976; Ziska et al., 1991) but not
discussed (Gwynn-Jones, 2001). But now it is hypothesized that a stimulation of leaf
respiration represents increased resource demands for protection and repair (cuticular
thickening, flavonoid biosynthesis and photoreactivation). The stimulation of
respiration in non-growing mature leaves supports this view as it can be used to reflect
maintenance of respiration.
UV-B and ascorbic acids
Ascorbic acid is one of the most powerful antioxidants that scavenges the H 2O2
and other ROS profoundly. It is commonly called as Vitamin-C. Protective effect of
ascorbic acid is possibly more related to its participation in direct scavenging of O 2 and
.
OH, and also the removal of H2O2 through Asada-Halliwell pathway thus, reducing
ROS induced damage to essential proteins and/or nucleic acids. Significantly, higher
ascorbic acid content in V. acontifolia leaves before (in control plants) and after UV-B
exposure showed its greater capability to scavenge ROS.
There may be two possibilities regarding increased ascorbic acid content; either
its synthesis has been amplified or its regeneration through Asada-Halliwell pathway.
UV-B and lipids
Oxidative damage to cellular membrane due to oxyradicals is measured in terms
of lipid peroxidation (LPO) that accessed via increase in MDA content. Single or
conjugated double bonded lipids can be photo chemically modified by the action of
UV-B. Plant cell membranes are composed of phospholipids and glycolipids which are
the main components of plant cell membrane and are made up of unsaturated fatty
acids, which are destroyed by UV-B in presence of oxygen (Kramer et al., 1991;
Panagolpoulas et al., 1990).
Oxidative damage can be detected by lipid peroxidation. Hydroxyl free radicals
and nascent oxygen reacts with methylene group forming dienes, lipid peroxy radicals
and hydroperoxides (Smirnoff, 1995). The peroxy radicals can extract hydrogen from
other polyunsaturated fatty acids, leading to a chain reaction of peroxidation. The
peroxidation of membrane lipids leads to break down of their structure and function.
One of the products of lipid peroxidation is malondialdehyde, MDA, which is often
used as a measure of peroxidation.
Other hydrocarbons such as ethylene, ethane and pentane can be measured
(Halliwell, 1987). Hydroxyl radical can denature proteins and reacts with bases in
DNA causing mutation.
UV-B and proteins
As we know that UV radiation causes modification and destruction of amino
acids and is also responsible for inactivation of whole proteins and enzymes
(Grossweiner., 1984; Prinsze et al., 1990). Due to UV radiation induced photolysis of
aromatic amino acids or disulfide groups, the active sites of these proteins and enzymes
becomes inactive. The absorption of UV-B within protein matrix causes damage far
away from the actual site by energy migration to functionally important amino acids of
an active centre as suggested for the sensitization of cysteine destruction by aromatic
residues.
Characteristic examples of this effect include Ribulose-1, 5-bisphosphate
carboxylase (Rubisco) (Vu et al., 1984; Strid et al., 1990), ATPase violaxanthin de-
epoxidase (Pfundel et al., 1992), and protein subunit of the photosystem I and II as well
as insulin, pepsin, trypsin, myosin.
UV-B and plant growth regulators
Plant growth regulators are one of the most important regulators in plant growth
and development and any alteration in their concentration influences or alters the
processes which are dependent on them (Yang et al., 1993). Photolytic degradation of
Indole–acetic acid (IAA) has been observed in sunflower seedling (Ros and Tevini,
1995).
The reduced concentration of IAA and growth inhibitors IAA photoproduct, 3-
methylene oxindole, is responsible for the inhibition of hypocotyls growth. Moreover,
the action of peroxidase functioning as IAA oxidase may also inhibit the elongation
since, the cell wall extensibility is reduced.
Effects of UV-B on phenology and growth
Growth parameters such as plant height and leaf area are reduced in UV-B
sensitive plants to various extents, depending on plants species and cultivar (Lydon et
al., 1988; Murali and Teramura, 1986). Increased levels of UV-B radiation delayed
both seedling emergence and flowering of several crop plants under controlled
condition (Basiouny, 1986; Saile-Mark and Tevini, 1997) and in field (Li et al., 1998).
Both artificially and naturally supplied levels of UV-B radiation decreased stem length,
leaf area, chlorophyll and carotenoids content in cucumber seedling.
Mark and Tevini (1996) observed that the mechanism of reduction in stem
elongation by UV-B might be due to changes in the phytohormones levels, especially
IAA which plays important role in stem elongation. Few studies told that breakdown of
IAA by UV-B exposure (Ros and Tevini, 1995; Huang et al., 1993) which results into
reduced cell length and plant height (Gonzalez et al., 1998). Effects on the stem also
include coiling of both attached and detached tendrils.
Similarly, leaf area is also a very sensitive growth parameter that responded to
elevated UV-B radiation. Under most of the experimental studies, leaf area decreases in
exposed plants and leaves becomes smaller in size (Nogues et al., 1998; Zhao et al.,
2003) that serves as a protective mechanism (Bornman and Teramura, 1993), reduction
in cell number (Gonzalez et al.,1998a) and by cell division and cell expansion
(Hofmann et al., 2001). In contrast, Nedunchezhian and Kulandaivelu (1997) reported
that slightly elevated UV-B radiation increases leaf area in cowpea. Even high UV-B
treated broad beans and wheat plant had higher leaf area. Out of few studies, in 54%
plants, reduction in biomass was observed in elevated UV-B, in 35% studies, no effect
was observed on dry weight and in few cases, increase in crop dry matter accumulation
was observed. These differences were probably associated with genotypes, UV-B doses
and PAR: UV-A: UV-B radio. Crop biomass production in response to UV-B radiation
was highly UV-B dosage dependent.
In some investigation it is observed that the effect of UV-B /PAR ratio on the
sensitivity of rye to increased UV-B radiation under controlled conditions, and
concluded that plants grown under higher total irradiance levels developed leaves that
were more tolerant to UV-B damage, while low PAR levels increases the sensitivity of
plants to the UV-B radiations. The effects of elevated UV-B radiation on plants growth
and dry mass accumulation in field conditions were usually much smaller than on those
in growth chamber (Caldwell et al., 1994; Olszyk et al., 1996).
Effects of UV-B on crop yield and biomass partitioning
Reduced rate of photosynthesis alters the processes of carbon assimilation in
different parts of the plant. The UV-B exposure to foliage causes the accumulation of
carbohydrates in the source leaves and reduced translocation to the sink which is
present distantly. The phloem loading is an active process which requires energy and
increased concentration of UV-B reduces this process. UV-B is responsible for the
oxidation of sensitive proteins involved in phloem loading. The stored carbohydrates
are reported to be modified in wheat and barley. This stored carbohydrate is affected by
both reduction in rate of carbohydrate production and by a shift of carbohydrate to
repair and replacement processes. The translocation of photosynthates from source to
sink is inhibited by UV-B, leading to the alterations in biomass partitioning.
Due to varied impact of UV-B on the translocation of photoassimilates from
leaves the relative effects on the growth of different parts of the plant is observed.
Photosynthates allocation patterns directly affect the growth and reproduction of the
plants. Partitioning of reducing sugars, sucrose and starch varies along with the
growing stages of the plants. The most UV-effective period occurred during the
transition time between vegetative and reproductive phases (Teramura and Sullivan,
1987).
At flowering and fruiting stages, the reproductive organ requires high
concentration of photosynthates and that’s why the photosynthates are diverted from
leaves and roots towards reproductive organs. In cereal crops, flag leaves are the active
assimilatory source during anthesis stage of the plant. Flag leaves are the penultimate
leaf sheath and peduncle photosynthesis provides assimilates for the grain but flag leaf
blade and spikes are the most important contributors to grain filling. In a observation it
is found that an increase in concentration of carbohydrates of wheat flag leaves
fumigated with ozone at the time of anthesis due to interference in transport processes
(phloem loading) caused by membrane damage of mesophyll or companion cells.
Senescence of flag leaves due to UV-B radiation results into loss of chlorophyll and
soluble protein. The duration of assimilate production and grain filling is a key factor
behind the yield reduction and is altered by UV-B. However, UV-B also affects the rate
of grain filling and reduces the yield.
Conclusions
The impact of UV-B on biological systems mainly on plants is found to be severe
because of the sessile nature of the plants. These impacts are the mixed result of
damage, repair and acclimatization adapted and showed by the plants. The
acclimatization mechanism of plants diverts the focus from many important targets of
UV-B, which also requires brief study to understand their ecological relevance. The
strong defense strategies of plants reduce the damaging effects induced by UV-B
because plants have to acclimatize themselves continuously from the varying UV-B
levels. Thus, future studies should be targeted not only on the activities showing greater
changes but also on the minor variations. While evaluating the effects of stress, other
climatic conditions and their interactions as well as its impacts on plants and
community should be taken care too. In addition to this, the future perspective should
not be limited up to the defense mechanism but also on the acclimatization processes
towards increasing UV radiations.
Acknowledgements:
The authors are thankful to the Head of the Department of Botany, B.H.U.,
Coordinator CAS in Botany, FIST (DST) and UPE (UGC) for providing necessary
facilities and financial assistance.
Table 1: Distribution of solar irradiance energy

Spectral Regions Wavelength (nm) % of Total Energy

Infra red ≥ 700 49.4
Visible 400-700 42.3
UV-A 320-400 6.3
UV-B 290-320 1.5
UV-C ≤ 290 0.5

Table 2: Defense responses showed by plants against enhanced UV-B

S.No. UV-B induced damages Repair and defense strategies

1. Genetic material Photoreactivation via photolyases
Excision repair via by passing damage,
removing damaged part, gao filling from sister
duplex
2. Physiology Increasing stomatal closure, water use
efficiency, reducing evapotranspiration.
3. Leaf surface (chlorosis, Increased reflectance through cuticle, wax,
necrosis, photobleaching) hair and trichomes formation
4. Epidermal region Increased production of pigments (flavonoids,
carotenoids, anthocyanin)
5. Oxidative stress Formation of antioxidants (SOD, APx, GSH)
and compounds (ascorbates, α-tocopherols,
polyamines)
6. Pest attacks Phytoalexins and anti fungal compounds
formation
 Fig.1: Imaginary diagram of UV radiation reaching to the Earth’s surface

Fig.2: Portion of electromagnetic spectrum comprising ultraviolet region, which causes

maximum damage to the vegetation and the main responses shown by the plants
against UV-B
 Fig.3: Factors controlling the entry of UV-B on Earth’s surface

Fig.4: Bronzing of leaves of Hordeum vulgare L. under elevated UV-B

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TIPE-TIPE EKOTIPE TUMBUHAN
 Variasi Karakteristik Morfologis dan Fisiologis Ekotipe Elymus nutans dari Altitude
yang berbeda di Dataran Tinggi Tibet Timur Laut

Tumbuhan memiliki kemampuan untuk mengubah dan morfologisnya ciri-ciri

fisiologis sebagai respons terhadap variasi lingkunga. Morfologis dan karakteristik fisiologis
spesies alpine mencerminkan mereka adaptasi lingkungan di bawah gradien ketinggian
tertentu. Kacang Elymus adalah rumput dan drama abadi asli peran ekologis yang penting
dalam memelihara kawasan menyebabkan keanekaragaman dan stabilitas ekosistem.

Pada sebagian besar spesies alpine, perawakan kecil adalah adaptasi genetik. pada
suhu rendah, dan karenanya, mereka mempertahankan fitur ini ketika tumbuh di lingkungan
yang hangat karena suhu rendah mempengaruhi proses pertumbuhan dan perolehan karbon
fotosintesis. Di lokasi eksperimental ini, tinggi tanaman, kedalaman akar, dan volume akar
nutans dari ketinggian berbeda menunjukkan tidak ada perubahan signifikan. Tanaman yang
berasal dari 2950 m dpl dan tumbuh pada ketinggian yang sama memiliki ukuran morfologi
terbesar dalam atribut seperti tanaman tinggi, panjang akar, luas daun, panjang total akar, dan
volume akar. Ini menunjukkan bahwa ekotipe lokal berkinerja lebih baik daripada tanaman
yang diperkenalkan dari ketinggian lain karena mereka lebih baik disesuaikan dengan kondisi
lingkungan lokal.

Berbagai ekotipe dari spesies yang sama dapat diadopsi strategi bertahan hidupnya
yang berbeda untuk beradaptasi dengan lingkungannya.Untuk tanaman yang tumbuh di
lingkungan yang dingin, misalnya, luas daun dan ukuran daun biasanya kecil tetapi akumulasi
bahan kering tanaman yang sesuai dan laju fotosintesis bersih mungkin lebih terpengaruh .
Pengukuran fisiologis yang berkaitan dengan fotosintesis diambil pada periode
pertumbuhan harian tercepat (sebelum berbunga) menunjukkan bahwa tanaman berasal dari
2.950 dan 3100 m dpl tumbuh lebih cepat, yang mendukung interaksi pretasi ini. Tumbuhan
dari ketinggian tertinggi (3300 m dpl) tidak dapat menyesuaikan diri dengan kondisi
pertumbuhan yang lebih hangat dalam satu generasi. Tanaman yang berasal dari dataran
rendah altitude mungkin memiliki beberapa perbedaan dalam morfologi dan karakteristik
fisiologis yang mungkin terjadi karena hasil seleksi alam tidak hanya faktor
ketinggian.Namun, secarakeseluruhan, masing-masing ecotype sebagian besar
mempertahankan asalnya karakteristik ini ketika sedang ditransplantasikan ke yang lain
Hindawi
Journal of Sensors
Volume 2020, Article ID 2869030, 11
pages
https://doi.org/10.1155/2020/2869030

Research Article
Variation in Morphological and Physiological Characteristics
of Wild Elymus nutans Ecotypes from Different Altitudes in
the Northeastern Tibetan Plateau

Juan Qi ,1 Wenhui Liu,2 Ting Jiao,1 and Ann Hamblin3

1
Key Laboratory of Grassland Ecosystem of Ministry of Education, College of Grassland Science, Gansu Agricultural
University, Lanzhou, 730070 Gansu, China
2
Key Laboratory of Superior Forage Germplasm in the Qinghai-Tibetan Plateau, Qinghai Academy of Animal Science and
Veterinary Medicine, Xining, 810016 Qinghai, China
3
School of Agriculture and Environment, The University of Western Australia, Perth WA 6009, Australia

Correspondence should be addressed to Juan Qi; qijuan0622@163.com

Received 26 September 2019; Revised 27 November 2019; Accepted 13 December 2019; Published 11 January 2020

Guest Editor: Yuan Li

Copyright © 2020 Juan Qi et al. This is an open access article distributed under the Creative Commons Attribution License, which
permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
The availability of suitable native plant species for local animal husbandry development and ecological restoration is
limited on the Qinghai-Tibetan Plateau. Therefore, comparisons of the ecological adaptability of native species to
alternative habitats and their introduction into new habitats are of high importance. This study is aimed at identifying the
alteration in morphological and physiological characteristics by measuring photosynthetic physiology, nutrient content, and
growth associated with adaptation of plants to conditions at different altitudes 2450, 2950, 3100, and 3300 m above sea
level (a. s. l.) on the plateau. Seeds of the dominant grass, Elymus nutans, were collected from locations at these altitudes
and grown at a test location of 2950 m a. s. l. Results indicated that altitude had no significant effect on plant height and
root depth. However, the leaf area and total root surface area of plants derived from 2950 and 3300 m a. s. l. showed a
parabolic response, being greater than those of plants derived from the lowest (2450 m) and highest (3300 m a. s. l.). Total
(root plus shoot) dry matter reduced progressively from 2450 to 3300 m a. s. l, while root : shoot ratio increased
progressively with altitude. Seed yield of plants originating from the test altitude (2950 m a. s. l) was significantly higher
than at any other altitude, being 20% lower at 2450 m, and 38% and 58% less in populations originating from the higher
altitudes (3100 and 3300 m a. s. l.). There was also a parabolic decline in response of Elymus nutans germplasm from
3100, 3300, and 2450 m, compared with plants from 2950 m a. s. l., to photosynthetic rate, total N, soluble sugar, and
starch contents. Germplasm from 2450 m a. s. l. had significantly lower shoot and higher root carbon content, lower shoot
nitrogen, and lower root carbon-to-nitrogen ratio compared with plants derived from the other three altitudes. It is
suggested that the stable, genetically determined morphological and physiological features of ecotypes showed parabolic
responses which means these ecotypes have become adapted to local habitats, whereas parameters such as dry matter, total
root : shoot ratio, photosynthetic rate, and intercellular CO2 concentration of plants reflected phenotypic linear response to
current abiotic conditions. It is postulated that introduced ecotypes from 2450, 3100, and 3300 m could adapt to the
environment at 2950 m a. s. l. gradually. We conclude that the increased thermal regime experienced by plants introduced
from high altitude to low altitude may facilitate the increased growth of Elymus nutans subtypes. It is important to
preserve local strains of native species, or ecotypes, for reintroduction into degraded environments and to maintain the
greatest ecosystem stability in the northeastern Tibetan Plateau.

1. Introduction [1, 2] and adjust the expression of these traits to accom-

modate their adaptability across multiple environments [3].
Plants have the ability to alter their morphological and Altitude can significantly influence plant growth, structure,
physiological traits in response to environmental variations function, and metabolism [4, 5]. The morphological and
physiological characteristics of alpine species reflect their
environmental adaption under certain altitudinal gradients
[6]. As a consequence, modern plant ecologists have paid
much attention to these plant characteristics in different bio-
logical and ecological zones to better understand their adap-
tive mechanisms [7, 8].
Alpine plants exhibit specific morphological, physiolog-
ical, and biochemical responses to an increasing altitude,
such as size and increases in the leaf thickness [9–11].
Decreases in plant growth and a higher proportion of
plant biomass in the roots usually result in a higher leaf
N content and lower C : N ratio, which lead to a higher
photosynthetic capacity in alpine plants [12]. Moreover,
the relationship between plant functional traits and envi-
ronmental factors has been recently gaining increasing
attention. Plant species may have an optimum altitude
for production of biomass and net photosynthetic rate;
their enzymatic activities can increase or decrease upon
deviation from this optimum altitude [13–15]. Grasses
exposed to high altitudinal areas with extreme climatic
factors (cold, frost, drought, salinity, low oxygen, high
wind velocity, intense UV radiation, and geographical dif-
ferentiation) provide opportunities to study such adaptive
mechanisms [16, 17]. However, the adaptation mechanism
in response to altitude variation and climate change is
largely unknown [18].
Elymus nutans is a native perennial grass and plays
an important ecological role in maintaining regional spe-
cies diversity and ecosystem stability. It grows extensively
across the Qinghai-Tibetan Plateau and Xinjiang of
Northwestern China where it is well adapted to a range
of environments and is extensively grazed by livestock
[19, 20]. It is also one of the important pasture species
sown to increase livestock production and groundcover
by perennial species. However, research on the species
is not equal to the scale of its resource utilization in
China. Most reports [21–24] have focused on the biology,
genetic diversity, nutrition value, and yield of the species,
but there has been little information on the morphologi-
cal and physiological characteristics of E. nutans and the
species’ local adaptation to variations in altitude [25, 26].
An understanding of these characteristics, particularly of
the plant morphological attributes and variations in pho-
tosynthesis, is essential to help identify the mechanism of
plant adaptability to local-scale environments. Our basic
question was whether the physiological and ecological
traits of plants of the same species grown in different
habitats differed in their responses when grown in alter-
native environments and how they adapted to their new
environment. We hypothesized that there was a set of
significant differences in plant morphological, physiologi-
cal, and biochemical responses of E. nutans to increasing
altitude that could be taken as a surrogate for differences
in thermal regime, solar radiation, and precipitation. Bas-
ing on previous work, we attempted to answer the fol-
lowing questions:
(1) How do the plant functional traits, photosynthesis,
and dry matter respond to altitudinal variation
(2) What are the differences in physiological plasticity
of the different physiological parameters of E.
nutans in the alpine area
We selected changes in shoot and root length, leaf area
and root area, dry matter and seed yield, soluble matter
concentration, the ratio of carbon and nitrogen, and pho-
tosynthetic parameters to elucidate the ecophysiological
processes. Because these processes may enable this plant
to adapt to varying environments, we could use them to
evaluate the potential of this species expanding into higher
altitudes. It is expected that findings from this study will
help to identify traits for plant breeding strains of E.
nutans that may be increasingly adapted to climatically
changing habitatsandforthedevelopmentof themanagement
strategies to rehabilitate degraded pastures both for pastoral
grazing production and environmental sustainability.
2. Materials and Methods
2.1. Experimental Material. Healthy E. nutans seeds were
obtained from wild plants growing in Tianzhu county of
Eastern Qilian Mountains (102 °23~102°78′ E, 37°11~37°18′
N), Qilian Mountains, China, which lies in the northeast
margin of the Tibetan Plateau, a key site to understanding
the species’ adaptation in the northeastern of Tibetan Pla-
teau. At least 15 plants of Elymus nutans per site were cut
from four sites (Dachaigou, Jinqianghe, Honggeda, Daiqian)
selected randomly from habitats at 2450, 2950, 3100, and
3300 m a. s. l., in an area of 100-1000 m 2 that was ecologically
homogeneous for the target ecotypes (see Figure 1).
The vegetation type in the sampling areas was
composed of alpine meadow grasses and forbs. The soils on
which each ecotype grew were of the same soil taxonomic
category being shallow, postglacial subalpine meadow soils
of high organic matter content. Livestock grazing is the
only land use. Elymus nutans is the dominant species in
this area and occurs natu- rally and abundantly at altitudes
between 2000 and 5000 m a.
l. in the Qinghai-Tibetan Plateau. After collection, the sam- ples
were bulked, dried to 30°C, and seeds threshed out. Seeds
were stored at a constant 4 °C temperature at the Seed Centre
of the College of Grassland Science, Gansu Agricultural
University, Lanzhou, China.
2.2. Site, Climate, and Design. Seeds of the 4 ecotypes
were sown at the Tianzhu Alpine Grassland Experimental
Station of Gansu Agricultural University at an altitude of
2950 m a. s. l., the northeastern margin of the Qinghai-
Tibetan Plateau, China. The climate is alpine, cold, and
semiarid, with thin air and low temperature, and strong solar
radiation, where there is no frost-free season, only cold and
cool seasons. The annual average temperature is 0.1 °C, with
the highest average temperature in July (mean 12.7 °C) and
the lowest in January (mean -18.3 °C). The average annual
precipitation is 328.7 mm, concentrated from June to
September. The 4 ecotypes were sown as a randomized
complete block design with 3 replicates and the plot size
was 2 m × 5 m = 10 m2 with a 1 m gap between plots.
Each plot has row spacing of 40 cm. Sowing depth was 3-4
cm and sowing rate was 22.5 kg/ha.
 102° 45′ 0″ E
N Haxizhen
Anyuanzhen
Daiqian
3,300 m
Honggeda 3,100 m
Zhuaxixiulong
Jinqianghe 2,950 m
Tangshanling
02.25 4.5 9 13.5 18 km
102° 45′ 0″ E
FIGURE 1: Sampling sites (dark spots) for Elumus nutans along eastern boundary Qilian Mountains in the Qinghai-Tibet Plateau.
The soil was a shallow, postglacial, subalpine scrub
grassland soil with a higher organic matter content (9.45%) highest point of the plant and averaged to give the mean for each
in the 0~20 cm soil layer.
2.3. Measurements
2.3.1. Plant Height and Root Depth, Root Surface Area,
and Volume. Establishment and vegetative growth of E.
nutans is slow at altitudes above 2000 m a. s. l., and plants
only reach flowering and maturity by the second year. The
first year’s shoots die back and the growing points lie below
the soil sur- face during the first winter, to reemerge in the
second spring [27]. Therefore, all the data presented are
from the second year of planting.
Selected measurements were made at different develop-
ment stages. The plant morphological parameters (shoot
height, root length, surface area, and volume) were
measured during the period of rapid shoot extension in the
second year (the end of July), flag leaf area was measured at
full emer- gence of the flag leaf before flowering (the early
of August), and the physiological parameters (soluble
sugars, starch, total carbon and nitrogen, and gas exchange
properties) and total aboveground (shoot) and belowground
(root) dry matter were measured at flowering (August 10 ). th
Plant height was measured by recording the height of 20
randomly selected plants of E. nutans within a plot before
each harvest with a 2 m ruler from the soil surface to the
103° 0′ 0″ E
37°
15′
0″
N
Dachaigou
Dachaigou 2,450 m
Shimenzhen
103° 0′ 0″ E
treatment plot. Sections of rows 33 cm long were then
randomly selected, whole plants were dug out, and root
depth was measured. Whole plants were stored in the self-
sealing, labeled bags and refrigerated. Cleaned roots were
put into the root plate submerging the root system, and root
surface areas and root volume were measured using Photo
Scanner and the data analyzed by Root Analysis software.
2.3.2. Leaf Areas. The areas of 10 flag leaves from
randomly selected plants taken when flag leaves had fully
emerged, and at flowering were determined using an AM-
300 Area Meter (Analytical Development Company, Herts,
UK).
2.3.3. Herbage Yield. Individual treatment plots were har-
vested for herbage yield at fully flowering period, with sub-
samples then taken from each plot, freshly weighed and
oven dried at 65°C for 48 hours before being ground.
2.3.4. Seed Yield. Seed yield was made at 80% seed
maturity (seeds drop easily) in mid-September. Seed
collection was carried out from randomly selected plots of
each ecotype, and the seed yield of each experimental plot
(10 m2) was determined and converted into kg/ha.
2.3.5. Total Soluble Sugar. The physiological traits were
all measured when plants were flowering. Soluble sugar was
extracted from a 0.05 g sample with 1-4 ml 80% (v/v)
aqueous
 ethanol in a water bath at 80 °C for 40 min. This sample
was centrifuged for 30 minutes at 12000 r/min the super-using
natant collected, the residue reextracted with 80% (v/v)
aqueous ethanol, and finally, the sample was centrifuged
and merged with the supernatant. The extracted solution
was diluted to 50 ml after extracting 2 times. 1 ml of the
extract obtained was mixed with 5 ml of anthrone-sulphuric
acid reagent. After cooling to room temperature, the absor-
bance was measured at 627 nm using a UV-2550 UV-
visible spectrophotometer.
2.3.6. Starch Contents. The residue from the soluble sugars
was boiled with 6 mol/l HCl in a water bath at 80 °C for
5 min, the sample centrifuged for 10 minutes at 4000 r/min
the supernatant collected, and the above step repeated twice.
Absorbance was measured at 580 nm using a UV-2550 UV-
visible spectrophotometer. Starch content was calculated by
multiplying by the coefficient of hydrolysis (0.9).
2.3.7. Determination of Total Organic Carbon Content. The
samples were air-dried and ground to pass a 0.25 mm mesh
for total organic carbon content. Approximately 0.015-
0.020 g of each leaf and root sample was put into clear flask,
mixed with 10 ml of K 2Cr2O7, and then heated 5 min. The
solution was cooled and then titrated with FeSO 4 [28].
2.3.8. Nitrogen Analysis. N was determined by a small-
scale Kjeldahl digestion [29]. 0.5 g of ground herbage from
each sample was added to a flask, with 10 ml of H 2SO4 and
3 g of CuSO4·5H2O and K2SO4 (CuSO4·5H2O: K2SO4 =1 :
10), and shaken until thoroughly mixed, heated from a low
to high flame until the solution became clear, topped up to
100 ml with ammonium-free distilled water, and 10 ml of
the solution mixed with 4 ml 40% NaOH and distilled using
a Kjeldahl apparatus for 4 min. NH 3 released through distil-
lation was absorbed by 1% boric acid and then titrated
against 0.02 mol l-1 HCl to determine the N content.
2.3.9. Gas Exchange. The Li-6400 portable photosynthetic
analyzer (Li-COR, USA) was used to determine the daily
change (8:30 am-17:30 pm) of photosynthetic parameters of
E. nutans in an open gas analysis system. All measurements were
carried out on healthy leaves in the field on sunny days at
flowering period. Three leaves from each plot were ran-
domly selected. The photosynthetic parameters included a
net photosynthesis rate (Pn, mmol CO 2 m-2 s-1), transpira-
tion rate (Tr, mmol H 2O m-2 s-1), stomatal conductance
(Cond, mmol m-2 s-1), and intercellular CO2 concentration
(Ci, μmol CO2 mol air-1). The parameters were calculated
as the mean value for the day.
2.3.10. Statistical Analyses. Normality of distribution and
homogeneity of variance were checked before any further
statistical analysis. An investigation into normality of the
data was carried out by performing the Kolmogorov-
Smirnov test using SPSS 19 software. The data were
normally distributed and better meet the assumptions of the
statistical tests used. Analysis of variance and calculation of
means were conducted using Excel and SPSS19 software.
Morphological data and photosynthetic responses of plant
were analyzed
a one-way analysis of variance (ANOVA), and the mean
values were compared using the least significant differ-
ence (LSD) at P = 0:05.
3. Results
3.1. Changes in the Plant Height and Root Depth of
Four E. nutans Populations from Different Altitudes. The
plants orig- inating from different altitudes showed no
statistically signif- icant differences in height and root depth
when grown at 2950 m a. s. l. (Figure 2), which indicated
that the altitude variations had less effect on the growth of
plant height and root depth in alpine zone.
3.2. Changes in Leaf and Root Surface Area. Leaf and
root area responses varied significantly along the altitudinal
gra- dient, increasing from 2450 to 2950 m and then
decreasing from 2950 to 3300 m a. s. l. Both of leaf areas
and root sur- face areas were significantly different and
smaller in value for plants collected from both the highest
and lowest alti- tudes compared with those from 2950 and
3100 m a. s. l. (Figure 3). The leaf area and root surface
area showed a sig- nificant negative correlation with
altitude, and the correla- tion coefficient was 0.9938 and
0.9393, respectively.
3.3. Changes in Total Root Length and Root Volume.
Original altitude significantly influenced total root length
and root volume but to different extents (Figure 4). There
was no sig- nificant difference in total root length from
2450 to 2950 m but root length decreased as altitude
increased from 2950 to 3300 m a. s. l. The root length from
3300 m was lower than that from 2450 m and 2950 m a. s.
l. 41% and 46%, respec- tively. Root volume increased as
altitude increased from 2450 m to 2950 m a. s. l. and then
decreased. The root volume from 3300 m was lower than
that from 2950 m a. s. l. 47%.
Figures 3 and 4 show that the smaller leaf areas and
root characteristics of plants from the lowest altitude
(2450 m a. s. l.) when grown at higher altitude, and the
inability of the plants from higher altitude (3310 and
3330 m a. s. l.) to increase their leaf and root size when
grown at a lower altitude, provide good evidence that local
adapta- tion has occurred, inhibiting the plants from taking
advan- tage of the conditions prevailing at 2950 m a. s. l.
3.4. Changes in Aboveground and Belowground Dry
Matter and Seed Yield. The aboveground dry matter
decreased with altitude increased while the belowground dry
matter showed a reverse trend. Ecotypes from high altitude
allocated signif- icantly (P < 0:05) greater dry matter yield
to roots than those adapted to low and mid altitudes.
Aboveground dry matter yield allocation averaged 875
kg/ha at the lowest altitude, nearly twice the value of the
plants from the highest altitude. It was observed that
ecotypes from lower altitudes allocated more dry matter to
the stems of plants than those from higher altitudes. Total
dry matter (combined root and shoot dry matter) values for
the four ecotypes showed that there was a reduction with
each increase in original elevation (Table 1), while root :
shoot ratios also increased, providing a clear indication that
the total abiotic stress increased with altitude, as root : shoot
ratio increases with nearly every
 2
y = -6E-06x + 0.0359x - 40.857
13 A R2 = 0.7825 P > 0.05 70
12 A
11 A 69
68
A 10
9 A

Plant height (cm)

Root depth (cm)
8 67
7
66
6
5 65
4 A
3 2
y = -2E-05x + 0.1091x - 90.025 64
A
2 R2 = 0.8602 P > 0.05
63
1 A
0 62
2400 2600 2800 3000 3200 3400
Altitude (m)
Root depth
Plant height

FIGURE 2: Plant and root depth of four E. nutans populations from different altitudes in the northeastern Tibetan Plateau, when grown at a
single elevation of 2950 m a. s. l. Values are shown as the mean ± SE of three replicated. Different letters indicate that the mean values are
significantly different among the treatments (P = 0:05).

285 y = -0.0006x2 + 3.6794x -

5173.9 R2 = 0.9393 P = 500
A
265 0.001
245
450
A
225

Root surface area (cm )

2
Leaf area (cm )

A
2

205
400
185 A
B
165
y = -0.001x2 + 5.8525x - 350
145 7988.5 B
125 R2 = 0.9938 P < 0.001
300

B 105
250
85

2400 2600 2800 3000 3200 3400

Altitude (m)
Leaf area
Root surface area

FIGURE 3: Changes in the plant and root area of four E. nutans populations from different altitudes in the northeastern Tibetan Plateau.
Values are shown as the mean ± SE of three replicated. Different letters indicate that the mean values are significantly different among the
treatments (P = 0:05).

abiotic stress. The plants selected from, and grown at 2450 22.4 kg/ha and then decreased markedly and reached a min- imum at the
3300 m (46.2 kg/ha), with the seed yields from
m
a. s. l., were the largest in total weight, while the plants
from the 2950 m a. s. l. were only slightly smaller, but they
parti- tioned more of their assimilates into roots or seeds
and less into dry matter. Plants from 3000 m a. s. l. were
consistently smaller in every respect and were not able to
take advantage of the milder conditions when grown at
2950 m a. s. l.
Seed yield of plants from 2450 to 2950 m a. s. l.
increased
3100 and 3300 m a. s. l. being significantly
lower than either of the lower altitudes. While
seed production of the 2450 m
a. s. l. ecotype was somewhat restricted by
being grown at the higher elevation, the lack of
capacity of the 3100 and 3300 m ecotypes to
exploit the more favourable growing con-
ditions at 2950 m a. s. l. again indicates that
substantial local adaptation has taken place.

3.5. Soluble Sugar and Starch Content.

Soluble sugar and starch content all showed
significant differences in the leaves
 4500 A 6
AB
4000
A 5
3500 y = -1E-05x2 + 0.079x - 108.75
A

Total root length (cm)

R2 = 0.979 P < 0.001

Root volume (cm )

3000 4

3
B
2500 C
B 3
2000
B
1500 2
y = -0.0066x2 + 36.371x - 45459
1000 R² = 0.9557 P > 0.001
1
500
0 0
2000 2200 2400 2600 2800 3000 3200 3400
Altitude (m)

Total root length

Root volume

FIGURE 4: Changes in the total root length and root volume of four E. nutans populations from different altitudes in the northeastern
Tibetan Plateau. Values are shown as the mean ± SE of three replicated. Different letters indicate that the mean values are significantly
different among the treatments (P = 0:05).

TABLE 1: Aboveground, belowground, and total dry matter with root : shoot ratios at flowering and seed yield at 80% maturity for four
different populations of E. nutans.

Aboveground dry Belowground dry Root : shoot Total plant Seed yield
Altitude (m)
matter (kg hm-2) matter (kg hm-2) ratio weight (kg hm-2) (kg hm-2)
a b a b
2450 875 ± 32:4 283:8± 24:5 0.32 ± 0.04c 1159 ± 8:9 85:6± 3:07
b a b b a
2950 707 ± 28:3 343:8± 4:09 0:49 ± 0:03 1051 ± 24:3 108 ± 2:71
bc a ab bc c
3100 640 ± 16:7 347:3± 14:2 0:55 ± 0:03 987 ± 22:7 67 ± 3:18
c a a c d
3300 588 ± 8:1 364:5± 20:2 0:62 ± 0:03 953 ± 28:3 46:2± 3:61

TABLE 2: Soluble sugar and starch content of seedlings along the altitude gradients.

