|
|
|
|
Review Article
|
|
Epiphytic Plants Responses to Light and Water Stress
|
|
M.S. Ruzana Adibah
and
A.N. Ainuddin
|
|
|
ABSTRACT
|
Epiphytes are plants susceptible to the current climate change due to continuous exposure of environmental changes. In this study, we review the epiphytes responses to fluctuations in their surrounding environments. Abiotic factors such as light and water are the important contributors towards the epiphytes growth. Epiphytes might suffer from environmental stresses namely high light intensity and water deficit, affecting its growth and physiological attributes. Epiphytes use several mechanisms to counter aforementioned problems and one of it is through changes of physiological pathways. Some of the epiphytes use Crassulacean Acid Metabolism (CAM) as protection system for survival in severe environments. Future studies should include more approaches used by this plant as defense mechanisms to such stresses and more studies on leaf anatomy, leaf structure and variations in biochemical components for further understanding of the mechanisms involved.
|
|
|
|
|
Received: March 07, 2011;
Accepted: May 04, 2011;
Published: June 10, 2011
|
|
INTRODUCTION
International community is widely concerned about climate change as one of
the most critical environmental issues faced by mankind (Black
et al., 2011). CO2 elevation and temperature rise has
its impacts on plants growth, development and its physiological functions
(Centritto, 2002) and the earth in general. Forest growth,
survival and structure are some of the major concerns from climate change as
an output from the interaction between forests and the environment (Chmura
et al., 2011). An understanding of forest canopy is important where
it operated as a medium for the energy, mass and momentum exchanges between
environment and the ecosystem of the forest (Song et
al., 2010). It contains myriads of plant populations and this includes
the parasites, hemi-epiphytes, vascular and non-vascular epiphytes (Benzing,
1990; Nadkarni et al., 2004). In tropical
forest, vascular epiphytes are included as a vital component of the forests
biological diversity (Wester et al., 2011). Existence
of epiphytes at plants and atmosphere interface made them vulnerable to climate
change thus, other components of the forest consequently will almost directly
affected from any negative impact occur to the epiphytes (Zotz
and Bader, 2009). There are also increases in awareness to the view that
the survival and continuation of the epiphytes community are gradually at risk
(Nadkarni, 1992). Besides, excessive logging and land
use to the tropical rain forests especially in the mountain rain forest are
harmful and have a dangerous effect to the epiphytes community (Barthlott
et al., 2001). Plants in this natural environment have higher risks
to be affected by several damages in relation to environmental stresses (Huang,
2006). Moreover, epiphytes are subjected to multiple abiotic and biotic
stresses of varying intensities and durations. The location of canopy dwelling
plants like epiphytes make it sensitive to environmental stress (Oberbauer
et al., 1996). Where, epiphytes are mainly habituated in a complex
light atmosphere (Martin et al., 2001) where
the main abiotic limitation in epiphytic habitat is the insufficiency of water
(Zotz and Hietz, 2001).
When the environment of epiphytes is affected by its climate, automatically
the plants physiological responses will be directly influenced. According
to Schurr et al. (2006), at any state of environmental
change, photosynthesis and growth processes are likely be affected. Climate
change affects the overall functions and operations of physiological processes
such as growth, transpiration and respiration (Brouder and
Volenec, 2008). In addition, the growth of plants is mainly influenced by
genetic traits or its surroundings (Kramer and Kozlowski,
1979). In fact, plants will respond to environmental stresses through their
physiological features such as modification organss growth, or by using
various types of ways to prevail against the stresses (Schurr
et al., 2006).
Therefore, it is necessary to discover how environmental factors especially light and water affect the epiphytes as they are mostly threatened by those two types of stresses. Their responses are vital to understand the epiphytes performances in fluctuating environments. This review will focus on the nature, contribution and response of epiphytic plants to light and water stress. Even though this paper touches on the entire globe, there is a clear focus on the growth and physiological responses of epiphytes to light and water stress. These observations also supplemented with reviews on epiphytic adaptive strategies through Crassulacean Acid Metabolism (CAM) in resistance against such stresses. EPIPHYTES
Epiphytes are plants that settle on other plants and their habitats vary from
the terrestrial understory to edge of the tree canopy (Zotz
and Hietz, 2001). The epiphytic plants use other plants like trees, shrubs
and woody vines as host. In contrast with the parasites, they are fully autotrophic
(Benzing, 1998) or are considered as true epiphytes
(Reinert, 1998). Ferns, orchids and bromeliads are embraces
as epiphytes where they have characteristics that include thick and waxy leaves
that allow them to require small amount of water (Ainuddin,
2007). There were plenty of epiphytic plants grew in wet tropical countries
(Freiberg, 2001: Benzing, 1998,
1990). Besides, the vascular epiphytes are distinct characteristic
element of tropical moist forests (Hietz et al.,
2002). Additionally, epiphytes are globally known as dominant elements of
the tropical rainforest (Fayle et al., 2009)
and most of the vascular epiphytes are tropical plants (Zotz
and Hietz, 2001). In addition, Benzing (1990) also
mentioned that the epiphytes rarely exist in drier places. However, he stated
that there are few types of epiphytes that could grow in the arid regions such
as the orchids and the bromeliads where they are supported by plants like the
Mexican and Peruvian cactus.
According to Diaz et al. (2010), administrative
practices in Chilean temperate rainforests prominently overlook the epiphytic
plants communities. They were removed due to misperception that they are the
indicators of deteriorating tree health and reducing production of timber. In
fact, epiphytes do act as a source of the tropical rainforest ecology where
it contributes to many forests functions such as storing water from rainfall
and holding nutrients (Benzing, 2004). In the process
of hydrological and nutrient cycles of a forest system, epiphytes are the vital
contributor (Benzing, 1998) since they engage and hold
nutrients from the surrounding (Benzing, 1990).
Epiphytes play a significant function in influencing their nearby area microclimate
particularly the canopy area (Stuntz et al., 2002).
Moreover, according to Rosdi and Ainuddin (2004), microclimate
of the surroundings area seems to be affected by the existence of plant. For
example, the surrounding microclimatic state at the forest floor, does show
a balance ecological system contained by much drier and warmer condition of
the atmosphere, which is as the reflection of the contribution of canopy epiphytes
and their accumulated dead organic matters (Freiberg, 2001;
Freiberg and Turton, 2007). The vascular and non-vascular
epiphytes contribute to the forest biomass. According to Nadkarni
(1984), these epiphytic plants contribute to more than a few tons per hectare
of biomass. In addition, these epiphytic plants also elevated the uptake of
carbon and productivity of the forest (Diaz et al.,
2010). For instance, a study of an epiphyte of Asplenium nidus shows
that it could accumulate its dry mass up to one tones of per hectare (Ellwood
et al., 2002).
