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Review ArticlePlant Phenotypic Plasticity in Response toEnvironmental Factors

Loretta Gratani

Department of Environmental Biology Sapienza University of Rome Ple A Moro 5 00185 Rome Italy

Correspondence should be addressed to Loretta Gratani lorettagrataniuniroma1it

Received 8 December 2013 Revised 21 February 2014 Accepted 24 March 2014 Published 22 April 2014

Academic Editor Shoji Mano

Copyright copy 2014 Loretta Gratani This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Plants are exposed to heterogeneity in the environment where new stress factors (ie climate change land use change andinvasiveness) are introduced and where inter- and intraspecies differences may reflect resource limitation andor environmentalstress factors Phenotypic plasticity is considered one of the major means by which plants can cope with environmental factorvariability Nevertheless the extent to which phenotypic plasticity may facilitate survival under environmental condition changesstill remains largely unknown because results are sometimes controversial Thus it is important to identify plant functional traitsin which plasticity may play a determinant role in plant response to global change as well as on the ecological consequences at anecosystem level for the competition betweenwild and invasive species considering that specieswith a greater adaptive plasticitymaybe more likely to survive in novel environmental conditions In the near future it will be important to increase long-term studieson natural populations in order to understand plant response to environmental factor fluctuations including climate changeThereis the necessity to analyze variations at phenotypic and genetic levels for the same species and in particular for endemic and rarespecies because these could have drastic effects at an ecosystem level

1 Introduction

Literature on phenotypic plasticity has increased expandingfrom the initial focus on abiotic factors to that of biotic ones[1ndash3] and in recent years taking into consideration plantresponse to global climate change land use change and plantinvasiveness [4 5] (Table 1) Thus fundamental questionsfor evolutionary ecologists in a global change context arehow plant species will respond to these new scenarios andwhat mechanisms will be involved in the process [6 7]The understanding of phenotypic plasticity will be crucialfor predicting changes in species distribution communitycomposition and crop productivity under global changeconditions [8 9] Nevertheless the theme of phenotypicplasticity is complex and researchers do not always arrive atthe same conclusions and results are sometimes controversial

Phenotypic plasticity has been defined as a change inthe phenotype expressed by a single genotype in differentenvironments Bradshaw [10] recognized that phenotypicplasticity could itself be under genetic control and thereforesubjected to selective pressure Scheiner and Goodnight [11]

show that there is no reason to believe that the selection ofplastic and genetic variations need necessarily be coupledNevertheless a population could respond to an extremelyvariable environment by becoming both more plastic andmore genetically variable Literature suggests that phenotypicplasticity can evolve when there is a sufficient genetic vari-ation [12 13] due to genetic correlations with other traitsthat are under selection or to genetic drift [14] Since pheno-typic plasticity influences environmental tolerance differentplastic responses may contribute to differences in the rangeof environments that species inhabit [15] In particular theenvironment can induce changes in the individualrsquos behaviorat a morphological andor physiological level [16] and suchchanges may be crucial to survival in heterogeneous andvariable conditions [17ndash20] For certain morphological traitsphenotypic plasticity has been shown to reflect genetic corre-lations relatively well and traits belonging to the same suiteof characters are more highly genetically and phenotypicallycorrelated than traits from different suites [21] The selectionfor photosynthetic traits may often operate indirectly viacorrelation with other traits emphasizing the importance of

Hindawi Publishing CorporationAdvances in BotanyVolume 2014 Article ID 208747 17 pageshttpdxdoiorg1011552014208747

2 Advances in Botany

Table 1 List of thementioned species and corresponding references

Species ReferencesAbies alba [27]Acer pseudoplatanus [27]Acer saccharum [28]Betula papyrifera [28]Campanula thyrsoides [29]Coffea arabica [30 31]Corylus avellana [32ndash34]Crepis pygmaea subsp pygmaea [35]Cyclobalanopsis multinervis [36]Epilobium fleischeri [29]Fagus sylvatica [27 37ndash39]Fraxinus excelsior [32ndash34]Geum reptans [29]Glycine max [40]Glycine soja [40]Hedera helix [41]Ilex aquifolium [42]Isatis apennina [35]Lythrum salicaria [43 44]Myrtus communis [45]Ostrya virginiana [28]Phillyrea latifolia [41 46]Picea abies [27 47]Pinus halepensis [48ndash50]Pinus nigra [48]Pinus pinaster [48]Pinus pinea [48]Pinus sylvestris [48 51]Pinus uncinata [48]Pistacia lentiscus [46 52ndash55]Poa alpina [29]Populus tremula [32 33]Populus tremuloides [28]Quercus aliena var acutiserrata [36]Quercus coccifera [50 56]Quercus faginea [48]Quercus ilex [19 46 48 55 57ndash61]Quercus mongolica var crispula [62 63]Quercus petraea [48]Quercus pyrenaica [48]Quercus robur [48]Quercus suber [48]Rhododendron ponticum [42]Rubia peregrina [41 64]Ruscus aculeatus [41]Sesleria nitida [65]Shorea disticha [66]Shorea trapezifolia [66]Shorea worthingtonii [66]

Table 1 Continued

Species ReferencesSmilax aspera [41]Stellaria longipes [67]Taraxacum officinale [68]Tilia cordata [32ndash34]Viburnum tinus [41]

viewing the phenotype as an integrated function of growthmorphology life history and physiology [22] The timingof plant development can itself be plastic [23] and manyphenotypic responses to environmental stress factors may bethe consequence of growth reduction due to resource limi-tations [24 25] Differences among species and populationsmay reflect different selective pressures on plasticity differentlimitations acting upon the maximization of plasticity or acombination of both [26] The potential plastic response ofa given trait may be large but the observed plasticity maybe lowered by resource limitations or environmental stressfactors [14]

The particular way by which a genotype varies in itsexpression across a range of environments can be describedby a reaction norm which is genetically determined [69]The reaction norm for any specific trait of a genotype canbe visualized as a line or a curve on a two-dimensionalplot of the environmental value versus the phenotypic value(Figure 1) Phenotypic plasticity can be visualized as a changein the slope of the reaction norm between ancestral andderived populations or species [70 71] Such change hasbeen shown to occur in nature between species subjectedto different selection pressures [72ndash74] Plasticity is whatmakes the appearance of an environmentally induced novelphenotype possible and a process of selection on the expres-sion of such phenotype in a new environment may end upldquofixingrdquo (genetically assimilating) it by altering the shape ofthe reaction norm [75] Thus plasticity could facilitate theexpression of relatively well-adapted phenotypes under novelconditions (eg after migration to new geographical areas)improving the performance of the population and resulting inthe genetic assimilation of the trait in the new environmentThis has the potential to explain a variety of evolutionaryecological processes [14 75]