Soluble sugar content (%) Starch content (%)

Altitude (m)
Aboveground Belowground Aboveground Belowground
b b b a
2450 0:694 ± 0:02 0:025 ± 0:0 0:035 ± 0:0 0:021 ± 0:0
a ab a b
2950 0:918 ± 0:01 0:043 ± 0:0 0:043 ± 0:0 0:035 ± 0:0
a a b b
3100 0:889 ± 0:01 0:053 ± 0:0 0:034 ± 0:0 0:033 ± 0:0
b b b c
3300 0:736 ± 0:02 0:032 ± 0:0 0:031 ± 0:0 0:014 ± 0:0

and roots of plants derived from different altitudes. The

soluble sugars followed the similar parabolic curve to the
root and shoot morphological traits increasing first with
altitude from 2450 to 2950 m a. s. l. and then decreasing
(Table 2). Soluble sugars of belowground roots reached
the highest value at 3100 m a. s. l. The aboveground
starch contents were only marginally different from plants
originating from 2950 m a. s. l., but the belowground
starch contents of plants from the highest and lowest alti-
tudes were significantly less than those from the interme-
diate altitudes.
3.6. Total C and Total N Concentration and the Ratios
of C: N. Table 3 shows that aboveground C contents were
not significantly different except in plants derived from
2450 m, although plants from 3100 and 3300 m a. s. l. had
numerically greater C contents. The root C was similarly
higher in the plants from the lowest altitude. There were no
significant dif- ferences in root C content among ecotypes
from high alti- tudes. The plants derived from lowest
altitude had a significantly lower aboveground nitrogen (N)
content and higher belowground N content than the other
ecotypes. The aboveground C : N increased as the altitude
increased,
 TABLE 3: Total C content, N content, and C : N of seedlings along the elevation gradients.

Carbon content (%) Nitrogen content (%) C:N C:N

Altitude (m)
Aboveground Belowground Aboveground Belowground Aboveground Belowground
b a b a bc a
2450 23:9± 1:4 48:57 ± 4:69 1:28 ± 0:01 2:23 ± 0:06 18:7± 1:2 21:78 ± 1:5
a b a ab bc b
2950 39:28 ± 3:6 33:06 ± 1:98 1:61 ± 0:05 2:11 ± 0:08 24:4± 1:49 15:67 ± 0:8
a b a b ab b
3100 49:5± 4:88 28:4± 3:14 1:65 ± 0:04 1:87 ± 0:07 30 ± 3:2 15:2± 1:2
a b a ab a b
3300 47:9± 1:52 30:8± 2:45 1:55 ± 0:04 2:05 ± 0:10 30:9± 0:4 15 ± 0:8

12 y = 1E-06x2 - 0.0116x + 29.912 4

A R2 = 0.9462 P > 0.001
3
10 ABBA
B 3
Pn (mmol/(m2·s))

Tr µmol/(m2·s)
8
2
B B
6
y = 2E-06x2 - 0.0131x + 19.403 2
R2 = 0.9918 P > 0.001
4
1

2 1

0 0
2000 2200 2400 2600 2800 3000 3200 3400
Altitude (m)
Pn
Tr

(a)
250 160
y = -0.0187x + 255.1
A R2 = 0.938 P > 0.001 140
200 A
B B 120 Cond (mmol/(m ·s))
C
2

100
150
Ci (ppm)

80
B
100 C
C 60

40
y = 8E-05x2 - 0.5378x + 969.58
50
R2 = 0.9999 P < 0.001 20

0 0
2000 2200 2400 2600 2800 3000 3200 3400
Altitude (m)

Ci
Cond
(b)

FIGURE 5: (a) Photosynthetic response (Pn—net photosynthetic rate) and transpiration (Tr). (b) Response of intercellular CO2
concentration (Ci) and stomatal conductance (Cond) measured on four E. nutans populations from different altitudes. Values are shown as
the mean ± SE of three replicated. Different letters indicate that the mean values are significantly different among the treatments (P =
0:05).

but the root C : N ratio was only significantly different in

the 2450 m a. s. l. ecotype. were measured during the period of maximum growth (the end of
July, second year). The results (Figure 5) are the means of
3.7. Photosynthetic Parameters of Leaves of Four E. data collected between 8:30 am-17:30 pm during 25 July.
nutans Populations from Different Altitudes. They showed the photosynthetic rate (Pn) and intercellular
CO2 concentration (Ci) responded in a similar manner to
Photosynthetic charac- teristics in leaves of the four ecotypes the shoot dry matter. Pn decreased as the altitude increased.
from different altitudes
The Pn of plants from 3300 m was 28% lower than those
from 2450 m a. s. l., but there was no significant difference thesis taken at the period of fastest daily growth (prior to
among values of plants from 2950, 3100, and 3300 m a. s. l.
However, Tr increased as the altitude from which the plants
were derived increased. The Tr from 3300 m was 43%
higher than that of 2450 m a. s. l. (Figure 5(a)). By
calculating the water use efficiency (WUE = Pn/Tr), it was
found the plant WUE gradually decreased from lower
altitude to higher alti- tude. The Cond and Ci responses
were highly correlated with the altitude of the original
populations and decreased signif- icantly as altitude
increased (Figure 5(b)). The Ci and Cond from 3300 m
were lower than that of from 2450 m a. s. l. 8% and 48%,
respectively.
nutans were generally similar in appearance and morpho-
4. Discussion
4.1. Variation in Morphological Traits of E. nutans with
Altitude Gradient Migration. Altitude is an important
eco- logical factor that affects population differentiation and
genetic variation. The high altitude especially in the alpine
region has a pronounced influence on the plants. Plants have
obvious adaptation strategies by modifying their
morpholog- ical and physiological attributes [30]. The long-
term effects of environment on plants can alter their
morphology, physio- logical function, and ecology [31, 32].
Only those that adapt to their environment can survive well,
while those that do not will gradually be eliminated from
the local ecosystem. Therefore, morphological
characterization of ecotypes pro- vides useful information
for evaluation of agronomic apti- tude and development of
new varieties [33].
In most alpine species, small stature is a genetic adapta-
tion to low temperatures, and hence, they retain this feature
when grown in a warm environment as low temperature
affects the growth process and photosynthetic carbon gain
[34]. In this experimental location, plant height, root depth,
and root volume of E. nutans from different altitudes
showed no significant change. These were the relatively
conservative traits among the morphological traits measured
along altitu- dinal gradients in an alpine region, similar to
those described by Zhu’s research [35]. However, ecotypes
from 3300 m had larger leaf areas and root surface areas
than those from 2450 m a. s. l. In the cold temperate zone,
an increase in tem- perature reduces abiotic stress and
improves the overall plant growth rate [36], especially
affecting the photosynthetic and nutrient absorption
processes. Our results are in line with other research
findings for trees [37]. Furthermore, the plants derived from
2950 m a. s. l. and grown at the same altitude had the
greatest morphological size in attributes such as plant
height, root length, leaf area, total root length, and root vol-
ume. This indicated that local ecotypes performed better
than the introduced plants from other altitudes because they
were better adapted to local environmental conditions [38].
In addition, different ecotypes of the same species may
adopt different survival strategies to adapt to the
environmental stress [39]. For plants growing in the cold
environments, for example, the leaf area and leaf size are
normally small but the corresponding plant dry matter
accumulation and net photosynthesis rate may be more
profoundly affected [40]. The physiological measurements
relating to photosyn-
flowering) showed that the plants derived from 2950 and
3100 m a. s. l. were growing faster, which supports this
inter- pretation. The plants from the highest altitude (3300
m a. s. l.) were not able to adjust to the warmer growing
conditions within a single generation, and the plants from
the lowest altitude (2450 m a. s. l.) were probably restricted
by the lower temperatures they encountered at 2950 m a. s.
l. [41].
4.2. Effect of Altitude Migration on Material
Accumulation and Distribution. Although the four ecotypes
of the species
logical characteristics, differences were observed in the dry
matter characteristics, carbon, and nitrogen content. Plants
from the lowest altitude maintained higher dry matter accu-
mulation and seed yield than those adapted to 2950 m a. s. l.
This is good evidence that there had been local adaptation to
the conditions occurring at different altitudes [42]. We
could expect that plants selected from the lowest altitude
and grown at a higher altitude would not grow so fast
because they were exposed to more cold, and that the plants
from the higher altitudes grown at lower altitude would
grow faster (and perhaps accumulate more belowground dry
matter) and also through regulating physiological activity to
adapt to the environment changes. When we compared
(Table 1) the way the plants from different altitudes
partitioned their assimi- lates, it was clear that the total
amount of plant production (aboveground and belowground
dry matter and seed yield) was significantly less in the
plants from the higher altitudes, despite being grown at a
more favourable (warmer) altitude, whereas the plants from
the two lower altitudes had a similar total biomass but
allocated their assimilates in different ways. The total
amount of aboveground herbage was greatest in the plants
from the lowest altitude (and probably if all ecotypes had
been grown at 2450 m a. s. l., these plants would have been
largest overall). The plants originating from the low alti-
tude may have had some differences in morphological and
physiological characteristics that could possibly have been
due to the results of natural selection not just the altitude
fac- tor [43]. However, overall, each ecotype largely kept its
orig- inal characteristic when being transplanted to another
altitude [44]. As we found a linear decrease in seed set with
altitudinal origin, it is likely that the higher growth rates of
plants from lower altitudes would be maintained in other
growing sites.
4.3. Effect of Altitude Migration on Physiological
Characteristics. Nonstructural carbohydrate (NSC) which
mainly refers to the sugar and starch has a great influence
on plant growth and adaptability [45]. NSC is the product
of photosynthesis. Therefore, factors affecting
photosynthesis will also affect NSC of plants [46]. When
photosynthesis changes, the NSC may change a variety of
ways that can be induced directly or indirectly by various
environmental fac- tors [47, 48]. Previous studies have
shown that photosyn- thetic capacity and plant N content
may have a positive correlation while higher photosynthetic
activity can increase CO2 assimilation so that NSC is also
enhanced [49, 50]. In our study, plants from the middle
altitudes (2950 and
3100 m a. s. l.) had higher soluble sugars, and root starch
con- tents, in the typical parabolic response form, whereas
the car- bon and nitrogen contents and C : N ratios were
significantly different only in the plants derived from the
lowest (2450 m a.
s. l.) altitude suggesting they were partitioning their assimi-
lates into structural components in different ways. The seed-
lings sourced from higher altitudes had better nitrogen
utilization ability than those from lower altitudes. This sug-
gests that ecotypes of Elymus nutans sourced from
different altitudes may have beneficial attributes of adaptive
value under the condition of future climate change.
We may postulate that plants from the lower elevations
(below 3000 m a. s. l.) are therefore most suited to being
sown in situations where the amount of grass for yak feed is
of most importance, whereas ecotypes that have developed
at higher specific altitudes are most suited for use in
rehabilitation pro- grams aimed at repairing degraded
natural grasslands that have suffered from erosion or
overgrazing.
5. Conclusions
We can conclude that local adaptation has occurred in Ely-
mus nutans growing naturally at different altitudes: these
adaptations include changes in the size of the plants, the
ratio of roots to shoots, the ratio of C : N, the total herbage
and seed produced over the growing season, and the extent
of the genetic by environment interaction (responsiveness)
when grown at intermediate elevations. We suggest that
eco- types from the lower altitudes will be most productive
for increasing grazing by yaks below 3000 m a. s. l., but that
locally adapted ecotypes should be used within their
specific local habitats for ecological restoration of degraded
grass- land. Adaptation is the result of a long-term
evolutionary process in concert with stress conditions.
Further studies are needed to fully understand how altitude
migration affects Elymus nutans growth on the Qinghai-
Tibetan Plateau.
Data Availability
The data used to support the findings of this study are
included within the article.
Conflicts of Interest
The authors declare there are no competing interests.
Acknowledgments
This work was supported by the National Natural Science
Foundation of China (grant number 31660684), the Key
Lab- oratory of Superior Forage Germplasm in the Qinghai-
Tibetan Plateau (grant number 2020-ZJ-Y09), and the Ear-
marked Fund for China Agriculture Research System (grant
number CARS-34). The authors are grateful to Changlin
Xu for his help and valuable technical assistance and those
students who were involved in part of the field and lab
work.
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PRODUKTIVITAS TUMBUHAN
Peningkatan produktivitas tanaman di Alaska tundra sebagai sebuah hasil pemanasan
eksperimental tanah dan lapisan es
Respons komunitas tumbuhan tundra utara terhadap suhu yang memanas karena
ekosistem permafrost memainkan peran kunci dalam penyimpanan karbon (C) global, dan
iklim- pergeseran ekologis yang diinduksi dalam komunitas tanaman akan mempengaruhi
transfer karbon dioksida di antara kolam biologis dan atmosfer. Penelitian ini berfokus pada
respon pertumbuhan tanaman tundra dan fenologi terhadap percobaan pemanasan, dilakukan
di proyek Penelitian Pemanasan Eksperimental Permafrost Karbon, terletak di kaki utara
Pegunungan Alaska menggunakan pagar salju ditambah dengan pegas salju untuk
meningkatkan suhu tanah dalam dan mencairkan kedalaman (pemanasan musim dingin), dan
open-top ruang untuk meningkatkan suhu udara musim panas (pemanasan musim panas).
Pemanasan musim dingin meningkatkan suhu tanah musim dingin (5–40 cm) sebesar
2,3 ° C, menghasilkan 10% peningkatan kedalaman musim tanam mencair. Pemanasan
musim panas secara signifikan meningkatkan udara musim tanam suhu; perbedaan suhu
puncak terjadi dekat tengah hari ketika plot pemanasan musim panas sekitar 1,0 ° C lebih
hangat dari plot sekitar. Perubahan lingkungan tanah sebagai akibat dari perlakuan
pemanasan musim dingin menghasilkan 20% peningkatan biomassa di atas tanah dan
produktivitas primer bersih (ANPP), sementara tidak ada mendeteksi efek pemanasan musim
panas pada ANPP atau biomassa tingkat ekosistem. Musim panas dan musim dingin
pemanasan memperpanjang musim tanam melalui istirahat tunas sebelumnya dan penuaan
lanjut, meskipun setara dengan hari bebas salju di seluruh perawatan. Seperti halnya ANPP,
pemanasan musim dingin meningkatkan kanopi N massa sebesar 20%, sementara tidak ada
efek pemanasan musim panas pada kanopi N.
Peningkatan ketersediaan N yang dimediasi oleh pemanasan, ditambah dengan
pergeseran fenologis, mungkin terjadi mendorong tingkat ANPP yang lebih tinggi di plot
pemanasan musim dingin, dan kurangnya tingkat-N ekosistem dan Respons ANPP terhadap
pemanasan musim panas menunjukkan berlanjutnya pembatasan N dalam plot pemanasan
musim panas. Hasil dari penelitian ini menyoroti peran dinamika tanah dan permafrost dalam
mengatur tanamanmenanggapi perubahan iklim dan memberikan bukti bahwa pemanasan
dapat meningkatkan akumulasi C yang lebih besartion dalam biomassa tanaman tundra.
Sementara suhu pemanasan diperkirakan akan meningkatkan mikroba dekomposisi kumpulan
besar bahan organik yang disimpan di tanah tundra dan permafrost, kerugian ratory dapat
diimbangi, setidaknya sebagian, oleh peningkatan pertumbuhan tanaman yang dimediasi oleh
pemanasan.
Journal of Ecology 2012, 100, 488–498 doi: 10.1111/j.1365-2745.2011.01925.x

Increased plant productivity in Alaskan tundra as a

result of experimental warming of soil and permafrost
Susan M. Natali*, Edward A. G. Schuur and Rachel L. Rubin
Department of Biology, University of Florida, Gainesville, FL 32611, USA

Summary
1. The response of northern tundra plant communities to warming temperatures is of critical
con- cern because permafrost ecosystems play a key role in global carbon (C) storage, and
climate- induced ecological shifts in the plant community will affect the transfer of carbon-
dioxide between
biological and atmospheric pools.
2. This study, which focuses on the response of tundra plant growth and phenology to
experimental warming, was conducted at the Carbon in Permafrost Experimental Heating
Research project, located in the northern foothills of the Alaska Range. We used snow fences
coupled with spring snow removal to increase deep-soil temperatures and thaw depth (winter
warming), and open-top
chambers to increase summer air temperatures (summer warming).
3. Winter warming increased wintertime soil temperature (5–40 cm) by 2.3 °C, resulting in a
10% increase in growing season thaw depth. Summer warming significantly increased growing
season air temperature; peak temperature differences occurred near midday when summer
warming plots were approximately 1.0 °C warmer than ambient plots.
4. Changes in the soil environment as a result of winter warming treatment resulted in a 20%
increase in above-ground biomass and net primary productivity (ANPP), while there was no detected
summer warming effect on ecosystem-level ANPP or biomass. Both summer and winter
warming extended the growing season through earlier bud break and delayed senescence,
despite equivalent snow-free days across treatments. As with ANPP, winter warming increased
canopy N mass by 20%, while there was no summer warming effect on canopy N.
5. The warming-mediated increase in N availability, coupled with phenological shifts, may have
driven higher rates of ANPP in the winter warming plots, and the lack of ecosystem-level N and
ANPP response to summer warming suggest continued N limitation in the summer warming plots.
6. Synthesis: These results highlight the role of soil and permafrost dynamics in regulating plant
response to climate change and provide evidence that warming may promote greater C
accumula- tion in tundra plant biomass. While warming temperatures are expected to enhance
microbial
decomposition of the large pool of organic matter stored in tundra soils and permafrost, these respi- ratory
losses may be offset, at least in part, by warming-mediated increases in plant growth.
Key-words: biomass, carbon, climate change, net primary productivity, open-top chamber, permafrost,
phenology, plant–climate interactions, snow fence, tundra

Introduction increasing temperature on photosynthetic C uptake relative to

Tundra ecosystems play a key role in biological feedbacks to
global carbon (C) cycling because of the large pool of ther-
mally protected C stored in permafrost soils (Schuur et al.
2008; Tarnocai et al. 2009) and the strong potential for
changes in C storage in a warmer climate (Schuur et al. 2008,
2009; Dorrepaal et al. 2009). The magnitude and direction of
these C inventory changes will depend upon the effect of
*Correspondence author. E-mail: natali@ufl.edu
respiratory losses (Shaver et al. 2000). On the one hand,
warm- ing may increase microbial decomposition rates and
organic substrate availability as previously frozen soil organic
matter warms and thaws (Aerts 2006; Davidson & Janssens
2006; Grogan & Jonasson 2006; Larsen et al. 2007; Natali et
al. 2011). However, some respiratory losses may be offset by
warming-mediated increases in plant biomass, as observed in
tundra over the past few decades (Hudson & Henry 2009).
Upland moist acidic tundra is characterized by strong nitro-
gen (N) limitation, short growing season length and a shallow
© 2011 The Authors. Journal of Ecology © 2011 British Ecological Society
490 S. M. Natali, E. A. G. Schuur & R. L. Rubin
active layer (seasonally thawed ground layer above perennially
frozen permafrost), all of which place limitations on plant
productivity and growth. Ecosystem models predict that
warming surface air temperatures will positively affect plant
productivity in northern regions (Keyser et al. 2000),
primarily as a result of warming effects on soil N availability
(Nadelhof- fer et al. 1991; Rastetter et al. 1991; Chapin et al.
1995). Fertil- ization experiments in Arctic tundra clearly
demonstrate the importance of N as a regulator of plant
growth and ecosystem C exchange (Chapin et al. 1995;
Chapin & Shaver 1996; Shaver et al. 2001; Mack et al.
2004). Warming tempera- tures may also bring about
phenological changes and shifts in the plant community
(Wookey et al. 1993, 2009; Arft et al. 1999; Aerts et al.
2004; Aerts, Cornelissen & Dorrepaal 2006) that, combined
with changes in ecosystem N, may further increase the
potential for warming temperatures to alter ecosystem
productivity.
Surprisingly, while there has been observational evidence of
increased plant biomass in the Arctic over the past few
decades (Hudson & Henry 2009), few experimental tundra
warming studies have resulted in greater plant biomass or N
pools at the ecosystem level, as would be expected if N
limitation was attenuated by warming. Experimental warming
in tundra has caused shifts in plant community structure
(Hollister, Webber & Bay 2005; Jonsdottir et al. 2005;
Wahren, Walker & Bret-Harte 2005; Walker et al. 2006) and
species ⁄ functional group-specific changes in biomass and
growth (Chapin et al. 1995; Chapin & Shaver 1996; Hobbie
& Chapin 1998; Dor- repaal et al. 2004), but these
individualistic species-level effects have often acted in
opposite directions so that there was no change in total plant
biomass at the ecosystem level (Chapin et al. 1995).
However, many previous studies using green- houses and
open-top chambers (OTCs) rarely warmed deep soils or
increased thaw depth (Marion et al. 1997) because of lateral
transfer of heat energy from the relatively small treat- ment
plots as opposed to vertical transfer of heat that will occur
with climate warming. While snow addition studies have been
successfully used to raise wintertime soil temperatures and
degrade permafrost, the delayed snowmelt associated with the
experimentally accumulated snowpack is not a likely climate
scenario and may decrease plant productivity (Wipf & Rixen
2010).
This study examines the responses of plant productivity and
biomass in a new type of air and soil warming experiment
that increased summer thaw depth and degraded surface
permafrost, without delaying snowmelt (Natali et al. 2011).
We hypothesized that both air and soil warming would
increase growing season length through changes in leaf
phenol- ogy, but that soil warming alone would increase plant-
avail- able N. We expected that these warming-mediated
changes in leaf phenology and nutrient availability would
increase plant productivity and biomass at the ecosystem
level. We tested these hypotheses at the Carbon in Permafrost
Experi- mental Heating Research (CiPEHR) project, located in
moist acidic tundra in Interior Alaska near Denali National
Park. The CiPEHR project combines OTCs to increase
summer air temperatures with snow fences, coupled with
spring snow
removal, to warm surface and deep-soil temperatures (Natali
et al. 2011). This novel approach achieves the type of whole
ecosystem warming and permafrost degradation that is
expected as a consequence of climate change.
Materials and methods
SITE DESCRIPTION
The CiPEHR project, which was established in 2008, is located in
the northern foothills of the Alaska Range (c. 700 m elevation) at
the Eight Mile Lake (EML) study site, Alaska (63°52¢59¢ N,
149°13¢32¢ W; Schuur et al. 2009; Natali et al. 2011). The site is
situ- ated on moist acidic tundra on a relatively well-drained gentle
north- east-facing slope. Soils are classified in the soil order
Gelisol and
are comprised of an organic horizon, 0.45–0.65 m thick, above a
cryoturbated mineral soil that is a mixture of glacial till and
wind- blown loess. The active layer, which thaws annually during
the grow- ing season, is c. 50–60 cm thick and is situated above
a perennially frozen permafrost layer. Mean monthly
temperatures range from
)16 °C in December to +15 °C in July, with a mean annual tempera-
ture (1976–2009) of )1.0 °C. Vegetation at the site is
dominated by the tussock-forming sedge, Eriophorum vaginatum,
and deciduous shrub, Vaccinium uliginosum. Other common
vascular plants include Carex bigelowii, Betula nana, Rubus
chamaemorus, Empetrum nigrum, Rhododendron subarcticum, V.
vitis idaea, Andromeda polifolia and Oxycoccus microcarpus.
Nonvascular plant cover is dominated by feather moss (primarily
Pleurozium schreberi) and Sphagnum spp., as well as several
lichen species (primarily Cladonia spp.; Schuur et al. 2007).
EXPE RIMENTAL DES IG N
The soil warming treatment, hereafter called winter warming, was
achieved using six replicate snow fences (1.5 m tall · 8 m long;
n = 6) that trapped insulating layers of snow. To ensure that water
input and timing of snowmelt were similar in warming and control
plots, we removed the accumulated snow from winter warming
plots prior to snowmelt in early spring. This is a key feature of this
experi- ment that differs from traditional snow fence experiments
and that allowed us to isolate the temperature effects of the snow
fence treat- ment from moisture and snowmelt effects. Fences were
removed at the time of snow removal to avoid shading of the plots
during the growing season (May–September). All plots were snow
free by 30 April in both 2009 and 2010. Each winter warming
treatment and winter warming control area contained two summer
warming plots and two summer warming control plots (n = 24).
Summer warming was achieved using 0.36 m 2 · 0.5 m tall OTCs,
which were set out during the snow-free period, between the first
week in May and the last week of September. Treatment plots will
hereafter be referred to as follows: Ambient (no warming), Winter
(winter warming only), Summer (summer warming only) and
Annual (both summer and win- ter warming). Further description
of the site and experimental design can be found in the study by
Natali et al. (2011).
ENVI RONME N TAL M ONITORING
An Onset HOBO (Bourne, MA, USA) weather station was used to
measure air temperature and rainfall. Growing season air tempera-
tures in 2009 (9.7 °C) and 2010 (9.8 °C) were similar to the 7-year
(2004–10) site average (10 °C). Growing season precipitation in
2009
490 S. M. Natali, E. A. G. Schuur & R. L. Rubin
© 2011 The Authors. Journal of Ecology © 2011 British Ecological Society, Journal of Ecology, 100, 488–498
(178 mm) was lower than the 7-year average (233 mm), while
2010 precipitation (250 mm) was slightly higher. Plot-level air
tempera- tures were also measured at 15 cm from the ground
surface using NTC thermistors and recorded to a Campbell
Scientific CR1000 (Logan, UT, USA) data logger.
Soil profile temperatures (5, 10, 20, 40 cm) were recorded in
each plot using constantan-copper thermocouples. Surface soil
moisture was estimated using site-calibrated DC half-bridge
resistance measurements (Natali et al. 2011). Volumetric water
content (hereaf- ter referred to as depth-integrated soil moisture)
was measured from the soil surface to a depth of 20 cm using
Campbell CS616 water con- tent reflectometer probes (WCR). Soil
moisture and temperature were measured half-hourly and recorded
to a Campbell Scientific CR1000 data logger. Water-table depth
was measured three times per week throughout the snow-free
period from two water wells per winter warming and control plots.
Thaw depth (thickness of unfrozen ground) was measured weekly
at each plot using a thin (3 mm diameter) metal depth probe. We
present here analyses of warming effects on micrometeorological
variables for the second treatment year (September 2009–
September 2010) and a summary of differences between the first
and second years. Full analyses of 2008–09 environmental effects
can be found in the study by Natali et al. (2011).
BI O M ASS AND A NP P
Above-ground biomass and net primary productivity (ANPP)
were determined in 2009 and 2010 with a nondestructive point-
frame method using a 60 · 60 cm point frame with a grid size
of 8 · 8 cm (Walker 1996). At each of the 49 intersecting grid
points, a metal rod (1 mm diameter) was placed vertically
through the plant canopy. We recorded species identity and tissue
type (leaf, stem or fruit) for every plant that touched the rod
(‘hits’). We estimated above-ground live biomass for each vascu-
lar plant species, moss and lichen by applying allometric equa-
tions developed for this site to the average number of point-
frame ‘hits’ per plot (Schuur et al. 2007). Vascular plant ANPP
was estimated as the sum of the current year’s apical growth
(leaves, stems, flowers and fruits) and secondary growth. We
based biomass values for plant tissue types on ratios of tissue
type to total biomass determined from destructive harvest of a
site adjacent to CiPEHR (Schuur et al. 2007). We estimated sec-
ondary growth using growth rates determined from tussock tun-
dra at Toolik Lake, Alaska (Shaver et al. 2001). While our
ANPP estimates do not account for potential warming effects on
plant allometry, we have not observed any warming effects on
the proportion of leaf to fruit ⁄ stem tissue (based on point-frame
‘hits’), leaf length, or leaf mass per unit area (S. Natali, data not
shown).
We estimated moss NPP by the cranked wire method, which
mea- sures vertical growth of moss using a stainless steel reference
wire inserted at the moss surface (Clymo 1970; Schuur et al. 2007).
We placed between three and five cranked wires in four moss types
in each treatment at all fences and measured growth from mid-May
to mid- September. The four dominant moss types measured were
S. fuscum, hydrophilic Sphagnum. spp. (which included S.
girgenshonii,
S. lenense, S. warnstorfii, and S. aongstroemii), Dicranum spp., and
feathermoss (primarily P. schreberi). With the exception of feather
moss, vertical growth was converted to biomass increment using
allo- metric equations developed for EML watershed (Schuur et al.
2007), and these point estimates of biomass increase were
multiplied by per cent moss cover in each plot. Feathermoss NPP
was estimated as
the product of linear growth per stem, stem density, biomass per
unit stem growth (Benscoter & Vitt 2007) and per cent cover. Moss
NPP was summed across groups for statistical analysis, but group-
level results are presented in Supporting Information (Fig. S1).
PLANT A ND SOIL ELEMENTAL A NALYSES
To assess warming effects on plant nutrient status, we collected
leaves at peak biomass (mid July) and at the end of the growing
season (late September) for total C, N and for stable isotope
analyses (July only). Nitrogen isotopes provide information on
N availability or sources to plants, and C isotopes provide
information about plant water status. We collected fully formed
green leaves from the current year’s growth from six species found
across plots. Leaves were dried at 60 °C, ground and analysed on
a ThermoFinnigan (Waltham, MA, USA) continuous flow isotope
ratio mass spectrometer coupled to a Costech (Valencia, CA, USA)
elemental analyzer. Canopy N was determined as the product of
leaf biomass and green leaf % N. We determined changes in N
resorption efficiency [(Ngreen ) Nsenesce) ⁄
Ngreen · 100] and proficiency (% N in senesced leaves), which are
indicators of plant nutrient status. Leaf litter N mass was
determined as the product of foliar biomass and senescent leaf
% N.
Warming effects on soil nutrient availability were assessed using
ion exchange resin bags (Giblin et al. 1994). Separate anion and
cation exchange bags (Biorad 20–50 mesh; 3 g wet weight resin
per bag) were placed in each plot at a depth of 10 cm during three
sea- sonal intervals (25 May–16 September 2009; 16 September
2009–24 May 2010; 24 May–14 September 2010). Upon removal,
resin bags were extracted for 1 h in 100 mL of 0.1 M HCl ⁄ 2.0
M NaCl and
analysed for NHþ4 and NO—3 on an Astoria Analyzer (Astoria-Pacific
Int., Clackamas, OR, USA). We calculated total dissolved
inorganic N (TDIN) as the sum of NHþ4 and NO3— . While ion
losses from resin exchange bags (due to microbial competition or
ion substitution) are
possible, ion exchange resins have been effectively used to provide
a relative measure of soil N availability (Binkley 1984; Giblin et
al. 1994). A summary of 2009 foliar elements and resin results can
be found in the Supporting Information and in the study by Natali
et al. (2011).
LEAF PHENO L OGY AND P LA NT REP R ODUCTI VE
EFFOR T
In 2010, we observed the timing of bud break from 11 to 29 May
and senescence from August 21 to September 23. We recorded the
date when bud break (V. uliginosum, B. nana) or green leaves
(C. bigelowii) were first observed in each plot, and we recorded
senes- cence as the date when no green leaves were present for
these same species as well as for R. chamaemorus. Senescence in
E. vaginatum was recorded as the percentage green leaves
remaining per tussock at the last sampling date. Senescence was
also detected using normalized difference vegetation index (NDVI)
images taken 3 September 2009 and 23 September 2010 using an
ADC multispectral digital camera (Tetracam, Chatsworth, CA,
USA). To examine warming effects on reproductive effort, in 2010
we recorded number of flowers per unit area for R.
chamaemorus, number inflorescence clusters for
E. vaginatum, B. nana, R. subarcticum and number of flowering
tillers for C. bigelowii (c. 1 male and 2 female spikes per tiller).
Hereafter, we use the term flowers to mean flowers, inflorescence
or flowering tillers. In late July in both 2009 and 2010, we recorded
the number of berries produced by R. chamaemorus, V. uliginosum
and
V. vaccinium idaea. While variation in sex ratio affect phenological, reproductive and
of dioecious species (i.e. R. chamaemorus) can

© 2011 The Authors. Journal of Ecology © 2011 British Ecological Society, Journal of Ecology, 100, 488–498
492 S. M. Natali, E. A. G. Schuur & R. L. Rubin

growth estimates, we do not expect this variation to be affected by P = 0.020). Temperature differences were greatest mid-day (11:00–15:00),
or correlated with our experimental treatments; our measurements when SW plots were 1.0 ± 0.1 °C warmer than control (F = 18.26, P
pre- sented here represent species-level averages that include all < 0.001). Air temperatures in 2010 were
individu- als within each experimental plot.

STATISTI CAL D E S IG N A ND ANALYSE S

Data were analysed with a mixed linear model analysis of

variance (ANovA; SAs 9.0; SAS Inst., Cary, NC, USA) using a
blocked split-plot design with winter warming (WW) as the main
plot factor, summer warming (SW) as the within plot factor,
and fence (random and
nested in block, also random) as the experimental unit for WW.
Soil depth was included as a fixed factor (nested within plot) for
analysis of treatment effects on soil temperature (5, 10, 20 40 cm
depths), and functional group or species were included as
additional fixed factors, also nested within plot, for tests of
treatment effects on foliar elements, ANPP ⁄ biomass and
phenology. We used repeated meas- ures ANovA to examine
changes in environmental variables over the
growing season and ANPP and biomass changes between years,
with
plot as the unit of replication for time effects. Family-wise error
rates were controlled using the Hochberg method for planned
contrasts or Tukey method for all pair-wise comparisons. Data
were transformed when necessary to meet assumptions of ANovA.
All errors presented
are one standard error of the mean.

Results

ENVIRO NMENTAL E FF ECTS O F WARMING

Winter warming increased wintertime soil temperatures

across the soil depth profile. In 2010, WW increased soil
temperature (5–40 cm depth) by 2.3 ± 0.4 °C from
December to March, when average ambient soil
temperature was )6.2 ± 0.1 °C. Differences were
significant in December for 5 and 10 cm depths, and from
January to March for all depths (P < 0.05
for all; Fig. S2). Surprisingly, warming effects continued
into the growing season when deep-soil (40 cm)
temperatures were higher with WW (2.9 ± 0.6 °C) than
control (1.6 ± 0.2 °C) during the months of July and
August (P < 0.05). As expected, soil temperatures
differed among depths (F = 210.0, P < 0.001) and
months (F = 488.3, P < 0.001). Winter warming effects
on soil temperature resulted in a c. 10% (2.9 ± 0.9 cm)
increase in growing season thaw depth (F = 31.02, P
< 0.001; Fig. S3). In late September, 2010, maximum
active layer depth was 58.2 ± 0.7 in control plots and
65.3 ± 1.7 in WW plots. There was no detected effect
of SW on thaw depth (F = 0.58, P = 0.464) or soil
temperature (F = 0.17, P = 0.685). Wintertime soil
temperature was
c. 3 °C lower in 2010 than in 2009, while growing season soil
temperature and thaw depth were slightly higher in 2010 than
in 2009; despite these differences, warming effects were
similar across years (Table S1).
Average air temperature in the SW plots (12.4 ± 0.1
°C)
was significantly warmer than control (11.9 ± 0.1 °C)
during all months of the 2010 growing season (F = 5.47,
492 S. M. Natali, E. A. G. Schuur & R. L. Rubin
slightly higher than 2009, but the magnitude
of the SW effect was similar across years
(Table S1).
In addition to direct effects of warming
on temperature and active layer depth, WW
also altered soil moisture, which proba- bly
resulted from surface subsidence in the
WW plots. Winter warming increased
depth-integrated soil moisture from June to
September of 2010 (F = 5.54, P =
0.029); there was also a sig- nificant SW
· WW effect (SW · WW · month; F =
3.46, P = 0.022), with lowest moisture
content in Ambient plots and highest in
Annual plots. Surface moisture (2010)
was also slightly, but not significantly,
higher with warming (Fig. S4). Winter
warming effects on soil moisture were
reflected in water- table depths, which were
closer to the ground surface (nonsig-
nificant) in WW (16.7 ± 1.7 cm) than
control plots (19.3 ± 1.1) throughout the
2010 growing season (Table S1, Fig. S4).
In 2009, winter warming similarly affected
soil moisture, resulting in significant
differences in water-table depth (Table
S1).
ABOV E -GROUND N ET PRIMARY P RODUCTI V
ITY AND BIOMASS
The environmental effects caused by the
WW treatment led to significant increases
in plant growth. Winter warming increased
both total above-ground biomass (F =
© 2011 The Authors. Journal of Ecology © 2011 British Ecological Society, Journal of Ecology, 100, 488–498
5.53, P = 0.023) and ANPP (F = 2.87, P = 0.096) after 2
years of warming (Fig. 1a,b). In the WW plots, above-
ground bio- mass and ANPP were 20% and 40% higher,
respectively, in 2010 compared to 2009 (biomass: F =
46.14, P < 0.001; ANPP: F = 33.71, P < 0.001), while
there was no change between years in the control plots. In
contrast to the strong effect of WW on plant growth, there
was no observed SW effect on biomass (F = 0.01, P =
0.92) or ANPP (F = 0.05, P = 0.82).
The observed WW effects on ANPP were driven by
enhanced graminoid growth in the WW plots after 2 years
of warming (F = 37.02, P < 0.01; Fig. 1c–f), while there
was no difference across years in control plots for this
functional group. These changes were primarily due to
increased E. vagin- atum ANPP, which was almost 40%
higher in WW plots com- pared to control in 2010 (F =
18.78, P < 0.001, Table 1). While there were no significant
SW effects on species or func- tional group ANPP in our
repeated measures analyses, we also ran individual ANOVAs
on each species and functional group
within each year to examine shifting trends in ANPP across
the plant community. In 2009, E. nigrum ANPP declined with
SW, while in 2010 evergreen ANPP, and R. subarcticum in
particular, were significantly higher in the Annual plots
relative to Ambient (P < 0.05; Table 1). Warming effects on
above- ground biomass at the functional group and species
level were similar to these ANPP results (Table S2). As
expected, both ANPP and biomass were significantly different
among species and functional groups (P < 0.001 for all).
LEAF AND S O IL C AND N
Consistent with warming effects on plant productivity, WW
significantly increased the total mass of N in green foliage
 (a) 400 (b) Ambient
650 * Summer * Winter Annual

ANPP (g m–2 year–1)

600 350

Biomass (g m–2)
550
300
500
250
450

400 200
2009 2010 2009 2010

(c) (d)
250 250
****
200 200
Biomass (g m–2)

Biomass (g m–2)
150 150

100 100

50 50

0 0
DEC EVG GRM MOS LIC DEC EVG GRM MOS LIC

250
(e) (f)
250
*** *
ANPP (g m–2 year–1)

ANPP (g m–2 year–1)

200 200

150 150

100 100

50 50

0 0
DEC EVG GRM MOS DEC EVG GRM MOS

Fig. 1. Warming effects on (a) total above-ground biomass; (b) total ANPP; functional group biomass in (c) 2009 and (d) 2010; and
functional group ANPP in (e) 2009 and (f) 2010. Abbreviations as follows: deciduous (DEC), evergreen (EVG), graminoids (GRM), moss
(MOS), and lichen (LIC). Significant differences: *WW effect; **SW effect; ***WW · SW interaction effect.