In both vascular and non vascular plants there are epiphytisms among them and
which comprise of pteridophytes, flowering plants, latter bryophytes, algae
and lichens (Reinert, 1998). Generally, vascular epiphytic
plants varieties are mostly localized in tropical regions (Dubuisson
et al., 2009). Furthermore, Otto et al.
(2009) reported that plenty of epiphytes that mainly ferns are absolutely
acclimatized to the environment that is airy. According to Lorenzo
et al. (2010), almost 80% species of the epiphytes fit into just
four families: Bromeliaceae, Orchidaceae Polypodiaceae and Araceae.
PLANT STRESS
Climate change is the present issue that manipulates the ecological features
of an ecosystem. The changes in the environment have huge effects especially
on plants growth and its distribution. Interaction between plants and the environment
will influence plants physiological functions thus affecting some ecological
processes (Hegland et al., 2009). When the environment
of a plant is affected by its climate, the natural processes of this plant will
be directly influenced. Plant stress is always influenced by adverse environmental
conditions, such as insufficient water supply, diseases, lack of nutrients or
insect damage. There are many types of stresses caused by the changes of its
surrounding area either in a minor or major way. These abiotic stresses will
effect growth and in the long run, it will exterminate the survival of plant.
Canopy act as a filter to plant beneath it and reduce the solar energy received
to the ground (Ainuddin and Lili, 2005). Environmental
stresses for example water deficit and high light intensity might occur to epiphytes
which live beneath the forest canopy. A species of Platycerium bifurcatum
developed in diverse habitat which always exposed by drought and stress of high
irradiance (Rut et al., 2008). The surrounding
microclimate of the epiphyte area will therefore affect their mortality and
as a result, it will affect the distribution of different species (Fayle
et al., 2009). Epiphytes were also reported as the first population
to be declined as their ecosystem was at risk and disturbed (Dubuisson
et al., 2009).
However, epiphytes also exhibit ecophysiological, morphological and anatomical
adaptation to survive under these harsh canopy conditions (Lorenzo
et al., 2010). According to Suzuki et al.
(2005), a complex system of transcription factors and other rigid genes
will control the multiple defenses of enzymes, proteins and specific pathways
if any plant is acclimatize to those abiotic stresses. Each plant will use different
mechanism dealing with abiotic stress. For instance in Mimosa strigillosa,
under environmental stress of soil pH, more growth is distributed to shoot under
optimum condition, while under stress, it allow more growth to the roots (Nuruddin
and Chang, 1999). This reflects that plant use different approach as an
adjustment to environmental stress.
LIGHT STRESS
Light is one of the stress factors that have a huge influence on plant. The
energy source for photosynthesis in plants is light and it is the vital requirement
for plant life (Long et al., 1994). Light intensity
and light quality fluctuation definitely have its effects on biochemical, physiological
and plants developmental processes where under the low light level, growth and
development are disturbed due to insufficient energy and under high light intensity,
photodamaged may occur due to overload of the plants system (Humby
and Durnford, 2006). Epiphytes can grow under different light condition
ranging from the nearly full sun which is out in the open branches to the deep
shade on base of the stem (Hietz and Briones, 2001).
Epiphytes environment is always exposed to such stress and the regulation of
plant growth and development are affected by the changes of the environmental
conditions. Epiphytes that live under plant canopy are typically exposed to
the elements of harsh atmosphere where light stress may arise among the epiphytic
plants.
Light stress is when an excess light is absorbed greater than what is needed
during the process of photosynthesis, where the excess of light is defined as
when the ratio of Photon Flux Density (PFD) and photosynthesis is high (Demmig-Adams
and Adams, 1992). High light intensity will lead to high temperature which
will influence the plant growth due to hotter and drier surrounding microclimate.
Different mechanisms shield the photosynthetic apparatus from over-energization
under the overload light but, if the mechanisms of photoprotective of plant
are insufficient, photoinhibition process will be turned on (He
et al., 1996). The trigger to photoinhibition occurs due to the overexposure
of plant to irradiance which it is higher than the irradiance usually obtained
by plant (Stancato et al., 2002). The photochemical
inactivation mostly of Photosystem II (PS II) is involved in photoinhibition
(Sarvikas et al., 2006). Therefore, every organism
that conducts photosynthesis is probably vulnerable to injury due to radiation
influences, but the level of susceptibility depends on factors such as environmental,
genotype, phenotype and physiological (Alves et al.,
2002).
The growth of plants is closely related to photosynthesis and without light,
photosynthesis will not occur and the growth of plants will be retarded. According
to Winter et al. (1983), many CAM plants are
not only could survive in the area with high light intensity but also under
shaded condition. Capability of some species to survive under certain light
range is probably dependent on how far they can adapt to new levels of light
by changing their photosynthetic response (Heschel et
al., 2004).
WATER STRESS
Meteorological term for drought is implied as restriction of water for a long
period of time while water stress is likely to signify the complex progression
of the effect of drought which is triggered by drought (Lombardini,
2006). Drought stress also has become more severe in some area due to the
global climate change (Elsheery and Cao, 2008). Living
in the canopy environments, water limitation is likely to occur among epiphytes.
Extensive environmental conditions of drought and salinity converge to lower
water accessibility of plants lead to the limitation of photosynthesis (Flexas
et al., 2004), growth and worldwide yield (Chaves
et al., 2003). The rate of CO2 assimilation of plants
may be reduced under the condition of water insufficiency (Stancato
et al., 2001). Closure of stomata and photosynthetic rates reduction
are also stimulated by the limitation of water availability (Angelopoulos
et al., 1996). For instance, in Mimosa strigillosa, the stomata
are closed and leaves are folded to reduce loss of water (Chang
et al., 1997). In addition, both stomatal closure and inhibition
of leaf growth are among the earliest reactions towards drought to defend the
plants from excessive water loss where it might lead to leaf cell dehydration
and runaway xylem cavitations thus, bring towards the mortality (Chaves
et al., 2003).
The main limitation of plant survival and growth is water stress and during
acclimatization of plants to water stress, it involves several physiological
and anti-oxidative apparatus (Upadhyaya et al., 2008).
Therefore, stress tolerance indicates the capability of plants to survive in
adverse environment through the adaptation and acclimatization from the state
of stress (Lombardini, 2006). Epiphytes must tolerate
the stress to survive in the harsh environment. Therefore, there were many defenses
applicable to epiphytic plants (Benzing, 1990). For instance,
the adjustment of conductance can defend a plant itself to drought or water
stress. Moreover, Benzing (1990) also stated that osmotic
adjustment and carbon dioxide fixation are other ways that can be used by plants
to overcome this situation. According to Luvaha et al.