Indexes can facilitate comparison of different studies [7677] set of species or populations within a given speciesby considering experimental data in research on plasticity[19 56 57] However at least 17 different indexes have beenemployed as a measure of the phenotypic plasticity but canbe flawed and applied in different ways Most of them cannotbe standardized across traits or compared among differentspecies [78] complicating comparison among studies [3 79]Moreover measures of phenotypic plasticity are stronglyrelated to the context and may not be comparable acrossdifferent studies where different gradients andor specieshave been used [77] Since information about plasticity isstructured in a way that makes it difficult for quantitative andcomparative analysis Poorter et al [79] proposed a methodto fill this gap by building a large database which currently

Advances in Botany 3

000005010015020025030035040

000

050

100

150

200

250

000050100150200250300350400

Air temperature

LA (m

2)

LMA

(Kg m

minus2)

T1 T2 T3

Air temperatureT1 T2 T3


Q ilexP angustifolia

P lentiscusS aspera

Chlab

Figure 1 The reaction norm for any specific traits of a genotype can be visualized as a line on a plot of the environmental value versus thephenotypic value In this example the response of four evergreen species (Quercus ilex Phillyrea angustifolia Pistacia lentiscus and Smilaxaspera) in three different sites inside the Castelporziano Estate (Latium coast near Rome Italy) to a gradient of air temperature (T1 = 165∘CT2 = 172∘C and T3 = 219∘C) is shown [55] Lines represent the species and slope the phenotypic response Among the cooccurring speciesS aspera growing in the understory of the forest has a larger morphological than a physiological plasticity Q ilex is the species with thelargest morphological and physiological plasticity Leaf area (LA) leaf mass area (LMA) and chlorophyll a to b ratio (Chl ab) are shown

contains data on 1000 experiments and 800 species Thisapproach could serve as a benchmark for future phenotypingefforts as well as for modelling global change effects on bothwild species and crops [79]

2 Physiological Anatomical andMorphological Plasticity

Physiological morphological and anatomical plasticity mayhave a different role in plant adaption to environmentalchanges In particular plasticity for physiological and life-history traits may allow plants to grow and reproduce in

spatially or temporally variable environments [46 80] Phys-iological plasticity is more linked to an enhanced capacityto colonize gaps and open areas [81 82] because it ensuresadjustments of gas exchange in response to environmentalfactor changes in a short term This aspect evidences theimportance of physiological plasticity in plant acclimatizationto adverse environments where morphological and anatomi-cal plasticity play a secondary role [83] In fact plants growingin stress conditions tend to have a conservative leaf mor-phological pattern to avoid the production of structures tooexpensive to be sustained [84 85] Moreover morphologicalplasticity is more linked to an enhanced plant capacity to


grow in forest understories [37 82] by having an importantrole in resource acquisition [64 86]

3 Plant Response to Light

The heterogeneous light environment within a plant canopybrings about different stress factors for leaves in differentcanopy positions One of the expressions of plant phenotypicplasticity is the modification of leaf traits to the light gradient[87] and the reduced redfar red ratio [2] from the top tothe bottom of the tree canopy mainly during leaf formation[69] One of the main morphological traits which changesin response to light variations is the specific leaf area (SLAratio between leaf area and leaf dry mass) The plasticityof SLA implies the morphogenetic control of leaves whichtends to increase leaf area in the shade in order to interceptmore light while on the contrary there is a genetic orphysiological limitation to the total leaf volume as well asa resource limitation [88] SLA reflects leaf thickness [89]and the relative proportion of assimilatory conductive andmechanical tissues [90] In particular the increased totallamina thickness in sun leaves compared to shade leavesis mainly due to the greater palisade parenchyma spongyparenchyma and epidermal tissue thickness suggesting thatleaf internal structure may play an important role in lightcapture [91] In a research on leaf morphology of woodyangiospermsWylie [92] shows that as a result of shading leafthickness decreased on an average by 54 the volume of thepalisade parenchyma by 60 and the epidermal thickness by17 McClendon [93] and Gratani et al [46] showed a strongcorrelation between leaf thickness and the light-saturated rateof photosynthesis per unit of leaf area

Sun leaves with respect to shade leaves on an averagehave a higher photosynthetic rate on a leaf area basis whichis associated to a higher chlorophyll (Chl) ab ratio asignificantly lower light-harvesting Chl ab protein (LHCII)a lower stacking degree of thylakoids [94 95] and a highernitrogen (N) content per unit of leaf area [46 96 97] sinceapproximately half of N is invested in the photosyntheticproteins [96] Hirose and Werger [98] suggest that N varieswith light availability in plant canopies in such a way asto optimize the daily canopy photosynthesis Thus the Ninvestment is related to light in that more N is allocated tocarboxylation in sun leaves and to light harvesting in shadeleaves with variations in the photosynthetic capacity [99](Figure 2) The photosynthetic capacity and N content aregenerally both higher in leaves under high light conditions[96 98 100] The higher photosynthetic rates of sun leavesare supported by higher stomatal conductance and stomataldensity to maximize CO

2absorption [101] On the contrary

leaf trait adjustments to low light increase the capacity oflight absorption at the expense of the photosynthetic capacityminimizing carbon loss through respiration [96]

Changes in the efficiency of light interception and inthe costs for light harvesting along the light gradient fromthe top to the bottom of the plant canopy are the majormeans by which an efficient light harvesting is achievedIn particular at shoot scale foliage inclination angle and

foliage spatial aggregation are themajor determinants of lightharvesting while at the canopy scale branching frequencyfoliage distribution and biomass allocation to leaves modifylight harvesting significantly [102] Intracanopy plasticityhas important impacts on many aspects of tree biologypotentially contributing to the whole-canopy performancevia effects of light penetration through the canopy and onthe energy carbon and water balance of the individual leaves[97 103 104] Plasticity within the same plant in a temporaryheterogeneous environment may play an adaptive role instrong seasonal climates such as the Mediterranean climate[20]