Table 1. Above-ground net primary productivity (g biomass m)2 year)1 ± SE) for ambient and warmed plots at Carbon in
Permafrost Experimental Heating Research in 2009 and 2010*

2009 2010

Ambient Summer Winter Annual Ambient Summer Winter Annual

Graminoid 129.4 ± 14.3 160.9 ± 34.4 127.0 ± 21.3 110.5 ± 23.0 146.7 ± 154.2 ± 33.2 231.0 ± 35.3 190.3 ±
15.8w 50.9
Eriophorum vaginatum 113.4 ± 11.9 139.9 ± 36.5 104.3 ± 21.2 86.9 ± 25.9 130.8 ± 130.8 ± 34.9 203.2 ± 36.8 163.0 ±
16.5w 54.4
Carex bigelowii 16.0 ± 21.1 ± 3.8 22.7 ± 2.9 23.5 ± 3.8 15.9 ± 2.3 23.4 ± 4.3 27.8 ± 3.6 27.3 ± 3.8
2.6
Deciduous 60.6 ± 68.0 ± 5.0 60.7 ± 3.5 54.3 ± 4.2 67.4 ± 2.9 72.6 ± 6.9 59.4 ± 3.4 62.0 ± 4.9
3.1
Betula nana 9.6 ± 2.1 11.3 ± 2.8 11.8 ± 2.9 13.0 ± 3.5 10.5 ± 2.7 13.0 ± 2.7 9.01 ± 2.8 11.0 ± 2.8
Rubus chamaemorus 14.7 ± 13.7 ± 0.9 13.9 ± 1.0 12.8 ± 0.9 17.2 ± 3.8 16.8 ± 1.6 13.6 ± 0.4 14.7 ± 0.7
1.4
Vaccinium uliginosum 36.6 ± 43.0 ± 4.3 35.0 ± 2.1 28.6 ± 4.0 40.0 ± 5.2 42.8 ± 6.1 36.8 ± 3.1 36.3 ± 4.1
2.8
Evergreen 55.7 ± 52.5 ± 2.2 56.7 ± 4.2 53.7 ± 5.0 51.7 ± 4.7s ·
54.8 ± 2.7 52.4 ± 2.2 66.5 ± 3.5*
3.9 w

Andromeda polifolia 5.2 ± 0.7 5.1 ± 0.4 5.2 ± 0.3 4.5 ± 0.1 4.8 ± 0.4 5.1 ± 0.5 4.6 ± 0.2 4.7 ± 0.2
Empetrum nigrum 12.1 ± 6.5 ± 1.5 12.6 ± 5.1 6.7 ± 1.5 9.9 ± 3.3 8.4 ± 2.4 9.6 ± 4.0 8.7 ± 2.3
3.6s
Rhododendron subarcticum 19.1 ± 19.6 ± 2.4 23.5 ± 4.1 20.2 ± 2.2 19.3 ± 2.5s ·
21.8 ± 1.5 22.4 ± 1.8 30.0 ± 2.5*
3.8 w

Vaccinium vitis idaea 14.7 ± 16.7 ± 2.9 11.7 ± 1.2 18.8 ± 4.0 13.6 ± 1.7 14.5 ± 2.6 12.7 ± 1.9 19.2 ± 2.6
2.5
Oxycoccus microcarpus 4.6 ± 0.9 4.6 ± 0.7 3.7 ± 0.6 3.5 ± 0.3 4.1 ± 0.6 5.0 ± 0.9 3.1 ± 0.1 3.9 ± 0.5
All Vascular 245.8 ± 14.1 281.5 ± 33.9 244.4 ± 21.7 218.6 ± 21.7 265.8 ± 281.6 ± 33.5 342.8 ± 35.1 318.8 ±
19.8w 47.6
Mosses 17.6 ± 4.2 16.7 ± 4.9 21.2 ± 2.3 22.8 ± 7.0 19.7 ± 3.6 13.9 ± 4.4 22.2 ± 1.7 22.1 ±
 4.5
Total† 263.4 ± 14.4 298.2 ± 33.5 265.6 ± 21.1 241.4 ± 18.1 285.5 ± 295.5 ± 31.9 365.0 ± 35.5 340.9 ±
20.4w 45.3
*S, significant SW effect; W, significant WW effect; S · W, significant interaction effect. When interaction effect, warming treatment
that differed from ambient. All significant effects (bold values) at P < 0.05.
†Lichen was not included in ANPP calculations. Biomass values for all species can be found in Table S1.

© 2011 The Authors. Journal of Ecology © 2011 British Ecological Society, Journal of Ecology, 100, 488–498
 4.0
(a) Ambient Summer * In contrast to observed WW effects on canopy N, SW
1.0
Foliar N (g N m–2)

3.5
Winter Annual (b) alone affected resin-available N (Fig. S5). In 2010, SW
0.9 * decreased resin NHþ4 (F = 4.24, P = 0.048) and TDIN
3.0 0.8
(F = 4.73,
0.7 P = 0.036) by almost 40%, but there was no change in NO—3
2.5
0.6 (F = 0.32, P = 0.577). Warming effects on resin N in 2009
2.0 0.5
were similar to 2010 trends (Fig. S5).
0.4
2009 2010 2010
LEAF PHENO L OGY AND R EPRODUCTIVE E FFORT

Warming advanced bud break and delayed senescence in 2010

Fig. 2. Warming effects on (a) N mass in green foliage and (b) in and control plots (Tables S3). In both years, there were strong differences
senescent leaves. Green leaf N mass represents the sum of six main among species for all foliar variables measured (P < 0.001).
species found across plots: Betula nana, Carex bigelowii, Eriophorum
vaginatum, Rhododendron subarcticum, Rubus chamaemorus and
Vac- cinium uliginosum. Senescent leaf N mass included these same
species with the exception of R. subarcticum. Significance noted as in
Fig. 1.

(Fig. 2). Foliar N mass in WW plots was significantly

greater in 2010 compared to 2009 (F = 11.09, P = 0.003),
while there was no change across years in the control
plots (F = 0.51, P = 0.484). This increase in canopy N
was pri- marily a result of higher biomass, and ANPP as
green leaf % N was not significantly affected by WW
treatment (F = 0.04, P = 0.853; Table S3). Changes in
canopy N were driven by higher foliar N mass in the
graminoids, where E. vaginatum canopy N was almost
70% greater in WW plots (2.33 ± 0.43 g Nm)2) than
control (1.38 ± 0.21 g Nm)2; F = 3.82, P = 0.053), and
C. bigelowii foliar mass was 40% greater in WW plots
(0.40 ± 0.04 g Nm)2) than control (0.28 ± 0.05 g Nm)2;
F = 4.92, P = 0.028). Litter N mass
also increased in the WW plots in 2010 (Fig. 2), driven by
a 50% increase in E. vaginatum litter N mass in the WW
plots (0.48 ± 0.07 g Nm)2) relative to control
(0.32 ± 0.04 g Nm)2; F = 14.13, P < 0.001). As with
can-
opy N, the increase in litter N input was driven primarily by
increased ANPP, as resorption proficiency (i.e. % N in senes-
cence leaves) and efficiency did not change for most species,
with the exception of C. bigelowii, which had higher % N in
senescent leaves and lower resorption efficiency with WW
(P < 0.05 for both; Table S4).
While changes in plant N uptake were dominated by
the WW treatment, both SW and WW altered plant N
dynam- ics, as reflected in foliar d15N (Table S3). There
was a signifi- cant WW · SW interaction effect on foliar
d15N for B. nana (F = 8.93, P < 0.001) and E.
vaginatum in 2010 (F = 2.79, P = 0.045), driven by
differences in the Annual plots where
B. nana d15N decreased and E. vaginatum d15N increased
rel- ative to all other treatments (P < 0.05 for all
comparisons).
C. bigelowii d15N also increased in the SW plots (F = 2.77,
P = 0.099), and both SW and WW increased d15N in
R. chamaemorus. There was also a slight, but significant, increase in
B. nana d13C (F = 5.85, P = 0.017) and a decrease in R.
subarcticum d13C with SW (F = 3.39, P = 0.068). In
2009, there were no WW effects on green leaf elements and
isotopes, but there were significant differences between SW
for all species measured, despite similar snowmelt
dates across treatments. Bud break occurred
earlier with WW in C. bige- lowii (F =
4.23, P < 0.042), and both SW and WW
advanced bud break in B. nana (F =
10.48, P < 0.001) and V. uligino- sum (F
= 6.47, P < 0.001, Fig. 3a). B. nana bud
break occurred significantly earlier in all
warming plots compared to Ambient, and
V. uliginosum bud break was earlier in
Winter and Annual plots compared to
Ambient (P < 0.05 for all).
Both warming treatments also extended
the end of the grow- ing season by
delaying senescence. Senescence occurred
latest in the Annual plots in all species
except B. nana, where there was no
observed difference among treatments.
Warming sig- nificantly delayed
completion of senescence in R. chamaemo-
rus (SW: F = 7.40, P = 0.009), C.
bigelowii (SW: F = 6.71, P = 0.014;
WW: F = 4.41, P = 0.070), E. vaginatum
(SW: F = 3.71, P = 0.058; WW: F =
23.86, P < 0.001), and
while not significant, similar trends were observed
for V. uligi- nosum (Fig. 3b–c). These
observed changes in senescence were
supported by late-season NDVI values,
which were signifi- cantly higher in WW
© 2011 The Authors. Journal of Ecology © 2011 British Ecological Society, Journal of Ecology, 100, 488–498
plots compared to control (F = 5.11, P = 0.037; Fig. 3d).
No NDVI differences were observed in 2009 (P > 0.1 for
all), and while we did not record leaf phenology in 2009,
no differences were observed in the field (S. Natali, pers.
obs.).
In addition to increasing growing season length,
warming also enhanced reproductive effort in most
species. Both WW and SW increased flower production in
R. subarcticum (WW: F = 9.10, P = 0.030; WW · SW;
F = 13.75, P < 0.001).
Winter warming also increased flower production in C. bige-
lowii (F = 5.08, P = 0.030) and E. vaginatum (F = 5.17,
P = 0.053), but we detected no SW effect in these species
(Fig. 4a). Warming effects on fruit production in 2010
were consistent with flowering results (Fig. 4c). Berry
production increased in V. uliginosum (F = 17.08, P =
0.002) and
vitis idaea (F = 4.32, P = 0.071) in response to WW, but
there were no SW effects. As with flowering, warming did
not alter R. chamaemorus berry production. Fruit
production in 2009 did not differ among treatments (Fig.
4b).
Discussion
Changes in the soil environment brought about by winter
warming treatment increased above-ground biomass and plant
productivity by 20% compared to control plots in 2010, and
this increase was associated with significantly higher canopy
N. While moist acidic tundra are strongly N limited, nutrient
limitation may be attenuated as warming temperatures
 147
(a) Ambient Summer Winter Annualdicted to increase as the climate warms (Rustad et al. 2001).
* However, annual ecosystem respiration losses may be greater
** **
146 than photosynthetic gains (Grogan & Jonasson 2006; Larsen
et al. 2007; Natali et al. 2011) so that plant C uptake may off-
Bud break, day of year

145
set some, but not all, respiratory losses associated with climate
144 warming.
In contrast to the strong effect of winter warming on pro-
143
ductivity and ecosystem N pools, summer warming had no
142 detected effect on above-ground biomass, ANPP or canopy
N, similar to previous air-warming experiments. In these ear-
141
lier studies, warming with greenhouses and OTCs caused
140 shifts in species dominance, but individual species-level
CB VU
responses often offset one another so that effects at the eco-
BN
system level were limited (Chapin et al. 1995). Furthermore,
(b)
in studies that manipulated both air temperature and soil
** **
270 nutrients, ecosystem-level effects of warming were small in
contrast to fertilization effects (Chapin et al. 1995; Dormann
& Woodin 2002; van Wijk et al. 2004). These results
Senescence, day of year

265
highlight the unique experimental design of CiPEHR, which
achieves whole ecosystem warming and surface permafrost
260 degrada- tion that more closely simulates future climate
warming scenarios for this region.
Surprisingly, summer warming significantly decreased resin-
255 available N, which was probably mediated by warming effects
on plant processes since summer warming altered air but not
250
soil temperatures. The negative effect of summer warming on
BN CB RC VU resin-available N may have been driven by an increase in
(c) (d) microbial competition for N or potential ion losses from the
45 0.48 *
** exchange resins during deployment (Giblin et al. 1994). The
Green leaves remaining (%)

opposing responses of canopy and resin N call into question

40
0.46 the ability of ion exchange resins to measure the plant-avail-
able N pool; our results suggest that resin-available N may not
NDVI

35 be capturing soil N dynamics from the full soil profile or

0.44
30
0.42
25
Amb Sum Win Ann
Fig. 3. Warming effects on date of plot-level (a) bud break; (b)
com- plete senescence; (c) percentage green leaves remaining on
Eriopho- rum vaginatum tussocks (23 September); and (d) NDVI
values on 23 September 2010. Species abbreviations as follows:
Betula nana (BN),
Carex bigelowii (CB), Vaccinium uliginosum (VU) and Rubus cha-
maemorus (RC). Significance noted as in Fig. 1.
accelerate rates of organic matter decomposition and N
miner- alization (Rustad et al. 2001; Schimel, Bilbrough &
Welker 2004; Aerts, Cornelissen & Dorrepaal 2006). Nitrogen
cycling in tundra plants and soils is tightly integrated so that
plant N uptake closely tracks soil N mineralization (Rastetter
et al. 1991). While winter warming treatment did not increase
resin- available N, the observed increase in canopy N suggests
that winter warming increased soil N availability as a result of
enhanced rates of N mineralization and ⁄ or an increase in the
thawed soil N pool. The effects of winter warming on ecosys-
tem productivity and N availability highlight the potential for
plant C uptake to offset respiratory C losses, which are pre-
© 2011 The Authors. Journal of Ecology © 2011 British Ecological Society, Journal of Ecology, 100, 488–498
track- ing plant-available soil N.
Changes in total above-ground biomass and ANPP with
winter warming at CiPEHR were dominated by enhanced
graminoid growth. This result supports the hypothesis that
Amb Sum Win Ann
warming temperatures in the Arctic will have the strongest
effect on deciduous species, which, because of faster rates of
leaf turnover than evergreen species, have a higher capacity to
respond to biological and environmental changes (Aerts &
Chapin 2000). Several other warming studies have found simi-
larly strong growth responses from graminoids to both air
(Arft et al. 1999) and soil warming (Brooker & van der Wal
2003). In contrast to our study, long-term snow additions at
Toolik Lake, AK, negatively affected E. vaginatum growth
and survival (Borner, Kielland & Walker 2008); however, the
additional snow at the Toolik experiment was not removed
from the experimental plots, which resulted in a 2-week delay
in melt-out. Species with early season development, such as
E. vaginatum, may be particularly sensitive to snowmelt date
(Wipf 2010). While we did not measure below-ground
produc- tion and growth, we expect that observed increases in
grami- noid biomass and ANPP at CiPEHR underestimated
total plant response, since root allocation in tundra graminoids
increases with higher air and soil temperatures (Kummerow &
Ellis 1984). Future research efforts are needed to quantify
 (a)
30
8 * * ***
25

Number of flowers m–2

6
20

15 4

10
2
5

0 0
BN CX RC
EV RS

Ambient Summer Winter Annual

50 (b) 50
(c)
* *
Number of berries m–2

40 40

30 30

20 20

10 10

0 0
RC VU VVI RC
VU VVI

Fig. 4. Warming effects on (a) flower production in 2010 and berry production in (b) 2009 and (c) 2010. Mean flower or inflorescence production
was analysed for the following species, followed by the day of year when flower production peaked: Betula nana (BN, 143), Carex bigelowii (CX,
162), Eriophorum vaginatum (EV, 131), Rhododendron subarcticum (RS, 162) and Rubus chamaemorus (RC, 155). Berry production was
measured for R. chamaemorus, (RC), Vaccinium uliginosum (VU) and V. vitis idaea (VVI). Significance noted as in Fig. 1.

warming impacts on C allocation and root production because
changes in below-ground plant biomass can have a profound
effect on ecosystem C storage.
We did not detect a positive warming effect on deciduous
shrub production, as has been found in long-term nutrient
experiments (Chapin & Shaver 1996; Shaver et al. 2001);
how- ever, a warming-mediated decrease in B. nana foliar
d15N indi- cates a shift in N dynamics, which may, over
longer timescales, positively affect plant growth. The decrease
in B. nana foliar d15N may have been driven by changes in
the ectomycorrhizal fungal community (Deslippe et al. 2011)
and a subsequent increase in the transfer of 15N-depleted
organic N through mycorrhizal networks (Hobbie & Hobbie
2008). In contrast, warming increased foliar d15N in several
graminoid and forb species (E. vaginatum, C. bigelowii and
R. chamaemorus). These changes in foliar d15N can result
from an increase in inorganic N availability (Craine et al.
2009), change in rooting depth (Nadelhoffer et al. 1996), or
changes in N sources to the plant community (Evans 2001;
Robinson 2001). While further research is needed to discern
the exact mechanism of the observed shifts in foliar d15N,
these species and functional group-specific responses indicate
resource shifts, which may drive changes in the plant
community as the climate warms.
Observed changes in plant N dynamics at CiPEHR may be
further accelerated by warming-mediated changes in litter bio-
mass and composition (Hobbie & Chapin 1998). Despite the
lack of warming effects on foliar N concentrations, variation
© 2011 The Authors. Journal of Ecology © 2011 British Ecological Society, Journal of Ecology, 100, 488–498
in foliar N across species and functional groups, coupled with
shifts in species abundance, may significantly impact the
distri- bution and cycling of N in this system. With the
exception of
C. bigelowii, we detected no change in litter N concentrations,
yet warming-mediated changes in litter biomass and composi-
tion significantly increased N mass returned to soils in leaf lit-
ter. The predominant increase in graminoid litter in the winter
warming treatment may further alter N cycling because grami-
noid litter decomposes faster than other functional groups
(Hobbie 1996).
In combination with observed changes in ecosystem N
dynamics, plant growth at CiPEHR may also have been
stimulated by warming-mediated shifts in leaf phenology. In
the winter warming plots, where higher soil temperatures
are expected to enhance wintertime N mineralization (Schi-
mel, Bilbrough & Welker 2004), earlier leaf-out and growth
may have increased plant access to early-growing-season N
pools. However, while phenological shifts can contribute to
higher plant productivity by extending the time period when
plants can assimilate C, earlier bud break and delayed senes-
cence will not necessarily translate into greater plant produc-
tivity if N limitation persists. In the case of our summer
warming treatment, in which phenological shifts were not
accompanied by an increase in canopy N, the short-term
benefit of advanced leaf-out may have limited plant growth
later in the season. An increase in plant N pools in the win-
ter warming treatment, combined with phenological shifts,
together supported higher plant growth throughout the
growing season. While the delay in senescence observed at
CiPEHR in the second year of warming would not have
affected biomass accumulation to date, these late-season
dynamics may be important for plant C stores in subsequent
growing seasons.
The observed warming effects on leaf phenology at
CiPEHR lend insight into processes governing bud break and
senescence in northern latitude ecosystems. Accelerated bud
break and early season plant growth, which have been
observed across the Arctic over the past few decades, have
been attributed to earlier snowmelt and warmer air
temperatures (Myneni et al. 1997; Arft et al. 1999; Walker,
Billings & De Molenaar 2001; Wipf 2010). An observational
study in an alpine ecosystem suggested a relationship between
phenology and soil tempera- ture (Holway & Ward 1965);
however, in that study, higher soil temperature co-occurred
with snowpack retreat, confounding the effect of these two
variables on phenology. Results from CiPEHR, where soil
temperature and active layer increased but snowmelt date was
held constant, demonstrate direct effects of warmer soil
temperature or advanced soil thawing on early-season leaf
phenology in northern latitude tundra. Fur- thermore, while
previous studies found that warming of air and surface soils
had limited effect on late-season leaf phenol- ogy (Arft et al.
1999), our results show that warming signifi- cantly delayed
senescence, with the strongest effect in the combined summer
and winter warming treatment (i.e. Annual warming). This
result is in agreement with that by Marchand et al. (2004),
who found that air and soil warming significantly delayed the
loss of green cover in high Arctic tundra. While photoperiod
plays a role in initiating senescence, our results demonstrate
that temperature and soil resources play a key role in
controlling the duration of plant senescence in this ecosystem.
The effects of winter warming treatment on reproductive
effort also point to an alleviation of N limitation with warmer
soils and degrading permafrost; increased reproductive effort
requires a higher nutrient investment, and without a concomi-
tant increase in N availability, higher reproductive investment
should occur at the cost of vegetative growth (Bazzaz et al.
1987; Aerts & Chapin 2000). Winter warming may have also
enhanced reproductive effort through protection of overwin-
tering reproductive buds by the insulating layer of the snow-
pack (Bokhorst et al. 2008). However, we observed no
change in flower (S. Natali, pers. obs.) or berry production
after the first year of warming, which suggests that warming
effects on reproductive investment resulted from increased
production rather than decreased loss of reproductive buds.
The 1-year time-lag of warming effects on reproductive effort
is not sur- prising because several tundra plant species form
flowering buds in the year prior to flowering (Mark & Chapin
1989). In a meta-analysis of ITEX experiments, Arft et al.
(1999) found that reproductive and vegetative responses of
plants to warm- ing varied across climatic zone and suggest
that in the low Arc- tic, where seedling establishment
opportunities are lower because of a closed plant canopy,
allocation to vegetative growth should be favoured. However,
at CiPEHR, where can-
© 2011 The Authors. Journal of Ecology © 2011 British Ecological Society, Journal of Ecology, 100, 488–498
opy cover is complete, we found that winter warming
increased both reproductive and vegetative growth, which
were probably supported by increased N availability. These
results highlight the importance of changes in the soil
environment, including nutrient availability, in determining
tundra plant responses to a changing climate.
Conclusions
This study examined the responses of plant productivity and
biomass to experimental warming of air, soil and permafrost
in moist acidic tundra. The CiPEHR project is the first warm-
ing experiment to degrade permafrost without additional
water inputs or delayed snow melt. We hypothesized that
warming would increase ecosystem-level plant productivity,
but only if nutrient availability also increased with warming.
Changes in the soil environment brought about by the winter
warming treatment increased plant-available N, extended the
period between bud break and senescence, and led to an
increase in above-ground C accumulation. While summer
warming also caused phenological shifts and altered species-
level ANPP, we detected no ecosystem-level increases in
plant productivity with summer warming, which we attribute
to con- tinued N limitation in the summer warming plots.
These results highlight the role of soil and permafrost
dynamics in regulating plant response to climate change and
suggest that phenological shifts coupled with increased
nutrient availability may pro- mote greater C accumulation in
tundra plant biomass. Cli- mate-induced changes in tundra
plant communities is of critical concern because permafrost
systems play a key role in global C storage, and as
demonstrated from this study, increased plant C uptake has a
strong potential to offset some respiratory losses expected as
the climate warms.
Acknowledgements
This work was made possible by assistance from A. Baron, G. Crummer,
C. Trucco, and the researchers and technicians of Bonanza Creek LTER.
This work was funded by NSF CAREER Program, NSF Bonanza Creek
LTER Program, and Department of Energy NICCR Program (E.A.G.S.)
and NSF OPP (S.M.N.).
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Received 16 June 2011; accepted 21 October 2011

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© 2011 The Authors. Journal of Ecology © 2011 British Ecological Society, Journal of Ecology, 100, 488–498
ANALISIS VEGETASI
Analisis Vegetasi Dan Perbedaan Dalam Variabel Lingkungan Lokal Di Daerah Proyek
PLTA Indrawati Di Nepal

Hutan dan vegetasi ekosistem tertentu umumnya dipengaruhi oleh faktor eksternal.
Braun-Banquet mengatakan bahwa vegetasi terdiri dari komunitas tumbuhan yang berbeda
dan cukup diskrit tertentu. Pandangan ini menganggap komunitas tumbuhan memiliki tingkat
intern yang bersama-sama memodifikasi lingkungan dengan batas tertentu dari komunitas
tumbuhan lainnya. Karenanya, dikembangkan cara untuk memperkirakan perubahan
lingkungan di suatu tempat tertentu menggunakan perbedaan vegetasi saat ini dibandingkan
dengan murni atau vegetasi alami yang potensial.
. Komposisi struktur tanaman terkait erat dengan faktor lingkungan biotik dan abiotik
yang membuat perubahan mendadak karena faktor eksternal dari gangguan. Vegetasi saat ini
mencerminkan kondisi lokasi dan gangguan dari waktu ke waktu. Kepadatan dipengaruhi
oleh berbagai faktor, termasuk ketinggian, jenis tanah, spesies dominan, faktor iklim,
stabilitas lingkungan, penggunaan lahan dan wilayah dan heterogenitas habitat merupakan
faktor yang sering dibahas sebagai faktor penentu variabilitas dalam kekayaan spesies.
Sebagai vegetasi yang kompleks, jumlah kerapatan berdiri cenderung menurun basal area dan
volume. Kepadatan dan dispersi cukup sensitif terhadap ukuran dan intensitas gangguan.
Perbedaan yang luar biasa dalam kepadatan berdiri antara daerah hutan dikelola dan
terganggu adalah karena intervensi pembangunan dan sejarah manajemen yang tepat. Luas
total basal yang lebih tinggi dalam plot 1 adalah hasil dari tingginya proporsi pohon lingkar
lebih besar dari 70 cm. Pohon dengan diameter yang lebih besar memiliki tutupan tajuk lebih
luas dan sebagai kanopi menjadi dekat mengintensifkan persaingan tanaman dan pohon-
pohon yang tumbuh lambat menjadi stunt dan mati. Kurangnya pohon kecil menunjukkan
bahwa hutan tidak mempertahankan itu sendiri. Hal ini mungkin disebabkan oleh gangguan
manusia berulang.Tingkat gangguan dapat dikaitkan dengan cara mudah, penggembalaan,
pengaturan yang tidak efisien dari spesies yang ditanam, dan kurangnya alternatif sumber
hasil hutan.
Jadi, Perbedaan jumlah pohon individu, spesies, family, total luas basal, dan
komposisi vegetasi mungkin karena perbedaan dalam variabel lingkungan setempat gradien
gangguan dan karakteristik vegetasi.
 Vol. 01, No. 01, pp. 01 –07 (2020)
ISSN: XXXX-XXXX

JOURNAL OF APPLIED SCIENCE AND TECHNOLOGY TRENDS

www.jastt.org

Spatiotemporal Analysis of Vegetation Cover in Kurdistan

Region-Iraq using MODIS Image Data

Yaseen T. Mustafa

Dept. of Environmental Science, Faculty of Science, University of Zakho, Kurdistan Region-Iraq (yaseen.mustafa@uoz.edu.krd)

Abstract
The rapidly and wide use of remote sensing and accurately obtain information on the spatiotemporal distribution of large-scale
vegetation is of great significance for improving and managing the Environment. To assess and analyze the spatiotemporal variation of
vegetation status in Kurdistan Region of Iraq (KRGI), we used time series NDVI-based vegetation that are extracted from MOD13Q1
MODIS product over 20 years (2000 - 2019). The results showed that vegetation was mainly distributed in the north-east to south-east of
the KRGI, while west region has less distributed and almost no vegetation. This is clearly remarkable in the south-west part of the
region (Garmian administration). While, the most dominated vegetation province was Duhok province in KRGI during study period.
There is a noticeable temporal variation in vegetation over a period of 20-year in the KRGI. The lower vegetated cover area is observed
in the years 2000, 2008, and 2009. The increase/decrease of vegetated cover area is not only effected by climate conditions. The
anthropogenic resource is also one of the main resources that has a major influence on the increase/decrease of vegetation.

Keywords: NDVI, MODIS Images, Vegetation, KRGI.

Received: January 5 / Accepted: February 20 / Online: March 10

of scientific mechanism of the evolution of the Earth’s environment

I. INTRODUCTION
Vegetation cover has a critical role in climate change by
sequestering, or storing, large quantities of carbon. Several
climate research projects focused on the quantification of
vegetation cover to study the drought severity [1-3].
Moreover, it has been used to investigate a relationship with
soil [4], temperature and urban form [5-8].
Vegetation mapping presents valuable information for
understanding the natural and man-made environments
through quantifying vegetation cover. Longtime monitoring
measurements of spatial vegetation variation can generate a
useful information regarding land surface cover changes and
its trends. Satellite data can provide a long-term and continues
information on spatial and temporal variation of vegetation.
Measures of remotely sensed vegetation cover and density
include foliage cover [9], woody and non-woody cover [10],
and absorbed photosynthetically active radiation[11].
Several researchers were utilized satellite images to reveal
the status of the vegetation coverage (forest, grass, crops, …
etc.) [12-17]. One of the satellite that provide continues data
(spatially and temporally) is Moderate Resolution Imaging
Spectroradiometer (MODIS). It also provides a new data
source that includes atmosphere, land and ocean for integrated
studies
and its changes. Mustafa [18] estimated Leaf Area Index
(LAI) in heterogeneous forests using MODIS data. He
provided approach for estimating the variation of LAI over
time. Gholamnia, et al. [19] analysed spatiotemporal
behaviour of vegetation cover in the Kurdistan province of
Iran using Normalized Difference Vegetation Index (NDVI)
time series derived MODIS observation. Moreover, an attempt
on the application of remote sensing data was achieved for
extraction of phonological variables for alluvial plain Kamrup
Sal forest of northeast India [20]. They used time series NDVI
datasets of MODIS product for a period of 10 years. Some
investigations on the application of remote sensing data for
vegetation analysing were conducted at parts of the Kurdistan
region of Iraq (KRGI). For example, Hussein, et al. [21]
assessed the spatiotemporal variations of vegetation index in
Erbil and its environment between 2000 and 2015, using
MODIS satellite data. Till date, no attempt has been made to
analyse spatiotemporal variation of vegetation cover in the
whole KRGI using remote sensing data. For this reason, the
current study is an attempt on the application of remote
sensing data for estimating and analysing of vegetation
coverage for KRGI over a period of 20 years (2000-2019).

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 Yaseen T. Mustafa / Journal of Applied Science and Technology Trends Vol. 01, No. 01, pp. 01 –07, (2020)

II. STUDY AREA

Kurdistan Region of Iraq (KRGI) is a feral region that corrections
is were performed, and the cloudy pixels were removed.
located in the northeast of Iraq. It is bordered by Turkey from The high quality pixels flagged were used for the analysis
the north, Iran from the east, Syria from the north-west and [25].
from the south and southwest is Iraqi part. KRGI located The form of NDVI [26] is shown in Eq. (1):
between
latitudes 33°57'58.5" – 37°20'33.55"N and longitudes 𝑁𝐼𝑅 − 𝑅𝑒𝑑
𝑁𝐷𝑉𝐼 = (1)
42°20'25.36" – 46°19'16.475 E (Fig. 1), and cover an area 𝑁𝐼𝑅 + 𝑅𝑒𝑑
2
around 50325.82 km with elevation ranges (88 m – 3600 m). It has Where NIR, Red, and Blue refer to the near-infrared, Red
three provinces (Duhok, Erbil, Sulaymaniyah), and Garmian and blue reflectance bands, respectively.
administration, where the city of Erbil is the capital. The
KRGI is characterized by a Mediterranean climate, which is In this study, 20 products (images) were collected from
cold and rainy in winter and hot and dry in summer [22]. 2000 to 2019, such that one image at June 10th for each year
KRGI can be divided into the Zagros Mountains and the were downloaded. They were used to determine variations of
Foothills. The climate of Kurdistan is governed by high vegetation extent over whole KRGI annually, for a period of
precipitation rates in the northern parts and drier climate in the 20 years.
plains [23]. The precipitation starts from October to May with
the amount of 350 in the southwestern parts to more than
1,200 mm in northern and north-eastern parts. While, the
mean daily temperature varies from 5°C in winter to 30°C in
summer; however, this might rise to 50°C in the southern parts
of the region [22, 23].

Fig. 2. Flow diagram showing the methodology steps.