(2008), in changing of environmental climate, it is beneficial for species
to apply avoidance of drought mechanisms and adaptation through active osmoregulation.
In addition, plants tolerate drought by avoiding tissue dryness and at the same
time sustaining water potential or enduring the low water potential (Chaves
et al., 2003). Generally, thick cuticles, succulence, sunken stomata
and a thicker layer of boundary on the leaf surface are some of the adaptations
applied by plants to conserve their water status (Hsu et
al., 2006). For C4 or CAM plants, they use other methods of to cope
with stress through carbon dioxide fixation for production of sugar with a minimum
water loss (Xoconostle-Cazares et al., 2010).
Water insufficiency in soil and plant tissue during drought leads to the adjustment
in the processes of plant photosynthesis and has its effect on plant growth,
development and survival in harsh environment (Lombardini,
2006).
GROWTH RESPONSE TO LIGHT AND WATER STRESS
Growth is a mechanism achieved by division of cell, cell enlargement and differentiation
and it is associated with the physiological, ecological, genetic and morphological
measures and their complex interactions (Farooq et al.,
2009). One of the important elements for plant growth and development is
light (Saifuddin et al., 2010). Nearly all plants
use solar radiation not only source of energy for photosynthesis, but also to
regulate their processes of growth and development (Lombardini,
2006). Cervantes et al. (2005) theorized
that individual epiphytes under extreme light intensity microhabitats within
the canopy in a tropical dry forest of Yucatan, Mexico may have a restriction
in their growth and reproduction. A study by Singh and Srivastava
(1985) conformed to this finding where the fern of Azolla pinnata R.
Brown recorded has the lowest value of mean leaf area in both of under the shade
and highest light intensity treatments (Table 1).
In terms of biomass, unlike C3 plants that grow in high light area,
plants that grown under shade would distribute more biomass to their photosynthetic
tissues, creating thin, horizontally oriented foliages with little intra-canopy
shadings thus, they have relatively higher concentrations of chlorophyll and
higher coefficients of light absorption, however, these shaded plants have smaller
value in root biomass indicating low rates of transpiration and low light saturated
rates of photosynthesis (Skillman et al., 2005).
Decline in the vegetative growth of plants are one of the initial consequences
of drought where water deficit will stimulate changes in terms of cell structure
of plants and its metabolism (Khaled, 2010). Another
consequence of water stress is turgor loss which reduces the size of cells leading
to reductions in leaf expansion and shoot extension plus the leaf area reduction
will definitely lessen the surface area for transpiration and thus, smaller
leaves will decrease the light absorption and photosynthesis (Lombardini,
2006). In a study by Ainuddin and Nur Najwa (2009),
water restriction lowered length and area of Asplenium nidus.
Table 1: |
Growth of fern and epiphytes species grown under different
light treatment |
 |
According to Vurayai et al. (2011), decline
in leaf area is the initial defense of plants to drought as in their study,
water stress reduces area of the leaf to transpires less water. In addition,
the reductions of leaf water potential and stomatal closure are the instantaneous
reaction to water insufficiency, which point towards to decline in CO2
uptake and photosynthesis (Li et al., 2008).
The reduction in photosynthesis results in a slower growth and lower plant biomass
(Du et al., 2010) because plants need water to
create biomass (Benzing, 1990). Furthermore, stomata closure
and slower plant growth are desirable approaches to decrease further water loss
(Sinclair and Purcell, 2005). However, only a few studies
were done on the direct and long term observation as in concern of the growth
of epiphytic plants (Hietz et al., 2002).
PHYSIOLOGICAL RESPONSE TO LIGHT AND WATER STRESS
Generally, the function of physiology of plant explains the growth of plants
and its respond to the surrounding factors and cultural treatments (Kramer
and Kozlowski, 1979). In extreme environments especially in high light intensity
and water stress condition, plants will respond to changes through their physiological
processes, such as the rate of photosynthesis, transpiration and stomatal conductance.
In plants leaves, the factors from plant nutrition, light regime, leaf
age, water stress and other physiological parameters can affect the photosynthetic
CO2 assimilation (Von Caemmerer and Farquhar,
1981).
Although light is essential for photosynthesis, the light intensity whether
it is low or high can affect plant growth (Valladares and
Niinemets, 2008). Light intensity determines the degree of opening of the
stomata and the guard cell, controlling water balance and influencing the photosynthesis
rate of a plant via the light receptors that drive fixation of CO2
and reduced intercellular CO2 concentration (Yu
et al., 2004). In addition, the environment plays an important role
in determining the photosynthesis efficiency, for example, plants that grow
in a low light regime, their leaves absorb lower photon energy and they are
depending on photon supplies for their photosynthesis rate (Miyake
et al., 2009). Moreover, in a tropical dry forest of Yucatan, Mexico,
plants that grow in the lower level of the canopy would have a lower photosynthetic
rate while and plants that grow in the higher level of the canopy would experience
photoinhibition (Cervantes et al., 2005). Roberts
et al. (1998) found similar results where maximum rates of photosynthesis
in shaded leaves are lower than the exposed ones while Schafer
and Luttge (1988) found the opposite findings (Table 2).
Epiphytes usually lived in a place that receives variability in light and is
high in PFD since their photosynthetic apparatus will be affected, resulting
in high evaporation rate which affects the plant water relations (Schafer
and Luttge, 1988).
Moreover, physiological and biochemical processes of photosynthesis were affected
by water stress (Ramanjulu et al., 1998). According
to Chang et al. (1995), in adjustment to water
stress condition, two physiological characteristics vital to plants are water
transport system efficiency and regulatory system for water loss. In declining
water availability, stomata closure has been noted as the earliest response
of plants physiological attributes towards drought (Flexas
and Medrano, 2002). Since there is known close correlation between stomatal
conductance (gs) and net CO2 assimilation (Anet),
it has been classified that in drought condition, stomatal closure has an influence
in limiting the CO2 uptake in the leaves (Flexas
et al., 2004). In the limitation of net photosynthesis rate, stomatal
or non-stomatal factors were involved in this situation but the limitation was
also dependable on the harshness and persistence of stress and also genetic
reaction of the plant species (Ramanjulu et al.,
1998). The survival capability of plantin severe drought is based on water
loss limitation through minimum opening of stomata (Sanusan
et al., 2010).
Table 2: |
Photosynthesis rate of epiphytes species grown under different
light treatment |
 |
Although the closure of stomata helps in sustaining high leaf water content
and its water potential however is also responsible for the decline in photosynthesis
(Ohashi et al., 2006). Moreover, in water deficit
condition, the decline in CO2 assimilation rate is due to electron
transfer in the Photosystem II was reduced, thus affecting the quantum yield
in its photochemical apparatus (Stancato et al.,
2001). In a study of drought tolerance in cereal species, it was found that
the value of the quantum yield of PS II in water deficit condition was reduced
with the increment in the stress level (Flagella et al.,
1998).