Moreover leaf trait variations in response to the lightgradient within the canopy change in different species andforest types [105ndash108] In forests with dense foliage the upperlayers absorb the majority of the incoming radiation Inbroadleaf and conifer forests of the temperate zone on anaverage 3ndash10 of the incident photon flux density (PFD)penetrates the tree canopy [69] Gratani and Foti [109] showthat SLA increases on an average by 21 from the dominanttree layer of a mixed deciduous broadleaf forest to thedominated layer in response to a decrease in the light levelThe same trend is measured from the dominant tree layer of aMediterranean evergreen forest to the dominated layer by the54 SLA increase associated with a 95 lower chlorophyllab ratio and 86 lower photosynthetic rate [110] Mendeset al [45] analyzed the large morphological and anatomicalleaf trait variations to different light conditions for Myrtuscommunis an evergreen sclerophyllous species which growsin Mediterranean areas from open clearings to understorieswith a 26 increase of the SLA from sun to shade conditionsNevertheless taxonomically different species cooccurringin the same habitat often share common morphologicaland physiological traits reflecting a convergent evolution inresponse to environmental factors [111] The large plasticityin the structure of the mesophyll in concert with othertraits seems to enable these species to cope with differentenvironmental regimes (ie Mediterranean type climate)attaining a wider habitats range [111]

4 Shade Tolerance

Shade tolerance is one of the most important ecologicalfactors with respect to interspecific competition among foresttrees of the temperate climate zone The shade toleranceof a given plant is defined as the minimum light underwhich a plant can survive however only a fraction of plantscan reproduce under these conditions Thus a biologicaldefinition of shade tolerance must consider the whole lifecycle of the plant from early survival and growth to repro-duction [112] In general sun and shade leaves are thinner intolerant species than in intolerant species [113] The overalltrend in literature suggests that early successional and lightdemanding species are more plastic than late-successionaland shade-tolerant species [114ndash116] Nevertheless there isincreasing evidence that indicates that adjustments are notnecessarily related to the successional status of the species[117 118] (Table 2)


000510152025303540

Sun leaves Shade leaves

0020406080

100120140

00051015202530

Morphological traitsDM 016 011 014LA 050 038 032

LMA 041 028 024SLA 041 029 024

Mean value 037 026 023

Anatomical traitsLeaf thickness 041 030 020

Palisade parenchyma thickness 047 037 028Spongy parenchyma thickness 041 025 012

Adaxial cuticle thickness 019 031 028Abaxial cuticle thickness 031 033 027

Adaxial epidermis thickness 027 028 018Abaxial epidermis thickness 014 005 001

Stomatal density 028 020 008Guard cell length 008 012 000


Biochemical traits015 012 012035 040 047

ChlCar 032 032 042016 015 008044 043 051


Physiological traits096 097 095067 056 059

WUE 086 092 085PNUE 092 095 093

014 012 010Mean value 071 070 069

Plasticity index Q ilex P latifolia P lentiscus

Q ilexP latifolia P lentiscus

Q ilex P latifolia P lentiscus


PNU

E (120583

mol

gminus1

sminus1)

Chlab

Chl a + b

Chl ab

N

ChlN

PNgs

Ψm

N (m

g gminus1)

Figure 2 Leaf trait variations in response to the light gradient from the top to the bottom of the canopy of three evergreen shrubs (Pistacialentiscus Phillyrea latifolia and Quercus ilex) cooccurring in the Mediterranean maquis [46] All the considered species have significantlythicker sun leaves compared to shade leaves (on an average 045 times) due to the palisade parenchyma (61mean value) spongy parenchyma(38 mean value) and the adaxial cuticle (36 mean value) thickness The higher leaf consistency (ie higher leaf mass area LMA) of sunleaves can be used as ameasure of investment per unit of leaf area in conditions of full sunMoreover shade leaves have a lower chlorophyll a tob ratio (Chl ab) (13mean of the considered species) due to the higher chlorophyll b content (89mean of the considered species) since it isusually themain component of the LHCP (light-harvesting protein) which is higher in the shade conditions Sun leaves allocate on an average16 higher nitrogen (N) content than shade leaves reflecting an increase in carboxylating enzymes (RUBISCO) and proteins responsible forthe photosynthetic electron transport in full sun The phenotypic plasticity of the considered species is higher for leaf physiological traits(086) and among them net photosynthesis (PN) and the photosynthetic nitrogen use efficiency (PNUE) have a larger plasticity (096 and093 resp) The largest phenotypic plasticity of Q ilex (041) among the cooccurring species (036 mean value) reflects its wider ecologicaldistribution area Leaf dry mass (DM) leaf area (LA) specific leaf area (SLA) total chlorophyll a + b content (Chl a +b) chlorophyll tocarotenoid ratio (ChlCar) chlorophyll to nitrogen ratio (ChlN) net photosynthesis (PN) stomatal conductance (G

119904

) water use efficiency(WUE) and leaf water potential at midday (Ψ

119898

) are shown

Numerous studies focus on acclimation of the photosyn-thetic properties of plant species to different light conditionsnevertheless results sometime disagree For example Coffeaarabica is an evergreen perennial tree from the African forestunderstory which is considered an obligatory shade speciesMatos et al [30] show that plasticity of physiological andbiochemical traits in C arabica is more important for accli-mation to intracanopy light variations than morphological

and anatomical trait plasticity Nevertheless Araujo et al [31]show that the apparent inability of C arabica shade leaves tooptimize carbon gain under low light and the successful abil-ity of sun leaves to prevent photoinhibition of photosynthesisunder high light conditions are consistent with the findingsthat it performs well at full sun exposure Niinemets et al[32] showed that in temperate deciduous forests species differin their shade tolerance with Corylus avellana having the


Table 2 Phenotypic plasticity of morphological and physiological leaf traits for the mentioned shade-tolerant shade-intolerant andintermediate species and corresponding references

Species Morphological plasticity Physiological plasticity References

Shade-tolerant

Fagus sylvatica 046 039 [37]Acer pseudoplatanus 031 034 [27]

Ilex aquifolium 054 024 [119]Quercus ilex 033 05 [46]

Acer saccharum 03 03 [108]

Intermediate

Acer rubrum 041 026 [108]Betula alleghaniensis 029 032 [108]

Picea abies 013 022 [27]Quercus rubra 041 027 [108]