Fig. 1. Location of the study area, (a) Iraq Map, (b) KRGI map with
weather stations location. B. Climate Data
Average temperature, and annual rainfall were collected
over the 20 year period (2000-2019) from 60 weather stations,
III. DATA AND METHODS which are distributed over KRGI. The location of these
The methodology steps in this study is presented in Fig. 2. stations are shown in Fig. 1(b). All climate data was provided
by Ministry of Agriculture and Water Resources and Ministry
A. MODIS Data of Planning at KRGI [22]. The most important climate data for
vegetation is the precipitation. Therefore, the plot of
This study is based on the MODIS Terra land satellite data.
precipitation along with the temperature are shown in Fig. 3.
MODIS has a 36-channel visible to thermal-infrared sensor
with an FOV (field of view) of ±55 o, a scene width of 2230
km, and a temporal resolution of 1–2 days. There are many
standard MODIS data products that scientists are using to
study global change. In this study MODIS NDVI 16-day level
3 product (MOD13Q1, collection 6) from Terra platform with
250-km spatial resolution was used. These data were
downloaded from the MODIS website [24]. The NDVI
product from MOD13Q1 MODIS is computed from
atmospherically corrected bi- directional surface reflectance
that have been masked for water, clouds, heavy aerosols, and
cloud shadows. The geometrical Fig. 3. Total annual rainfall and average temperature of 20 years for
60 stations in KRGI.
2
 Yaseen T. Mustafa / Journal of Applied Science and Technology Trends Vol. 01, No. 01, pp. 01 –07,
(2020)
C. Methodology
1) MOD13Q1 MODIS pre-processing: The time series
MOD13Q1 MODIS data of 20 years (2000 – 2019) were
acquaried from the Land Processes Distributed Active
Archive Center (LP DAAC). The dataset were obtained
in hdf format. They first converted to geo-tiff format and
reprojected to WGS84/UTM Zone 38 N. Moreover, the
pixel size was resampled to 250m. Next, the study area
(KRGI) were masked out. These steps were achieved for
all 20 images.
2) MOD 13Q1 MODIS processing: In this stage, a Fig. 5. The vegetated area with non-vegetated area of KRGI during
vegetated area from non-vegetated area was identified. 20 years.
This is done through selecting a threshold experimentally
for each NDVI image at each year. For the 20 years, the
threshold values range was between 0.23 and 0.27. Next TABLE I. VEGETATED AREA FOR A PERIOD OF 20 YEARS OF KRGI
the area of vegetation is calculated for each year and a Vegetated Area
time series graph was plotted. Further, the spatial Year
No. of Pixel Area (km2)
variation was compared among these year and reported. 2000 157860 9866.25
2001 223153 13947.06
2002 219456 13716.00
IV. RSULTES AND DISCSSION 2003 212609 13288.06
The mean, maximum, and minimum values of NDVI for 2004 267047 16690.44
the 20 years are shown in Fig. 4. It is reported that the NDVI 2005 233729 14608.06
values are low in 2000, 2008, and 2009. This is matching with 2006 287364 17960.25
the rainfall amount at the same year (Fig.3) as the amount of 2007 253012 15813.25
the rainfall in these year was lower than other years. 2008 147152 9197.00
2009 74824 4676.50
2010 249751 15609.44
2011 257182 16073.87
2012 217917 13619.81
2013 231588 14474.25
2014 230314 14394.63
2015 240972 15060.75
2016 251965 15747.81
2017 243846 15240.37
2018 293509 18344.31
2019 312450 19528.12

The spatial variation of the NDVI-based vegetation results

Fig. 4. NDVI time series from 2000 – 2019 in KRGI, comparing
mean, minimum, maximum values.
Fig. 5 presents the vegetated area along with non-vegetated
area over 20 years for the KRGI. The vegetated area is
calculated from total number of vegetated pixels (Table 1). By
comparing Fig. 5 with Fig. 3, a significant observation can be
concluded as clear a relationship exist between precipitation
and vegetated area. This is confirmed by Gaznayee and Al-
Quraishi [27]. They found a strong relationship between
vegetation and precipitation. However, the increase or
decrease of vegetated area is not only effected by high/low
amount of precipitation. The anthropogenic resource is also
one of the main resources that has a major influence on the
increase/decrease vegetation.
is displayed in Fig. 6. This results were confirmed and agreed
with the statistical reports of the Ministry of Agriculture and
Water resource in the KRGI, which indicated that low rainfall
and high temperature in the KRI had happened in 2000, 2008,
and 2009. It is also noticeable that the highest NDVI-based
vegetation area was in the year 2018, and 2019. The NVDI-
based vegetation that is higher than 0.6 value is observable in
2012 for both provinces Duhok and Erbil, and part of
Sulimanyha province. However, in years of 2018 and 2019
with same NDVI-based vegetation value (> 0.6) was only
appear in Duhok province with small part of Erbil. The NDVI-
based vegetation area with value between 0.2 and 0.6 was
more marked in most of the study year except in the year of
2000, 2008, and 2009. Nonetheless, the larger are of NDVI-
based vegetation within the range 0.2 – 0.6 was measurable in
the year of 2019. This results match with the amount of
precipitation that is recorder in the study area between 2000
and 2019 (Fig.5).

3
 Vol. 01, No. 01, pp. 01 –07 (2020)
ISSN: XXXX-XXXX

JOURNAL OF APPLIED SCIENCE AND TECHNOLOGY TRENDS

www.jastt.org

Fig. 6. Spatial variation of the NDVI-based vegetation from 2000 to 2019 in KGRI.

Fig. 7 illustrated the distributed vegetated cover area over
KRGI for 20 years (2000 – 2019). In general over 20 years,
Duhok province comes in the first place as it has the largest
vegetated cover area. Followed by Sulaymaniyah and Erbil,
while the lower vegetated cover area is in Garmian. Here is
also confirmed that the lower vegetated cover area in KRGI is
observed in the years 2000, 2008, and 2009. The larger
vegetated cover area in KRGI during this 20 years is in the
years 2018, and 2019 (Table 2, Fig.7). Moreover, the
moderate vegetated cover area is observed in the years 2001,
2003, 2005,
2010, 2014, and 2017. However, the lower vegetated cover area
is in the years 2000, 2008, and 2009.
The spatial variation of vegetated cover area are
distributed in the east part of KRGI from the north (large area)
to the south (smaller area). This is due to the fact that these
areas are mountainous areas which are suitable for vegetation
and they are far from the human influences.
It is worth mentioning that this results is based on a coarse
resolution (250 m) satellite data (MOD13Q1 MODIS).
Therefore, calculated area might not be precise as the pixel

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 Yaseen T. Mustafa / Journal of Applied Science and Technology Trends Vol. 01, No. 01, pp. 01 –07,
(2020)
cannot be break it down. For example, if more than half of the could be used. However, finer resolution images might not be
pixel is vegetation, then as an average the pixel will give one available always at the same harmonic date as what is
value indicating that the whole pixel is vegetation. Thus, to get available in MODIS. From the other side, MODIS product is a
rid of this limitation a satellite imagery with a finer resolution composite data which facilitate the process of getting results.

Fig. 7. Vegetated area of KRGI for the period of 20 year after NDVI
threshold value selection of each year.

 T
h
e
la
rg
er
v
e
g
et
at
e
d
c
o
v
er
ar
ea
in
K
 Yaseen T. Mustafa / Journal of Applied Science and Technology Trends Vol. 01, No. 01, pp. 01 –07,
(2020)

V. CO years was in the years

NC 2018, and 2019.
LU However, the
SIO smaller vegetated
N cover area was in
This study attempted to the years 2000,
analyse the spatiotemporal 2008, and 2009.
variations of vegetation
 The spatial
coverage in KRGI between
distribution of
2000 and 2019 using
NDVI-based
MODIS data. This is
vegetation in KRGI
performed by using time
was generally
series NDVI-based
focused in the
vegetation that is obtained
northeast to
from MOD13Q1 MODIS
southeast.
product. The results of this
study provide the following  During the period of
conclusions: 20 years (2000 –
2019), the most
 The lower NDVI
dominated
values in KRGI
vegetation province
between 2000 and
was Duhok province
2019 was in the
in KRGI.
years 2000, 2008,
and 2009.

5
 Yaseen T. Mustafa / Journal of Applied Science and Technology Trends Vol. 01, No. 01, pp. 01 –07, (2020)
 Considering vegetation distribution in KRGI and
according to collected MODIS data, the KRGI
manifested high levels of vegetation regardless of the
period of the year.
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[11] R. B. Myneni, R. Ramakrishna, R. Nemani, and S.
W. Running, "Estimation of global leaf area index
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Series MSAVI2."
KOMPLEKSITAS TUMBUHAN
 Signifikansi ekologis dan kompleksitas preferensi sumber-N pada tanaman

Tumbuhan terestrial mengambil nitrogen anorganik dari tanah terutama dalam bentuk
amonium yaitu NH4 dan NO3 dua ion itu ketika diperoleh memiliki genetik dan metabolisme
yang sangat berbeda konsekuensi dalam pabrik. Banyak faktor lingkungan lainnya yang
mempengaruhi penyerapan N, dengan efek divergen ditemukan untuk NO3
dan NH4. Salah satunya yang paling penting adalah suhu tanah yang dapat berfluktuasi sangat
pada skala waktu berbulan-bulan, berhari-hari atau berjam-jam. Secara umum, NO 3 serapan
tampaknya lebih terhambat oleh suhu rendah daripada yang terjadi NH4 serapan yang dapat
dijelaskan oleh kebutuhan energi yang lebih tinggi untuk akuisisi dan pengurangan. PH tanah
juga menunjukkan tinggi dan mempengaruhi NO3 dan NH4 transportasi berbeda, dengan
optima cenderung lebih basa untuk NO3 serapan daripada NH4 serapan. Ini agak
mengejutkan mengingat bahwa ada kebutuhan proton yang lebih tinggi untuk NO3 serapan
daripada NH4.
Mekanisme proton-symport interaksi nutrisi kompleks lebih lanjut dengan
signifikansi luas dapat dipertimbangkan dalam tiga kelompok. Kelompok pertama terdiri dari
interaksi antara sumber N, tanah penggunaan air dan kelembaban. Misalnya, peningkatan
adaptasi kekeringan telah diamati dengan NH4+ nutrisi dalam beberapa sereal sementara
penelitian lain, terutama dalam dikotil, telah menunjukkan penurunan efisiensi penggunaan
air di bawah NH4. Penulis ini menemukan bahwa NO3 adalah sumber pilihan untuk semua
spesies di bawah kondisi kering, sedangkan di tanah paling tebal NH4 + hampir secara
eksklusif bekas.
Kelompok interaksi kedua adalah antara sumber N dan intensitas cahaya. Cahaya
memainkan peran penting dalam mengatur komponen-komponen utama dari NO3. Kelompok
interaksi ketiga adalah antara sumber N dan perubahan CO2 atmosfer: topik ini telah
menghasilkan hasil yang beragam, tetapi peningkatan CO2 bisa menghasilkan efek
diferensial yang cukup besar pada akuisisi.
See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/251878199

Ecological significance and complexity of N-source preference in plants

Article in Annals of Botany · July 2013

DOI: 10.1093/aob/mct157 · Source: PubMed

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Dev Britto Herbert J. Kronzucker

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Annals of Botany 112: 957– 963, 2013
doi:10.1093/aob/mct157, available online at www.aob.oxfordjournals.org
VIEWPOINT

Ecological significance and complexity of N-source preference in plants

Dev T. Britto and Herbert J. Kronzucker*
Department of Biological Sciences, University of Toronto, 1265 Military Trail, Toronto, Ontario, Canada M1C 1A4
* For correspondence. E-mail: herbertk@utsc.utoronto.ca

Received: 29 April 2013 Returned for revision: 20 May 2013 Accepted: 29 May 2013 Published electronically: 24 July 2013

† Background Plants can utilize two major forms of inorganic N: NO3 2 (nitrate) and NH4 + (ammonium). In some cases,
the preference of one form over another (denoted as b) can appear to be quite pronounced for a plant species, and
can be an important determinant and predictor of its distribution and interactions with other species. In many other
cases, however, assignment of preference is not so straightforward and must take into account a wide array of
complex physiological and environmental features, which interact in ways that are still not well understood.
Scope This Viewpoint presents a discussion of the key, and often co-occurring, factors that join to produce the
†
complex phenotypic composite referred to by the deceptively simple term ‘N-source preference’.
† Conclusions N-source preference is much more complex a biological phenomenon than is often assumed, and
general models predicting how it will influence ecological processes will need to be much more sophisticated Do
than those that have been so far developed. wn
loa
Key words: Ammonium, nitrate, N-source preference, succession, competition, soils, amino acids, complexity. de
d
INTRODUCTION fro
specialists (Gerenda´ s et al., 1997; Britto and m
Terrestrial plants take up inorganic nitrogen from the soil Kronzucker, 2002) and atrophied nitrate uptake systems in the htt
mainly in the forms of ammonium, NH+4 and3 nitrate, NO2, roots of ammo- nium specialists (Kronzucker et al., 1997). p:/
two ions that, when acquired, have highly distinct genetic and Fundamental ques- tions remain unanswered in this branch of /ao
metabolic consequences in the plant (Haynes and Goh, 1978; physiology, such as that of why many plants, especially b.
Britto and agricultural crop species
and early-successional pioneer species, appear to prefer NO2 ox
Kronzucker, 2002, 2005a; Stitt et al., 2002). Some plant + 2 3 for
species have been shown to produce more biomass, or to NH4 , despite the fact that NO 3 must be taken up against +a dj
accumu- late greater quantities of nitrogen, when growing on steep electrochemical gradient, then reduced to NH 4 ou
one N source compared with another, i.e. they appear to before entering the organic N pool. Both processes require a rn
display a pref- erence. Despite the importance of N as a consider- able additional expenditure of fixed carbon als
frequently growth- limiting nutrient in both agricultural and compared with NH+4 acquisition (Bloom et al., 1992; .or
wild ecosystems (Tilman, 1985; Vitousek and Howarth, 1991), Kurimoto et al., 2004; Britto and Kronzucker, 2005a). One g/
however, no precise definition of N-source preference answer to this appears to lie in the rapid entry of NH+4 into by
(denoted here as b, after Boudsocq et al., 2012) has emerged roots, which occurs even in NO2 specialists, and can result in gu
in the literature, nor has a robust, broad classification of plant pronounced
3 accumulation of NH+4 (Givan, 1979; Gerenda´ s est
species2 adapted + et al., 1997; Britto et al., 2001). Ammonium build-up can on
to NO or NH (although a few preliminary attempts have No
3 4 consequently have toxic effects,
including the suppressed uptake of important cationic nutrients, ve
been made, e.g. Krajina et al., 1973; Falkengren-Grerup, 1995; m
Britto and Kronzucker, 2002). This is in part because the such as K+, Ca2+ and Mg2+ (Kirkby, 1968; Salsac et al., 1987; be
interac- van Beusichem et al., 1988;
2 Lewis, 1992; Britto and Kronzucker, r
tions between plant acquisition of NO 2 or3NH+ and4 multiple 2002). By typically
contrast, NO3 toxicity is fairly uncommon and
environmental variables, such as temperature, soil pH and
nutrient supply, produce a complex of effects that can greatly occurs at very much higher soil concentrations (Britto and
influence and shift plant growth responses to variable N Kronzucker, 2005b, and references therein). Among the strategies
sources. In an ecological setting, this physiological complexity used by plants to decrease the amount of free NH+4 in
is compounded by the variability inherent in many ecosystems, tissues is increased NH+4 assimilation (Givan, 1979;
where large changes in soil characteristics frequently occur Magalhaes et al., 1995; Gerenda´ s et al., 1997;
over short distances and short spans of time (Hodge, 2004). In Schortemeyer et al., 1997). However, this requires an
this paper we shall discuss the complexities involved in elevated supply of carbohydrate to the roots, because only a
accurate- ly modelling b within ecological contexts, and the small amount of NH+4 is translocated to shoots (Wang et al.,
significance of such preferences for ecological processes such 1993; Kronzucker et al., 1998; Finnemann and Schjoerring,
as succession. 1999), leaving less reduced carbon available for growth and
maintenance (Lewis, 1992). Another strategy is to
increase the efflux of NH+4 to the external medium, which can,
PHYSIOLOGICAL UNDERPINNINGS OF however, result in an energetically costly futile cycle (Britto
N- SOURCE DIFFERENCES et al., 2001; Li et al., 2012). Energy lost in this cycle, in addition
to the frequently suggested uncoupling of energy gradients in
The reasons underlying apparent N-source preferences are cellular organelles by NH+4 (Krogmann et al., 1959; Crofts,
poorly understood, but include ammonium toxicity in nitrate 1967; this possibility is disputed, however – see Gerenda´ s et
al., 1997;
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958 Britto & Kronzucker — Ecological significance and complexity of N-source
Britto and Kronzucker, 2002), may eliminate any energetic
advan- tages conferred by the uptake +of reduced N. Although
elevated res- piration under high-NH 4 conditions has been
attributed to futile NH+4 cycling in roots (Britto et al., 2001),
the link between carbo- hydrate limitation and preference
against NH+4 is not straightfor- ward, since increased light
intensity may aggravate rather than alleviate NH+4 toxicity
(Gerenda´s et al, 1997; Zhu et al., 2000).
Deficiency, sufficiency and toxicity occur for both inorganic
N forms, with very different set points, and growth optima are
expected and commonly observed (Fig. 1; Gray, 1983; Eck,
1984; Westfall et al., 1990; Miller and Timmer, 1994; Padgett
and Allen, 1999; Cabrera, 2000; Gan et al., 2012; Hall, 2002).
Such optimum curves, and how they differ with N source for a
given plant species, should inform any fundamental appraisal
of the N-source preference(s) of that species, since they are
dir- ectly linked with plant productivity. Root transport
systems spe-2
cific for NO3 and NH+4 acquisition fundamentally influence the
shapes of growth – response curves , since their activities not
only determine the amount of excessive, detrimental transport
that may occur at high substrate concentrations (Britto et al.,
2001) but also govern the lowest soil N concentration from which
a species can abstract the limiting resource and at which it can
survive. This concentration minimum is frequently referred to
as the Cmin, and may be as low as 0 .001 mM for both NO2 and
NH+4 (Deane-Drummond and Chaffey, ~ 1985; Marschner 3
et al., 1991). The Cmin concept is important in modelling pro-
cesses such as competition and succession, and is similar to
important ecological principles such as Justus von Liebig’s
‘law of the minimum’, and Tilman’s R* rule, which predicts
the outcome of competitive interactions between species based
on their ability to survive on the lowest amount of a limiting
resource (Tilman, 1982; McGill 2005; Wilson et al., 2007).
However, it should be emphasized here that Cmin (like b, as
will be discussed) is not constant for a plant species, but varies
with root activity, which in turn strongly depends on factors
such as temperature and plant nutrient status (Drew et al.,
1984; Marschner et al., 1991).
Because the regulation of inorganic N transport largely deter-
mines the uptake of nutrients at both limiting and toxic
concentra-
tions, it is crucial to examine it in the present context.
Particularly
important is the physiological principle that the transport
systems moving inorganic N across root plasma membranes, as
well as the metabolic systems assimilating N within the cell, are
typically downregulated by increasing soil nutrient content,
especially
that of N itself (Glass et al., 2002; Tang et al., 2012). The
curves in Fig. 2 exemplify this pattern of regulatory feedback by
long- term N supply and plant N status on the kinetics of N
uptake (Wang et al., 1993; Rawat et al., 1999; Kronzucker et al.,
3 4
2000). Similar patterns are seen for both NO2 and NH+, but
with unique kinetic parameters for each. It is important to note
that these curves are typically hyperbolic in shape, as in Monod
or Michaelis– Menten equations, under most ecologically
relevant supply conditions; in other words, they saturate, as does
the growth response to increasing soil N. Under toxicity or
‘luxury consumption’ conditions, however, linearly rising
patterns of uni- directional influx are sometimes observed, but
elevated influx is largely compensated for by elevated efflux
under these conditions (Brittoand Kronzucker, 2006) anddoes
nottranslateinto increased growth (Gezelius and Na¨sholm,
1993; de Mazancourt et al., 2012). An added layer of
regulatory complexity can be seen in the case ofdownregulatedin
thenitrateacquisitionapparatus, which is greatly
3
the absence of NO2 (Kronzucker et al., 1999a; Glass et al.,
2001). The induction of this apparatus by the appearance of Do
nitrate can be quite rapid in some species, taking only a few wn
hours (Siddiqi et al., 1989; Kronzucker et al., 2000), while in loa
others, such as white spruce, it can take several days de
(Kronzucker et al., 1995; Min 3et al., 1998). Oncestimulated, d
NO2 transportis usuallydownregu-
3 lated by further NO2 fro
acquisition, but this is not well understood; there appear to be m
species-specific differences in the metabolites responsible for htt
this effect (Glass et al., 2002; Tang et al., 2012). Regardless of p:/
the mechanism, it is well known that changes in soil N pools /ao
can exert powerful influences on N-acquisition char- acteristics, b.
and bring changes in apparent N-source preferences, even at sub- ox
toxic concentrations (Tylova-Munzarova et al., 2005; for
Munzarova et al., 2006; Houlton et al., 2007). dj
Many other environmental factors influence the uptake of ou
N, with divergent effects found for NO23and NH+.4 One of the rn
most important is soil temperature (Haynes and Goh, 1978; als
Sasakawa and Yamamoto, 1978; Clarkson and Warner, 1979; .or
Kafkafi, 1990; Macduff and Jackson, 1991; Gessler et al., g/
1998; Vaast et al., 1998; Kumar et al., 2008), which can by
fluctuate greatly on time scales of months, days or hours. In gu
general, NO2 uptake appearsto be more inhibited by low 3 est
temperature than does on
No
NH uptake (Frota and Tucker, 1972; Clarkson et al., 1994),
+ ve
4
m
which can be explained by its higher energy requirement for be
r
Plant
nutrient status

Low-N
N uptake by roots

Deficient Toxic
Plant biomass

Moderate-N
Optimal

High-N

Available nitrogen Soil N concentration

FIG . 1 . Optimal curve relating plantbiomass gainto N supply. Generalized from FIG . 2. Influence of plant N status on concentration-dependent N-uptake
published data (see citations in text). kinetics by plant roots. Generalized from published data (see citations in text).
acquisition and reduction (see above). Soil pH also 2shows high
variability (Farley and Fitter, 1999) and affects NO and NH+
3 4
transport differentially, with optima tending to be more
alkaline
for NO2 uptake than for NH+ uptake (Haynes and Goh, 1978;
3 4
von Wire´ n et al., 1997; Hawkins and Robbins, 2010). This
is somewhat surprising given that there is a higher proton
require-
ment for NO2 uptake than for NH+, since it is driven by a
3 4
proton-symport mechanism (McClure et al., 1990; +Britto and
Kronzucker, 2006; Miller et al., 2007), while NH 4 uptake
prob- ably occurs in a uniport manner, in exchange for protons
(though not directly coupled to H + transport), under most
conditions [Ludewig et al., +2002; Mayer et al., 2006; at very
low concentra- tions, NH 4 uptake involves a symport
mechanism with protons (Ortiz-Ramirez et al., 2011), while at
high concentrations NH 3 permeation may be possible through
aquaporins (Jahn et al., 2004)]. The mechanisms of transport
for the two ions themselves have distinct consequences for soil
pH: alkalinization by NO 2 nutrition and acidification by NH+4
nutrition (Raven and Smith, 1976; Runge, 1983; van 3 The third group of interactions are those between N source
Beusichem et al., 1988; Marschner et al., 1991; Falkengren-
Grerup, 1995; Britto and Kronzucker, 2002). These processes
can result in unpredictable feedback
cycles
inhib- that can be intensified by other factors, such as (1)
ition of nitrification rates by soil bacteria as the rhizosphere
acid- ifies (Haynes and Goh, 1978; Falkengren-Grerup, 1995)
and (2) changes in the availability of nutrients, such as P, or
toxicants, such as Al, as soil pH changes differentially
depending on which N source dominates in plant acquisition
patterns (Riley and Barber, 1971; Ruan et al., 2000).
Other majorcomponents of plant nutrition interact
profoundly with plant roots to produce divergent effects
when grown on
NO2 or NH+. One of the most notable examples of this is the
3 4
alleviation of NH+4 toxicity by K+ supply (Mengel et al.,
1976; Santa-Maria et al., 2000; Roosta and Schjoerring, 2008;
Balkos et al., 2010; ten Hoopen et al., 2010; Li et al., 2012).
Another lies in the interactions between NH+4 and NO2
them- selves, such as the significant, and variable, inhibition
3 Melillo, 1979). Moreover, the horizontal and vertical
of NO2 3 patchiness
uptake by (Minotti et al., 1969; Lee and Drew, 1986;
NH+4
Marschner et al., 1991; Kreuzwieser et al., 1997; Kronzucker
et al., 1999a) and the synergistic effect on N uptake and
growth often seen when the two N sources are combined (Cox
and Reisenauer, 1973; Kronzucker et al., 1999a, b). A third
important example is seen in the strong interactions between
carbohydrate supply and growth on different N sources (Haynes
and Goh, 1978; Aslam et al., 1979; Givan, 1979; Kafkafi,
1990), while a fourth is that between inorganic and
organic
N. Regarding this last example, inorganic vs. organic, the soil
N content in some ecosystems, such as boreal forests, can be
pre- dominantly in the form of amino acids, which can be
taken up by roots in substantial quantities (Na¨sholm et al.,
1998; Lipson and Na¨sholm, 2001). This has significance in
terms of providing an alternative source of N when this
resource is limiting, thus redu- 2
cing plant demand for NO and NH+. Moreover, the
downregu- 3 4
latory effect of amino acids on the uptake of NO 2 and NH+ is
3 4
well known (Imsande and Touraine, 1994; Padgett and
Leonard, 1996; Rawat et al., 1999; Gessler et al., 2004).
Further complex nutritional interactions of broad
significance should be mentioned here, and can be considered
in three groups. The first group consists of interactions among
N source, soil moisture and water use. For instance, increased
drought adapta-
(Mihailovic´ et al., 1992; Yin and Raven, 1998; Guo et al.,
2008), while other studies, mainly in dicotyledons, have shown
decreased water-use efficiency under NH+4 (Raven et al., 1992;
Høgh-Jensen and Schjoerring, 1997; Claussen, 2002; Lu et al.,
2005). Moreover, in a striking study of N-source preference
among a functionally diverse group of tropical forest species,
Houlton et al. (2007) showed abrupt community-wide changes
in b resulting from changes in precipitation. These authors
found that NO32 was the preferred source for all species under
dry conditions, while in the wettest soils NH+4 was almost
exclu- sively used.
The second group of interactions are those between N
source and light intensity. Light plays a key role in
regulating key com- ponents of +the NO2-acquisition
pathway (Stitt et al.3, 2002), while NH 4 -grown plants tend
to be more sensitive to light stress than NO2-grown plants
(Magalhaes and 3 Wilcox, 1983; Zornoza et al, 1987; Zhu et
al., 2000).
and changes in atmospheric CO 2: this topic, of considerable
recent interest, has yielded mixed results, but elevated CO 2 can
produce considerable differential effects on the acquisition of
NO2 and NH+, at times causing switches in plant preference
3 4
(Bassirirad et al., 1996, 1997; Zerihun and Bassirirad, 2001).
The plasticity of plant responses to environmental variability
reflectsthe complexity inherentin all ecosystems. This is
particu- larly true in the case of the multifarious environmental
factors influencing b, which must be included when
comprehensively modelling the ecological consequences of
such preferences. For example, even a seemingly simple
agricultural system such as a rice paddy can be dauntingly
complex in terms of modelling
nitrification and nitrate use (Kirk and Kronzucker, 2005), since
these activities, and the resulting magnitudes of N pools, can
vary substantially over temporal and spatial scales. Indeed, the
modelling of nitrification alone can require the consideration
of as many as nine independent processes (Vitousek and
of soils with respect to water and nutrients is well known
(Hodge,
2004); the variability of resources can be 2 as great over the
rooting zone of a plant as it is over a 120-m plot (Jackson and
Caldwell, 1993). Such patchiness extendsto substantial, and
unpredictable, temporal variations in nutrient availability,
including that of
NH and NO23(Drew and Saker, 1975; Farley and Fitter,
+
4
1999). An additional layer of complexity arises from the
ability of vegetation to strongly influence the nutrient
composition of soils; in one study, 10-fold variation in net
mineralization was observed within 3 years in initially
identical soils, as a result of the presence of different plant
species (Wedin and Tilman, 1990). In all these considerations,
it is important to understand that nutrient pool sizes do not
necessarily reflect the importance of a pool in an ecosystem.
While some pools may be small, this may simply be due to the
very rapid turnover caused by intensive
utilization and replenishment of the pool (Robertson and
Vitousek, 1981; Schulze et al., 1994; Eviner and Chapin,
1997; Hart and Stark, 1997; Kirk and Kronzucker, 2005).
Taken together, theabove considerations strongly indicate
that the concept of N-source preference cannot be easily
defined, but depends on a wide and dynamic range of
environmental and physiological factorsthatoverlap
simultaneously. Strictlyspeak- ing, any assignment of a rigid
preference index is valid only for
tion has been observed with nutrition in some cereals the composite of conditions under which it was experimentally
NH+4

Do
wn
loa
de
d
fro
m
htt
p:/
/ao
b.
ox
for
dj
ou
rn
als
.or
g/
by
gu
est
on
No
ve
m
be
r
960 Britto & Kronzucker — Ecological significance and complexity of N-source
determined. Moreover, it may be valid only for a given plant microorganisms in terms of their competition, cooperation and
variety or subspecies (e.g. Zornoza et al., 1996) or N-source preferences, which can change depending on the pres-
developmen- tal stage (Haynes and Goh, 1978; Jing et al., ence or absence of mycorrhizal associations (Plassard et al.,
2012). 1991; Stewart et al., 1993; Clemmensen et al., 2008; Warren,
2009; Paulding et al., 2010; Piao et al., 2012; Wu et al., 2013).
MODELLING THE INFLUENCE OF N- SOURCE Nevertheless, many other plants have eluded simple classifi-
PREFERENCE ON ECOLOGICAL PROCESSES cation as preferring NO2 or NH+. For example, some apparent
3 4
Despite the complex physiological nature of b values, plants NO23 specialists can thrive on NH+ when K+ provision is suffi-
have certainly evolved nutritional adaptations to NO 23 or NH+4, ciently high (Britto and Kronzucker, 2002). Most strikingly in
and thus can often be found on soils enriched in the particular this regard, a quintessentially ‘NH+4 -preferring’ plant such
N source to which they are most adapted for a given condition. as rice (Oryza sativa) can show significant variations in its
Indeed, some plants appear to be so well adapted to a specific apparent b, depending on factors such as soil depth and
N source that they appear to prefer it under a wide range of nutritional com- position, and can be very effective in NO 2
con- ditions. For example, in one study seedlings of Picea utilization (Kronzucker et al., 2000; Kirk and 3 Kronzucker,
glauca and Pinus radiata showed greater growth and N 2005; Balkos et al., 2010). Another such example is that of
uptake with NH+4 than with NO2, regardless of pH, Vaccinium species, which are often considered to be
temperature or type of growth medium (McFee and Stone,
3
NH+4 specialists (Claussen and Lenz, 1999; Britto and
1968). The slow growth of these late-successional conifers on Kronzucker, 2002), but in some studies the co-presence of
NO2 may be particularly limited due to highly atrophied NO2 and NH+ appears to be preferable (Ingestad, 1973). Thus,
transport systems for the ion, as has been3 demonstrated in P. the development of a general model to 3predict the effect of b Do
glauca (Kronzucker et al., 1997), wn
on ecological outcomes loa
while their superior growth on reflects the high (e.g. of competition) should assume the multifactorial nature of de
NH+4 NH+4 d
content and low nitrification potential of boreal forest soils and N-source preference or, more precisely, a set of preferences fro
other climax systems (Rice and Pancholy, 1972; Haynes and rather than a fixed singularity. m
Goh, 1978). Other studies have indicated at times The sheer complexity of possible plant responses to htt
extraordinary plant preferences for one inorganic N source inorganic N source is a major reason why no comprehensive p:/
over another, at various developmental stages and under models yet exist to map and predict the effects of b on /ao
differing nutritional conditions (Rygiewicz and Bledsoe, 1986; ecological processes. Recently, an attempt was made to model b.
Knoepp et al., 1993; van den Driessche and Ponsford, 1995; species replacement dy- namics and ecosystem-level plant ox
Gessler et al., 1998). productivity, using a measure of N-source preference for
In such species and under such conditions, where N-source (Boudsocq et al., 2012). Unfortunately, a very simple dj
preferences appear to be pronounced, soil nitrogen speciation designation of b was used in the process; it was defined as a ou
(and changes in it) has been shown to be a significant linear coefficient for NH+4 uptake, ranging from 0 to 1, while rn
determinant of plant productivity, competition, coexistence (1 2 b) was assigned to be the corresponding coeffi- cient for als
and ecological succession (McFee and Stone, 1968; Rice and NO2 uptake. A fixed N-source preference was thereby assumed .or
Pancholy, 1972; Haynes and Goh, 1978; Lodhi, 1979; Lodhi for a given 3 plant species, as was a linear proportionality g/
and Killingbeck, 1980; Robertson and Vitousek, 1981; between uptake and substrate concentrations. As discussed by
Kronzucker et al., 1997, 2003; Kirk and Kronzucker, 2005; here, however, a fixed b value does not take into account the gu
Kahmen et al., 2008). Such work extends to interactions genetic and physiological plasticities of plant responses to NO 2 est
among plant species and soil or NH+4 within the matrix of changing environmental 3
on
conditions No
ve
m
PHYSIOLOGICAL ATTRIBUTES ENVIRONMENTAL ATTRIBUTES be
r
Growth rates Energy use Nutrient use Soil nutrient stocks
Efficiency Inorganic N pools Organic N pools Other nutrient pools (esp. K+)
Pools vs. turnover
Soil heterogeneity
Vertical Horizontal Temporal
Cmin Temperature Moisture
Induction Luxury consumption Toxicity pH
Nutrient interactions Light availability/intensity Mycorrhization
Inhibition Synergism Toxicity CO2
INTERACTIONS
Varieties, subspecies Developmental stage

F IG . 3. Physiological and environmental factors influencing N-source preferences (b values) in plants.

(e.g. Fig. 2). In addition, this definition neither considers
Monod-like (or Michaelis – Menten-like) growth and uptake
pat- terns nor allows for luxury or toxic consumption (Fig. 1).
For purposes of ecosystem management and study, it is
worth- while to develop general models that describe and
predict effects of N source on plant populations and their
competitive interac- tions. What must be kept in mind is that
pronounced differences
exist in plant responses to NO2 or NH+, but how3 these 4
translate
into ‘preferences’ depends on many complex, and
interacting, factors. Indeed, a simple assessment of b is not
generally feasible or applicable to realistic models, despite
recent effort to do so (Boudsocq et al., 2012). The numerous
factors, physiological and environmental, that coalesce to
influence N-source preference are outlined in Fig. 3; each has
its own set of complexities and interactions with other factors.
In some cases, such as that of many boreal conifers, a strong
specialization emerges despite myriad complexities (but cf.
Heiskanen, 2005), while in cases like tropical lowland rice
apparent preferences are notsoclear-cut. To conclude, a
quotation from D. Tilman (1985) is instructive: ‘Clearly, the
uniqueness of the species involved in successions in different
areas, the uniqueness of each particular habitat, and various
historical factors all limit the potential predictive ability of any
model of vegetation dynamics and structure’.
ACKNOWLEDGEMENTS
We thank the Natural Sciences and Engineering Council
of Canada (NSERC; grant # 217277-2009) and the Canada
Research Chairs programme (CRC) for supporting this work.
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KARAKTERISTIK KOMUNITAS TUMBUHAN
 Pengaruh Lindi Serasah pada Karakteristik Komunitas Tumbuhan Alpine
Padang rumput di Dataran Tinggi Tibet Qinghai

Perubahan iklim dan penggembalaan yang diluar kendali dapat mengubah struktur
komunitas tumbuhan padang rumput di Dataran Tinggi Qinghai-Tibet (QTP). Perubahan
komposisi ini dapat menghasilkan variasi dalam pergantian sampah, sehingga mengubah
proses ekosistem seperti siklus nutrisi dan tanaman karakteristik tumbuhan, serta sifat
fungsional tanaman.

Model persamaan struktural (SEM) digunakan untuk mengevaluasi hubungan antara

lindi serasah dan tanaman karakteristik komunitas untuk memahami bagaimana lindi akan
mempengaruhi komunitas tanaman padang rumput. Struktural pemodelan persamaan
menunjukkan penambahan lindi serasah komunitas tanaman padang rumput yang terkena
dampak melalui efek yang kuat pada biomassa di atas permukaan tanah, kekayaan spesies
tanaman, dan komunitas keanekaragaman spesies.. Efek negatif langsung yang kuat dari lindi
diatas biomassa tanah mungkin melalui efek dari alelopati. Senyawa sekunder yang berbeda
terkandung dalam lindi serasah bisa menghambat pertumbuhan tanaman.