Compared to other climatic elements in nature, light varies through its amplitude
and radiation quantity and quality obtained by plants (Alves
et al., 2002). When plants are subjected to strong light, their physiological
features will respond. The declines in capability for photosynthesis were stimulated
by exposing photosynthetic organisms, structures or organelles to visible light
which has been denoted in various terms such as photoinhibition, photooxidation,
photoinactivation, photolability, solarization and photodynamic reactions (Powles,
1984). Photoinhibition were used to explain the inhibition of photosynthetic
capacity (Demmig-Adams and Adams, 1992) and the independence
of gross adjustment in pigment concentration caused by excessive light (Powles,
1984). Long et al. (1994) also supported
that photoinhibition was considered as light dependent and a gradual reduction
of photosynthetic rate (Demmig-Adams and Adams, 1992)
which was independent of any developmental change.
Furthermore, it is known that exposing green plants to excessive light has
caused damages to photosynthetic apparatus (Powles, 1984).
Moreover, tremendously too much light obtained by plants possibly will damage
photosynthetic pigments (Powles, 1984) and the structure
of plants which leading to photodamage (Larcher, 2003).
In tropical region, high irradiance and high temperature arise concurrently
with drought will direct the plants towards increasing their photon energy in
chloroplast, which also decreases photochemical efficiency, thus leading to
photosynthetic apparatus damages (Elsheery and Cao, 2008).
Chlorophyll fluorescence technique is a good indicator in determining the response
from stresses. Whereby, in understanding adaptation system of plant and resistance
to stress from the environment, chlorophyll fluorescence act as an assistant
regards to this matter (Siam et al., 2008). This
technique is handy and be used broadly by plant physiologists and ecophysiologists
(Maxwell and Johnson, 2000). Chlorophyll fluorescence
measuring techniques has currently improved and therefore is a vital instrument
in the basic and applied physiology of plant (Krause and
Weis, 1991). Using this technique, it calculates the modifications in photosystem
II (PS II) action through the Chlorophyll a fluorescence changes which stimulated
by the stress (Percival, 2005). There have been plenty
of evidences associated with PS II acting as the main site of lesion in photoinhibition
(Powles, 1984). The apparatus of photosynthesis in plants
could possibly be affected provisionally by environmental stresses prior to
the permanent morphological injury (Naumann et al.,
2008; Percival and Sheriffs, 2002). Under various
conditions and at various times, this technique of chlorophyll fluorescence
measurement can estimate the parameters of the actual photosynthetic efficiency
of the leaf (Maxwell and Johnson, 2000). It also measures
the potential maximum of the quantum efficiency of Fv/Fm
(Duraes et al., 2001).
Plant responses to stress conditions in this technique can be quantified through
the measurement of fluorescence sign from dark adapting leaves of a plant for
a certain period of time. As reported by Baker and Rosenqvist
(2004), when the leaf was subjected to immediate light, fluorescence increases
to a level of minimal fluorescence (Fo) which at this state the reaction
centre of PS II.
CRASSULACEAN ACID METABOLISM: AS DEFENSE MECHANISM FROM STRESS FOR EPIPHYTES
Plant reacts to numerous stresses imposed by the climate change such as high
and low concentrations of carbon dioxide, high light intensity and high temperature,
which all have effects on carbon fixation and anatomical pathway (Holtum
and Winter, 1999). There are three types of photosynthesis pathway, C3,
C4 and Crassulacean Acid Metabolism (CAM) and many dynamic defense systems exist
for epiphytics (Benzing, 1990). In fact, plants that grow
in arid land modify their physiological metabolic system via CAM (Grams
and Thiel, 2002). CAM is a CO2 concentrating mechanism that activates
the Phosphoenolpyruvate Carboxylase (PEPC) enzyme at night for detaining the
respiratory and atmospheric CO2. Physiologically, CAM preserves carbon
and water in plants that grow in surroundings with limited accessibility those
two resources either in short or long term basis (Borland
and Taybi, 2004). In CAM photosynthesis, plant use a metabolic strategy
in which during the cooler period at night, the stomata of the plants open to
allow the nocturnal uptake of carbon dioxide (CO2) and during the
day, stomata close to prevent the loss of water (Dodd et
al., 2002; Rut et al., 2008). Thus, by
this processes during day and night, it is considered that water stress could
be adapted by CAM plants through the reduction of water loss (Luttge,
2004).
There have been many studies on the availability of this pathway on plants
especially the epiphytes (Borland et al., 1998;
Herrera et al., 2000; Hsu
et al., 2006; Rut et al., 2008). A
study by Holtum and Winter (1999) found that the tropical
epiphytic and lithophytic ferns are the common plants that undergo CAM than
it is presently investigated. In this study, eventhough the Polypodium crassifolium
and Polypodium veitchii did not showed a strong CAM features, CAM activity
still happened and was shown in the increase of titratable acidity. This shows
that there is an occurrence of the CAM indirectly.
In a study by Wanek et al. (2002), there was
an activity of CAM cycle in all stages of development of Clusia species
which was the Clusia osaensis Hammel-ined., Clusia peninsulae
Hammel-ined. and Clusia valerii Standl. This study shows that from the
titratable protons and malic and citric acid there was a significant day-night
flux cycle. Therefore, they advocate that the accessibility of water and light
intensity created the appearance of CAM. Among epiphytes, the broad occasions
of CAM are not expected as an outcome from short, but probably frequent phases
of drought stress (Hsu et al., 2006). According
to Rabas and Martin (2003), plants that are succulent
will regularly uptake CO2 through CAM and additionally to the mechanism
of C3.
Stresses from ecological factors could alter the isotope composition of C13
in many expected ways, ultimately via the effects on the balance among stomatal
conductance and carboxylation (Robinson et al., 2000).
Leavitt and Long (1982) reported that light intensity
has an effect on the photosynthesis rate and in turn, it manipulates the composition
of the carbon isotopic of plant and stresses from water could also influence
stomata conductance and availability of water for photosynthesis. Epiphytes
might survive via CAM where this mechanism allows plants to defense themselves
through several stresses such as light and drought.