Shade-intolerantQuercus robur 024 06 [37]Cistus incanus 018 038 [120]Abies procera 029 032 [108]

largest tolerance followed byTilia cordata Fraxinus excelsiorand Populus tremula [33 34] Wyka et al [27] by comparingseedlings of two conifers (the shade-tolerant Abies alba andthe moderately shade-tolerant Picea abies) and two decidu-ous angiosperms (the highly shade-tolerant Fagus sylvaticaand the moderately shade-tolerant Acer pseudoplatanus) intwo-year studies tested the hypothesis that light-inducedplasticity of physiological and anatomical traits was lowerin highly shade-tolerant species than in moderate shade-tolerant ones The authors concluded that shade tolerancewas not a consistent predictor of anatomical plasticity andthat for many traits differences between the light treatmentswere magnified in the second year showing that anatomicaland physiological adjustment to shade is a long-term processValladares et al [37] investigated phenotypic plasticity oftwo species differing in their shade tolerance (the mostshade-tolerant Fagus sylvatica and the more light-demandingQuercus robur) hypothizing a lower plasticity in the speciesof deep shade than in the more light-demanding speciesaccording to comparative studies of others woody plants [5685 105] Moreover the authors suggested that an alternativehypothesis was also feasible (ie that shade tolerance can beachieved by enhanced plasticity) as argued previously for thesame two species [121]The results showed amean phenotypicplasticity similar to the two species (Q robur and F sylvatica)due to the fact that while Q robur has a higher physiologicalplasticity F sylvatica has a higher morphological plasticitywith one group of traits counteracting the effect of the othergroup on the mean plasticity index [37]

Differences in forest structure determine changes in thelight gradient and consequently in the presence of shade-tolerant and intolerant species In particular the deciduousforests may consist of an upper layer with shade-intoleranttree species and a lower layer with shade-tolerant tree species[32] while in mixed forests deciduous and evergreen specieswith contrasting ecological potentials can occupy differentlayers [122] Poorter et al [48] analyzed shade tolerancein tree species growing in some forests of ContinentalSpain showing that the wider canopy lower height andflat leaves of the Fagaceae (Quercus faginea Quercus ilex

Quercus petraea Quercus pyrenaica Quercus robur andQuercus suber) enhanced their shade tolerance compared toPinaceae (Pinus halepensis Pinus nigra Pinus pinaster Pinuspinea Pinus sylvestris and Pinus uncinata) On the contraryresistance to fire [123] drought tolerance [124] and allometricplasticity of the shade-intolerant pines increased their rapidoccupation of open spaces [125] and could be relevant toexplain species ecological dominance The shade-intolerantPopulus tremuloides and Betula papyrifera common speciesof the broad ecotone between the boreal and cold-temperateforests of central and eastern North America possess traitsthat maximize whole plant carbon dioxide (CO

2) exchange

leading to long-term growth and survival disadvantages invery low light while the shade-tolerant Acer saccharumand Ostrya virginiana minimize CO

2losses in low light

at the expense of maximizing CO2gains in high light

[28] The same authors conclude that the shade-intolerantspecies have a larger plasticity than the shade-tolerant speciesKe and Werger [36] showed that the deciduous Quercusaliena var acutiserrata is a gap-dependent species havingadvantage over the evergreen Cyclobalanopsis multinervis inforest gaps and clearings by the greater morphological andphysiological plasticity of seedlings The ability to acclimateto contrasting light environments is particularly importantfor tropical woody species because tree seedlings grown inthe forest understory are prone to experience photoinhibi-tion under an increased light level through formation of agap [126] High irradiance in tropical latitudes can causechronic photoinhibition through impairment of photosystemII (PSII) reaction centres in the leaves of plants that haveexperienced gap openings [127 128] Nevertheless speciesvary in their shade tolerance to the increased light after agap creation For example in deciduous broadleaf forests ofnorthern Japan Quercus mongolica var crispula is a gap-dependent species because its seedlings could survive atmost a dozen years under a closed canopy even though theycan germinate in low light environments [62 63] Koikeet al [129] in a research on early successional species gapphase species mid-successional species and late successionalspecies showed that acclimation potential of the species was


expressed by their plasticity which was closely linked to thephotosynthetic capability [130]

Despite the assumption that shade leaves develop inresponse to reduced light other factors may also be involvedsuch as temperature and water stress [113] It has beenhypothesized that plants cannot tolerate combined shade anddrought as a result of a morphological trade-off [49 131]Nevertheless Sack et al [41] investigated six species (Phillyrealatifolia Viburnum tinus Rubia peregrina Ruscus aculeatusHedera helix and Smilax aspera) that cope with strongsummer drought in the understory of mixed Quercus forestsin southern Spain All the species persisted in the shade(ca 3 daylight) and converged in features that conferredtolerance to shade plus drought by reducing the demandfor resources In particular demand for water was reducedthrough amoderate-to-high below-groundmass fraction andlow-to-moderate SLA while demand for both low irradianceand water was reduced through a low-to-moderate leaf Ncontent and leaves with a long life span On an average SLAis the trait most strongly correlated to shade tolerance [132]

Generalist species that grow in a range of moistureand light conditions within a forest on an average have alarger morphological plasticity than specialist species [66]In particular the more generalist Shorea disticha occurringonmost sites within the evergreen forests and extending overmost areas of the South and Southeast Asia has a greaterplasticity than Shorea trapezifolia which is restricted to thelower slopes of the valley within the forest and Shoreaworthingtonii which is restricted to the ridge-tops

5 Ecotypes

Long-term selection can lead to the development of mor-phological and physiological adaptations to the local envi-ronment generating ecotypic differentiation in functionaltraits [133 134] Genotypes adapted to local environmentalconditions are referred to as ecotypes [135] When environ-ments within the distribution area of a species differ it isunlikely that any single phenotype confers high fitness in allsituations The distinction between phenotypic plasticity andlocal adaptation of an ecotype is based primarily upon geneticanalysis and transplantation experiments [52] In particularspatial genetic differentiation along climatic gradients hasbeen documented for many species [136ndash138] as well as forecotype formations [52 136 138] For example ecotypesof Pinus taeda [139] Picea abies [47] Pinus sylvestris [51]Fagus sylvatica [38 39] and Quercus coccifera [50] haveadaptive features which are probably driven by the climateof the locality from which they originate Moreover specieswith extensive geographical ranges have the potential toexhibit a larger intraspecific variation in physiology mor-phology phenology and growth rate [140] Gratani et al[19] Bonito et al [57] and Pesoli et al [58] comparedplant and leaf trait plasticity in Quercus ilex seedlings fromdifferent provenances in Italy and grown in a commongarden (Figure 3) Quercus ilex is a deep-rooted evergreenspecies widely distributed in the Mediterranean Basin [59]extending 6000 km longitudinally from Morocco to France