Studi lain, termasuk penelitian tentang Leymus padang rumput chinensis dan sabana
Kanada, juga porting bahwa peningkatan konsentrasi lindi litter menurun komunitas
tumbuhan. Lebih lanjut, ada kemungkinan konsentrasi yang lebih tinggi lindi lindi
memengaruhi proses siklus karbon dan nitrogen, dekomposisi bahan organik tanah,
nitrifikasi dan mineralisasi), dan aktivitas mikroorganisme tanah menyebabkan penurunan
pada tanaman yang tersedia nutrisi, yang akan berdampak pada pertumbuhan dan
pertumbuhan tanaman berkontribusi pada pengurangan biomassa di atas permukaan tanah.
 Rangeland Ecology & Management 73 (2020) 147e155

Contents lists available at ScienceDirect

Rangeland Ecology & Management

journal homepage: http://www.elsevier.com/locate/rama

Effects of Litter Leachate on Plant Community Characteristics of Alpine

Grassland in Qinghai Tibetan Plateau*
Zhouwen Ma a, Yingxin Wang a, Yongchao Gu a, Saman Bowatte a, Qingping Zhou b,
Fujiang Hou a, *
a
State Key Laboratory of Grassland Agro-ecosystems, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs,
College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, 730020, China
b
Institute of Qinghai-Tibet Plateau, Southwest University for Nationalities, Chengdu, 610041, China

articleinfo
abstract
Article history:
Received 21 January 2019 Plant litter dynamics are sensitive to grassland productivity and the spatial heterogeneity of plant
Received in revised form community. In this study, we investigated the effects of litter leachates on plant community character-
29 September 2019 istics using three plant species that represent different successional stages of alpine grasslands located
Accepted 11 October 2019 on the Qinghai-Tibetan Plateau (QTP). We tested four concentrations of leachates (0, 50, 100, and 200 g L
—1
) from Kobresia setchwanensis, Elymus nutans, and Ligularia virgaurea. The leachates from the three
Key Words: plant species generally responded similarly, but the responses to the varying concentrations were
Alpine meadow significantly different. Addition of litter leachates negatively impacted the aboveground biomass and
community structure species richness. The Shannon-Wiener diversity index was positively correlated with the litter leachate
plant functional group addition. The effects of the litter leachate’s addition on plant functional groups varieddgrasses were
grassland
inhibited, forbs and legumes were promoted, and sedges were not significantly affected. This study
litter leachates
demonstrates that litter leachates are a critical determinant of species diversity, grassland productivity,
species diversity
and community structure in QTP alpine grasslands.
© 2019 The Authors. Published by Elsevier Inc. on behalf of The Society for Range Management. This is an
open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction
Litter plays an important role in plant growth and soil
properties (Chapman and Newman 2010; Bradford et al. 2016;
Climate change and unreasonable grazing can alter grassland
Harrop-Archi- bald et al. 2016). Decomposition of litter can impact
plant community structure in Qinghai-Tibetan Plateau (QTP) (Lu
nutrient cycling (Meier and Bowman 2008), as well as seed
et al. 2016; Dong et al. 2019), resulting in spatially heterogeneous
germination (Zhang et al. 2017) and establishment of seedlings
litter accumulation. These compositional changes can result in
(Yuan et al. 2015). Furthermore, litter contributes to interspecific
variation in litter turnover, thereby altering ecosystem processes
competition of grassland community structure and succession
such as nutrient cycling (Hobbie and Sarah 2015) and plant com-
(Donath and Eckstein 2010; Hobbie and Sarah 2015; Xiao et al. 2015).
munity characteristics, as well as plant functional traits (Makkonen
Litter can also provide favorable sites and energy for the life
et al. 2012; Yuan et al. 2015; Dai et al. 2016). The heterogeneity
activities of microorganisms, soil fauna, and small herbivores. It
introduced by the patchy accumulation of litter can also affect the
also affects the structure and function of grassland ecosystems,
plant community structure (Elgersma et al. 2012; Loydi et al. 2015),
which drives the progressive succession of plant communities (Hou
but the mechanisms driving such impacts in QTP grasslands have
et al. 2004; Bork et al. 2012; Hang 2014; Ma et al. 2017). Although the
rarely been investigated and therefore are poorly understood.
effects of physical changes induced by litter on grassland
communities are well documented, the mechanisms of grassland
community re- sponses to chemical changes are not.
*
This study was supported by the Project of the Second Tibetan Plateau Sci- Plant litter can influence establishment of seedlings and
entific Expedition (2019QZKK0302), the Strategic Priority Research Program of
germination by allelopathy effects of litter leachates (Rice 1979;
Chinese Academy of Sciences (XDA20100102), the National Natural Science Foun-
dation of China (31672472), the program for Changjiang Scholars and Innovative
Samedani et al. 2013; Dai et al. 2016). Allelochemicals can also play a
Research Team in University (IRT_17R50) and the 111 project (B12002). role in regulating ecosystem functions, including herbivory,
* Correspondence: Professor Fujiang Hou, Lanzhou University, Lanzhou, 730000, decomposition, and nutrient mineralization (Hou et al. 2013; Li et
Gansu, China. al. 2014; Malenke et al. 2014). The strength of the allelopathy can be
E-mail address: cyhoufj@lzu.edu.cn (F. Hou).
different between plant species where the chemical properties

https://doi.org/10.1016/j.rama.2019.10.003
1550-7424/© 2019 The Authors. Published by Elsevier Inc. on behalf of The Society for Range Management. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
 Z. Ma et al. / Rangeland Ecology & Management 73 (2020) 147e155
of the litter leachates depend on substances accumulated in plant
organs before senescence and biochemical transformations during
decomposition. Most previous studies have investigated the re-
sponses of individual species to litter leachate addition (Olson and
Wallander 2002; Tian and Hou 2009; Mudr´ak and Frouz
2012; Samedani et al. 2013), but the responses to individual species
may not reflect the combined response of plant communities
composed of various functional groups such as in the natural
grasslands in the QTP. The plant community responses to litter
leachates of grassland species in the QTP have never been
investigated, and such infor- mation is vital for developing the best
management strategies for healthy grasslands in the QTP that are
experiencing constant changes in vegetation composition (Zhou et
al. 2012).
Here we report a 2-yr field experiment conducted in alpine
meadow grassland in the QTP to investigate the impacts of litter
leachates on grassland species composition and functional traits.
We investigated the effects of litter leachates from three
grassland species dominant during early, mid, and late stages of
succession in alpine meadow grasslands of QTP. The litter
leachates were ob- tained from 1) Kobresia setchwanensis, a
perennial sedge belonging to the Cyperaceae family; 2) Elymus
nutans, a perennial grass belonging to the Gramineae family; and
3) Ligularia virgaurea, a perennial noxious forb belonging to the
Asteraceae family. In nat- ural conditions, leachates of litter
consist of materials leached by washings from rainwater falling
through litter or from chemical compounds released during the
decomposition of litter. In our study, we used water extracts of
pulverized dried litter as a means to examine maximum
potential effects of chemical composition of litter leachates. We
hypothesized that litter leachates from plant species
representing three different successional stages would affect the
grassland community composition and functional traits
differently due to the differences in the chemical composition of
the litter for the three species. We also tested the effects of
different concentrations of litter leachate because under natural
conditions, the concentration of litter leachate released to the
soil can vary spatially and temporally. The objective of our
study was to inves- tigate the effects of litter leachates from
three representative plant species of different successional
stages in alpine grasslands in the QTP on aboveground biomass
and plant community diversity.
Materials and Methods
Study Site
This experiment was conducted in 2015 and 2016 at the QTP
Research Base of Southwest Minzu University, located in
Hongyuan (31○47'34”N, 102○33'07”E), on the northeastern
boundary of the QTP in China (3485 m above sea level). The mean
annual temper- ature is 1.4 ○— C, ranging from 9.5○C in January to
○
11 C in July, the temperature varies greatly between day and night,
where average relative — humidity is 60 70%. Mean annual sunshine
duration is 2 159 hours, and mean annual precipitation is 791.95
mmd80% of which occurs from May to September. The study area
belongs to the continental alpine temperate monsoon climate zone.
The soil type is classified as Mat Cry-gelic Cambisols (Chinese Soil
Taxonomy 1995). The annual growth season of the vegetation at the
study site is from April to the end of September (Fig. 1). The return
to the green period is mainly concentrated in April to May,
reaching peak growth in mid August, with vegetation average
coverage of > 80%. The plant community comprises of 53% forbs,
26% grasses, 17% sedges, and 4% legumes. All the grasses, sedges,
and legumes were perennials. Of the forbs present in this study, 5%
were annuals. Dominant grasses included Elymus nutans and Poa
pratensis. Dominant sedges included kobresia setchwanensis and
Kobresia Pygmaea. Dominant perennial forbs included Saussurea
purpurea, Anemone trullifolia, Anaphalis lactea, Potentilla fragarioides,
Aster
14
tartaricus, and Ligularia virgaurea. Legumes included Tibetia hima-
laica and Oxytropis.
Litter Collection and Leachate Preparation
Plant litter of Elymus nutans (En), Kobresia setchwanensis (Ks),
and Ligularia virgaurea (Lv) was collected from the QTP Research
Base of Southwest Minzu University, after the grass withered and
turned yellow in late October of 2014 and 2015. The litter was air
dried at room temperature. The litter was then pulverized into
powder and packed in polyethylene bags and stored 4 mo at room
temperature. Pulverized dry powder (200 g) of three types of litter
was steeped in 1 L of distilled water for 48 h at room temperature
(15○C) and filtered through a double layer of nylon gauze (Yuan
2009). The leachate was then diluted with distilled water to obtain
concentrations of 50, 100, and 200 g L—1. Distilled water was used
as the control (0 g L—1).
Experimental Design
The experimental area at the study site is a moderately
degraded grassland. Since 2014, yak have grazed the site from late
November to February. The randomized complete block design
was used in the experiment. We established a concentration
gradient using litter collected from three different species. Each
plot was 2 ×2 m, arranged in three blocks. The buffer of each plot
was 1 m, and blocks were separated by a 2-m strip. Each treatment
had 3 replications. In early May 2015 and 2016, all aboveground
plant materials were removed from all plots by cutting 2-cm
aboveground herbage and removing litter by hand. We added four
concentrations of leachate (0, 50, 100, and 200 g L—1) of each litter
type by hand sprayer in early May, June, and July in each yr. Each
plot received 4 L of leachate. The volume of leachate application (4
L) was based on an estimation, assuming leachate incorporation of
100 g litter L—1 (Yuan 2009) over 3 mo in a grassland where
average litter accumulation of 300 g m—2 (Yuan et al. 2015) was
occurring. The litter leachate concentration treatments were
adjusted (half and double) by the quantity of litter used to
prepare the leachate, and the volume of leachate application
was kept constant.
Field Sampling and Measurements
In August (peak of growing season) of each yr, plant
community species richness, plant density, plant height, and
aboveground biomass were measured for each species × by
harvesting 0. 5 0.5 m quadrats at 2-cm height above in a randomly
selected area within each plot. Plant community species richness
was estimated by counting the number of all species in the quadrat.
Plant density was estimated by summation of all the number of
individuals in the quadrat. Plant height was measured using ruler
measures for ab- solute height of each plant. The aboveground
biomass was har- vested, separated by species, oven dried at 65○C
for 48 h, and weighed. All plant species were classified according to
life form (annual and perennials) and four plant functional groups
(PFGs) (grasses, sedges, legumes, and forbs).
Data Analysis
Calculation of plant community species diversity was used
for analysis of the ShannoneWiener diversity index (H0 ) and
important value (IV) (Smith and Wilson 1996; Liu and Nie 2012;
Pizzio et al. 2016), with the following equations:
IV ¼ ð rd þ rh þ rb Þ = 3 [1]

P
Statistical summary of the effects (P values) of litter leachate concentrations, litter type, yr, and interactions on aboveground biomass, species diversity, functional groups. Significant effects (P < 0.05) are highlighted in bold. Table 1

Yr ● Litter type

0.629
X
H0 ¼ — Pi ln ðPiÞ [2]

F
Where rd is the relative density, rh is the relative height, and rb is

0.73
Litter type●●Concentration
the relative aboveground biomass. Pi is the proportion of species i
based on percent biomass data.

P
We used structural equation modeling (SEM) to estimate the

0.479
contributions of litter leachate to aboveground biomass and com-

Concentration
munity diversity (Grace 2006). In the model, we assumed that litter
leachate addition had the potential to alter aboveground biomass

F
directly, as well as indirectly changing community diversity. The

0.939
standard path coefficients were estimated to indicate the strengths
of these multiple effects. We used the chi-square test, Akaike in-
formation criteria, and the root mean square error of approxima-

P
tion to evaluate the fit of model. The SEM analyses was performed

0.251
Concentration
using AMOS 17.0 (Amos Development Company, Greene, ME) for
Windows (SPSS Inc., Chicago, IL).
The effects of litter leachate type, leachate concentration, yr,

F
Yr ●

1.424
and their interactions on plant community characteristics were
analyzed using the analysis of variance procedure, and means
were separated by the LSD test at the 5% probability level, using

P
Statis- tical Product and Service Solutions software version 17.0

Yr ● Litter type

0.294
(SPSS Inc., Chicago, IL). Principal component analysis (PCA)
was carried out using the vegan package of R program (R Core
Team 2013) to illustrate the plant community composition

F
variation responses to the leachate addition.

Results 1.263
P
0.253

Litter Leachate Effects on Plant Community Aboveground Biomass

The plant community aboveground biomass response to the

F

addition of litter leachate was similar in both years and for all three
1.347
Yr

litter types (Table 1). In both years, irrespective of litter type, the
aboveground biomass of community, grasses, forbs, perennial, and
annual species significantly decreased with increasing concentra-
P

tion of the added litter leachate (P < 0.0001) (Figs. 2E, 2A, 2D, 2H,
< 0.0001

and 2G) and had no impact on sedges, legumes, and litter (Figs. 2B,
2C, 2F). The aboveground biomasses of the grasses and legumes
Concentration

were significantly lower in 2015 than in 2016, but forbs showed an

opposite trend (Table 1).
F
111.82

Litter Leachate Effects on Plant Species Diversity

P

The response of litter leachate addition on plant species

0.414

richness and Shannon-Weiner index were similar for all three

litter types (Table 1). The plant species richness of total
Litter type

community decreased with increasing concentration of added

F

leachate in 2015 (Fig. 3A), annual species richness was decreased

0.903

in both 2015 and 2016 (Fig. 3B), and had no impact on perennial
species (Fig. 3C). The Shannon-Weiner index was significantly
higher in treatment plots than the control in 2016 (P < 0.05) but
al species aboveground biomass Grasses aboveground biomass

not affected in 2015 (Fig. 3D).

Litter Leachate Effects on Plant Functional Groups

The responses of plant functional groups (PFGs) to the addition

of litter leachates were estimated by the importance value; an in-
dex to indicate relative dominance of a species in a plant commu-
nity. The responses of PFGs to three litter leachate types were
Variable

similar (Table 1). The effects of litter leachates addition on PFGs

varied. Compared with the control, addition of litter leachates
increased the legumes and forbs, decreased grasses, and had no
 Z. Ma et al. / Rangeland Ecology & Management 73 (2020) 147e155
Figure 1. Monthly mean precipitation and temperature from 2014 to 2016 at the study site located in Hongyuan (31 ○47'34”N, 102○ 33'07”E) at the Qinghai Tibetan Plateau, China.
impact on sedges (Fig. 4). These responses were consistent in both
yrs (Table 1). The grasses and forbs composition in the plant
community was significantly lower in 2016 than in 2015 (Table 1),
which may have been due to the lower rainfall during the plant
growing season in 2016 (Fig. 1).
Variation in Plant Community Composition by Litter Leachate
Addition
The first two axes of the PCA accounted for 61.8% of the total
variance, which can reflect the characteristics of community
composition. There was no discernible pattern in the
distribution of litter types in the principal component ordination
space (Fig. 5). Axis 1 accounted for 47.9% of the variance and
illustrated the plant community structure changes with the
decreasing of concentration of litter leachate. No separation of
these groups was evident on axis 2.
Relationships Between Litter Leachate Addition and Plant
Community Characteristics
The structural equation model (SEM) (Fig. 6) was used to
eval- uate casual relationships between the litter leachate and
the plant community characteristics to understand how litter
leachate would affect the grassland plant community. There
were significant direct negative effects of litter leachate on
aboveground biomass, which further indirectly affected plant
species richness and species di- versity estimated by the
Shannon-Weiner index.
Discussion
The results of our study contribute to the numerous previous
research that demonstrates the profound effect litter can have on
grassland productivity (Fig. 2) and botanical composition of
plant community structure (Figs. 4 and 5). More importantly, it
provides new evidence for a potential mechanism driving such
impacts, through litter leachates in an alpine grassland in QTP
(Fig. 6). Contrary to our hypothesis, the responses of leachates
from the tested plant species were generally similar, but the
responses to the concentrations of the litter leachate were
significant. Structural equation modeling (Fig. 6) indicated the
addition of litter leachates affected grassland plant community
through strong effects on aboveground biomass, plant species
richness, and community species diversity. This result is
consistent with Xiong et al.’s (1999) general view, established
from a meta-analysis using the data from 35 studies worldwide,
that plant litter has a significant effect on vegetation. Their meta-
analysis indicated overall litter effects were
15
stronger on species richness than on aboveground biomass. In our
study, which considered litter leachate effects only, the effects on
aboveground biomass were much stronger than the species di-
versity effects (Fig. 6).
The strong direct negative effect of litter leachate on above-
ground biomass (Fig. 2) was possibly through the effects of
allelopathy. The different secondary compounds contained in the
litter leachates could have inhibited plant growth (Ma et al. 2005;
Liu et al. 2017). Other studies, including research on Leymus
chinensis grassland and the Canadian savannah, similarly re-
ported that increasing concentrations of litter leachate decreased
plant community biomass (Wang 2011; Nyanumba and Cahill
2012). Furthermore, it is possible that higher concentrations of
litter leachate impacted carbon and nitrogen cycle processes
(Meier and Bowman 2008), soil organic matter decomposition,
nitrification and mineralization (Zhang et al. 2014), and soil
microorganism activity (Makkonen et al. 2013; Li et al. 2016;
Yahdjian et al. 2017), resulting in a decrease in plant available
nutrients, which would have an effect on plant growth and
contribute to the reduction in aboveground biomass. We found
that increased litter leachate concentration changed the propor-
tion of different plant families, affected vertical (grasses) and
rhizomatous (forbs) plant growth (Fig. 2A and 2D), and may have
increased spatial variation in plant growth, resulting in reduced
aboveground biomass as suggested by Wen et al. (2013). The loss
of dominant PFGs from grassland ecosystems can result in sig-
nificant aboveground biomass reduction as observed by Pan et al.
(2016) in an Inner Mongolian grassland. In our study, increased
inhibition of the grasses (Fig. 4A) indicates that such a mecha-
nism may be involved.
We found that plant species richness, an important indicator of
species diversity and species competitive coexistence (Liu et al.
2016; Tredennick et al. 2017), decreased with increasing concen-
tration of added leachate (Fig. 3A and B); however, the Shannon-
Weiner index estimates indicated that the addition of leachate
significantly increased plant community diversity in 2016 (Fig. 3D).
The Shannon-Weiner diversity index is a measure of the degree of
diversity and heterogeneity at the species level, which compre-
hensively reflects the species richness and evenness of the com-
munity. So, it is somewhat different from the results of species
richness (Chen et al. 2013). Part of this effect may be due to litter
phytotoxins leaching into the soil and impeding seedling recruit-
ment (Vellend et al. 2000; Yu 2012). Alpine plants have low levels of
seedling establishment from seed (Yuan et al. 2015), but most
annual plants (Scrophulariaceae, Gentianaceae, Caryophyllaceae)
and some perennial plants (grasses, Asteraceae ect.) are primarily
established from seed. High concentrations of litter leachate
Figure 2. The response of aboveground biomass to the addition of litter leachates. Different letters for mean values indicate signi ficant difference among litter leachate treatments
at P < 0.05 level.
Figure 3. The response of litter leachate addition on plant species diversity. Different letters for mean values indicate signi ficant difference among litter leachate treatments at
P < 0.05 level in the same year.

consequently inhibited the annual plant seed germination, thus

impacted differently by litter leachate type and concentration. For
reducing annual plant species richness. Perennials can be multi-
example, similar to our study, sedges did not respond to litter in
plied by other means (Zhao et al. 2006), so there was less of an
Wang et al’s (2010) study and speculated the neutral responses to
impact on the species richness of perennials. However, this possi-
litter was due to crowd-short rhizomatous growth form and
bility should be considered cautiously as we do not have long-term
inherent developmental constraints. In comparison, the positive
data on annual and perennial plant recruitment and seedling
response of forbs to the leachate addition was due to the
establishment within these plots. High-concentration litter
competitive advantage of negative response by grasses (Chamane
leachate weakened the relative importance of the dominant species
et al 2017). The positive responses by forbs to leachate is impor- tant
such as grasses (Fig. 4A) and indirectly enhanced the relative
for vegetation dynamics, especially in grasslands like our
importance and development of other species such as legumes and
experimental site in which forbs contribute to 53% of the plant
forbs (Fig. 4C and 4D) in the community, which is an important
community. Forbs contribute to much of the plant diversity in
cause of the increase in plant diversity. Zhang et al. (2015) sug-
grasslands, enrich the seed bank (Laforgia et al. 2018), and often
gested that allelopathy may be an important mechanism of plant
show considerable trait plasticity in response to changes in spe-
dominance that allows certain plants to modify community di-
cies richness and composition (Lipowsky et al. 2015). Therefore,
versity by affecting the seedling establishment of co-occurring
forbs are important for both convergence and divergence between
species. In addition, litter leachate can affect plant community
species for specific traits (Mitchell et al. 2016). Chemical, physical,
indirectly through their effects on soil fauna that are known to
and biological feedback from litter varies with functional groups
affect the composition of natural vegetation strongly (De Deyn et
(Ma et al. 2017), and so litter can regulate the structure and function
al. 2003).
(Fig. 5) of grassland ecosystem in many ways. Litter of Ligularia
Different PFGs’ important values were inhibited, promoted, or
virgaurea has been previously shown to affect the composition of
unaffected by litter leachate (Table 1, Fig. 4). Grasses were inhibited
plant communities (Shi et al. 2011; Xie et al. 2014). However, its
by the addition of litter leachate (Fig. 4A), while legumes and forbs
effect is concerning, as it is a noxious weed that in- dicates severe
were promoted by leachate addition (Fig. 4C and D). The sedges
degradation of grasslands. In other studies, invasive plant species
were not significantly affected by litter leachate addition (Fig. 4B).
have increased their impact on the existing plant community
Part of this impact may be through different species of functional
through the litter they produce, as in the case of sage brush-steppe
groups having different requirements for seedling emergence and
plant communities being altered by the invasion of annual grasses
survival (Yuan 2009; Rayamajhi et al. 2012). In addition, growth
(Bansal et al. 2014). This impact can be through general impacts on
mechanisms may play a role, with the varying growth mechanisms
soil nutrient cycling, as well as production of alleochemicals.
of different genera and plants being
Figure 4. The responses of plant functional groups (PFGs) to the addition of litter leachates. Different letters for mean values indicate signi ficant difference among litter leachate
treatments at P < 0.05 level.

The SEM (Fig. 6) demonstrated that leachate-driven changes

importance of grazing-induced plant composition changes on litter
to forbs and grass biomass influenced plant community
chemistry was also highlighted by Campanella and Bisigato (2010).
diversity. Such PFGs or plant species changes can add further
Our study showed such litter quality impacts are possibly through
feedbacks to the plant community in future years through
litter leachates. Li et al. (2015) reported that in a desert step
variable levels of litter accumulation, spatially and in time (Li
grassland the green-up dates can be advanced up to 7 d when litter
2014). Plant species provide a strong source of variation in
accumulation reaches 300 — 400 g m—2, benefiting healthy grass-
standing litter mass and litter chemistry (Ren et al. 2014,) and
land systems by maintaining community stability. Identifying such
any factors that affect plant com- munity composition (Fig. 5)
critical levels for litter leachate accumulation under varying
would therefore influence litter mass accumulation and hence
grazing management regimes would be beneficial for developing
litter leachate dynamics. It is well recog- nized that grazing
best practices for sustainable grassland management. In the QTP,
regimes and environmental factors can sub- stantially influence
climate change and intensive animal grazing has been attributed to
the plant community composition (Garibaldi et al. 2007; Shen et
plant community changes and grassland degradation (Hautier et al.
al. 2016). Semmartin et al. (2004) showed ev- idence that grazing,
2015). Therefore, future studies are warranted for the environ-
rainfall, and their interactions induced plant community
mental and grazing effects of litter leachate feedbacks and their
changes and altered litter quality, causing major changes in
impact on plant community changes.
ecosystem functions such as in nutrient cycling. The

Figure 5. Principal component analysis illustrating the variation in plant community composition by litter leachate addition.
Figure 6. A structural equation model of treatment effects on above-ground biomass and community diversity. The structural equation model considered all plausible pathways
through which experimental treatments influence community aboveground biomass and diversity. Solid and dashed line arrows represent significant and nonsignificant pathways,
respectively. Numbers indicate the standard path coefficients. Arrow width is proportional to the strength of the relationship. R2 represents the proportion of variance explained
for
each dependent variable in the model. *P < 0.05, **P < 0.01, ***P < 0.001; (a)c2 ¼ 1.241, df ¼ 2, P ¼ 0.538; root mean square error of approximation (RMSEA) ¼ 0.000.
In summary, we found litter leachate additions to a native
mixed-grass alpine grassland community generated a strong
response to the aboveground biomass and plant community di-
versity, highlighting the importance of litter leachate in maintain-
ing grassland community structure and ecosystem functions.
Implications
An important implication of our study is improved under-
standing of the link between litter feedbacks on plant community
composition through litter leachates. Such understanding is
important for the management of natural grasslands. We found
that at higher leachate concentrations, there were significant
changes in herbage biomass, species richness, and composition of
PFGs, indicating potential impacts on grassland community sta-
bility. These feedbacks can also have broader implications on
spatial variability, biodiversity, and ecosystem processes. Our re-
sults also indicate that litter dynamics may have the potential to
shift vegetation succession of the plant community, as species
availability, species functional characteristics, and site availability
are three primary causes of succession (Krueger-Mangold et al.
2006), and litter leachate can have an impact on all three of these.
In our study, the impact of leachate concentration was much
stronger than the litter identity. As litter mass is one of the key
factors that would influence leachate concentration, standing total
litter mass can be considered as a critical factor influencing litter
leachate feedback effects on grassland community. In addition,
environmental factors such as temperature, rainfall, and snow
melting can also be important for the concentration of litter
leachates.
Our approach and findings pave way for wider empirical eval-
uation of spatial heterogeneity in a range of systems, highlighting
feedback links between plant spatial heterogeneity and litter dy-
namics. This study reports only a short-term response of litter
leachate addition to enclosed grassland during two plant growing
seasons. Future studies should explore long-term effects of litter
leachates on animal-grazed grasslands.
Acknowledgments
The authors are grateful to the Qinghai-Tibet Plateau Research
Base of Southwest Minzu University for supporting the field work.
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SUKSESI TUMBUHAN
 Gangguan dan Suksesi Tanaman di Gurun Mojave dan Sonoran di Amerika Barat Daya
Gangguan seperti kebakaran, pembukaan lahan, dan pembangunan jalan menghilangkan vegetasi
dan dapat memiliki pengaruh besar pada kesehatan masyarakat melalui efek pada kualitas udara,
estetika, peluang rekreasi, ketersediaan sumber daya alam, dan ekonomi. Pemulihan tanaman dan
suksesi setelah gangguan tidak dipahami dengan baik di lahan kering relatif terhadap daerah yang
lebih beriklim sedang. Studi ini secara kuantitatif meninjau pembangunan kembali vegetasi setelah
berbagai gangguan di Gurun Mojave dan Sonoran di barat daya Amerika Utara.

spesies pra-gangguan adalah penjajah awal dari daerah yang terganggu di Gurun Sonoran, dan
bahwa suksesi sejati tidak ada karena penjajah awal tidak mengubah lingkungan untuk memfasilitasi
penjajahan oleh spesies selanjutnya. Sebaliknya, pada tahun 1961 Wells meneliti sebuah kota hantu
berusia 33 tahun di Gurun Mojave Nevada dan mengamati bahwa spesies perintis (berbeda dari
vegetasi yang tidak terganggu di sekitarnya) telah menjajah situs tersebut dan Suksesi telah terjadi,
meskipun tidak cukup waktu telah berlalu untuk menentukan apakah komunitas yang utuh dan
tidak terganggu akan terbentuk.

Demikian pula, pada tahun 1979, Vasek menduga bahwa suksesi terjadi pada area lubang
pinjaman tepi jalan yang telah dibersihkan di Gurun Mojave California, klaim yang disengketakan
oleh Rowlands pada tahun 1980 , yang percaya bahwa data dari satu situs (yang mungkin berbeda
dalam sifat tanah, pola vegetasi yang membingungkan) tidak menunjukkan suksesi. Webb et al
mencatat bahwa beberapa kebingungan tentang suksesi lahan kering dihasilkan dari definisi yang
tidak jelas tentang suksesi dan pemulihan, data lapangan yang terbatas, ketidakpastian dalam
menerapkan konsep-konsep suksesi gurun dari daerah-daerah lembam di mana suksesi lebih
dipahami, dan laju perubahan lambat dalam tanaman tahunan komunitas di gurun. Skala yang lebih
lambat ini menyulitkan para peneliti untuk mempelajari perubahan dalam gurun pada siklus
pendanaan penelitian singkat yang khas dan menimbulkan tantangan logistik untuk menemukan
situs yang memiliki waktu yang cukup untuk benar- benar mencatat suksesi . Baru-baru ini,
berbagai penelitian di gurun Amerika Barat Daya telah memeriksa pembentukan tanaman setelah
gangguan tetapi literatur ini terpecah-pecah dan mungkin mendapat manfaat dari sintesis yang
mengevaluasi bukti untuk terjadinya konsep dan pola umum
Int. J. Environ. Res. Public Health 2010, 1249
7
OPEN ACCESS

International Journal of
Environmental Research and
Public Health
ISSN 1660-4601
www.mdpi.com/journal/ijerph
Review
Disturbance and
Plant Succession
in the Mojave and
Sonoran Deserts
of the American
Southwest
Scott R. Abella

School of Environmental and Public

Affairs, University of Nevada Las
Vegas, Las Vegas, NV 89154- 4030,
USA; E-Mail: scott.abella@unlv.edu;
Tel.: +1-702-895-5163; Fax: +1-702-
895-4436

Received: 22 December 2009; in

revised form: 23 March 2010 /
Accepted: 24 March 2010 /
Published: 25 March 2010

Abstract:
Disturbances such as
fire, land clearing, and
road building remove
vegetation and can
have major influences
on public health
through effects on air
quality, aesthetics,
recreational
opportunities, natural
resource availability,
and economics. Plant
recovery and
succession following
Int. J. Environ. Res. Public Health 2010, 1249
7
d nds relative to more
i temperate regions.
s This study
t quantitatively
u reviewed vegetation
r reestablishment
b following a variety of
a disturbances in the
n Mojave and Sonoran
c Deserts of
e southwestern North
America. A total of 47
a studies met inclusion
r criteria for the review.
e The time estimated by
29 individual studies
p for full
o reestablishment of
o total perennial plant
r cover was 76 years.
l Although long, this
y time was shorter than
an estimated 215 years
u (among 31 individual
n studies) required for
d the recovery of species
e composition typical of
r undisturbed areas,
s assuming that recovery
t remains linear
o following the longest
o time since disturbance
d measurement made by
the studies.
i
n Keywords: arid land;
recovery; revegetation;
fire; management;
a
resource damage; dust
r
mitigation; diversity
i