CONCLUSION Climate changes have been manipulating the ecological value of an ecosystem. Light and water plays an important role in epiphytes growth and physiological performances. Many of epiphytes growth and physiological parameters are being affected, including the decline in biomass, photochemical efficiency and many more. Plants especially epiphytes have many ways in adapting to stressful conditions, which in such cases, CAM are vital for epiphytes in surviving harsh environment. The fixation of CO2 at night and the closing of stomata during day are the essential mechanisms for the epiphytes. Through these adjustments on their physiological functions, epiphytes certainly have a higher percentage in survivability by preventing themselves from dying water loss and increasing temperature. Other mechanisms encountered by plants to defense themselves from such stresses should be further investigated to get better idea of other stress responses in plants. In order to obtain a larger picture on the underlying explanation on what other parameters that are affected by light and water stress, things such as leaf anatomy, leaf structure and biochemical components variations in epiphytes need to be explored in the future. ACKNOWLEDGMENT We would like to thank every person involved in this project and we are also most grateful for each individual that give valuable suggestion and manuscript review. Financial support from the Research University Grant Scheme (RUGS) No. 03/01/07/0035RU are gratefully acknowledged.
|
REFERENCES |
1: Ainuddin, N.A. and D.A.N. Najwa, 2009. Growth and physiological responses of Asplenium nidus to water stress. Asian J. Plant Sci., 8: 447-450. CrossRef | Direct Link |
2: Ainuddin, N.A., 2007. The forest canopy: Unexplored resources. Technology Park Malaysia. ISSN 1551-3426, Symbiosis, pp: 39-41.
3: Alves, P.L.C.A., A.C.N. Magalhaes and P.R. Barja, 2002. The phenomenon of photoinhibition of photosynthesis and its importance in reforestation. Bot. Rev., 68: 193-208. CrossRef |
4: Angelopoulos, K., B. Dichio and C. Xiloyannis, 1996. Inhibition of photosynthesis in olive trees (Olea europaea L.) during water stress and rewatering. J. Exp. Bot., 47: 1093-1100. CrossRef | Direct Link |
5: Barthlott, W., V. Schmit-Neuerburg, J. Nieder and S. Engwald, 2001. Diversity and abundance of vascular epiphytes: A comparison of secondary vegetation and primary montane rain forest in the Venezuelan Andes. Plant Ecol., 152: 145-156. Direct Link |
6: Benzing, D.H., 1990. Vascular Epiphytes: General Biology and Related Biota, Cambridge University Press, Cambridge, UK., ISBN: 0521266300, pp: 354.
7: Benzing, D.H., 1998. Vulnerabilities of tropical forests to climate change: The significance of resident epiphytes. Climatic Change, 39: 519-540. CrossRef |
8: Benzing, D.H., 2004. Vascular Epiphytes. In: Forest Canopies, Lowman, M.D. and H.B. Rinker (Eds.). Academic Press, New York, ISBN: 0-12-457553-6, pp: 175-211.
9: Black , M.J., C. Whittaker, S.A. Hosseini, R. Diaz-Chaveza, J. Woods and R.J. Murphy, 2011. Life cycle assessment and sustainability methodologies for assessing industrial crops, processes and end products. Ind. Crops Prod., 10.1016/j.indcrop.2010.12.002
10: Borland, A.M. and T. Taybi, 2004. Synchronization of metabolic processes in plants with Crassulacean acid metabolism. J. Exp. Bot., 55: 1255-1265. CrossRef |
11: Borland, A.M., L.I. Tecsi, R.C. Leegood and R.P. Walker, 1998. Inducibility of Crassulacean Acid Metabolism (CAM) in Clusia species; physiological/biochemical characterization and intercellular localization of carboxylation and decarboxylation processes in three species which exhibit different degrees of CAM. Planta, 205: 342-351. CrossRef |
12: Brouder, S.M. and J.J. Volenec, 2008. Impact of climate change on crop nutrient and water use efficiencies. Physiol. Plant, 133: 705-724. CrossRef |
13: Centritto, M., 2002. Interactive effects of climate change and water stress: implications for water-limited environments. First FAO-UCEA Technical Workshop of the Mediterranean Component of the Clim-Agri Project on Climate Change and Agriculture. Rome, Italy: FAO. http://www.fao.org/sd/climagrimed/pdf/ws01_33.pdf.
14: Cervantes, S.E., E.A. Graham and J.L. Andrade, 2005. Light microhabitats, growth and photosynthesis of an epiphytic bromeliad in a tropical dry forest. Plant Ecol., 179: 107-118. CrossRef | Direct Link |
15: Chang, M., C.M. Crowley and A.A. Nuruddin, 1995. Responses of herbaceous mimosa (Mimosa strigillosa), a new reclamation species, to cyclic moisture stress. Resources Conserv. Recycl., 13: 155-165. CrossRef | Direct Link |
16: Chang, M., A.A. Nuruddin, C.M. Crowley and M.D. MacPeak, 1997. Evapotranspiration of herbaceous mimosa (Mimosa strigillosa), a new drought-resistant species in the southeastern United States. Resour. Conserv. Recycling, 21: 175-184. CrossRef |
17: Chaves, M.M., J.P. Maroco and J.S. Pereira, 2003. Understanding plant responses to drought-from genes to the whole plant. Funct. Plant Biol., 30: 239-264. CrossRef | Direct Link |
18: Chmura, D.J., P.D. Anderson, G.T. Howe, C.A. Harrington and J.E. Halofsky et al., 2011. Forest responses to climate change in the northwestern United States: Ecophysiological foundations for adaptive management. For. Ecol. Manage., 261: 1121-1142. CrossRef |
19: Demmig-Adams, B. and WW. Adams III, 1992. Photoprotection and other responses of plants to high light stress. Annu. Rev. Plant Physiol., 43: 599-626. CrossRef | Direct Link |
20: Diaz, I.A., K.E. Sieving, M.E. Pena-Foxon, J. Larrain and J.J. Armesto, 2010. Epiphyte diversity and biomass loads of canopy emergent trees in Chilean temperate rain forests: A neglected functional component. For. Ecol. Manage., 259: 1490-1501. CrossRef |
21: Dodd, A.N., A.M. Borland, R.P. Haslam, H. Griffiths and K. Maxwell, 2002. Crassulacean acid metabolism: Plastic fantastic. J. Exp. Bot., 53: 569-580. CrossRef |
22: Du, N., W. Guo, X. Zhang and R. Wang, 2010. Morphological and physiological responses of Vitex negundo L. var. heterophylla (Franch.) Rehd. to drought stress. Acta Physiol. Plant., 32: 839-848. CrossRef | Direct Link |
23: Dubuisson, J.Y., H. Schneider and S. Hennequin, 2009. Epiphytism in ferns: Diversity and history. C R. Biol., 332: 120-128. PubMed |
24: Duraes, F.O.M., E.E.G. Gama, P.C. Magalhaes, I.E. Marriel and C.R. Casela et al., 2001. The usefulness of chlorophyll fluorescence in screening for disease resistance, water stress tolerance, aluminium toxicity tolerance and use efficiency in maize. Proceedings of the 17th Eastern and Southern Africa Regional Maize Conference, Feb. 11-15, CIMMYT, Mexico, DF, pp: 356-360.