This species seems to be limited to the southern range due toincreased summer drought and in altitude (it is distributedfrom the sea level to 1100m asl) by factors associatedwith low temperature [60] The results show that seedlingsfrom the more xeric provenance have a higher tolerance todrought stress by a higher leaf mass area (LMA) limitingtranspiration and a higher stomata sensitivity to changes inwater potential allowing a higher relative leaf water content(RWC) On the contrary the reduced leaf area appears to bethe best adaptive trait in response to winter cold stress at thenorthern limit of the distribution area while the largest shootproduction reflects the more favorable climatic conditions atthe centre of the distribution area Thus while the favorableenvironmental conditions increase the phenotypic plasticityof Q ilex morphological and physiological traits the lessfavorable conditions (ie cold and drought stress) allowspecialization Michaud et al [61] observed a homogeneousgenetic structure of Q ilex in the Mediterranean region withonly slight geographic variations due to isolation (ie NorthAfrica and Sicily) which supports the hypothesis that Q ilexcorresponds to a single genetic entity According to thesehypotheses Balaguer et al [56] show that phenotypic plastic-ity varies across the geographical range of Quercus cocciferaand among populations suggesting that Q coccifera ecotypicdifferentiation accounts for its occurrence in contrastinghabitats Wen et al [40] studied the origin and evolutionof cultivated soybean They investigated genetic diversitygeographic differentiation and genetic relationship amonggeographic ecotypes of cultivated (Glycine max) and wild(G soja) soybeans growing in South-Central China South-West China and South China The results showed that thewild accessions had relatively small genetic distances with allcultivated accessions and the Middle and Lower Changjiangvalleys wild ecotypes were smaller compared to other wildones including their local wild counterparts Thereforeit is inferred that the wild ancestors in southern Chinaespecially those from Middle and Lower Changjiang valleysmight be the common ancestors of all cultivated soybeansNevertheless exploitation of new habitats may be associatedwith the loss of plasticity and evolution of specialization [16]Adaptation of species to geographic environmental variationsoften depends on genetic variations among seed sources[19 141] Nahum et al [52] showed that Pistacia lentiscusecotypes growing in diverse habitats along a climatic gradientin Israel do not have any pattern of ecologically relatedgenetic differentiation and morphological and physiologicaldifferences are probably due to phenotypic plasticity Thusadaptive plasticity can expand environmental tolerance con-tributing to a wide distribution [53] of P lentiscus around theMediterranean region [52 54] Emery et al [67] show thatecotypes of Stellaria longipes an herbaceous perennial speciesgrowing along an altitudinal gradient on Plateau Mountain(Alberta) from the alpine tundra (ie higher altitude) has alower plasticity than the ecotype from the prairie (ie loweraltitude)

To accurately determine patterns of plasticity and inves-tigate the ecological and evolutionary implications it isimportant to better understand the environmental context inwhich phenotypes are expressed [2]


Plasticity index A

A

B

B

C

C

Physiological traits

073 073 067073 079 077

E 084 084 082WUE 088 087 082

089 093 093

Morphological traits

LA 024 027 033DM 019 040 032SLA 015 027 015LMA 015 027 015LTD 021 032 015


PN

gs

Ψpd

0

50

100

150

200

0

25

50

75

100

0

50

100

150

200

0

25

50

75

100

0

50

100

150

200

0

25

50

75

100

T(∘

C)T

(∘C)

T(∘

C)

T

T

T

A

BC

R(m

m)

R(m

m)

R(m

m)

R

R

R

J F M A M J J A S O N D



Figure 3 Physiologicalmorphological and anatomical leaf trait variations ofQuercus ilex ecotypes fromdifferent provenances in Italy grownfrom seeds collected in the native environments Seedlings from the more xeric provenance (Frassanito 40∘131015840N 18∘261015840E at sea level site C)have a larger tolerance to drought by a larger leaf mass area (LMA) and leaf tissue density (LTD) and a higher stomatal sensitivity to changesin leaf water potential at predawn (Ψpd) contributing to a better water use efficiency (WUE) than the other seedlings [58] In particular thereduced leaf area (LA) appears to be the best adaptive trait in response to the winter stress at the northern distribution limit (Nago 45∘551015840N10∘531015840E 260m asl site A) while the larger shoot and leaves production of Castelporziano seedlings reflects the favorable climatic conditionof this locality (41∘451015840N 12∘261015840E at sea level site B) The favorable environmental conditions at Castelporziano are expressed throughout alarger phenotypic plasticity while the cold stress at Nago and the drought stress at Frassanito allow specializationMoreoverQ ilex phenotypicplasticity is larger for physiological than for morphological and anatomical traits due to the capability of this species to grow in full sun aswell as in shade conditions and colonize successfully new areas after fire by vegetative regeneration [142] Frassanito shrubs by their largertolerance to high temperature and limited water availability might have an advantage in response to the forecasted increase of air temperatureand drought in the Mediterranean Basin Net photosynthesis (119875