l 1. Introduction
a
Int. J. Environ. Res. Public Health 2010, 1249
7
H hot deserts of the American
u Southwest since the mid-1800s
m (Figure 1). Some of these
a disturbances have facilitated, or
n attempted to facilitate,
s widespread public benefits, but
h not without environmental costs.
a Mining, for example, has
v
e
b
e
e
n
e
xt
e
n
si
v
el
y
di
st
u
r
bi
n
g
th
e
e
n
vi
r
o
n
m
e
nt
o
f
th
e
exported natural resources from the region since the 1800s and remains prevalent today, producing
materials such as gypsum, cinders, gold, and copper used for a variety of societal products [1]. Water
and energy transmission corridors carry resources within and through the region, yet result in long,
linear areas of cleared disturbed land [2]. Dry-land agriculture provided brief booms to local
settlements in the early and mid-1900s, and while agriculture continues on a limited basis today,
abandoned fields have left a legacy of de-vegetated lands [3,4]. Road building has enabled access to
large tracts of public land for recreational use. However, proliferation of roads and unauthorized off-
road vehicle use has left persistent scars in the desert [5]. For example, in their analysis of the road
network in the 6,475-km2 Mojave National Preserve in southern California, Vogel and Hughson [6]
found that roads proliferated from 605 km in total length in 1885 to 3,701 km in 1994. The US military
extensively used the deserts for World War II training operations, and its largest training facilities still
reside in southwestern deserts [7,8]. Intensive clearing of the desert also has occurred for human
settlements, some of which were abandoned in the early 1900s (often following brief mining booms) to
become ghost towns with dirt street systems still clearly visible [9]. Today, two of the largest cities in
the USA (Las Vegas, Nevada, metropolitan area with 1.9 million people, and Phoenix, Arizona, with
4.3 million people) are located in southwestern deserts.
There are environmental and public health costs associated with some of the benefits of these
disturbances, however. The disturbances remove plant cover, which can negatively impact wildlife
species, such as desert tortoise (Gopherus agassizii) listed under the USA Endangered Species
Act [10]. De-vegetated areas can incur severe soil wind erosion, releasing fugitive dust as air pollution
that can be a serious public health hazard. Grantz et al. [11] found that air quality standards for
particulate matter, which causes respiratory problems in humans, were breached for 11−25 days/year
downwind of abandoned agricultural land in the western Mojave Desert of California. Blowing sand
also disrupted airport operations and resulted in hazardous driving conditions. These immediate effects
on public health are in addition to longer term effects associated with soil loss, including reduced
potential for agriculture, carbon sequestration, and other land uses.
Fires, not considered common historically in southwestern deserts but increasing in extent in recent
decades partly because of fuel provided by non-native annual grasses (e.g., red brome [Bromus rubens]
and buffelgrass [Pennisetum ciliare]), are having significant economic and environmental
impacts [12]. Fire has killed the charismatic Joshua tree (Yucca brevifolia) in areas of Joshua Tree
National Park in California and the renowned giant saguaro cactus (Carnegiea gigantea) in Saguaro
National Park in Arizona [13,14]. Joshua tree and saguaro are not considered well adapted to fire
(which was not part of their evolutionary environment), as fire readily kills them and they rarely
resprout [15]. These species often require protection (e.g., shading) by existing vegetation (―nurse
plants‖) from the harsh desert environment for reproduction, so regeneration of new individuals is slow
because the nurse plants must first become established after fire [13]. Areas containing these species
are national and international tourist destinations. From an economic standpoint, the tourism industry
(e.g., resorts, golf courses, businesses dependent on visitation to area parks) is concerned about having
scenery and tourist attractions disrupted [14]. Furthermore, fires have threatened human habitations
and cost millions of dollars to suppress, such as the 100,000 ha Cave Creek Fire in 2005 near Phoenix,
Arizona, in the Sonoran Desert [16].
Int. J. Environ. Res. Public Health 2010, 1251
7
Figure 1. (a) View of part of the ghost town of Rhyolite, Nevada, in the Mojave Desert,
showing distinct bands of recovering disturbed plant communities (foreground), relatively
undisturbed creosote bush communities (center band of darker vegetation), and a de-
vegetated band disturbed by mining in the middle-top of the photograph. (b) The 2005
Tramp Fire in the eastern Mojave Desert showing clearly demarcated burned habitat (right)
and unburned Joshua tree woodland (left). (c) With its light color in the middle-top of the
photo, the 2005 Loop Fire west of Las Vegas, Nevada, in the Mojave Desert illustrates the
landscape-scale scars created by disturbance in the desert. (d) Example of undisturbed
desert habitat containing the columnar cactus giant saguaro in the Sonoran Desert uplands
of Saguaro National Park, Arizona. Photos by S.R. Abella in 2006 (a), 2007 (c), and 2008
(d), and by E.C. Engel in 2008 (b).
 Most disturbed areas in the desert are simply left to natural recovery processes, rather than being
revegetated through active management treatments such as seeding, planting, or soil manipulation [17].
Active revegetation has shown some success in southwestern deserts for enhancing and accelerating
recovery [3]. However, revegetation has generally been confined to small areas because of its expense,
logistical challenges associated with implementing treatments across vast desert regions, and
unpredictable weather that makes effectiveness uncertain [18]. Understanding natural vegetation
reestablishment after disturbance is important for several reasons. First, determining whether natural
reestablishment will meet environmental management objectives (e.g., for minimizing dust pollution,
promoting wildlife habitat or aesthetics) can assist decision-making on whether attempting active
revegetation is desired or worth the expense. Second, understanding natural recovery could help inform
how to make active revegetation more effective by mimicking natural processes. Third, knowledge of
recovery can allow estimates of how long original plant communities may take to reestablish, such as
Joshua tree and saguaro communities, or even if they will fully recover since present climates may
differ from the past evolutionary environments of the species. This type of information can inform
management decisions such as where to attempt the most aggressive fire suppression to protect
resources from disturbance in the first place to avoid long recovery times.
There is a body of theory on succession in ecological and environmental science that may help
provide a framework for understanding changes induced by disturbance in desert ecosystems. The
process of biological communities becoming established following disturbance is termed succession by
ecologists and is differentiated into primary and secondary succession [19]. Primary succession occurs
on newly created geomorphic surfaces (e.g., volcanic islands surfacing in oceans, or debris flows
forming alluvial fans in deserts) not previously containing vegetation. Secondary succession occurs in
areas that were vegetated prior to a disturbance. Disturbance is defined as a physical force (e.g.,
hurricane, fire, road building) that removes most or all of plant biomass. Ecologists have had various
interpretations of the definitions of succession, ranging simply from changes in biological communities
over time, to directional changes where communities pass through relatively distinct post-disturbance
seral stages that culminate in the reestablishment of the pre-disturbance community [5,20]. In this
paper, post-disturbance recovery is defined as the return of any variable (e.g., plant cover, or the
number of species termed species richness within a defined area) to those of nearby levels found on
undisturbed areas. Succession is considered to have occurred if there is at least one intermediary
community that becomes established after disturbance followed by reestablishment of communities
resembling adjacent undisturbed areas.
Succession in arid lands has long puzzled ecologists and environmental managers. For example, in
1940, Muller [21] concluded that no succession occurred in creosote bush (Larrea tridentata)
Chihuahuan Desert shrub communities of western Texas following soil disturbance because the early
colonizers had been components of the previous late-successional community occupying the site. In
1942, Shreve [22] also concluded that pre-disturbance species were the initial colonizers of disturbed
areas in the Sonoran Desert, and that true succession was absent because the early colonizers did not
alter the environment to facilitate colonization by later species. In contrast, in 1961 Wells [23]
examined a 33-year-old ghost town in the Mojave Desert of Nevada and observed that pioneer species
(different from the surrounding undisturbed vegetation) had colonized the site and succession had
occurred, though insufficient time had elapsed to determine if the full undisturbed community would
become established. Similarly, in 1979, Vasek [24] surmised that succession occurred on a cleared
roadside borrow pit area in California’s Mojave Desert, a claim disputed by Rowlands in 1980 [5],
who believed that data from a single site (which may have differed in soil properties, confounding
vegetation patterns) did not demonstrate succession. Webb et al. [20] noted that some of the confusion
about arid land succession resulted from unclear definitions of succession and recovery, limited field
data, uncertainty in applying to deserts successional concepts from moister regions where succession is
better understood, and the slow rates of change in perennial plant communities in deserts. This slower
scale makes it difficult for researchers to study changes in deserts on the typical short research funding
cycles and poses logistical challenges for finding sites that have had sufficient time to actually record a
succession [25,26]. More recently, a variety of studies in American Southwest deserts have examined
plant establishment after disturbances (e.g., [27-29]), but this literature is fragmented and may benefit
from a synthesis evaluating evidence for the occurrence of general concepts and patterns.
Several concepts have been advanced in the literature about succession in deserts. Disturbance type
has been theorized to influence succession, where the most severe disturbances (e.g., those that remove
surface soil layers such as clearing by bulldozers), or those that heavily compact soils, retard
succession and recovery [30]. Plant community type (e.g., creosote bush versus blackbrush [Coleogyne
ramosissima] communities) also is suggested to affect succession, with some community types
recovering more quickly than others after disturbance [31]. Webb et al. [20] noted that the age of the
previous community (such as those established by primary succession then being disturbed to invoke
secondary succession) can influence succession, generally with the older the community, the longer the
recovery time. Vasek [32] concluded that unlike in temperate regions where annual plants often
comprise the initial seres after disturbance, annuals occur throughout succession in deserts because
annuals are prominent components of mature communities. Several authors noted that early
successional perennial plants usually have short life spans and often inhabit washes, which are
disturbed naturally by periodic floods [23,24,33]. Some have hypothesized that if disturbed, the oldest
communities may not actually recover and succession will proceed to alternative stable states [20]. The
reasoning is that climate and other conditions (e.g., invasion of exotic species, anthropogenic N
deposition) have changed since the communities developed, so another stable community will become
established instead of the original community. Synthesizing data from a variety of studies may provide
insight into how general these suppositions may be in a variety of environmental settings.
The purpose of this study was to synthesize the status of knowledge of disturbance effects on
vegetation and post-disturbance recovery and succession in the Mojave and Sonoran Deserts of the
American Southwest. A systematic, quantitative review approach was employed. Specific questions
examined included:
(1) What is the relationship of plant community cover, species richness, and species composition
with time since disturbance (TSD), and do these measures change at different rates?
(2) Are there differences in successional pattern between primary and secondary succession and
among disturbance and community types in secondary succession?
(3) Which species are dominant early successional colonizers?
(4) Do successional patterns differ between annual and perennial species?
Int. J. Environ. Res. Public Health 2010, 1253
7
(5) Is there evidence supporting generalizations proposed in the literature about arid land
succession, such as successional sequences being similar to more temperate regions but requiring
longer time periods to develop?

2. Methods

2.1. Study Area

The Mojave Desert, approximately 124,000 km2 in size [34], occupies parts of California, Nevada,
Utah, and Arizona in the southwestern USA (Figure 2). About 310,000 km 2 in size, the Sonoran Desert
is in parts of California and Arizona, USA, and Sonora and Baja California, Mexico [35]. The two
deserts share a boundary at the southeastern part of the Mojave and the northwestern part of the
Sonoran. Both are classified as warm deserts, although the Mojave has cooler winter temperatures
while the Sonoran has more of a subtropical climate [36]. Much precipitation occurs in winter in the
Mojave Desert, whereas precipitation is more bimodal (summer and winter) or evenly distributed
throughout the year in the Sonoran Desert. An example weather station (Las Vegas, Nevada, USA, 662
m elevation) in the eastern Mojave Desert has reported averages of 11 cm/yr of precipitation, July daily
maximum temperature of 40 oC, and January daily minimum temperature of 1 oC (1937–2008
records; [37]). At Ajo, Arizona, at a comparable weather station (elevation 549 m) in the north-central
Sonoran Desert, averages of 21 cm/yr of precipitation, 39 oC July daily maximum, and 5oC January
daily minimum have been recorded from 1914−2008. Precipitation can vary substantially among years
in these deserts, resulting in some years having large blooms of annual plants and other years with few
annuals [38].
Topography of the deserts is diverse, including mountain ranges, dry lakes (playas), relatively flat
plains, bajadas (alluvial fans or debris flows), washes that are intermittent stream drainages, and
various volcanic landforms [39]. Major soil orders, following the US classification system, include
Aridisols and Entisols [40]. These different environmental complexes support different plant
communities. Some characteristic species that differ between the deserts include the Joshua tree
inhabiting the Mojave Desert and the columnar cactus giant saguaro of the Sonoran Desert
uplands [39]. Creosote bush shrublands occupy vast areas of plains in both deserts at the lower
elevations. The typical vegetation appearance of the deserts is scattered perennial shrubs, cacti, forbs,
and grasses, separated by interspaces that consist of sparsely vegetated soil or annual plants during
moist years [36]. Perennial shrubs form ―fertile islands,‖ which are microsites containing fertile soils
and ameliorated microclimates [41]. These fertile islands often contain the greatest overall
concentrations of annual plants, although some annual species are most abundant in interspaces.
Livestock grazing (primarily cattle and sheep) was common in the region in the late 1800s to the past
several decades [1]. Localized livestock grazing still occurs, as does plant consumption by wild burros
(Equus asinus) and horses, (neither considered native) and native herbivores such as bighorn sheep
(Ovis canadensis) and black-tailed jackrabbit (Lepus californicus).
 Figure 2. Location of 47 studies meeting selection criteria for a quantitative analysis of
plant recovery and succession in the Mojave and Sonoran Deserts of the American
Southwest. Studies are distinguished by disturbance type (fire or land-clearing disturbances
such as roads) and are numbered according to the Appendix and References Section.

2.2. Literature Search

The article databases of Academic Search Premier (coverage 1975–present), Agricola (1400s–
present), Biological Abstracts (1969–present), JSTOR (individual journals since their inception up to
2005–2006), ScienceDirect (variable years), and Google Scholar (http://scholar.google.com/; all
years) were searched in June 2009 using combinations of the following search words: Mojave,
Sonoran, disturbance, succession, recovery, revegetation, and change. Article titles, key words, and
abstracts were scanned for these search words. Reference lists within located papers also were searched
for relevant citations, and a cross-reference search was conducted using Google Scholar to identify
articles that cited located papers. To qualify for inclusion in the quantitative analysis, articles had to
have: (1) reported on studies conducted in the Mojave or Sonoran Deserts, (2) examined plant
establishment following a discrete disturbance of known age that removed plant biomass in the case of
secondary succession or created a new geomorphic surface in primary succession, and (3) provided
quantitative data (e.g., plant density, cover) for both disturbed areas and undisturbed controls. The
second criterion excluded grazing, because grazing is a diffuse disturbance not linked to a specific date
as currently practiced with burro, horses, or livestock in this region [79].

2.3. Data Preparation

Quantitative data from articles meeting the inclusion criteria outlined in Section 2.2 were entered
into a database. Studies used several different measures for quantifying plant community
characteristics. Frequency is the proportion of sampling units occupied by a species, with sampling
units commonly ranging between 1 m 2 and 0.1 ha in size. Cover is often defined as the percent of
ground area occupied by vegetation, usually allowing overlap of different species to be counted
separately, such as if small plants are growing below larger plants. Density is the number of plant
individuals per unit area, which I standardized for analysis to be on a per hectare basis.
There were two general types of studies in terms of the data they provided. Some studies provided
only a total community measure (e.g., total plant cover, not broken down by species), and others
provided community data by species, which also results in providing the total community measures.
Studies that provided data by species supported analyses of the effects of disturbance on species
composition (the species present and their relative abundance). After updating species nomenclature to
the PLANTS Database [80], I calculated a relative measure of abundance from the data for each
species in each sampling unit of these studies. Studies often reported more than one community
measure (e.g., cover, density) and I used cover whenever available to calculate relative abundance. I
chose cover because most studies (68%) reported cover and cover is important for ecosystem functions
such as sheathing soil to limit wind erosion [11]. When cover was not available, I used whatever
measure the authors provided. I computed the relative abundance measure as the proportion of the total
abundance of all species provided by a given species, converted to a percentage summing to 100% on a
sampling unit basis. For example, if total community cover was 20% and species A had a cover of 2%,
the relative cover of species A is 10%. This relativization procedure allows species composition to be
isolated from total community abundance [81], a standardization especially useful in this analysis
because studies used different measures of abundance and even the same measure (e.g., frequency with
different sampling unit sizes) could be measured differently by different investigators. I calculated the
relative measure separately for annual and perennial plant groups, as classified by the PLANTS
Database [80]. Any species with potential to be longer lived than annual was classified into the
perennial group (some species can function as annual-perennial depending on weather conditions).
 Some studies had specific nuances to their data which I dealt with prior to analysis.
Callison et al. [51] provided cover of a grass that was seeded on the disturbance, and I did not include
the species in this analysis. Webb et al. [20] combined several perennial grasses difficult to identify to
species into a ―grass‖ category, which I included in analyses of total community cover but deleted
from analyses of species composition. Also for Webb et al. [20], different sampling units were used to
measure cover and density by species, and so in using cover in this analysis, I added a nominal 0.01%
raw cover to species occurring in the density (but not cover) sampling units to capture site-level
species composition. I averaged data from multiple sites of the same TSD in Minnich’s [55] study. To
save journal space, some studies (fewer than 15%) grouped the least abundant species into an
―other species‖ category. I did not use these studies in the analysis of species richness, but I retained
them in analyses of species composition because the ―other‖ category typically comprised less
than 5% of relative abundance.

2.4. Data Analysis

Addressing the study questions required using different subsets of studies and parts of the data set
suitable for each question. To assess relationships of plant cover and richness with TSD, I expressed
measures for disturbed areas as a percentage of undisturbed controls for each study. I then used linear
regression to relate the relativized measures to TSD since linear equations typically provided as high or
higher r2 values as non-linear equations. For species composition, I related the Sørensen community
similarity index, calculated in PC-ORD software [82] as the average percent similarity of disturbed to
undisturbed areas in each study, to TSD. I calculated these regressions both within studies that
examined multiple TSDs (either through chronosequence or permanent plot sampling) and among
studies that reported on only one TSD. Chronosequences are space for time substitutions, where
different aged disturbances are sampled. With permanent plots, the same disturbance is measured
repeatedly through time. To compare species composition among studies, I averaged post-disturbance
species composition on a study basis and used non-metric multidimensional scaling (NMS; autopilot
thorough setting) ordination in PC-ORD [82]. To compare individual species, I calculated a mean
disturbed:undisturbed ratio (based on relative abundance). I also used two- (disturbed and undisturbed,
not differentiated by desert) and four-category (disturbed Mojave, undisturbed Mojave, disturbed
Sonoran, undisturbed Sonoran) indicator species analysis with the relative abundance of species as the
data. Indicator species analysis combines the relative abundance and frequency of a species within a
group to produce an indicator value that ranges from zero (no fidelity to a group) to 100 (maximum
fidelity [83]). Species with indicator values ≥ 50 are considered strong indicator species [81]. For
species with values ≥ 50, significance of indicator values at P < 0.05 was assessed using a Monte Carlo
test with 1,000 permutations.
3. Results

3.1. Literature Description

The systematic search procedure uncovered 43 studies of secondary succession that met inclusion
criteria for the quantitative review (Appendix). Publication dates ranged from 1961 to the present. The
Mojave Desert housed 74% of the studies and the Sonoran Desert 26%. Fire was the disturbance type
examined in 31% of the Mojave studies and 64% of the Sonoran studies, with other disturbances
studied including transmission lines (powerline, natural gas), abandoned roads and agricultural fields,
and other cleared areas such as ghost towns and military sites. Data on both annual and perennial
plants were reported in 33% of the studies, annuals only in 5%, and perennials only in 63%. Recovery
patterns with TSD, where three or more TSD repeated measurements were included, were assessed in
33% of the studies for at least one recovery measure, using chronosequence or permanent plot
sampling methods. Results for perennial plants for secondary succession are presented first, followed
by annual plants and then for four studies of primary succession.

3.2. Time since Disturbance Relationships

In analyzing the reestablishment of perennial plant cover irrespective of the species providing the
cover, cover exhibited correlations (r2) between 0.07 and 0.99 (mean = 0.60 ± 0.32 standard deviation)
with TSD among studies, with 8 of 12 studies (67%) having correlations > 0.50 (Table 1, Figure 3).
Estimates of reestablishment of cover on disturbed areas to 100% of the cover on undisturbed areas
ranged from one study that found divergence with time (Hessing and Johnson [70]) to 334 years
(Scoles-Sciulla and DeFalco [66]). Excepting Hessing and Johnson [70], 6 of the 11 studies (55%) had
estimated reestablishment times of ≤ 41 years, and nine of 11 (82%) had estimates of ≤ 88 years
(mean = 70 ± 92 years). In comparing disturbance types (fire versus land clearing), TSD correlations
were generally higher for fire studies: 6 of 7 (86%) fire studies had r2 values > 0.66, while 0.66 was the
maximum value of the five studies examining clearing disturbances. The maximum estimate for
reestablishment of total cover after fire was 65 years, whereas in three of five non-fire studies recovery
times exceeded 88 years. In those two remaining studies, however, cover reestablished rapidly within
five years (Johnson et al. [65]) or exhibited fast initial recovery followed by divergence from levels
found on undisturbed areas (Hessing and Johnson [67]). Data combined from 29 studies (seven of
which examined fires) that each measured only one particular year after disturbance revealed an r2 of
0.46 with TSD and a recovery time within the range of individual studies making repeated temporal
measurements after disturbance.
Species richness exhibited a different pattern with TSD than cover (Table 2, Figure 3). Richness
showed weak relationships with TSD, with 8 of 10 studies displaying r 2 values < 0.22. Those eight
studies also had y intercepts equaling ≥ 64% recovery, indicating that substantial recovery had already
occurred by the initial TSD measurements made by studies. These findings were supported using
combined data from 30 studies (6 fire, 24 other), each with one temporal measurement, where the r 2
was only 0.01 and the y intercept was within 8% of full recovery.
 Table 1. Relationship of time since disturbance (TSD) and perennial plant cover in the
Mojave and Sonoran Deserts of the American Southwest.
Sampling No. Cover2 = mTSD + b Yrs.
To
Reference Disturbance type TSD (yr) Method1 yrs.1 m b r 100%3
Johnson et al. [68] Powerline corridor 1–6 PP 6 16.294 20.5 0.42 5
Hessing and Johnson [70] Powerline corridor 1–5 PP 5 −7.372 88.1 –0.81 ––
Callison et al. [51] Fire 1–37 CS 7 2.256 13.9 0.82 38
Medica et al. [53] Fire 2–8 PP 3 4.522 –7.0 0.95 24
Minnich [55] Fire 1–47 CS 9 1.854 44.5 0.82 30
Bolling and Walker [27] Abandoned road 5–88 CS 7 0.457 33.4 0.49 146
Brooks and Matchett [61] Fire 6–14 CS 3 1.630 33.5 0.26 41
Webb and Thomas [62] Ghost town 19–92 CS 24 1.130 0.0 0.66 88
Webb et al. [63] Fire 4–41 PP 3 1.416 7.9 0.99 65
Alford et al. [29] Fire 5–21 CS 4 2.635 21.9 0.99 30
Scoles-Sciulla and DeFalco [66] Abandoned road 1–7 CS 4 0.299 0.0 0.73 335
Vamstad and Rotenberry [67] Fire 2–65 CS 6 1.589 38.1 0.96 39
29 studies, 1 year of data each Fire, other 1–74 –– –– 0.801 39.0 0.68 76
1
CS = chronosequence, PP = permanent plot. No. yrs. represents how many different years were
represented by the sampling.
2
Cover is expressed as a percentage of undisturbed areas.
3
Years required for cover to reach 100% of the cover on undisturbed areas, as estimated by the
regression equation.

Table 2. Relationship of time since disturbance (TSD) and perennial plant species richness
in the Mojave and Sonoran Deserts of the American Southwest.
Sampling No. Richness2 = mTSD + b Yrs. to
Reference Disturbance type TSD (yr) method1 yrs.1 m b r 100%3
Hessing and Johnson [70] Powerline corridor 1–5 PP 5 1.175 75.2 0.26 21
Callison et al. [51] Fire 1–37 CS 7 −0.020 71.7 0.00 ––
Lei [56] Fire 1–17 CS 4 1.068 38.6 0.46 58
Bolling and Walker [27] Abandoned road 5–88 CS 7 0.237 63.8 0.20 152
Brooks and Matchett [61] - 0.01 ha Fire 6–14 CS 3 0.357 74.2 0.00 72
Brooks and Matchett [61] - 0.1 ha Fire 6–14 CS 3 −0.398 84.2 −0.33 ––
Webb et al. [63] Fire 4–41 PP 3 3.482 55.3 1.00 13
Scoles-Sciulla and DeFalco [66] Abandoned road 1–7 CS 4 13.861 0.0 0.73 7
Vamstad and Rotenberry [67] Fire 2–65 CS 6 −0.379 92.9 −0.26 ––
30 studies, 1 year of data each Fire, other 1–74 –– –– 0.208 92.0 0.10 38
1
CS = chronosequence, PP = permanent plot. No. yrs. represents how many different years were
represented by the sampling.
2
Richness is expressed as a percentage of undisturbed areas.
3
Years required for richness to reach 100% of the richness on undisturbed areas, as estimated by
the regression equation.
 Figure 3. Examples of studies that examined time since disturbance (TSD) relationships
with variables of plant recovery in the Mojave and Sonoran Deserts of the American
Southwest. Plant cover and richness are expressed as the percent of levels found on
undisturbed areas ([disturbed/undisturbed] × 100). (a) Perennial plant cover [51]. (b)
Perennial plant cover using data from 29 individual studies that each made one TSD
measurement. (c) Annual plant cover [67]. (d) Perennial species richness [51]. (e)
Perennial species richness using data from 30 individual studies that each made one TSD
measurement. (f) Annual plant richness [67]. (g) Disturbed:undisturbed similarity of
perennial species composition [51]. (h) Disturbed:undisturbed similarity of perennial
species composition using data from 31 individual studies that each made one TSD
measurement. (i) Disturbed:undisturbed similarity of annual species composition [67].

The relationship of the similarity of species composition of disturbed to undisturbed areas with TSD
was mixed among studies (Table 3, Figure 3). Five of 12 studies (42%) showed r 2 values > 0.52, while
the remaining seven studies all were ≤0.30. Similarly, time to full recovery ranged from divergence
(where composition of disturbed areas became less similar to undisturbed areas over time) in four
studies to approximately 600 years to recovery in Vamstad and Rotenberry [67] and Webb et al. [63].
Combined data from 31 studies (seven of which examined fire) also showed a weak correlation of
similarity with TSD and an estimated full recovery time of over 200 years.
 Int. J. Environ. Res. Public Health 2010, 1261
7
Table 3. Relationship of time since disturbance (TSD) and community percent similarity
(Sørensen index) for perennial plants in the Mojave and Sonoran Deserts of the
American Southwest.
Sampling No. Similarity = mTSD + b Yrs. to
Reference Disturbance type TSD (yr) method1 yrs.1 m b r 100%2
Johnson et al. [68] Powerline corridor 1–6 PP 6 10.600 7.4 0.80 9
Hessing and Johnson [70] Powerline corridor 1–5 PP 5 −1.250 95.5 −0.55 ––
Callison et al. [51] Fire 1–37 CS 7 −0.518 24.9 −0.30 ––
Medica et al. [53] Fire 2–8 PP 3 2.833 47.2 0.97 19
Minnich [55] Fire 1–47 CS 9 0.560 42.8 0.51 102
Lei [56] Fire 1–17 CS 4 −0.448 23.4 −0.32 ––
Bolling and Walker [27] Abandoned road 5–88 CS 7 0.295 44.7 0.35 187
Brooks and Matchett [61] Fire 6–14 CS 3 −0.692 12.5 −0.72 ––
Webb et al. [63] Fire 4–41 PP 3 0.147 14.3 0.45 582
Alford et al. [29] Fire 5–21 CS 4 2.160 28.0 0.91 33
Scoles-Sciulla and DeFalco [66] Abandoned road 1–7 CS 4 4.158 0.0 0.73 24
Vamstad and Rotenberry [67] Fire 2–65 CS 6 0.127 25.4 0.14 587
31 studies, 1 year of data each Fire, other 1–74 –– –– 0.285 38.6 0.30 215
1
CS = chronosequence, PP = permanent plot. No. yrs. represents how many different years were
represented by the sampling.
2
Years required for similarity to reach 100% between disturbed and undisturbed areas, as estimated
by the regression equation.

3.3. Community and Disturbance Type Comparisons

Only four studies, all in the Mojave Desert, directly compared post-disturbance changes among
plant community types. Vasek et al. [45] compared recovery along a power transmission corridor as it
passed through creosote scrub and saltbush dry lake flats. In the saltbrush community, fourwing
saltbush (Atriplex canescens), cattle saltbush (Atriplex polycarpa), and Mojave seablite (Suaeda
moquinii) dominated undisturbed areas and also had recolonized 1- and 36-year-old transmission lines.
Big saltbush (Atriplex lentiformis) was not recorded in undisturbed vegetation but comprised 17–24%
of the relative cover in the disturbed areas. Different species, such as creosote bush, white bursage
(Ambrosia dumosa), and cheesebush (Hymenoclea salsola), colonized the line within the creosote
scrub community. Carpenter et al. [31] compared succession on agricultural fields abandoned 52–79
years earlier among four elevation belts (ranging from 1,100 m creosote scrub to 1,615 m sagebrush-
juniper [Artemisia tridentata-Juniperus osteosperma]) in the central Mojave Desert. Middle elevations
with Joshua tree woodland had 20-30% fewer species on disturbed than undisturbed areas, while the
low- and high-elevation communities showed little difference in species richness with disturbance
status. There was less difference in cover between disturbed and undisturbed areas in the low-elevation
communities (1–3% absolute difference in cover) than in the high-elevation communities (5–8%
difference). The species composition similarity of disturbed areas among the four community types
ranged from 18% (1,100 m creosote scrub versus 1,615 m sagebrush-juniper) to 70% (1,280 m versus
1,430 m, both Joshua tree woodland community types). There was little difference in disturbed:
undisturbed similarity among community types, as similarities ranged from 71% in creosote scrub to
85–86% in the Joshua tree woodland communities. At Yucca Mountain, Nevada, Gabbert et al. [54]
compared species composition among four community types disturbed by clearing with heavy
equipment 6–12 years earlier. Disturbed creosote-bursage communities were more than twice as
similar (61% Sørensen similarity) to their paired undisturbed areas as blackbrush (22%), boxthorn-
hopsage (Lycium andersonii-Grayia spinosa; 28%), or mixed species communities (26%).
Minnich [55] was the only study that directly compared TSD effects among community types. He
used a chronosequence of 6–20 years TSD in blackbrush and 1–47 years in Joshua tree woodland to
examine post-fire recovery in Joshua Tree National Park in California. Regression equations of the %
reestablishment of cover with TSD were similar for the two community types: y = 2.426TSD + 49.2,
r = 0.77, 21 years to 100% recovery (blackbrush), and y = 1.832TSD + 41.4, r = 0.84, 32 years to
100% recovery (Joshua tree woodland). Disturbed:undisturbed similarity was 62% on a 20-year-old
blackbrush burn and 69% on a 21-year-old Joshua tree woodland burn.
In comparing disturbance types, based on the TSD relationships presented in section 3.2, cover
reestablished more rapidly overall after fire than other types of disturbance involving land clearing
(Table 1). Results for recovery of species richness and species composition were mixed (Tables 2, 3).
Within land-clearing disturbances, several authors have noted the possibility that the intensity of
disturbance (e.g., amount of surface soil removed) or the degree of soil compaction influences
recovery. For example, by studying abandoned roads in the eastern Mojave Desert, Bolling and
Walker [27] found that road type (either track roads created simply by driving, or bladed roads created
by bulldozing a path) influenced some soil properties, but its effects on plant establishment were not
fully clear. At 56-year-old military disturbances in the western Sonoran Desert in Arizona, Kade and
Warren [8] found that plant cover was six-fold greater on former vehicle staging areas than in former
tent areas, even though the degree of soil compaction did not differ significantly between the areas. In
a different abandoned military training area (40 years old at the time of the study), in the eastern
Mojave Desert, Prose et al. [52] reported that cover was lowest on roads compared to tent areas and
parking areas. Roads overall had the most compacted soils. Similarly, Webb and Wilshire [48] found
that cover was three times lower on a former road than housing areas at the ghost town site of
Wahmonie in the northern Mojave Desert. While compaction was greatest on the road, TSD differed as
the road was abandoned 18 years earlier and the housing areas 51 years earlier. Based on examining a
chronosequence of a variety of ghost town disturbances varying in age from 19-92 years, Webb and
Thomas [62] concluded that effects of soil compaction on vegetation recovery could not be discerned
due to high variability. Examining the amount of soil removed by disturbance, Vasek [24] noted that
succession was slower on the bottoms of a pit (where more soil had been removed) than on pit sides at
a California site in the Mojave Desert.
Int. J. Environ. Res. Public Health 2010, 1262
7
Figure 4. Illustration of species composition patterns among studies examining post-
disturbance plant recovery in the Mojave and Sonoran Deserts of the American Southwest.
Studies are distinguished by desert and disturbance type (fire or land-clearing disturbances
such as old roads). (a) Undisturbed vegetation, where species are shown as vectors. Vector
lengths and directions indicate correlations with different study groupings. Only species
exhibiting an r2 ≥ 0.15 are shown. Species are abbreviated as the first three letters of the
genus and species given in Table 4, and for four species in (a) and (b) not given in Table 4,
as ACACON = Acacia constricta, ASTNUT = Astragalus nuttallianus, EPHTRI =
Ephedra trifurca, and ERIANG = Eriodictyon angustifolium. (b) Disturbed vegetation. (c)
Successional vectors showing the difference between disturbed and undisturbed species
composition of each study, where increasing lengths of vectors represent greater
differences. (d) Successional vectors standardized to unit length, comparing the direction
of species compositional change among studies.
3.4. Among-Study Comparisons

Ordinations allowed patterns of average disturbed and undisturbed community composition to be

compared among studies. There was some separation of undisturbed vegetation by desert, with
Sonoran studies generally located on the right side of the ordination, but some intermingling occurred
with Mojave studies in the center of the ordination (Figure 4a). Studies in the Sonoran uplands (those
containing saguaro cacti and mixed shrub-trees) were the best separated from Mojave studies, whereas
Sonoran studies in creosote scrub were less distinct from Mojave studies.
Disturbance was associated with a loosening of the groupings (Figure 4b). For instance, Mojave
Desert undisturbed vegetation for fire studies was tightly grouped, whereas burned plots were
dispersed and intermingled with other disturbance types. Deserts still separated, with Sonoran studies
in the upper part of the ordination, but intermingling occurred with Mojave studies in the ordination
center as with undisturbed vegetation. Community groupings also remained recognizable based on
study groupings and species correlation vectors, as creosote scrubland grouped in the upper part of the
ordination, blackbrush shrubland on the bottom, and mixed species communities on the left.
There were no clear patterns in the lengths of successional vectors, indicative of the relative amount
of difference in species composition between disturbed and undisturbed areas, among studies of
different disturbance type or between deserts (Figure 4c). However, the three longest vectors,
suggesting the greatest amount of difference between disturbed and undisturbed vegetation, all
originated from studies of non-fire disturbances. There also was considerable overlap in the direction
of vectors, indicative of successional trajectories, between disturbance type and deserts (Figure 4d).

3.5. Individual Perennial Species

Occurrences of individual species were diffuse (i.e., many absences) across the diversity of studies,
and as a result, indicator species analysis did not identify any species (out of 199 species recorded
across studies) that had indicator values >49 for disturbed/undisturbed categories by desert. This is
below the cutoff of 50 to be considered strong indicator species. However, the most abundant species
could be classified into the general response types to disturbance as increasers, versatile (species
important in both disturbed and undisturbed habitats), and decreasers (Table 4). Increasers exhibited a
high disturbed:undisturbed abundance ratio averaged across studies and also had high abundance when
present in a study in disturbed areas relative to undisturbed areas. This measure of abundance when
present was important to examine because, owing to the diversity of studies and sites, few species
occurred in more than half of the studies. The most common species included creosote bush (occurring
in 48% of disturbed studies and 64% of undisturbed studies), Nevada jointfir (Ephedra nevadensis;
45% disturbed, 52% undisturbed), cheesebush (52% disturbed, 42% undisturbed), and white bursage
(45% disturbed, 42% undisturbed).
Major increasers included forbs and shrubs such as brittlebush (Encelia spp.), desert trumpet
(Eriogonum inflatum), whitemargin sandmat (Chamaesyce albomarginata), broom snakeweed
(Gutierrezia sarothrae), rubber rabbitbrush (Ericameria nauseosa), desert globemallow (Sphaeralcea
ambigua), and brownplume wirelettuce (Stephanomeria pauciflora). Two grasses—Indian ricegrass
(Achnatherum hymenoides) and desert needlegrass (Achnatherum speciosum)—also were prominent
increasers, especially considering that the species were among the most frequently detected disturbance
species among studies. Versatile species had disturbed:undisturbed ratios near 1, and were typified by
Nevada jointfir, white bursage, and boxthorn. The grass big galleta (Pleuraphis rigida) also was
versatile, as were banana yucca (Yucca baccata) and Mojave yucca (Yucca schidigera), at least on a
relative abundance basis even if their absolute abundance declined on disturbed compared to
undisturbed areas. Blackbrush exemplified decreasing species and exhibited the largest absolute
decline after disturbance when present in a study. Triangle bursage (Ambrosia deltoidea) and creosote
bush also incurred major reductions after disturbance when present, but these species still maintained
relative abundances >11% in disturbed areas. Other decreasers included Joshua tree and various cacti
(e.g., pencil cholla [Cylindropuntia ramosissima], Engelmann's hedgehog cactus [Echinocereus
engelmannii]), and hopsage.

Table 4. Categorization of response to disturbance for major perennial species in the

Mojave and Sonoran Deserts of the American Southwest.
Species 1 AD AU OD OU ADP AUP
R
Increasers –––––––––––––– % ––––––––––––––
Acamptopappus sphaerocephalus 1.6 1.4 0.9 12 18 11.4 4.8
Achnatherum hymenoides 4.3 1.2 0.3 21 15 5.7 1.9
Achnatherum speciosum 7.4 5.9 0.8 30 33 19.5 2.4
Baileya multiradiata 2.9 1.3 0.5 18 12 7.2 3.7
Bebbia juncea 4.9 0.2 0.0 9 12 2.6 0.4
Chamaesyce albomarginata 36.5 1.2 0.0 9 6 12.8 0.5
Encelia farinosa 1.6 1.5 0.9 21 15 7.1 6.2
Encelia frutescens 84.2 1.4 0.0 9 6 15.9 0.3
Encelia virginensis 5.1 1.6 0.3 21 18 7.7 1.8
Eriogonum inflatum 85.0 0.2 0.0 9 3 2.1 0.1
Ericameria nauseosa 237.6 0.5 0.0 15 3 3.5 0.1
Gutierrezia sarothrae 7.6 2.6 0.3 18 21 14.6 1.6
Hymenoclea salsola 2.1 7.0 3.4 52 42 13.6 8.0
Prunus fasciculata 2.0 0.5 0.2 15 15 3.1 1.5
Salazaria mexicana 1.9 0.5 0.3 24 24 2.2 1.1
Senna covesii 5.4 0.5 0.1 6 6 7.7 1.4
Sphaeralcea ambigua 4.9 3.0 0.6 36 24 8.3 2.5
Stephanomeria pauciflora 14.8 2.2 0.1 24 21 9.2 0.7
Thamnosma montana 6.2 1.6 0.3 24 21 6.4 1.2
Xylorhiza tortifolia 26.7 0.4 0.0 18 9 2.0 0.1
Versatile
Acamptopappus shockleyi 0.8 0.3 0.3 18 15 1.4 2.2
Ambrosia dumosa 0.7 7.5 10.3 45 42 16.5 24.3
Atriplex canescens 0.6 0.1 0.2 12 15 1.0 1.4
Cylindropuntia echinocarpa 1.0 0.5 0.6 21 27 2.6 2.1
Ephedra nevadensis 1.0 4.2 4.1 45 52 9.3 7.9
Ephedra viridis 1.3 0.1 0.1 12 12 1.2 0.9
Eriogonum fasciculatum 1.0 0.5 0.5 24 27 1.9 1.7
Lycium andersonii 0.9 2.2 2.5 36 42 6.0 6.0
 Table 4. Cont.
Parkinsonia microphylla 1.5 1.8 1.2 9 9 19.6 13.0
Pleuraphis rigida 0.7 2.0 2.9 12 21 16.6 13.6
Yucca baccata 0.9 0.3 0.3 12 12 2.5 2.7
Yucca schidigera 0.5 0.2 0.5 9 15 2.6 3.0
Decreasers
Ambrosia deltoidea 0.3 1.0 3.9 9 9 11.3 42.6
Coleogyne ramosissima 0.1 1.0 13.9 33 39 2.9 35.3
Cylindropuntia acanthocarpa 0.2 0.1 0.3 18 24 0.4 1.3
Cylindropuntia bigelovii 0.3 0.3 1.0 9 12 3.2 8.4
Cylindropuntia ramosissima 0.2 0.0 0.1 9 21 0.3 0.5
Echinocereus engelmannii 0.1 0.0 0.1 6 15 0.1 0.6
Ericameria cooperi 0.5 0.6 1.4 24 27 2.7 5.1
Grayia spinosa 0.1 0.8 5.1 15 24 5.0 21.1
Juniperus californica 0.0 0.0 0.9 6 12 0.6 7.1
Krameria erecta 0.4 0.2 0.5 18 21 1.2 2.5
Krascheninnikovia lanata 0.2 0.1 0.7 18 21 0.8 3.4
Larrea tridentata 0.4 8.1 21.5 48 64 16.7 33.8
Menodora spinescens 0.3 0.2 0.6 12 15 1.7 4.0
Prosopis glandulosa 0.0 0.0 0.4 3 6 0.1 6.8
Yucca brevifolia 0.1 0.1 0.9 15 21 0.6 4.3
1
R = ratio of disturbed:undisturbed abundance; AD = mean relative abundance for disturbed areas
among studies; AU = mean relative abundance for undisturbed areas among studies; OD = percent
occurrence (out of 33 studies for which individual species data could be extracted) for disturbed
areas; OU = percent occurrence (out of the same 33 studies) for undisturbed areas; ADP = relative
abundance only when present for disturbed studies; AUP = relative abundance only when present
for undisturbed studies.