25: Ellwood, M.D.F., D.T. Jones and W.A. Foster, 2002. Canopy ferns in lowland dipterocarp forest support a prolific abundance of ants, termites and other invertebrates. Biotropica, 34: 575-583. CrossRef | Direct Link |
26: Elsheery, N.I. and K.F. Cao, 2008. Gas exchange, chlorophyll fluorescence and osmotic adjustment in two mango cultivars under drought stress. Acta Physiol. Plant., 30: 769-777. CrossRef | Direct Link |
27: Farooq, M., A. Wahid, N. Kobayashi, D. Fujita and S.M.A. Basra, 2009. Plant drought stress: Effects, mechanisms and management. Agron. Sustain. Dev., 29: 185-212. CrossRef | Direct Link |
28: Fayle, T.M., A.Y.C. Chung, A.J. Dumbrell, P. Eggleton and W.A. Foster, 2009. The effect of rain forest canopy architecture on the distribution of epiphytic ferns (Asplenium spp.) in Sabah, Malaysia. Biotropica, 41: 676-681. CrossRef |
29: Flagella, Z., R.G. Campanile, M.C. Stoppelli, A. de Caro and N. di Fonzo, 1998. Drought tolerance of photosynthetic electron transport under CO2-enriched and normal air in cereal species. Physiol. Plant, 104: 753-759. CrossRef | Direct Link |
30: Flexas, J. and H. Medrano, 2002. Drought-inhibition of photosynthesis in C3 plants: Stomatal and non-stomatal limitations revisited. Ann. Bot., 89: 183-189. CrossRef | PubMed | Direct Link |
31: Freiberg, M. and S.M. Turton, 2007. Importance of drought on the distribution of the birds nest fern, Asplenium nidus, in the canopy of a lowland tropical rainforest in North-Eastern Australia. Aust. Ecol., 32: 70-76. CrossRef |
32: Freiberg, M., 2001. The influence of epiphyte cover on branch temperature in a tropical tree. Plant Ecol., 153: 241-250. CrossRef |
33: Grams, T.E.E. and S. Thiel, 2002. High light-induced switch from C3-photosynthesis to Crassulacean acid metabolism is mediated by UV-A/blue light. J. Exp. Bot., 53: 1475-1483. CrossRef |
34: He, J., C.W. Chee and C.J. Goh, 1996. Photoinhibition of Heliconia under natural tropical conditions: The importance of leaf orientation for light interception and leaf temperature. Plant Cell. Environ., 19: 1238-1248. CrossRef |
35: Hegland, S.J., A. Nielsen, A. Lazaro, A.L. Bjerknes and O. Totland, 2009. How does climate warming affect plant-pollinator interactions. Ecol. Lett., 12: 184-195. CrossRef |
36: Herrera, A., M.D. Fernandez and M.A. Taisma, 2000. Effects of drought on CAM and water relations in plants of Peperomia carnevalii. Ann. Bot., 86: 511-517. CrossRef |
37: Heschel, M.S., J.R. Stinchcombe, K.E. Holsinger and J. Schmitt, 2004. Natural selection on light response curve parameters in the herbaceous annual, Impatiens capensis. Oecologia, 139: 487-494. CrossRef |
38: Hietz, P. and O. Briones, 2001. Photosynthesis, chlorophyll fluorescence and within-canopy distribution of epiphytic ferns in a Mexican cloud forest. Plant Biol., 3: 279-287. CrossRef |
39: Hietz, P., J. Ausserer and G. Schindler, 2002. Growth, maturation and survival of epiphytic bromeliads in a Mexican humid montane forest. J. Trop. Ecol., 18: 177-191. CrossRef |
40: Holtum, J.A.M. and K. Winter, 1999. Degrees of crassulacean acid metabolism in tropical epiphytic and lithophytic ferns. Aust. J. Plant Physiol., 26: 749-757. CrossRef |
41: Hsu, C.C., T.C. Lin, W.L. Chiou, S.H. Lin, K.C. Lin and C.E. Martin, 2006. Canopy CO2 concentrations and crassulacean acid metabolism in Hoya carnosa in a subtropical rain forest in Taiwan: Consideration of CO2 availability and the evolution of CAM in epiphytes. Photosynthetica, 44: 130-135. CrossRef |
42: Huang, B., 2006. Cellular Membranes in Stress Sensing and Regulation of Plant Adaptation to Abiotic Stresses. In: Plant-Environment Interaction, 3rd Edn., Huang, B. (Ed.). Taylor and Francis Group, Boca Raton, pp: 1-25.
43: Humby, P.L. and D.G. Durnford, 2006. Photoacclimation: Physiological and Molecular Responses to Changes in Light Environments. In: Plant-Environment Interaction, 3rd Edn., Huang, B. (Ed.). Taylor and Francis Group, Boca Raton, pp: 69-99.
44: Khaled, S.A., 2010. Effect of watering regime on yield and its components of Triticum aestivum var. el-phateah L. Am. J. Plant Physiol., 5: 291-294. Direct Link |
45: Kramer, P.J. and T.T. Kozlowski, 1979. The Role of Plant Physiology. In: Physiology of Woody Plants, Kramer, P.J. and T.T. Kozlowski (Eds.). Academic Press, Inc., San Diego, pp: 1-12.
46: Krause, G.H. and E. Weis, 1991. Chlorophyll fluorescence and photosynthesis: The basics. Ann. Rev. Plant Physiol. Plant Mol. Biol., 42: 313-349. CrossRef | Direct Link |
47: Larcher, W., 2003. Gas Exchange in Plants. In: Physiological Ecology: Ecophysiology and Stress Physiology of Functional Groups, Larcher, W. (Ed.). 4th Edn., Springer-Verlag, Berlin, pp: 91-139.
48: Leavitt, S.W. and A. Long, 1982. Stable carbon isotopes as a potential supplemental tool in dendrochronology. Tree-Ring Bull., 42: 49-55. Direct Link |
49: Li, F., W. Bao, N. Wu and C. You, 2008. Growth, biomass partitioning and water-use efficiency of a leguminous shrub (Bauhinia faberi var. microphylla) in response to various water availabilities. New For., 36: 53-65. CrossRef |
50: Lombardini, L., 2006. Ecophysiology of Plants in Dry Environments. In: Dryland Ecohydrology, D`Odorico, P. and A. Porporato (Eds.). Springer, Dordrecht, The Netherlands, pp: 47-65.