119873

) stomatal conductance (119892119904

) leaf transpiration (E) and specific leaf area(SLA) are shown


6 High Altitude Mountain Plants

The impact of global warming on terrestrial ecosystemshas been shown to be greater in arctic tundra and highmountain regions than in low latitude areas [143] In par-ticular the projected rate of global warming in mountainecosystems is expected to be up to three times higherthan the global average rate of warming recorded duringthe 20th century [144] The biodiversity scenarios for the21st century forecasts the reduction of alpine habitat andloss of many European high-mountain plants [145 146]Dirnbock et al [147] hypothesize a rapid increase in plantspecies extinction risk Moreover species-specific reductionin fitness and diversity could change community dynamicsby altering species competitive abilities Recent studies [35]indicate substantial adaptive potential as reflected by highheritability estimates for traits likely to be selected [148]Nevertheless there is little information on the adaptivepotential in environments that are particularly threatened byclimate change such as high altitude mountain areas One ofthe predicted consequences of global climate change is themovement of plant species to higher elevations and latitudesas the climate to which they are adapted is displaced [149]A drastic decrease of the distribution area or even extinctionof plant species can be the consequence of migration pro-cesses towards higher altitudes Rates and patterns of thesedynamics will be highly dependent on the habitat preferenceof a particular species and on its functional traits [150]Steep environmental gradients and patchy distribution ofhabitats lead to small size and spatial isolation of populationsand restrict gene flow [29] It has been hypothesized thatplant species populations may persist in their current areasand withstand environmental changes if they have a largeadaptive capacity [151] Gratani et al [35] in a comparativestudy on two populations of Crepis pygmaea subsp pygmaeaand Isatis apennina growing at different altitudes on theGran Sasso massif (Italy) addressed the question whetherplasticity of morphological and physiological traits couldbe indicative of their future adaptive potential to surviveglobal warming The results underline that C pygmaea hasa significantly higher plasticity of both physiological andmorphological traits than I apenninaThus the hypothesizedair temperature increase could drive C pygmaea and Iapennina to higher altitudes in the Gran Sasso massif withC pygmaea being favored by the highest plasticity Studieson Sesleria nitida a perennial herbaceous species growingat different altitudes along a narrow altitudinal gradient inthe Central Apennines (Monte Terminillo Italy) show thatthe lower photosynthetic rates at the higher elevation arejustified by the stronger wind action and the lower soil watercontent of this site while the lower SLA (ie the highestleaf mass area LMA) contributes to limit leaf transpiration[65] The extent to which SLA is phenotypically plastic orgenetically fixed has important implications for the survivalof populations under environmental condition changes [152]Moreover the results show a larger plasticity for physiologicalthan for morphological and anatomical leaf traits of S nitidathe first being more useful under strong stress conditionswhich change in a short-term (Table 3) The relatively large

phenotypic plasticity of S nitida reflects its capability tomaintain function under different environmental stress con-ditions and sustain the air temperature increase through apotential shift toward higher elevations Stocklin et al [29]studied the consequences for the alpine landscape due to theevolutionary processes in four typical alpine plant species(Epilobium fleischeri Geum reptans Campanula thyrsoidesand Poa alpina) The within-population genetic diversity ofthe four species is large and mostly not related to altitudeand population size Nevertheless genetic differentiationamong populations is strongly increased with distance thussuggesting considerable genetic drift among populations ofalpine plants Phenotypic variability is shaped by adaptiveas well as by random evolutionary processes and plasticresponses to growth conditions seem to be crucial for survivalof plants in the alpine landscape

7 Competition between Invasive andNative Species

The increase of air temperature and carbon dioxide (CO2)

concentration over recent decades has determined novelenvironmental conditions [153] which might act as a potentagent of natural selection among species favoring morephenotypically plastic species [154] and resulting in a com-petition between invasive over cooccurring native species[153 155] The phenotypic plasticity of cooccurring nativeand invasive species in the broadleaf forest developing inthe Natural Reserve Siro Negri (45∘1210158403910158401015840N 9∘310158402610158401015840 E Italy)attests to the considered species responsiveness to lightvariations Q robur (a native species) and R pseudoacacia(an invasive species) have a similar physiological plasticityNevertheless the significantly higher morphological andanatomical plasticity of R pseudoacacia than Q robur con-firms its past capability of colonizing the forest and thengrowing successfully into both the dominant and dominatedlayers (data Catoni et al not published)

Introduced species frequently exhibit little genetic varia-tions in the new environment due to the genetic bottleneckand drift experienced by the small founding populations[156] Even with genetic variations local adaptation maynot arise if selection is weak or unpredictable or if consid-erable gene flow occurs among populations [157] Despitethese limitations local adaptation often contributes to thesuccess of plants introduced in the new environments [158ndash162] In agreement with this hypothesis Niinemets et al[42] show higher plasticity of the invasive Rhododendronponticum in respect to the native Ilex aquifolium in highlight environments by its higher N investment in lightharvesting and in photosynthetic machinery allowing theproduction of more leaf area with equal photosynthetic andlight-harvesting characteristics The high phenotypic plas-ticity in photoprotective strategies and performance of theinvasive Taraxacum officinale enhances its competitive abilityin alpine environments [68] considering that light intensityis one of the most changing conditions along altitudinalgradientsTheT officinale plants fromhigher altitudes wherelight conditions are more variable possess greater plasticity


Table 3 Plasticity index (PI) of morphological and physiological leaf traits for Crepis pygmaea subsp pygmaea Isatis apennina [35] andSesleria nitida [65]

Morphological traits PI Physiological traits PI

Crepis pygmaea subsp pygmaea

LA 020 119875119873

063DM 039 119892

119904

065LMA 038 119877 053LTD 042 WUE 036

Ψ119898

073Chl 031RWC 021119875119892

055Mean value 035 Mean value 050

Isatis apennina

LA 025 119875119873

042DM 032 119892

119904

048LMA 030 119877 072LTD 033 WUE 026

Ψ119898

048Chl 017RWC 015119875119892


Sesleria nitida

Leaf thickness 024 119875119873

018Height of the major lateral vascular bundle 030 119892

119904

039Width of the major lateral vascular bundle 024 E 033Height of the major lateral vascular bundle 039 119877 037

Width of the central vascular bundle 032 119877119875119873

047Diameter of the xylematic vessels 018

Mesophyll cell density 019Thickness of the upper sclerenchyma layers 031

Total surface area of bulliform cells 007Adaxial stomatal length 006

Abaxial epidermis thickness 006Adaxial epidermis thickness 007

Leaf mass area 015Leaf width 021Mean value 020 Mean value 035

Leaf area (LA) leaf dry mass (DM) leaf mass area (LMA) leaf tissue density (LTD) net photosynthesis (119875119873) stomatal conductance (119892

119904) leaf respiration (119877)

water use efficiency (WUE) leaf water potential at midday (Ψ119898) total chlorophyll content (Chl) relative water content (RWC) gross photosynthesis (119875

119892) leaf

transpiration (E) ratio between leaf respiration and net photosynthesis (119877119875119873) are shown

than plants from lower altitudes suggesting that plasticity inecophysiological traits will be one of the main strategies tocolonize environments with variable light conditions Highadaptability can be due either to the adaptive strategy tocope with resource fluctuations in the native region [163164] or to a rapid evolution in novel environments aftercolonization [165] Davidson et al [153] show that invasivespecies are more plastic in their response to greater resourceavailability than noninvasives but this plasticity is onlysometimes associated with a fitness benefit and noninvasivespecies maintain greater fitness homoeostasis when compar-ing growth between low and average resource availabilitiesFunk [166] investigated the plastic responses of five invasive-native pairs in low resource environments of the Hawaiian