3.6. Annual Vegetation

Annual plant cover rebounded rapidly after disturbance, with two of four TSD studies showing y-
intercepts reflecting cover greater in disturbed than undisturbed areas (Table 5, Figure 3). The other
two studies showed reestablishment to amounts found on undisturbed areas in two years or less.
Species richness exhibited a similar trend, as two studies had intercepts near 100%, and the other three
studies had estimated recoveries of ≤13 years. For disturbed and undisturbed community similarity,
intercepts ranged from 50–92%, indicating high similarity, though completing the rest of recovery was
estimated to require much longer.
It was difficult to make quantitative comparisons of annual plant species composition and individual
species among studies because fewer studies examined annuals than perennials. However, some trends
appeared from the collective results of individual studies. First, several studies reported a strong
temporal influence (linked to precipitation) on the reestablishment of annual plants, where rainfall
amounts in a given year could overwhelm any effects of disturbance (e.g., [53,60,76]). In some years of
low rainfall virtually no annuals may be recorded, whereas in moist years, biomass and cover may
increase several orders of magnitude. Second, Brooks [60] and Cave and Patten [72] highlighted the
 effects of microsite (e.g., below shrubs versus in interspaces between shrubs) on the distribution and
abundance of annual plants in both disturbed and undisturbed areas. Overall, annual plants were more
abundant below shrubs in both areas, but some annual species showed contrasting patterns.
Third, different annual species have been reported to show different responses to disturbances. For
example, the non-native grass red brome has often decreased the first few years following disturbance
in permanent plot studies [53,60,72]. Redstem stork's bill (Erodium cicutarium), in contrast, has
increased rapidly [53,57,60,65,73]. Native annuals reported to colonize disturbed areas include desert
Indianwheat (Plantago ovata) following fire and land clearing in both the Mojave and Sonoran
Deserts [64,72,76], whitestem blazingstar (Mentzelia albicaulis) after nuclear detonation tests in the
northern Mojave Desert [42], flatcrown buckwheat (Eriogonum deflexum) on abandoned roads and
cleared areas in the Mojave Desert [57,64], and species such as cryptantha (Cryptantha spp.) and
sandmat (Chamaesyce spp.) in various studies. Fourth, studies making fewer than three temporal
measurements of disturbed:undisturbed community composition similarity typically supported the
TSD studies in showing high similarity between disturbed and undisturbed areas. For example, Brown
and Minnich [73] found that community composition was 73% similar between burned and unburned
areas 3-5 years after fire in the upper Sonoran Desert. Prose and Wilshire [28] reported that similarity
ranged between 73 and 84% 22 and 43 years after military disturbances in the eastern Mojave Desert.

Table 5. Relationship of time since disturbance (TSD) and annual plant community
characteristics in the Mojave and Sonoran Deserts of the American Southwest.
Disturbance Sampling No. yrs. y2 = mTSD + b Yrs. to
Reference type TSD (yr) method1 sampled1 m b r 100%3
Cover
Johnson et al. [68] Powerline 1–6 PP 6 412.520 −149.3 0.43 1
Callison et al. [51] Fire 1–37 CS 7 −8.681 420.1 −0.43 ––
Brooks and Matchett [61] Fire 6–14 CS 3 35.468 39.4 0.99 2
Vamstad and Rotenberry [67] Fire 2–65 CS 6 −0.221 121.2 0.20 ––
Richness
Callison et al. [51] Fire 1–37 CS 7 −0.897 94.3 −0.30 ––
Brooks [60] - below shrub Fire 1–4 PP 4 6.661 13.5 0.97 13
Brooks and Matchett [61] - 1 m2 Fire 6–14 CS 3 5.559 59.7 0.92 7
Brooks and Matchett [61] - 0.01 ha Fire 6–14 CS 3 2.860 63.5 0.64 13
Vamstad and Rotenberry [67] Fire 2–65 CS 6 0.132 110.1 0.41 ––
Similarity
Callison et al. [51] Fire 1–37 CS 7 0.522 50.4 0.55 95
Brooks and Matchett [61] Fire 6–14 CS 3 −5.596 92.2 −0.91 ––
Vamstad and Rotenberry [67] Fire 2–65 CS 6 0.099 52.1 0.14 480
1
CS = chronosequence, PP = permanent plot. No. yrs. represents how many different years were
represented by the sampling.
2
Cover and richness are expressed as a percentage of undisturbed areas.
3
Years required for measures to reach 100% of levels on undisturbed areas, as estimated by the
regression equation.
3.7. Primary Succession

Four studies of primary succession that met selection criteria were uncovered, each of which
examined different geomorphic surfaces varying in age [20,33,77,78]. Specifically, these studies
assessed debris flows (also termed alluvial fans), resulting from the transport and deposition of soil
material at the mouths of canyons and below mountains. Relative ages of these flows can be estimated
by known dates of flood events for recent flows and the degree of soil development for older
flows [33,78]. Ages of flows examined by these four studies ranged from 5 years to tens of thousands
of years. All of the studies reported on perennial plants; none reported on annuals.
Bowers et al. [33] examined debris flows ranging in age from 5 to 3,100 years along the Colorado
River in Grand Canyon National Park in Mojave-Sonoran transitional ecosystems. In using the 3,100-
year-old flow as the undisturbed data and flows 5 to 485 years old as the successional sites, the
relationship between TSD and cover reestablishment was: % of undisturbed = 0.1476TSD + 73.8
(r = 0.69). For species richness, all nine TSDs except for two exceeded 100% of richness of
undisturbed areas, resulting in a y intercept of 152%. There was a close correspondence between TSD
and the Sørensen similarity with undisturbed areas: similarity = 0.052TSD + 3.4 (r = 0.88). These
authors noted that there was a relatively orderly progression where short-lived species (e.g., broom
snakeweed, brittlebush, brownplume wirelettuce) dominated the young flows and longer lived species
like creosote bush (which was not detected on flows < 285 years in age) inhabited the older flows.
In Death Valley National Park in the western Mojave Desert of California, Webb et al. [20,30]
reported that a young debris flow (age 5 years) in Wood Canyon was occupied by grape soda lupine
(Lupinus excubitus) and threadleaf snakeweed (Gutierrezia microcephala), species not detected on
older surfaces. In contrast, blackbrush cover increased from 0.2% on the young flow to 18% on the
intermediate-aged flow (thousands of years old) and 21% on the oldest flow (tens of thousands of years
old). Total perennial cover ranged from 4% on the young flow to 28% on the oldest flow. In a different
chronosequence in Gold Valley, species such as cheesebush, narrowleaf goldenbush (Ericameria
linearifolia), Nevada jointfir, and white bursage dominated density on the youngest (<100 years in age)
flow, whereas creosote bush, white bursage, boxthorn, hopsage, and Nevada jointfir dominated the
oldest (late Pleistocene) flow.
Similarly, McAuliffe [77] found that debris flows ranging in age from several centuries to several
millennia supported different suites of species in the western Sonoran Desert. Creosote bush was only
found on the intermediate and oldest surfaces and was most abundant on the oldest. In another study,
this one in the eastern Sonoran Desert Uplands of Arizona, McAuliffe [78] also noted that abundance
of creosote bush was linked to surface age and stability, but specific patterns depended on local soil
characteristics like the presence of clay-rich argillic horizons.
4. Discussion

4.1. Analysis Challenges

Several aspects of synthesizing the available data may have affected results of the analysis of
secondary succession studies. A first challenge in analyzing species composition data from the
literature is that due to data summary techniques or journal space limitations, all species are not always
reported in publications (often only major species are reported). However, since the relative abundance
of these non-reported species is low (often precisely why they are chosen not to be reported), their
effect on community similarity analyses such as the Sørensen index used in this analysis is minimal.
For example, Minich [55] included an ―other‖ species category in his data, but these species averaged
only 6% of the total relative community cover in both burned and unburned areas. I avoided this issue
of not having access to full species lists for the analysis of species richness, as I did not include any
study in TSD-richness analyses that did not report actual richness or all species from which I could
calculate richness. A second challenge is that different measures (e.g., cover, density) of plant
abundance are reported among studies, and these measures may emphasize different aspects of the
community. In this study, cover was chosen as the primary measure for analysis, as cover was reported
in 68% of community studies of secondary succession and is a long-used measure in vegetation
sampling [84]. Whatever measure was reported had to be used to analyze data from studies that did not
report cover. Analyzing different measures, as well as the possibility that different investigators
measured cover differently, was attempted to be overcome by calculating a relative abundance measure
standardized across all studies to range from 0-100% for species. A further challenge in the analysis of
TSD-species richness relationships is that sample areas differed among studies (richness increases with
increasing area sampled) and some did not even report areas. Brooks and Matchett [61] was the only
study that reported richness for different sized sample areas, and TSD-richness results did differ among
two scales in that study (Table 2). This observation suggests that different scales of analysis could have
resulted in some of the variation in the TSD-richness relationships. In addition, the amount of recovery
after disturbance was compared in a relative manner to nearby undisturbed areas. However, as studies
such as Turner et al. [85] illustrate, humans have long impacted vegetation in southwestern deserts.
Vegetation in the ―undisturbed‖ control areas may itself have been disturbed in ways difficult to
detect, although these areas still served as comparison areas not subject to the recent intensive
disturbances on disturbed areas.
The number of sites and years since disturbance in chronosequence and permanent plot studies
could have affected TSD relationships, as some studies had as few as three sites or repeated measures.
Finding sufficient sites and TSDs is challenging in many disturbance-related research projects.
Disturbances such as wildfire are by nature unplanned events, and similar to past disturbances such as
ghost towns, researchers work with what disturbances are available and have a documented history. As
Webb et al. [86] note, recovery is not necessarily linear, which makes extrapolating from short TSDs
difficult. While linear equations generally fit the data as well or better than non-linear equations for
available TSD relationships (Tables 1–3), the short time periods available for analysis in some studies
may not have enabled a full representation of post-disturbance recovery rates. It should be noted,
however, that estimating long-term recovery was not necessarily a goal of the original studies, such as
Scoles-Sciulla and DeFalco [66], whose study objective was to quantify early recovery patterns. Short-
term studies that measured only 1–2 years were useful for the regressions of combined studies of
overall patterns. Webb et al. [20,86] provide a further discussion of the challenges inherent in
extrapolating recovery, such as when droughts may result in shifts in recovery patterns [87].
It was difficult to isolate overall desert, community, and disturbance type effects in the analysis,
because other variables (e.g., TSD) were not necessarily constant among studies. This is to be expected
since study contexts differed. Averaging post-disturbance species composition in the ordinations
resulted in averaging different TSDs among studies, although this analysis provided an overall
disturbed-undisturbed comparison across studies. There is a need for additional studies that try to keep
as many external variables constant, such as TSD, to isolate disturbance and community type effects
within their study. This is again challenging due to the unplanned and retrospective aspect of
disturbances, and is probably why Minnich [55] was the only study to compare recovery of community
types through time. Even in Minnich’s [55] study, however, the available TSD was 47 years for the
Joshua tree community and only 20 years for the blackbrush community.
It also was difficult to isolate patterns of individual species statistically (through indicator species
analysis and as vectors in the ordinations) because of the diversity of species composition across the
studies that spanned different deserts, sites, and communities. Therefore, a species might have high
fidelity to disturbance but only occur in a small subset of studies that were conducted in habitat
suitable for the species, meaning that the species had many absences. Simple descriptive measures
such as the disturbed:undisturbed abundance ratio and mean abundance when present appeared
effective for an overall characterization of species responses to disturbance (Table 4).

4.2. Evidence for Desert Succession Concepts

Data gathered by the synthesis can be used to assess evidence concerning several concepts about
succession in arid lands advanced in the literature. Succession was purported by some early authors not
to actually occur in deserts [21,22]. The four studies of primary succession (Appendix) provide the
strongest evidence that succession can occur in deserts, as these studies illuminated a long-term
progression of plant community development perceived using the chronosequence approach. Studies of
secondary succession illustrated that there are multiple stages of colonizing communities after
disturbance, and four studies estimated that succession resulted in the reestablishment of communities
typical of undisturbed areas in 9–33 years (Table 3). However, other studies reported that disturbed
communities continued to diverge from undisturbed communities with increasing TSD, or estimated
recovery times for species composition of >500 years [63,67]. Divergence could imply that succession
was not occurring, change was proceeding to a different community or set of communities than nearby
undisturbed areas, or methodological challenges (e.g., durations of studies, limitations of the
chronosequence approach) made estimating successional progression and time scales difficult.
Several authors have asserted that during succession in deserts, perennial community composition
generally progresses from short- to long-lived species (e.g., [32,33]). Data on the life spans of
individuals are required to assess this concept, such as the life-span data in Bowers et al. [33]. This
Int. J. Environ. Res. Public Health 2010, 1271
7
postulate appears supported by the data, as several species reported to increase after disturbance
(Table 4) are considered short lived. For example, the early colonizers sweetbush (Bebbia juncea),
broom snakeweed, and brownplume wirelettuce are reported to live only 20 years, rather than the
hundreds and thousands of years reported for some late-successional species like honey mesquite
(Prosopis glandulosa) and creosote bush [33]. Life-history data are not available for many of the other
species, and such information could be useful for refining our understanding of the traits typifying
early versus later colonizers.
Annuals have been purported to be major components of both young and old communities in
deserts [32]. This synthesis found strong evidence supporting this supposition, as annual plant cover
and richness rebounded rapidly after disturbance to levels similar to or exceeding old, undisturbed
communities (Table 5). In the three studies assessing recovery of annual species composition, y
intercepts exceeded 50% similarity with undisturbed communities, also implying rapid recovery. Data
from studies of old desert communities also suggest that annuals are important in old communities in
moist years [53,61,72]. The prevalence of annuals in young and old communities in deserts differs
from common views of succession in temperate regions, where annuals are considered to be prominent
mainly during early succession [5].
Another concept advanced in the literature is that many of the post-disturbance increasing species
also inhabit washes, which are disturbed naturally by periodic floods [23]. To evaluate evidence for
this, I compared the early successional species in Table 4 with studies of desert wash species
composition (e.g., [88]). Some of the early colonizers in Table 4 have been reported as dominants in
washes; for example, cheesebush, brittlebush, and desert almond (Prunus fasciculata). Reciprocally,
many species dominating washes, such as honey mesquite, have not been reported as major early
colonizers of disturbances. These species may have water and other habitat requirements that are met
in washes but not in upland ecosystems, independent of disturbance.
Contingency effects, in particular disturbance type, severity, and community type, have been
suggested to affect recovery rates and the course of succession (e.g., [30]). Overall it appeared that
recovery after fire versus land-clearing disturbances did differ, with perennial cover generally
rebounding faster after fire compared to other disturbances (Table 1). Post-disturbance species
composition also differed between fire and land-clearing disturbance types based on the ordinations
(Figure 4). Although fire influences soil physical and chemical properties [56], soils may still remain
more intact after fire than land-clearing disturbances where they are scraped away or heavily
compacted. Furthermore, unlike after land-clearing disturbances, roots and seeds are not necessarily
entirely removed by fire. These residual propagules may enhance plant reestablishment on fires
relative to other disturbance types [89].
Within land-clearing disturbances, definitive conclusions about the effects of factors such as the
amount of soil removed or the degree of soil compaction on recovery cannot be made from the
available data. Studies produced mixed results, or high variability precluded detecting any potential
trends (e.g., [27,62]). It appeared that due to vehicle traffic, abandoned roads had more soil compaction
than many other disturbance types, which may hinder plant recovery [48,52]. On the other hand, the
narrow, linear configuration of roads may facilitate seed dispersal from surrounding undisturbed areas
for recolonization readily compared to larger disturbances further from seed sources [90]. This
example illustrates the difficulties in isolating effects of disturbance type and severity from other
confounding variables in the retrospective study of non-experimental disturbances. Understanding
effects of factors such as the amount of soil removal and compaction on plant recovery is important for
making management decisions when revegetation is a goal. For instance, it is important to know
whether the benefits outweigh the expense of ameliorating soil compaction through ripping with heavy
equipment or salvaging soil to re-apply after disturbance.
In comparing succession among community types, Carpenter et al.’s [31] study of old fields in the
Mojave Desert indicated that post-disturbance species composition differed among four communities.
There was little difference, however, among community types in the similarity of each to their own
undisturbed control. In contrast, Gabbert et al. [54] found that creosote-bursage communities in the
northern Mojave Desert were more than twice as similar to paired undisturbed areas as blackbrush and
two other community types, implying that the creosote communities had recovered the fastest. More
work is needed to understand how succession may differ among community and soil types [59].
Differences could hinge on several factors, such as the elevation of the community affecting
precipitation, soil moisture and rooting depth, and local genetic adaptations and traits of the species in
the community [31,36,91]. For example, blackbrush does not resprout after disturbance, whereas
creosote bush has some sprouting ability, potentially hastening its reestablishment [15].
Several other contingency effects could have major influences on post-disturbance succession. For
example, rainfall amounts in years following a disturbance could affect the type of vegetation that
initially establishes, which in turn could influence subsequent community development [13,63]. The
differences in seasonality of precipitation, where rainfall is more bimodal or evenly distributed in the
Sonoran compared to the Mojave Desert [36], between deserts also could influence post-disturbance
establishment of both annual and perennial species [38]. Grazing by herbivores such as wild burros and
jackrabbits is another example of a contingency effect that could filter which species are able to inhabit
the post-disturbance environment and could influence the total cover of post-disturbance
vegetation [79].

4.3. Conservation and Management Implications

If a management objective is to maintain old perennial plant communities such as those containing
Joshua tree, giant saguaro, creosote bush, and blackbrush, probably the best strategy is to avoid
disturbing these communities in the first place. Strategies to accomplish this could include minimizing
unauthorized off-road driving through the desert, limiting unnecessary land clearing, reducing damage
by non-native animals such as burros, and actively suppressing and reducing wildfires [1,79,92]. These
strategies will not always be possible, such as for fire suppression where fuel-producing non-native
annual grasses have invaded even relatively undisturbed desert, challenging fire suppression efforts
across large landscapes [93]. When old plant communities are disturbed, the literature suggests that
recovery times for species composition are on the order of decades to centuries at a minimum
(Table 3). In fact, examples of long-term community composition establishment must largely be
derived from studies of long primary successions, as typically only initial regeneration trends were able
to be captured in the <100 year time frames available for studies of secondary succession. Furthermore,
Int. J. Environ. Res. Public Health 2010, 1272
7
as Webb et al. [20] note, climate and ecological conditions (e.g., relatively recent establishment of
non-native species) have changed from the conditions in which many of the old communities became
established. This further complicates making recovery estimates.
Land managers can expect, however, that colonization by early successional communities will
facilitate the reestablishment of total perennial cover (to amounts found on undisturbed areas)
generally within 100 years, and in fewer than 40 years in some situations (Table 1). These early
successional communities may provide habitat favorable for some wildlife species. For instance,
Simons [94] found that Merriam’s kangaroo rat (Dipodomys merriami), a species that forages in open
areas, increased after fire in Sonoran Desert upland habitat. Additionally, annual communities seem to
reestablish fairly rapidly, and in moister years little difference may exist in cover and species
composition between disturbed and undisturbed areas after some disturbances (Table 5). In fact, total
annual cover may actually increase following disturbance, although it is important to differentiate
responses of non-native versus native species. Early successional communities of both perennial and
annual species can be quite diverse given the commonly observed rapid reestablishment of species
richness, which could promote landscape heterogeneity. Further research would be useful to determine
the habitat and resource value (e.g., habitat for wildlife, carbon sequestration) of different aged desert
communities, as this has not been well studied.
Understanding natural recovery patterns may be valuable for informing revegetation treatments if
decisions are made to actively revegetate disturbed areas by either augmenting establishment of early
colonizers, reintroducing late-successional species, or both. Early successional species apparently do
not require the below-shrub fertile island microsites to become established that are critical for the
establishment of many late-successional species like creosote bush [95]. It is not understood, however,
whether creating fertile islands also could enhance establishment of early colonizers. Further studies
such as Carrillo-Garcia [96] and Butterfield and Briggs [97] that examine the formation of fertile
islands and plant transitions on these microsite scales may be helpful for determining if creating fertile
islands would hasten succession [98,99]. Likewise, augmenting establishment of early successional
species may help establishment of later colonizers, if the facilitation model of succession of moist
regions applies to deserts [100]. If facilitation occurs, the early colonizers would ameliorate the post-
disturbance environment, making it more habitable for later colonizers. For actively revegetating with
late-successional species, a recent review of revegetation practices in the Mojave Desert concluded that
seeding and planting are prone to failure but can be successful in some instances [18]. Success can
hinge upon many factors including species selection, genetics of the plant stock, climate, short-term
weather after revegetation, the severity of the disturbance to be revegetated, and the revegetation
technique itself (e.g., seeding versus directly planting greenhouse-grown seedlings). For example,
creosote bush was not observed naturally colonizing new surfaces (which would have to be via seed) in
primary succession for at least several hundred years, supporting the observation that creosote rarely
establishes by seed [33,77]. Consistent with these natural patterns, directly planting creosote seedlings
in active revegetation projects was more effective than seeding [18]. Planting enabled the rarely
successful seed germination and vulnerable early seedling establishment phases to be bypassed. This
type of knowledge, informed by studying patterns of natural post-disturbance recovery, may be crucial
to the success of revegetation and restoration projects.
4.4. Summary and Conclusion

A quantitative review uncovered 47 studies that have evaluated post-disturbance plant recovery and
succession in the Mojave and Sonoran Deserts of the American Southwest. Succession seems to occur
in deserts but transpires over a longer time period than in more temperate regions. After disturbances
such as fire that do not physically remove or heavily compact soils, perennial plant cover in these
deserts can rebound, in some instances, to levels similar to undisturbed areas within 40 years. Species
richness, although derived from different actual species on disturbed versus undisturbed areas, often
reestablishes more rapidly than cover owing to an influx of new species arriving after disturbance.
Both species richness and cover rebound more rapidly than species composition. Annual plant
communities appear to recover more rapidly than perennial vegetation, and may even exhibit greater
post-disturbance cover on disturbed than undisturbed areas. It is important to distinguish responses of
native and non-native species, however. The observation of rapid annual recovery, together with the
observation that many of the early colonizing perennials generally have short life spans, support the
supposition that communities generally shift from short- to long-lived species as succession proceeds.
This is not unlike the concept of succession for temperate regions, although in deserts annuals remain
abundant in old communities during wet years. Versatile desert species, however, such as white
bursage and Nevada jointfir, may be long lived and inhabit both young and old communities. For some
species, their versatility may result primarily from establishment by seed (e.g., white bursage) or
sprouting (e.g., Mojave yucca). As in temperate regions, deserts contain species that are benefited or
reduced by disturbance.
Future research on desert succession could refine our understanding of differences among
disturbance and community types and how much time is required for recovery of different vegetation
characteristics. Most research has been constrained to studying existing disturbances, which has often
made it difficult to directly compare disturbance and community types because variation in other
variables confounds these comparisons. Experimental research together with revisiting studies of
existing disturbances to generate longer term records of succession could advance knowledge of
specific variables influencing succession. These contingency effects, including climate, the presence or
absence of non-native species, or the occurrence of multiple disturbances, could have major influences
on succession but are poorly understood. The traits (e.g., growth rate, seed germination, nutrient
requirements) of early colonizers also are not well understood, and this type of information could be
useful for identifying species most amenable to different active revegetation treatments. Similarly,
processes, such as the formation of fertile islands important for establishment of some species, could
have major influences on succession but are not well known [97]. Especially given the large land area
in deserts already occupied by burns, we need a better understanding of the function provided by
different aged burns. For instance, future research could examine how carbon storage capability and
suitability of wildlife habitat could change with increasing time since disturbance. While successional
communities may have unique values, the data suggest that protecting deserts from disturbance (e.g.,
unauthorized off-road driving, fire) is critical for sustaining old communities. Since disturbances can
leave scars in the desert visible for multiple human generations, great care should be exercised before
disturbing the desert, including with human-caused fire ignitions.
 This synthesis can help us understand the consequences of disturbance and recovery of land and
how they influence public health and well being. Disturbing the desert has a variety of effects on
human habitations and structures (e.g., wildfires that threaten homes, soil erosion that can damage
roads), biodiversity including genetic material, soil and plant productivity (influencing capability for
agriculture, ranching, and other land uses), natural resource availability, economics (e.g., tourism
industry and scenic landscapes), aesthetics, carbon sequestration, air quality (e.g., generation of
hazardous dust on de-vegetated landscapes), and many other features that directly affect public
health [1,14,17]. An additional, emerging public health consideration in deserts is the potential for the
establishment of broad-scale alternative energy projects [101]. Owing to their abundant open land and
sunshine, deserts are considered good candidate locations for technologies such as solar energy. For
example, hundreds of square kilometers of public land held by the US Bureau of Land Management
are under consideration for solar energy projects in the Mojave Desert and surrounding arid lands. As
currently envisioned, these projects involve blading the soil and clearing vegetation for constructing
solar structures and support facilities [102]. While alternative energy can be viewed as providing
extensive public benefits, ironically environmental damage from these projects can be severe [101].
These projects, for example, can impact aesthetics, consume large amounts of resources such as water,
limit other land uses, preclude public access to public land, and destroy habitat for endangered species.
Unfortunately, this synthesis found that no studies have evaluated disturbances associated with
alternative energy in these deserts. Given the broad-scales of disturbance proposed by these projects, it
is important to understand how damage to natural resources can be minimized and how ecosystems can
recover from short-term (e.g., temporary roads associated with construction of facilities) and long-term
(e.g., off-site impacts) disturbances connected with energy installations. The long recovery estimates
associated with some of the land-clearing disturbances documented in this review may be applicable
for how long plant communities require for recovery following similar disturbances linked with energy
development. However, this review suggests that specific disturbances resulting from alternative
energy projects have not been studied at all. Documented information is urgently needed for supporting
project planning to assess the impacts of these disturbances, how the disturbances can be minimized,
and how recovery from the disturbances can be promoted.

Acknowledgements

This project was supported through a cooperative agreement between the National Park Service
(Lake Mead National Recreation Area) and the University of Nevada Las Vegas. I thank Sharon
Altman for preparing the figures, formatting references, and reviewing the manuscript. I also thank two
anonymous reviewers for helpful comments on the manuscript. After this article was written, an
additional article by Rickard and Sauer [103] was located that provided a remeasurement of an earlier
study [42,104] analyzed by this review.
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 Appendix. Summary of 47 studies meeting inclusion criteria for a quantitative analysis of plant recovery following disturbance in the
Mojave and Sonoran Deserts of the American Southwest.
Temporal Community Species Species included
Reference1 Disturbance type TSD (yr)2 sampling3 type4 metric5 Annuals Perennials
Mojave Desert
Wells [23] Ghost town (roads, townsite) 33 – MS D, F ×
Rickard and Shields [42,104] Nuclear detonation, clearing 2–3 – MS II × ×
Davidson and Fox [43] Vehicle staging area 1 – CR D, F × ×
Vasek et al. [44] Pipeline corridor 12 – CR – ×
Vasek et al. [45] Powerline corridor 1, 36 CS CR, SB – ×
Vasek [24] Borrow pit 9 – CR C, D, F ×
Lathrop and Archbold [46] Aqueduct corridor 9, 66 CS CR – ×
Lathrop and Archbold [47] Powerline, pipeline corridor 1–55 CS CR – ×
Webb and Wilshire [48] Ghost town (roads, townsite) 51 – MS C, D ×
Lathrop [49] Military (roads, clearing) 36 – CR C, D ×
Webb et al. [50] Old agricultural field 20 – CR C, D ×
Callison et al. [51] Fire 1–37 CS BB C × ×
Prose and Metzger/Prose et al. [7,52] Military (roads, clearing) 40 – CR C, D ×
Carpenter et al./Carpenter [31,105] Old agricultural field 52–79 CS CR, JT, MS II ×
Webb et al. [30,20] Pipeline corridor, ghost town 42–74 – BB-MS C, D ×
Medica et al. [53] Fire 2–8 PP MS C, D × ×
Gabbert et al. [54] Clearing 6–12 – CR, BB, MS D ×
Minnich [55] Fire 1–47 CS BB, JT C, D ×
Lei [56] Fire 1–17 CS BB D ×
Walker and Powell [57] Abandoned road 3 – JT D × ×
Bolling and Walker/Bolling [27,106] Abandoned road 5–88 CS CR C, D ×
Loik et al. [58] Fire 1 – JT-MS C, F ×
Int. J. Environ. Res. Public Health 2010, 7 1283

Appendix. Cont.
Prose and Wilshire [28] Military (roads, clearing) 22–43 – CR C, D ×
Steiger and Webb [59] Military (roads, clearing) 42 – CR-MS C, D ×
Brooks [60] Fire 1–4 PP CR – ×
Brooks and Matchett [61] Fire 6–14 CS BB C × ×
Webb and Thomas [62] Ghost town (roads, townsite) 19–92 CS MS – ×
Webb et al. [63] Fire 4–41 PP BB-MS C, D ×
Abella et al. [64] Pipeline corridor 8, 38 CS CR C, D × ×
Abella et al. [65] Fire 2 – CR-BB C, D, F × ×
Scoles-Sciulla and DeFalco [66] Abandoned road 1–7 CS CR C ×
Vamstad and Rotenberry/Vamstad [67,107] Fire 2–65 CS BB-JT C × ×
Sonoran Desert
Johnson et al. [68,108] Powerline corridor 1–6 PP MS – × ×
O'Leary and Minnich [69] Fire 5 – CR F ×
Hessing and Johnson [70] Powerline corridor 1–5 PP SU – ×
McLaughlin and Bowers [71] Fire 1–2 – SU C, D ×
Cave and Patten [72] Fire 1–2 – SU D × ×
Brown and Minnich [73] Fire 3–5 – CR C × ×
Roundy and Jordan [74] Plowing 12 – SU D × ×
Wilson et al. [75] Fire 1 – SU D ×
Kade and Warren [8] Military (roads, clearing) 56 – CR C, D ×
Alford et al. [29] Fire 5–21 CS SU – ×
Abella et al. [76] Fire 1–2 PP SU C, F × ×
Primary succession
Webb et al. [30,20] Debris flow 5-millennia CS BB-MS C, D ×
McAuliffe [77] Debris flow 100s-millennia CS MS D ×
McAuliffe [78] Debris flow Various6 CS CR-MS C ×
Bowers et al. [33] Debris flow 5–3,100 CS MS C, D ×
 1
Studies of secondary succession by desert are given first, then studies of primary succession (Webb et al. [30,20] was conducted in the Mojave
Desert, McAuliffe [77,78] in the Sonoran, and Bowers et al. [33] in Mojave-Sonoran transitional ecosystems). Studies within these categories are
arranged chronologically. Multiple references are given when more than one document reported on a study or when additional data were derived from
theses associated with an article. Note that Webb et al. [30, 20] examined both secondary and primary succession.
2
Time since disturbance.
3
For studies that compared recovery through time, methods used were either chronosequences (CS) or permanent plots (PP).
4
BB = blackbrush (Coleogyne ramosissima), CR = creosote bush (Larrea tridentata), JT = Joshua tree (Yucca brevifolia), MS = mixed shrub, SB =
saltbush (Atriplex spp.), and SU = Sonoran upland.
5
C = cover, D = density, F = frequency, II = importance index, and – = data not broken down by species, provided as a single measure of total
community abundance.
6
Holocene and Pleistocene deposits were examined, with ages estimated based on the degree of soil development.

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TIPE-TIPE VEGETASI
 Toleransi Kekeringan Pada Berbagai Jenis Vegetasi Untuk Atap Hijau Yang Luas: Efek
Penyiraman Dan Keanekaragaman

Keragaman spesies yang tinggi dapat meningkatkan produktivitas dan stabilitas ekosistem.
Dalam komunitas yang lebih beragam, perbedaan di antara spesies (misalnya, arsitektur komunitas
tanaman) memungkinkan penggunaan sumber daya yang saling melengkapi (cahaya, nutrisi,
ruang). Sebagai contoh,arsitektur komunitas tanaman terukur dengan sistem yang lebih beragam
menunjukkan tutupan persen lebih besar dan lebih banyak kontak dengan pin sampling yang
didistribusikan di antara sejumlah besar kelas ketinggian. Oleh karena itu, ekosistem dengan
keanekaragaman yang lebih tinggi mencegat lebih banyak cahaya karena mereka memiliki kanopi
pengisi ruang tiga dimensi yang lebih baik, mungkin menjelaskan perbedaan dalam produktivitas
dan respirasi masyarakat.
Campuran tanaman yang beragam lebih menguntungkan daripada monokultur ketahanan
hidup yang lebih besar dan peringkat visual yang lebih tinggi dalam kondisi kering dari penelitian
ini. Itu ditunjukkan kombinasi spesies yang berbeda dalam keanekaragaman fungsional dan
kompleksitas dapat mencapai ini lebih banyak secara efektif. Jika spesies sedum saja digunakan
untuk atap hijau yang luas, sistem irigasi mungkin tidak diperlukan karena mereka dapat bertahan
lebih dari 3 minggu tanpa penyiraman. Namun, penting untuk diperhatikan menyadari perbedaan
toleransi kekeringan pada spesies sedum yang berbeda. S. spurium 'Coccineum' menunjukkan
tingkat kelangsungan hidup yang lebih rendah di bawah rezim pengairan kering. Jika forb atau
rumput digunakan, itu mungkin lebih baik untuk mempertimbangkan irigasi untuk menjaga
kualitas visual yang baik meskipun itu tergantung pada lingkungan, seperti iklim mikro, ketebalan
lapisan media dan jenis bahan substrat. Dalam forbs dan rumput, spesies yang pulih sepenuhnya
dari kekeringan, seperti A. maritima, P. vulgaris,S. uniflora, K. macrantha, dan T. flavescens
mungkin merupakan kandidat potensial untuk atap hijau luas di Indonesia Inggris (iklim laut
sedang).
Spesies tanaman dalam percobaan ini tidak universal dan sebenarnya diperlukan untuk
menggunakan spesies tanaman yang sesuai secara regional. Tanaman yang digunakan dalam
percobaan ini banyak lebih kecil dari yang ada di atap hijau sebenarnya dan percobaan ini
mempertimbangkan tanaman itu pendirian belum mencapai keseimbangan komunitas tumbuhan.
Karena itu, hasilnya diperoleh dalam penelitian ini mungkin valid untuk tahap pendirian, dan
percobaan serupa lebih lama. Selain itu, memang juga merekomendasikan bahwa toleransi
kekeringan dipelajari dalam kaitannya dengan desain penanaman yang berbeda untuk hijau atap,
seperti padang rumput, dan kepadatan tanam yang berbeda.
 Landscape and Urban Planning 97 (2010) 318–327

Contents lists available at ScienceDirect

Landscape and Urban Planning

journal homepage: www.elsevier.com/locate/landurbplan

Drought tolerance in different vegetation types for extensive green roofs:

Effects of watering and diversity
∗
Ayako Nagasea, , Nigel Dunnettb,1
a
Chiba University, Graduate School of Horticulture, Environmental Science and Landscape Architecture Course, 648 Matsudo, Matsudo-city 271-8510, Japan
b
University of Sheffield, Department of Landscape, Floor 3, Arts Tower, Western Bank, Sheffield S10 TN, UK

a r t i c l e i n f o a b s t r a c t
Article history:
Received 15 December 2009 The harsh and stressful growing environment of extensive green roofs means that only a limited range
Received in revised form 15 June 2010 of plant species is routinely used. However, ecological theory suggests that highly diverse or species-
Accepted 9 July 2010 rich vegetation might be more resistant and resilient to severe environmental stress. This paper
Available online 16 August 2010 describes an experiment investigating the influence of vegetation diversity on green roof plant survival
following an imposed drought. Twelve species were selected from the three major taxonomic and
Keywords: functional plant groups that are commonly used for extensive green roofs (forbs, sedums and grasses).
Urban
Four species were chosen from each group and planted in combinations of increasing diversity and
landscape Green
complexity: monocul- tures, four-species mixtures and twelve-species mixtures. Three watering regimes
roofs Drought
Irrigation were imposed: wet, moderate and dry (watering every 1 week, 2 weeks and 3 weeks, respectively). It
Species richness was concluded that a diverse plant mix was more advantageous than a monoculture in terms of
Competition greater survivability and higher visual rating under dry conditions. It was shown that combinations of
species differing in func- tional diversity and complexity achieved this more effectively compared to
plants of the same taxonomic group that compete for resources when grown together. Drought
tolerance in sedums was superior to that in forbs and grasses. Little difference in drought tolerance was
observed between forbs and grasses, which must be watered before reaching a permanent wilting point.
Plants that exhibited over 50% leaf desiccation were unable to survive to the end of the study.
© 2010 Elsevier B.V. All rights reserved.