51: Long, S.P., S. Humphries and P.G. Falkowski, 1994. Photoinhibition of photosynthesis in nature. Ann. Rev. Plant Physiol. Plant Mol. Biol., 45: 633-662. CrossRef |
52: Lorenzo, N., D.G. Mantuano and A. Mantovani, 2010. Comparative leaf ecophysiology and anatomy of seedlings, young and adult individuals of the epiphytic aroid Anthurium scandens (Aubl.) Engl. Environ. Exp. Bot., 68: 314-322. CrossRef |
53: Luttge, U., 2004. Ecophysiology of crassulacean acid metabolism (CAM). Ann. Bot., 93: 629-652. CrossRef | Direct Link |
54: Luvaha, E., G.W. Netondo and G. Ouma, 2008. Effect of water deficit on the physiological and morphological characteristics of mango (Mangifera indica) rootstock seedlings. Am. J. Plant Physiol., 3: 1-15. CrossRef | Direct Link |
55: Martin, C.E., R. Hsu and T.C. Lin, 2001. Comparative photosynthetic capacity of abaxial and adaxial leaf sides as related to exposure in two epiphytic ferns in a subtropical rainforest in Northeastern Taiwan. Am. Fern J., 99: 145-154. CrossRef | Direct Link |
56: Maxwell, K. and G.N. Johnson, 2000. Chlorophyll fluorescence-A practical guide. J. Exp. Bol., 51: 659-668. CrossRef | Direct Link |
57: Miyake, C., K. Amako, N. Shiraishi and T. Sugimoto, 2009. Acclimation of tobacco leaves to high light intensity drives the plastoquinone oxidation system-relationship among the fraction of open PS11 centers, non-photochemical quenching of Chl fluorescence and the maximum quantum yield of PS11 in the dark. Plant Cell Physiol., 50: 730-743. Direct Link |
58: Moreira, A.S.F.P., J.P. de Lemos Filho, G. Zotz and R.M. dos Santos Isaias, 2009. Anatomy and photosynthetic parameters of roots and leaves of two shade-adapted orchids, Dichaea cogniauxiana Shltr. and Epidendrum secundum Jacq. Flora, 204: 604-611. CrossRef |
59: Nadkarni, N.M., 1984. Epiphyte biomass and nutrient capital of a neotropical elfin forest. Biotropica, 16: 249-256. Direct Link |
60: Nadkarni, N.M., 1992. The conservation of epiphytes and their habitats: Summary of a discussion at the international symposium on the biology and conservation of epiphytes. Selbyana, 13: 140-142. Direct Link |
61: Nadkarni, N.M., G.G. Parker, H.B. Rinker and D.M. Jarzen, 2004. The Nature of Forest Canopy. In: Forest Canopies, Lowman, M.D. and H.B. Rinker (Eds.). 2nd Edn., Elsevier Academic Press, Burlington, pp: 3-10.
62: Naumann, J.C., D.R. Young and J.E. Anderson, 2008. Leaf chlorophyll fluorescence, reflectance, and physiological responseto freshwater and saltwater flooding in the evergreen shrub, Myrica cerifera. Environ. Exp. Bot., 63: 402-409. CrossRef |
63: Nuruddin, A.A. and M. Chang, 1999. Responses of herbaceous mimosa (Mimosa strigillosa), a new reclamation species to soil pH. Conserv. Recycl., 27: 287-298. CrossRef |
64: Nuruddin, A.A. and L. Tokiman, 2005. Air and soil temperature characteristics of two sizes forest gap in tropical forest. Asian J. Plant Sci., 4: 144-148. CrossRef | Direct Link |
65: Oberbauer, S.F., K. von Kleist, K.R.T. Whelan and S. Koptur, 1996. Effects of hurricane andrew on epiphyte communities within cypress domes of Everglades National Park. Ecology, 77: 964-967. Direct Link |
66: Ohashi, Y., N. Nakayama, H. Saneoka and K. Fujita, 2006. Effects of drought stress on photosynthetic gas exchange, chlorophyll fluorescence and stem diameter of soybean plants. Biol. Plant., 50: 138-141. CrossRef | Direct Link |
67: Otto, E.M., T. Janben, H.P. Kreier and H. Schneider, 2009. New insights into phylogeny of Pleopeltis and related Neotropical genera (Polypodiaceae, Polypodiopsida). Mol. Phylogenet. Evol., 53: 190-201. CrossRef |
68: Percival, G.C. and C.N. Sheriffs, 2002. Identification of drought-tolerant woody perennials using chlorophyll fluorescence. J. Arboricult., 28: 215-223. Direct Link |
69: Percival, G.C., 2005. The use of chlorophyll fluorescence to identify chemical and environmental stress in leaf tissue of three oak (Quercus) species. J. Arboric., 31: 215-227. Direct Link |
70: Powles, S.B., 1984. Photoinhibition of photosynthesis induced by visible light. Annu. Rev. Plant Physiol., 35: 15-44. CrossRef | Direct Link |
71: Rabas, A.R. and C.E. Martin, 2003. Movement of water from old to young leaves in three species of succulents. Ann. Bot., 92: 529-536. CrossRef | Direct Link |
72: Ramanjulu, S., N. Sreenivasalu, S.G. Kumar and C. Sudhakar, 1998. Photosinthetic characteristic in mulberry during water stress and rewatering. Photosynthetica, 35: 259-263. CrossRef | Direct Link |
73: Reinert, F., 1998. Epiphytes: Photosynthesis, Water Balance and Nutrients. In: Ecophysiological Strategies of Xerophytic and Amphibious Plants in the Neotropics. Scarano, F.R. and A.C. Franco (Eds.). Vol. 4. Series Oecologia Brasiliensis, PPGE-UFRJ, Rio de Janeiro, Brazil, pp: 87-108.
74: Roberts, A., A.M. Borland, K. Maxwell and H. Griffiths, 1998. Ecophysiology of the C3-CAM intermediate Clusia minor L. in Trinidad: Seasonal and short-term photosynthetic characteristics of sun and shade leaves. J. Exp. Bot., 49: 1563-1573. CrossRef | Direct Link |
75: Robinson, D., L.L. Handley, C.M. Scrimgeour, D.C. Gordon, B.P. Froster and R.P. Ellis, 2000. Using stable isotope natural abundances (γ15 N and γ 13 C) to integrate the stress responses of wild barley (Hordeum spontaneum C. Koch.) genotypes. J. Exp. Biol., 51: 41-50. CrossRef | Direct Link |
76: Rosdi, K. and A.N. Ainuddin, 2004. Microclimatic modification of three timber species stands on ex-tin mining land. Malaysia For., 67: 44-53.