Islands and found that the maximum photosynthetic rateand the organic leaf N concentration were positively relatedto the invasive species fitness in response to N availabilitySince adaptive plasticity may allow certain species to colonizeenvironmentally diverse areas without the lag time requiredfor local adaptation it may enhance their invasiveness andrapid geographic spread contributing to the displacement ofnative species [4]

Nevertheless despite the effort over the last decadesthe evolutionary mechanisms leading to invasiveness remainunclear [167] Molina-Montenegro et al [68] show thatinvasive species have significantly greater plasticity thannative species On the contrary Drenovsky et al [168]suggest that native and invasive species may converge on


functionally similar traits demonstrating comparable abilityto respond to change in resource availability In additionGodoy et al [169] show that despite reasonable argumentsin favour of linking phenotypic plasticity to plant invasionno general pattern between phenotypic plasticity and inva-siveness emerged DeWalt et al [170] tested the hypothesisthat the tropical shrub Clidemia hirta is more abundantin the introduced (Hawaiian Islands) than in the nativerange (Costa Rica) because of genetic differences in resourceacquisition allocation and phenotypic plasticity betweennative and introduced genotypes Nevertheless the resultsunderline the fact that genetic shifts in resource use resourceallocation or plasticity do not contribute to differences inhabitat distribution and abundance An increased plasticitymay not increase fitness (nonadaptive plasticity) or may evendecrease it and the correlation among different plant traitsmay confers invasiveness by reducing the cost of maladaptiveandor nonadaptive plastic traits [14 171] Bastlova andKvet [43] evidenced the phenotypic variability in nativepopulations of Lythrum salicaria a Eurasian species whichsuccessfully invaded north American wetlands competingwith native plant species [44] The authors showed thatplants originating from more southern Eurasian localitieswere more similar to the invasive plants in North Americathan to plants fromnorthern Eurasian localities Variability ingrowth characteristics across the north-south gradient withinthe native range could result from long-term adaptationto prevailing environmental conditions particularly day-length Moreover variability for some growth characteristics(ie dry weight and number of lateral branches root dryweight) both between and within Eurasian populationsindicates a plastic growth response to the local environmentalconditions

8 Conclusions

Overall climate change has been shown to affect abundanceand distribution of plant species as well as plant communitycomposition [172 173] Recent studies indicate that underrapid climate change phenotypic plasticity rather than geneticdiversity is likely to play a crucial role in allowing plantsto persist in their environments [174] Different responsesto climate occur not only between populations throughouta species range but also between cooccurring individualswithin a population [149] Nevertheless studies of geneticstructure based on enzyme polymorphism in populations offorest trees have shown significant levels of intrapopulationvariability and little interpopulation differentiation [61 175176] Increased summer drought will exacerbate the regen-eration of many tree species at their lower latitudinal andaltitudinal distribution limits and the introduction of moredrought tolerant species in vulnerable habitats is consideredto facilitate forest persistence [177] Nevertheless introducingmore drought tolerant species to mitigate climate changemight not necessarily be successful due to trade-offs betweendrought tolerance and growth plasticity Nicotra et al [178]sustain the fact that autochthonous provenances have thepotential for resistance to change in climatic conditions

as a function of both phenotypic plasticity and genotypicvariations

Assessment of vegetation vulnerability and climatechange resilience require understanding of the diversityamong plant species in the current vegetation and theirgrowth strategies in response to fluctuating resource avail-ability [179] Since species with extensive geographical rangehave the potential to exhibit large intraspecific variationsin physiology morphology and phenology they may begood models for the study of local and regional adaptations[140] Nevertheless adaptation to future global change couldrequire the evolution of a number of different traits that maybe constrained by correlations between them [180] Thusit is necessary to identify plant functional traits in whichplasticity is likely to be a determinant in plant responseto global change contributing to predict species distribu-tion changes and shifts [178] Moreover it is important tofully understand the ecological consequences at a speciesand ecosystem level considering that species with a greateradaptive plasticity may be more likely to survive novelenvironmental conditions since such changes typically occurtoo rapidly to allow for an evolutionary (or in some cases amigratory) response Plasticity is recognized to be a majorsource of phenotypic variations in the real world because itwill influence natural selection and consequently patternsof diversification among populations and ultimately species[2 181] Plasticity promotes evolutionary diversification ifthe produced phenotypes provide adaptive diversity thatunder selection becomes evolutionarily fixed [2 182 183]Nevertheless the extent to which phenotypic plasticity mayfacilitate survival under changing environmental conditionsstill remains largely unknown Although phenotypic plas-ticity may facilitate short-term adaptation to environmentalchanges genetic adaptationmight ultimately be necessary forthe persistence of species in extreme habitats [177]

In the near future it will be important to collect data byworking in the field and in particular in primary forestsandor in well-conserved habitats where new stress factorsare limited in order to define standard protocols usefulfor comparative studies Among the strategies environ-ment conservation should protect heterogeneity betweenand within habitats in order to maintain larger intraspecificvariability and thereby conserving a variety of phenotypicspecializations thatwill be able to buffer future environmentalextremities due to climate and land-use changes [184]

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

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[2] S E Sultan ldquoPromising directions in plant phenotypic plastic-ityrdquo Perspectives in Plant Ecology Evolution and Systematics vol6 no 4 pp 227ndash233 2004


[3] F Valladares D Sanchez-Gomez and M A Zavala ldquoQuan-titative estimation of phenotypic plasticity bridging the gapbetween the evolutionary concept and its ecological applica-tionsrdquo Journal of Ecology vol 94 no 6 pp 1103ndash1116 2006

[4] W E Spencer J Teeri and R G Wetzel ldquoAcclimation ofphotosynthetic phenotype to environmental heterogeneityrdquoEcology vol 75 no 2 pp 301ndash314 1994

[5] LGratani P PesoliM F Crescente KAichner andW LarcherldquoPhotosynthesis as a temperature indicator in Quercus ilex LrdquoGlobal and Planetary Change vol 24 no 2 pp 153ndash163 2000