1. Introduction
of buildings can be used for installing an intensive green roof.
On the contrary, extensive green roofs are characterised by a
Green roofs (vegetated roof surfaces) are increasingly seen
thin- ner layer of substrate (20–200 mm) and are relatively
in cities because they are an important strategy that addresses
lightweight (Johnston and Newton, 1993). As a result, a greater
some key urban environmental issues. Green roofs can reduce
range of appli- cation is possible because little or no additional
surface water runoff, provide a habitat for wildlife, moderate the
structural support is required on the building. This, combined
urban heat island effect, improve building insulation and energy
with lower mainte- nance requirements, and a reduced need for
efficiency, improve the air quality, create aesthetic and amenity
irrigation has led to wider adoption of extensive green roofs,
value, provide opportunities for urban food production and pre-
particularly where large areas of the roof surface are to be
serve the roof’s waterproofing (English Nature, 2003; Dunnett
greened. However, because of the thin substrate layer, the
and Kingsbury, 2008). Green roofs are mainly divided into two
extensive roof environment is a harsh one for plant growth:
types: intensive and extensive. Intensive green roofs are charac-
limited water availability, wide tem- perature fluctuations, high
terised by a thick layer of growing medium or substrate (more
exposure to wind and solar radiation create a highly stressed,
than 200 mm), in which a wide range of plants and vegetation
and sometimes disturbed, environment. As a result, a relatively
can be grown, particularly if irrigation is available. However,
small range of plant species is normally used for extensive green
the relatively heavy weight of the substrate requires additional
roofs. Sedum species are the most com- monly used green roof
struc- tural support on the building and therefore only a limited
plants (Dunnett and Kingsbury, 2008), as they are highly
range
adapted to dry environments. The evergreen nature of low-
growing sedum species enables green roofs to retain a veg-
etation cover year-round, and their ease of propagation makes
∗ Corresponding author. Tel.: +81 047 308 8946; fax: +81 047 308 8946. them commercially viable. Previous studies have shown that
E-mail addresses: a-nagase@faculty.chiba-u.jp (A. Nagase), n.dunnett@shef.ac.uk (N. Sedum spp. survive well under severe drought (Gurevitch et al.,
Dunnett). 1986; Iijima, 2001; Terri et al., 1986). This is the result of several
1
Tel.: +44 0114 222 0600; fax: +44 0114 275 4176. factors: the Crassulacean acid metabolism (CAM)
photosynthetic pathway,

0169-2046/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.landurbplan.2010.07.005
 A. Nagase, N. Dunnett / Landscape and Urban Planning 97 (2010) 318–327
which reduces water loss through evapotranspiration during the
day, and their succulent nature and thick waxy leaf cuticles that
also promote water conservation. One study examined drought
tolerance in Sedum spp. and several non-succulent perennials on
extensive green roofs. Even after 4 months, the Sedum spp.
survived and maintained active photosynthetic metabolism to a
greater extent than the non-succulent grass species
Schizachyrium sco- parium and the forb species Coreopsis
lanceolata (Durhman et al., 2006). However, it is important to
note that growing C. lanceolata is prohibited in Japan as it is
extremely invasive in its environ- ment (Hatase et al., 2008). In
some cases, hardy succulents such as Sedum spp. might be the
only choice for thin substrate non- irrigated extensive green
roofs (Snodgrass and Snodgrass, 2006). Whilst ensuring some
degree of success under stressful growing conditions, the
widespread use of sedum-only green roofs also has
disadvantages that are typical of any ecological system with lim-
ited species diversity. Experimental evidence indicates a positive
relationship between plant species richness and ecosystem func-
tioning (Aarssen, 1997; Freitas, 1999; Naeem et al., 1994; Spehn et
al., 2000; Tilman and Downing, 1994). High species diversity may
increase the productivity and stability of an ecosystem. In more
diverse communities, differences among species (e.g., plant
com- munity architecture) may allow complementary use of
resources (light, nutrients, space) (Naeem et al., 1994; Spehn et al.,
2000). For example, Naeem et al. (1994) measured plant
community archi- tecture with the more highly diverse systems
showing greater percent cover and a greater number of contacts
with sampling pins distributed among a greater number of
height classes. Hence, the higher-diversity ecosystems
intercepted more light because they had better three-
dimensional, space filling canopies, probably accounting for the
difference in productivity and community res- piration. A
highly diverse mixture of plants may result in greater space
filling above and below ground and diversity can compen- sate
for the failure of a single species due to poor germination,
growth or survival (Spehn et al., 2000). Nutrient leaching loss from
ecosystems should decrease because of greater nutrient capture
and/or immobilisation in more diverse ecosystems (Freitas, 1999).
In more diverse communities, there is a greater probability of
the presence of productive and/or drought-tolerant species
(Aarssen, 1997; Tilman and Downing, 1994). Moreover, monocultural
or sim- ple plant systems may support reduced faunal
biodiversity (Knops et al., 1999).
There is, as a result, increasing interest in creating extensive
green roofs with more diverse vegetation, particularly to increase
their potential for supporting invertebrate and avian biodiversity,
and to increase their ecological integrity under harsh growing con-
ditions. The ability to withstand summer drought would be the
main factor deciding plant choice (Dunnett and Kingsbury, 2008),
particularly where irrigation is limited or not available. For exam-
ple, eighteen Michigan native plants were evaluated over 3 years
for growth, survival during both establishment and overwintering,
and visual appearance in Michigan, USA. For non-irrigated sub-
strate 100 mm thick on an extensive green roof, plant survival was
limited; Allium cernuum, C. lanceolata, Opuntia humifusa and Trades-
cantia ohiensis were suitable. If irrigation is available, other native
species are potential candidates for selection (Monterusso et al.,
2005).
Previous plant selection studies for green roofs tended to
focus only on individual plants (e.g., Boivin et al., 2001;
Durhman et al., 2007; Rowe et al., 2006). In this paper, we
consider whether increasing the diversity and complexity of
green roof vegetation has any benefit on what might be termed
wider ecosystem properties: Does greater taxonomic and
functional diversity and complexity within green roof
vegetation confer increased resistance to drought stress? Does
increased plant diversity result in increased vegetation survival,
biomass production, and improved visual appearance fol-
319
Table 1
The twelve species and their ecological characteristics (Brickell, 2003; Hubbard,
1984; Snodgrass and Snodgrass, 2006; Stephenson, 1994).
Plant name Typical habitats
Armeria maritima Coasts, immature soils over a wide range of
rock types.
Origanum vulgare Infertile, usually calcareous soils.
Prunella vulgaris Grassland, typically associated with moist,
moderately fertile soils.
Short turf, particularly in lawns and permanent
pasture.
Silene uniflora Coastal cliffs, shingle and gravelly soils.
Sedum acre ‘Minor’ Dry sand dunes and steeply sloping, S-facing
exposure of rock
Sedum album ‘Coral carpet’ It grows at very contrasting altitudes and in a
great variety of soils.
Sedum rupestre A multiple of settings from costal sand dunes
to about 2000 m in the mountains.
Sedum spurium ‘Coccineum’ On rocks in the middle and upper alpine zones.
Anthoxanthum odoratum A wide range of grasslands and to a lesser
extent, open habitats particularly on slightly
acidic soils.
Festuca ovina Dry habitats include xerophylly and an early
shoot phenology and seed-set.
Koeleria macrantha Infertile calcareous grassland and rock
outcrops.
Trisetum flavescens Dry grassland and, to a lesser extent, rocky
habitats, particularly on base-rich soils.
lowing drought conditions, compared with more simple systems
or monocultures?
2. Methods
An experiment was established in the glass greenhouse of the
experimental gardens at the University of Sheffield, UK to inves-
tigate the influence of vegetation diversity on plant response to
differing watering regimes in simulated green roof systems.
Twelve plant species were used to create vegetation cover of the
same plant density but differing species composition. The
twelve species were chosen from the three major taxonomic and
functional groups regularly used for extensive green roofs:
Sedums (Sedum acre ‘Minor’, S. album ‘Coral Carpet’, S. rupestre,
S. spurium ‘Coccineum’), grasses (Anthoxanthum odoratum,
Festuca ovina, Koeleria macran- tha, Trisetum flavescens), and
herbaceous plants other than grass and sedums, referred to as
forbs in this study (Armeria maritima, Origanum vulgare, Prunella
vulgaris, Silene uniflora). From each of these groups, four
representative species were chosen and planted in combinations
ranging from pure monoculture through to highly diverse
mixtures. The twelve species and their ecological charac- teristics
are shown in Table 1. Combinations were as follows: (a) each
species grown in monoculture; (b) three mixtures of single
taxonomic or functional types: forbs, grasses and sedums; and
(c) all twelve species in combination (Table 2).
The seeds of forbs and grasses were obtained from
Emorsgate Wild Seeds (Norfolk, UK) and were sown in 160 plug
trays on March 5, 2006. The plug trays were obtained from LBS
(Lancashire Bale and Stacksheet Company, Lancashire, UK).
After germination, the plants were thinned to one plant in each
plug cell. Sedum spp. were obtained from the Alpine and Grass
Nursery (Lincolnshire, UK). Sedum leaf cuttings were taken on
March 5, 2006 again in plug trays, with one cutting per plug cell.
John Innes No. 1 Com- post (by volume: seven parts loam, three
parts peat and two parts sand; each cubic metre of mix: 0.6 kg
ground limestone, 1.2 kg hoof and horn meal, 1.2 kg
superphosphate and 0.6 kg potassium sul- phate are added) was
used for the propagation. The plug trays were placed in the
greenhouse under full sunlight and were watered
every other day. The greenhouse was heated to a constant tem-
◦
perature of more than 20 C during the experiment term. The
plug
Table 2
The combination of plants. Table 3
The plant size at the starting point of the experiment (n = 27).
Combination Plant name
Plant name Plant type Shoot Diameter
Monoculture Armeria maritima only length (cm) (cm)
Origanum vulgare only
Armeria maritima Forb 7.44 10.73
Prunella vulgaris only
Origanum vulgare Forb 15.77 9.85
Silene uniflora only
Prunella vulgaris Forb 7.18 12.37
Sedum acre ‘Minor’
Silene uniflora Forb 20.20 20.99
only
Sedum acre ‘Minor’ Sedum 3.55 6.98
Sedum album ‘Coral carpet’ only
Sedum album ‘Coral carpet’ Sedum 8.61 10.55
Sedum rupestre only
Sedum rupestre Sedum 12.79 11.43
Sedum spurium ‘Coccineum’ only
Sedum spurium ‘Coccineum’ Sedum 17.33 14.74
Anthoxanthum odoratum only
Anthoxanthum odoratum Grass 18.74 18.31
Festuca ovina only
Festuca ovina Grass 11.55 13.28
Koeleria macrantha only
Koeleria macrantha Grass 5.81 7.47
Trisetum flavescens only
Trisetum flavescens Grass 12.75 14.76
4 species mixture Mixture of forbs
(Armeria maritima, Origanum vulgare, Prunella vulgaris,
Silene uniflora)
Mixture of sedums In December 2006, all plants were harvested and the roots
(Sedum acre ‘Minor’, Sedum album ‘Coral carpet’, Sedum were carefully washed. The plants were then dried out in a dry-
rupestre, Sedum spurium ‘Coccineum’)
ing oven at room temperature for 7 days, after which shoot dry
Mixture of grasses
(Anthoxanthum odoratum, Festuca ovina, Koeleria
weight and root dry weight were measured. To test for significant
macrantha, Trisetum flavescens) differences between the treatments and the interaction, two-way
ANOVA (Minitab Release 14) was used. When there were signifi-
12 species mixture Mixture of 12 species
Armeria maritima, Origanum vulgare, Prunella vulgaris,
cant differences, means were separated by Tukey–Kramer test at
Silene uniflora, Sedum acre ‘Minor’, Sedum album ‘Coral the probability level P < 0.05.
carpet’, Sedum rupestre, Sedum spurium ‘Coccineum’,
Anthoxanthum odoratum, Festuca ovina, Koeleria
macrantha, Trisetum flavescens 3. Results

3.1. Survival
plants were transplanted into flats (368 × 216 57 mm) in the mid-
dle of May 2006. The flats were obtained from LBS. This size of The mean survival of plants in response to watering and veg-
flat was chosen because of limited space in the greenhouse. The etation diversity is shown in Fig. 1 (total) and Table 4 (individual
transplanting medium was a mixture of commercial green roof species), respectively. In Table 4, only results of moderate
substrates based on crushed tile or brick with organic matter regime and dry regime are shown because all plants survived in
con- tent of 10–15% (Zinco sedum substrate and Zinco semi- wet regime. Both results show that after 3 weeks of no watering,
intensive substrate 1:1). Each flat was prepared with 3000 g of the per- centage of surviving plants decreased significantly. This
substrate and 12 plants were planted at regular spacing result may suggest that the plants reached a permanent wilting
intervals, with four rows of three plants. There were three point between 2 and 3 weeks after the withdrawal of watering.
replicates for each vege- tation type, resulting in a grand total of ‘Permanent wilt- ing point’ may be defined as the amount of
48 flats. This replication may be the minimum number for water per unit weight or per unit bulk volume in soil that is held
statistical analysis; however, this was unavoidable due to the so tightly by the soil matrix that the roots cannot absorb the
limited space in the greenhouse. The flats were watered every water and the plant wilts (Kirkham, 2005). Watering had a
other day until the experiment started. The plant flats were significant effect on the survival of all forbs and grasses.
arranged in blocks according to the water- ing regime and the However, all Sedum spp. except S. spurium ‘Coccineum’ were
flats were randomised within each block. On September 1, 2006, unaffected by the watering treatments.
the watering treatment was started. There were three watering Under the dry regime, only the Sedum spp. and a low per-
regimes: wet (watered once a week); mod- erate (watered once centage of A. maritima were able to survive. S. acre ‘Minor’ and S.
every 2 weeks); and dry (watered once every 3 weeks). Enough
water was supplied to each flat until it started to drain off.
Measurements of plant height (longest shoots or leaves),
diam- eter (average of length and width) were taken at the
starting point of the experiment (Table 3). Measurements of
relative appearance were taken every 2 weeks from 8 September
2006 to 19 November 2006 (in total six times). The growth and
the appearance of a rep- resentative plant from each flat for each
species was measured to obtain three replicates for each species
in total. The relative appear- ance of the plants was assessed by
classifying their visual quality into five categories (Monterusso et
al., 2005): 1 = severely stressed and completely dried out; 2 =
stressed, with less than 50% of the leaves retaining green
pigmentation; 3 = mildly stressed with 50% of the leaves
retaining green pigmentation; 4 = minor stress with over 50% of
the leaves appearing to be healthy; and 5 = Unstressed with all
leaves appearing healthy. At the end of the experiment, total
plant survival was recorded. Plants that were completely dried
out and did not produce any new shoots after several weeks
follow- ing resumption of watering were regarded as being Fig. 1. Total survival per flat in response to watering and vegetation diversity
dead. (n = 36). Error bars represent standard error.
 A. Nagase, N. Dunnett / Landscape and Urban Planning 97 (2010) 318–327 321

Table 4
Survival of individual plants per flat in response to watering and vegetation diversity (n = 3).

Watering Moderate Dry SE P

1 species 4 species 12 species 1 species 4 species 12 species

Armeria maritima 97.23a 100a 100a 25.0b 0b 0b 8.38 Watering

P < 0.01
Origanum vulgare 8.33b 88.89a 100a 0b 0b 0b 4.63 Watering
P < 0.01
Diversity
P < 0.01
Watering × diversity
P < 0.01
Prunella vulgaris 66.67a 88.89a 100a 0b 0b 0b 11.71 Watering
P < 0.01
Silene uniflora 100a 88.89a 100a 0b 0b 0b 3.70 Watering
P < 0.01
Sedum acre ‘Minor’ 100 100 100 100 100 100 – –
Sedum album ‘Coral carpet’ 100a 100a 100a 100a 88.89a 100a 3.70 Ns
Sedum rupestre 100 100 100 100 100 100 – –
Sedum spurium ‘Coccineum’ 100a 100a 100a 19.44b 88.89a 100a 4.44 Watering
P < 0.01
Diversity
P < 0.01
Watering × diversity
P < 0.01
Anthoxanthum odoratum 77.78a 100a 100a 0b 0b 0b 4.90 Watering
P < 0.01
Festuca ovina 97.22a 100a 100a 0b 0b 0b 0.93 Watering
P < 0.01
Koeleria macrantha 100 100 100 0 0 0 – –
Trisetum flavescens 100 100 100 0 0 0 – –

P = probability; watering = watering treatments; diversity = vegetation diversity; watering × diversity = interaction between watering treatments and vegetation diversity.
Letters of Tukey–Kramer multiple comparison are comparing values within a row. Means with the same letter do not differ significantly from each other.

rupestre showed 100% survival regardless of the treatment.
Over- all, Sedum spp. were the most drought tolerant and, except
for S. spurium ‘Coccineum’, they were able to survive well even
after 3 weeks of no watering. Only two species, O. vulgare and S.
spurium ‘Coccineum’ were significantly affected by vegetation
diversity. Under the moderate regime, O. vulgare showed 100%
survival in the twelve-species mixture. However, survival
decreased to 88.89% and 8.33% in the four-species mixture and
monoculture, respectively. The same trend was observed in P.
vulgaris under the moderate regime and S. spurium ‘Coccineum’
under the dry regime. A. mar- itima, A. odoratum and F. ovina
under the moderate regime showed a lower percentage of
survival in the monoculture, whereas they
showed 100% survival in both the four-species and twelve-
species mixture.
3.2. Dry weight
The mean total dry shoot weight and dry root weight per flat
in response to watering and vegetation diversity are shown in
Figs. 2 and 3, respectively. It was predicted that watering would
have a significant positive effect on the growth. However, the
total dry shoot weight was significantly affected only by
vegetation diversity. In the total dry root weight, there was no
significant dif- ference between treatments. Interestingly, both
the total shoot and

Fig. 2. Mean total dry shoot weight per flat in response to watering and
vegetation diversity (monoculture n = 36, four-species mixture n = 12, twelve-
species mixture n = 3). Error bars represent standard error. Means with the same
letter do not differ significantly from each other.
Fig. 3. Mean total dry root weight per flat in response to watering and vegetation
diversity (monoculture n = 36, four-species mixture n = 12, twelve-species mixture
n = 3). Error bars represent standard error. Means with the same letter do not
differ significantly from each other.
Fig. 4. Mean dry shoot weight of individual species (forbs) per flat in response to watering and vegetation diverstiy ( n = 3). Error bars represent Standard Error.
Statistical analysis is compareing values within a species. Means with the same letter do not differ significantly from each other. P = probability, watering = watering
treatments, diversity = vegetation diversity.

root weight tended to show the lowest figures in the four-

species mixture. This result might suggest greater competition
among the plants when those of a similar structure are grown
together rather than those of exactly the same structure or
completely different structure.
The effects of watering and vegetation diversity on dry shoot
weight and dry root weight of the individual species are shown
in Figs. 4–6 and Figs. 7–9, respectively. The different taxonomic
plant groups are shown in separate figures. Overall, greater
biomass production was evident with more frequent watering,
although the shoot biomass of seven species (O. vulgare, P.
vulgaris, all Sedum
spp., A. odoratum) was not significantly affected by watering,
and the root biomass of six species (A. maritima, O. vulgare, all
Sedum spp.) was not affected. S. acre ‘Minor’ and S. album ‘Coral
Carpet’ showed better growth under the drier conditions.
In both shoot and root biomass production, more than half the
species were significantly influenced by vegetation diversity. In dry
shoot weight, O. vulgare, S. acre ‘Minor’, S. rupestre, A. odoratum, K.
macrantha, and T. flavescens were significantly affected by diver-
sity. In dry root weight, O. vulgare, P. vulgaris, all Sedum spp., K.
macrantha and T. flavescens were significantly affected by diver-
sity. Various responses were observed among the plants tested.

Fig. 5. Mean dry shoot weight of individual species (sedums) per flat in response to watering and vegetation diverstiy (n = 3). Error bars represent Standard Error.
Statistical analysis is compareing values within a species. Means with the same letter do not differ significantly from each other. P = probability, watering = watering
treatments, diversity = vegetation diversity, watering × diversity = interaction between watering treatments and vegetation diversity.
Fig. 6. Mean dry shoot weight of individual species (grasses) per flat in response to watering and vegetation diverstiy (n = 3). Error bars represent standard error.
Statistical analysis is compareing values within a species. Means with the same letter do not differ significantly from each other. P = probability, watering = watering
treatments, diversity = vegetation diversity, watering × diversity = interaction between watering treatments and vegetation diversity.

Some species showed the same response to species richness

less vigorous. The root biomass of P. vulgaris was much higher
regard- less of the watering regime; the shoot growth of O.
than that of the other species. A. maritima and all four Sedum
vulgare, and S. acre ‘Minor’ and K. macrantha was always greater
spp. had fine, fibrous roots and the root biomass was relatively
in monoculture, whereas A. odoratum showed the opposite
small.
trend. However, for most of the species, the greatest biomass in
the different species com- binations in which they were present
was not achieved under the same watering regimes. 3.3. Change in moisture stress symptoms over time
Overall, P. vulgaris, S. uniflora, S. rupestre, A. odoratum, and F.
ovina showed vigorous shoot growth, whereas the shoot biomass The effects of plant diversity on the appearance of moisture
growth of O. vulgare, S. album ‘Coral Carpet’ and T. flavescens was stress symptoms over time are shown in Fig. 10. Only the results
of the moderate and dry watering regime are shown because all

Fig. 7. Mean dry root weight of individual species (forbs) per flat in response to watering and vegetation diverstiy ( n = 3). Error bars represent standard error. Statistical
analysis is compareing values within a species. Means with the same letter do not differ significantly from each other. P = probability, watering = watering treatments,
diversity = vegetation diversity.
Fig. 8. Mean dry root weight of individual species (sedums) per flat in response to watering and vegetation diverstiy (n = 3). Error bars represent standard error.
Statistical analysis is compareing values within a species. Means with the same letter do not differ significantly from each other. P = probability, watering = watering
treatments, diversity = vegetation diversity, watering × diversity = interaction between watering treatments and vegetation diversity.

plants under the wet regime showed a constant rating of ‘5’.

the results of the moderate and dry watering regime are shown.
Under the moderate watering regime, significant differences
The plants that were evaluated as less than ‘3’ at 3 weeks after
were not observed during the former half of the trial period;
the start of the experiment did not survive at all. This result sug-
however, the visual rating was significantly lower in the
gests that these plants must be watered before they reach the
monoculture than in the four-species mixture and twelve-
stage where half their leaves have dried out. For the forbs, A.
species mixture in the latter half of the experiment (from 51 days
maritima showed the best visual rating followed by P. vulgaris,
after starting the watering regime). On the contrary, statistical
S. uniflora and O. vulgare. For the Sedum spp., only S. spurium
analysis showed that the visual rate was not significantly
‘Coccineum’ showed symptoms of stress; however, compared
affected by vegetation diversity under the dry watering regime.
to the other taxonomic groups, the symptoms appeared grad-
The change in the visual rating for individual species over
ually. T. flavescens fully recovered from the drought under the
time is shown in Figs. 11–13. The different taxonomic plant
moderate regime and showed a rating of ‘5’ in the final measure-
groups are shown in separate figures. The same as above, only
ment.

Fig. 9. Mean dry root weight of individual species (grasses) per flat in response to watering and vegetation diverstiy (n = 3). Error bars represent standard error.
Statistical analysis is compareing values within a species. Means with the same letter do not differ significantly from each other. P = probability, watering = watering
treatments, diversity = vegetation diversity, watering × diversity = interaction between watering treatments and vegetation diversity.

Fig. 10. Change of mean visual rating of different vegetation diversity over time
in the moderate and the dry watering regime ( n = 36). Values are mean ±
standard error.
Fig. 11. Change of mean visual rating of individual species (forbs) over time (n = 3).
Fig. 12. Change of mean visual rating of individual species (sedums) over time
(n = 3).
4. Discussion
4.1. Effect of diversity
From above results, it was shown that the diverse plant mix
was more advantageous than a monoculture for some species
Fig. 13. Change of mean visual rating of individual species (grasses) over time (n =
3).
in terms of greater survivability and higher visual rating under
dry conditions. O. vulgare and S. spurium ‘Coccineum’ showed
significantly greater survivability in diverse plant mix than
mono- culture and the overall visual rating was significantly
lower in the monoculture than in the four-species mixture and
twelve-species mixture in moderate watering regime. This result
is consistent with previous research on biodiversity and
ecosystem function- ing (Tilman and Downing, 1994). There are
many explanations for this; however, moisture absorption and
retention may be an impor- tant reason. Rixen and Mulder
(2005) explained that the complex canopy architecture of highly
diverse vegetation slows down the rate at which water hitting
the top of a canopy reaches the soil, and thus increases the
amount of water absorbed by the vegeta- tion.
Each species showed a different response to being in a
diverse mixture and no particular plant mix appeared to
promote high biomass production. According to Bach and Hruska
(1981), various plant parameters are influenced by plant diversity.
For example, leaf area is greater or lesser in monocultures than
in mixtures depending on the density and particular species
studied. In this study, the shoot biomass of O. vulgare in
particular decreased sig- nificantly with increased species
richness. This is probably due to competition with other species
that are better able to obtain certain limited resources in the
mixture. This result may suggest that diver- sity in vegetation
reduces the vigour of potential dominant species. In general, the
greatest species diversity is promoted at a moderate intensity of
environmental stress/or disturbance (Dunnett, 2004), and
extensive green roofs, with a relatively thin substrate layer,
would be appropriate for species-rich vegetation. On the
contrary, some species such as A. odoratum showed the best
growth in the twelve-species mixture regardless of the watering
regime. Inter- estingly, the overall biomass of the four-species
mixture tended to be less than that of the twelve-species
mixture. According to Yeaton and Cody (1976), interspecific
competition occurs among species with similar morphologies. In
this study, the combinations of four species belong to the same
taxonomic and functional group and thus they may be expected
to have similar structures: com- petition may be greater within
such mixtures compared to the twelve-species mixtures with
greater diversity of growth forms among each other in the 4
species mixture than in the 12 species mixture. Díaz et al. (2001)
also indicated that functional differences rather than species
richness have more influence on ecosystem processes.
Although there appeared to be a link between species rich-
ness and species survival, there was no apparent relationship
between species richness and vegetation productivity. In a
discus- sion of similar experiments investigating the influence of
green roof vegetation diversity on stormwater runoff, Dunnett et
al. (2008) concluded that greater vegetation complexity and
diversity appeared to have no greater advantage in terms of
runoff reduc- tion. Indeed, they suggest that contrary to the
view that increasing the number of species present results in
greater resource efficiency and strengthened ecosystem
properties, the evidence suggests that the introduction of less
efficient species into the vegetation reduces the overall efficiency
of that mixture: the sum is not greater than the whole.
Another important reason for using a wide range of plants
for a green roof is the improvement in aesthetic and visual
quality due to the different flowering times and the enhanced
visual and structural diversity. Sedum mixtures or turf can be
rather dull and uninteresting if used on a large scale (Dunnett,
2004). Studies using video images of actual green roofs showed
that mixed planting was preferable to monoculture for the
public (Nagaoka et al., 2003). Moreover, mixed planting allows
greater flexibility in green roof planting design. These features
add to the value of a building and help to attract and retain
clients.
4.2. Effect of watering
symptoms under the moderate watering regime at the begin-
ning of the experiment; however, they gradually recovered over
If a green roof is carefully designed, with an appropriate
the period of the experiment. These two species showed vigor-
plant mix and thickness of substrate, and if the plants are well
ous growth with sufficient watering. They were larger in physical
estab- lished, there should be little need for irrigation except in
size than other species, which may be problematic in maintain-
the most arid climate (Dunnett and Kingsbury, 2008). However,
ing water supply to the most distal parts (Hitchmough, 1994). O.
because the benefits and functions of green roofs partly depend
vulgare was the least drought tolerant among the forbs. The other
on the pres- ence of living and healthy vegetation, it would be
species had creeping habits whereas this species exhibited only
pragmatic to allow for the possibility of supplemental watering,
a limited capacity for lateral spread. Difference of plant size at
especially where non-succulent plants are used. In this
the time of starting of experiment in each species might cause
experiment, all forbs and grasses reached a permanent wilting
effect on growth and survival. However, it was unclear whether
point between 2 and 3 weeks after cessation of watering, and
or not these different morphologies and plant size were related to
water application was required once a week to maintain high
the degree of drought tolerance. Further research is necessary to
visual quality. Water availability to green roof plants may differ
evaluate drought tolerance among species with different morphol-
among green roofs due to vegetation composition, microclimate,
ogy.
substrate type and substrate thickness. Moreover, it is assumed
Among the grass species, A. odoratum had a lower survival
that the green roof environment is harsher then glasshouse.
rate than the other three species. Although the natural habitats
Usually, plants experience strong wind, full sun and fluctuation
of all four species tend to be dry and infertile soils, A. odoratum
of temperature. Hence, it is impossible to gener- alise that
reaches maximum abundance in damp pastures and meadows,
supplemental watering is always necessary after 2 weeks of no
where there is higher moisture availability. F. ovina would
watering to grow forbs and grasses on extensive green roofs. It
appear to succeed in dry habitats because of its xerophilous
might be reasonable to judge drought from the appearance of
characteris- tics and an early shoot phenology and seed-set. Both
the plants as well; in this study, plants that exhibited over 50%
leaf desiccation were not able to survive to the end of the K. macrantha and T. flavescens are associated with a range of soil
experiment. As Handreck and Black (2002) pointed out, careful types, mois- ture and fertility levels. Generally, F. ovina is more
observation is necessary to give the appropriate irrigation xeromorphic than K. macrantha (Grime et al., 1988). However, K.
regime by learning to recognise subtle changes in plant colour macrantha showed the better performance in recovery under the
and appearance that are early warnings of unacceptable stress. moder- ate watering regime in this study. T. flavescens was able
Moreover, it is important to use collected rainwater for green to fully recover from the drought, although A. odoratum and F.
roof irrigation, especially in rainy countries. ovina main- tained the same visual rating (Fig. 11). Kemp and
As expected, it was shown that drought tolerance in sedums Culvenor (1994) pointed out that the most important strategy for
was superior to that in forbs and grasses. However, the drought adaptation to dry conditions is not maintenance of production
response of sedums differed among species, a finding supported during drought, but the ability to survive and recover rapidly
by the other study (Van Woert et al., 2005). In this experiment, S. after obtaining water.
spurium ‘Coccineum’ was less drought tolerant than other sedum
species. In a study on the effect of substrate thickness on initial
5. Conclusion
growth, coverage, and survival of 25 succulent green roof taxa, S.
acre, S. album ‘Bella d’Inverno’ and S. rupestre showed 100% sur-
It was concluded that a diverse plant mix was more advanta-
vival under all regimes; however, S. spurium ‘Summer Glory’ had
geous than a monoculture in terms of greater survivability and
75% survival in 25 mm of substrate and 87% in 75 mm, respec-
higher visual rating under dry conditions from this study. It was
tively (Durhman et al., 2007). In the current experiment, S. acre
shown that the combination of species differing in functional
‘Minor’ and S. album ‘Coral Carpet’ showed better growth under
diver- sity and complexity can achieve this more effectively. If
the drier regime. A negative response of Sedum spp. to additional
sedum species alone are used for an extensive green roof, an
watering was reported for S. mexicanum under high temperatures
irrigation sys- tem may be not required since they can survive
in a greenhouse (Iijima, 2001). Wet substrates may promote root
more than 3 weeks without watering. However, it is important
rot in more sensitive species. Stephenson (1994) also pointed out
to be aware of the dif- ference in drought tolerance in different
that Sedums are generally more likely to be harmed by overwa-
sedum species. S. spurium ‘Coccineum’ showed lower
tering than by underwatering. S. rupestre showed the best growth
survivability under the dry watering regime. If forbs or grasses
under the wet regime, and also exhibited 100% survival under
are used, it may be better to consider irrigation to maintain good
the dry regime. This result suggests that S. rupestre may be able
visual quality although it depends on the environment, such as
to tolerate both wet and dry conditions. According to the study
microclimate, thickness of substrate layer and type of substrate
by Stephenson (1994), S. kamtschaticum var. floriferum ‘Weihen-
material. In forbs and grasses, the species that fully recovered
stephaner Gold’ can also tolerate both wet and dry conditions. This
from the drought, such as A. maritima, P. vulgaris,
characteristic would be highly suitable for extensive green roofs
S. uniflora, K. macrantha, and T. flavescens may be potential can-
since fluctuations in water availability tend to be high in thinner
didates for extensive green roofs in the UK (temperate maritime
substrates.
climate). The plant species in this experiment are not universal
For the forbs, A. maritima had the best drought tolerance,
and it is necessary to use regionally appropriate plant species.
although both shoot and root biomass were small and growth
The plants used in this experiment were much smaller than
was relatively slow. According to Woodell and Dale (1993), A. those on actual green roofs (Table 3) and this experiment
maritima ranges from mild moist climates to extreme alpine considers that plant establishment had not yet reached the
envi- ronments at its altitudinal limits. It withstands exposure to equilibrium of a plant community. Therefore, the results
severe winds and can tolerate extreme drought because its tap obtained in this study may be valid for the establishment stage,
root enables utilisation of water from lower soil levels. Deep tap and similar experiments over a longer term, not only in a
rooted species may not be suitable for extensive green roofs; greenhouse but also on a roof, may be required in future
however, shallow tap root species such as Armeria can adapt to a research. In addition, it is also recommended that drought
thin sub- strate layer and be more drought tolerant than forbs tolerance be studied in relation to different planting designs for
with shallow spreading fibrous roots. P. vulgaris and S. uniflora green roofs, such as a meadow, and different planting density.
showed drought
 Acknowledgements

We express our appreciation to Almasc for providing the exper- imental materials, to Dr. Noel Kingsbury for his valuable advice
and to Mr. Min-Sung Choi for helping to set up the experiment.

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