77: Rut, G., J. Krupa, Z. Miszalski, A. Rzepka and I. Slesak, 2008. Crassulacean acid metabolism in the epiphytic fern Platycerium bifurcatum. Photosynthetica, 46: 156-160. CrossRef | Direct Link |
78: Sanusan, S., A. Polthanee, A. Audebert, S. Seripong and J.C. Mouret, 2010. Growth and yield of rice (Oryza sativa L.) as affected by cultivars, seeding depth and water deficits at vegetative stage. Asian J. Plant Sci., 9: 36-43. CrossRef | Direct Link |
79: Saifuddin, M., A.M.B.S. Hossain and O. Normaniza, 2010. Impacts of shading on flower formation and longevity, leaf chlorophyll and growth of Bougainville glabra. Asian J. Plant Sci., 9: 20-27. CrossRef | Direct Link |
80: Sarvikas, P., M. Hakala, E. Patsikka, T. Tyystjarvi and E. Tyystjarvi, 2006. Action spectrum of photoinhibition in leaves of wild type and npq1-2 and npq4-1 mutants of Arabidopsis thaliana. Plant Cell Physiol., 47: 391-400. CrossRef | PubMed |
81: Schafer, C. and U. Luttge, 1988. Effects of high irradiances on photosynthesis, growth and crassulacean acid metabolism in the epiphyte Kalanchoe unilora. Oecologia, 75: 567-574. CrossRef |
82: Schurr, U., A. Walter and U. Rascher, 2006. Functional dynamics of plant growth and photosynthesis-from steady-state to dynamics-from homogeneity to heterogeneity. Plant Cell Environ., 29: 340-352. CrossRef | Direct Link |
83: Siam, A.M.J., K.M. Radoglou, B. Noitsakis and P. Smiris, 2008. Physiological and growth responses of three Mediterranean oak species to different water availability regimes. J. Arid Environ., 72: 583-592. CrossRef |
84: Sinclair, T.R. and L.C. Purcell, 2005. Is a physiological perspective relevant in a genocentric age. J. Exp. Bot., 56: 2777-2782. CrossRef | Direct Link |
85: Singh, A. and O.N. Srivastava, 1985. Effect of light intensity on the growth of Azolla pinnata R. Brown at Ranchi, India. Hydrobiologia, 126: 49-52. CrossRef | Direct Link |
86: Skillman, J.B., M. Garcia, A. Virgo and K. Winter, 2005. Growth irradiance effects on photosynthesis and growth in two co-occurring shade-tolerant neotropical perennials of contrasting photosynthetic pathways. Am. J. Bot., 92: 1811-1819. Direct Link |
87: Song, C., M.B. Dickinson, L. Su, S. Zhang and D. Yaussey, 2010. Estimating average tree crown size using spatial information from Ikonos and Quick Bird images: Across-sensor and across-site comparisons. Remote Sens. Environ., 114: 1099-1107. CrossRef |
88: Stancato, G.C., P. Mazzafera and M.S. Buckeridge, 2001. Effect of a drought period on the mobilization of non-structural carbohydrates, photosynthetic efficiency and water status in an epiphytic orchid. Plant Physiol. Biochem., 39: 1009-1016. CrossRef |
89: Stancato, G.C., P. Mazzafera and M.S. Buckeridge, 2002. Effects of light stress on the growth of the epiphytic orchid Cattleya forbesii lindl. X Laelia tenebrosa rolfe. Rev. Bras. Bot., 25: 229-235. CrossRef | Direct Link |
90: Stuntz, S., U. Simon and G. Zotz, 2002. Rainforest air-conditioning: The moderating influence of epiphytes on the microclimate in tropical tree crowns. Int. J. Biometeorol., 46: 53-59. CrossRef | Direct Link |
91: Suzuki, N., L. Rizhsky, H. Liang, J. Shuman, V. Shulaev and R. Mittler, 2005. Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c. Plant Physiol., 139: 1313-1322. CrossRef | Direct Link |
92: Upadhyaya, H., S.K. Panda and B.K. Dutta, 2008. Variation of physiological and antioxidative responses in tea cultivars subjected to elevated water stress followed by rehydration recovery. Acta Physiol. Plant., 30: 457-468. CrossRef | Direct Link |
93: Valladares, F. and U. Niinemets, 2008. Shade tolerance, a key plant feature of complex nature and consequences. Annu. Rev. Ecol. Evol. Syst., 39: 237-257. CrossRef | Direct Link |
94: Von Caemmerer, S. and G.D. Farquhar, 1981. Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta, 153: 376-387. CrossRef | Direct Link |
95: Vurayai, R., V. Emongor and B. Moseki, 2011. Effect of water stress imposed at different growth and development stages on morphological traits and yield of bambara groundnuts (Vigna subterranea L. Verdc). Am. J. Plant Physiol., 6: 17-27. CrossRef | Direct Link |
96: Wanek, W., W. Huber, S.K. Arndt and M. Popp, 2002. Mode of photosynthesis during different life stages of hemiepiphytic Clusia species. Functional Plant Biol., 29: 725-732. Direct Link |
97: Wester, S., G. Mendieta-Leiva, L. Nauheimer, W. Wanek, H. Kreft and G. Zotz, 2011. Physiological diversity and biogeography of vascular epiphytes at Rio Changuinola, Panama. Flora, 206: 66-79. CrossRef |
98: Winter, K., B.J. Wallace, G.C. Stocker and Z. Roksandic, 1983. Crassulacean acid metabolism in Australian vascular epiphytes and some related species. Oecologia, 57: 129-141. CrossRef | Direct Link |
99: Xoconostle-Cazares, B., F.A. Ramirez-Ortega, L. Flores-Elenes and R. Ruiz-Medrano, 2010. Drought tolerance in crop plants Am. J. Plant Physiol., 5: 241-256. CrossRef |
100: Yu, Q., Y. Zhang, Y. Liu and P. Shi, 2004. Simulation of the stomatal conductance of winter wheat in response to light, temperature and CO2 changes. Ann. Bot., 93: 435-441. CrossRef | Direct Link |
101: Zotz, G. and P. Hietz, 2001. The physiological ecology of vascular epiphytes: Current knowledge, open questions. J. Exp. Bot., 62: 2067-2078. CrossRef | Direct Link |
102: Zotz, G. and M.Y. Bader, 2009. Epiphytic plants in a changing world-global: Change effects on vascular and non-vascular epiphytes. Prog. Bot., 70: 147-170. CrossRef |
103: Baker, N.R. and E. Rosenqvist, 2004. Applications of chlorophyll fluorescence can improve crop production strategies: An examination of future possibilities. J. Exp. Bot., 55: 1607-1621. CrossRef | Direct Link |
104: Flexas, J., J. Bota, F. Loreto, G. Cornic and T.D. Sharkey, 2004. Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol., 6: 269-279. CrossRef | Direct Link |
|
|
|
 |