[6] C Parmesan ldquoEcological and evolutionary responses to recentclimate changerdquo Annual Review of Ecology Evolution andSystematics vol 37 pp 637ndash669 2006

[7] S Matesanz E Gianoli and F Valladares ldquoGlobal change andthe evolution of phenotypic plasticity in plantsrdquo Annals of theNew York Academy of Sciences vol 1206 pp 35ndash55 2010

[8] M van Kleunen and M Fischer ldquoProgress in the detection ofcosts of phenotypic plasticity in plantsrdquo New Phytologist vol176 no 4 pp 727ndash730 2007

[9] R Lande ldquoAdaptation to an extraordinary environment byevolution of phenotypic plasticity and genetic assimilationrdquoJournal of Evolutionary Biology vol 22 no 7 pp 1435ndash14462009

[10] A D Bradshaw ldquoEvolutionary significance of phenotypic plas-ticity in plantsrdquo Advances in Genetics vol 13 pp 115ndash155 1965

[11] S M Scheiner and C J Goodnight ldquoThe comparison ofphenotypic plasticity and genetic variation in populations of thegrass Danthonia spicatardquo Evolution vol 38 pp 845ndash855 1984

[12] S Via and R Lande ldquoEvolution of genetic variability ina spatially heterogeneous environment effects of genotype-environment interactionrdquo Genetical Research vol 49 no 2 pp147ndash156 1987

[13] S Via R Gomulkiewicz G De Jong S M Scheiner C DSchlichting and P H Van Tienderen ldquoAdaptive phenotypicplasticity consensus and controversyrdquo Trends in Ecology andEvolution vol 10 no 5 pp 212ndash217 1995

[14] M van Kleunen and M Fischer ldquoConstraints on the evolutionof adaptive phenotypic plasticity in plantsrdquoNewPhytologist vol166 no 1 pp 49ndash60 2005

[15] D D Ackerly S Dudley S E Sultan et al ldquoThe evolutionof plant ecophysiological traits recent advances and futuredirectionsrdquo BioScience vol 50 no 11 pp 979ndash995 2000

[16] T D Price A Qvarnstrom and D E Irwin ldquoThe role ofphenotypic plasticity in driving genetic evolutionrdquo Proceedingsof the Royal Society B Biological Sciences vol 270 pp 1433ndash1440 2003

[17] L Gratani ldquoLeaf and shoot growth dynamics ofQuercus ilex LrdquoActa Oecologica vol 17 no 1 pp 17ndash27 1996

[18] A Pintado F Valladares and L G Sancho ldquoExploring phe-notypic plasticity in the lichen Ramalina capitata morphologywater relations and chlorophyll content in North- and South-facing populationsrdquoAnnals of Botany vol 80 no 3 pp 345ndash3531997

[19] L Gratani M Meneghini P Pesoli and M F CrescenteldquoStructural and functional plasticity ofQuercus ilex seedlings ofdifferent provenances in Italyrdquo TreesmdashStructure and Functionvol 17 no 6 pp 515ndash521 2003

[20] M Zunzunegui M C D Barradas F Ain-Lhout L Alvarez-Cansino M P Esquivias and F G Novo ldquoSeasonal physio-logical plasticity and recovery capacity after summer stress inMediterranean scrub communitiesrdquo Plant Ecology vol 212 no1 pp 127ndash142 2011

[21] D E Waitt and D A Levin ldquoGenetic and phenotypic cor-relations in plants a botanical test of Cheverudrsquos conjecturerdquoHeredity vol 80 no 3 pp 310ndash319 1998

[22] M A Arntz and L F Delph ldquoPattern and process evidence forthe evolution of photosynthetic traits in natural populationsrdquoOecologia vol 127 no 4 pp 455ndash467 2001

[23] S E Sultan ldquoPhenotypic plasticity for plant developmentfunction and life historyrdquo Trends in Plant Science vol 5 no 12pp 537ndash542 2000

[24] L Gratani and M F Crescente ldquoPhenology and leaf adaptivestrategies of Mediterranean maquis plantsrdquo Ecologia Mediter-ranea vol 23 pp 11ndash19 1997

[25] L A Dorn E H Pyle and J Schmitt ldquoPlasticity to light cuesand resources inArabidopsis thaliana testing for adaptive valueand costsrdquo Evolution vol 54 no 6 pp 1982ndash1994 2000

[26] F Valladares E Gianoli and J M Gomez ldquoEcological limits toplant phenotypic plasticityrdquo New Phytologist vol 176 no 4 pp749ndash763 2007

[27] T Wyka P Robakowski and R Zytkowiak ldquoAcclimation ofleaves to contrasting irradiance in juvenile trees differing inshade tolerancerdquo Tree Physiology vol 27 no 9 pp 1293ndash13062007

[28] M B Walters and P B Reich ldquoSeed size nitrogen supply andgrowth rate affect tree seedling survival in deep shaderdquo Ecologyvol 81 no 7 pp 1887ndash1901 2000

[29] J Stocklin P Kuss and A R Pluess ldquoGenetic diversity phe-notypic variation and local adaptation in the alpine landscapecase studies with alpine plant speciesrdquo Botanica Helvetica vol119 no 2 pp 125ndash133 2009

[30] F S Matos R Wolfgramm F V Goncalves P C Cavatte M CVentrella and FMDaMatta ldquoPhenotypic plasticity in responseto light in the coffee treerdquo Environmental and ExperimentalBotany vol 67 no 2 pp 421ndash427 2009

[31] W L Araujo P C Dias G A B KMoraes et al ldquoLimitations tophotosynthesis in coffee leaves fromdifferent canopy positionsrdquoPlant Physiology and Biochemistry vol 46 no 10 pp 884ndash8902008

[32] U Niinemets O Kull and J D Tenhunen ldquoAn analysis of lighteffects on foliar morphology physiology and light interceptionin temperate deciduous woody species of contrasting shadetolerancerdquo Tree Physiology vol 18 no 10 pp 681ndash696 1998

[33] H Ellenberg Vegetation Ecology of Central Europe CambridgeUniversity Press Cambridge UK 4th edition 1988

[34] H J Otto Waldokologie Eugen Ulmer Stuttgart Germany1994

[35] L Gratani R Catoni G Pirone A R Frattaroli and LVarone ldquoPhysiological and morphological leaf trait variationsin twoApennine plant species in response to different altitudesrdquoPhotosynthetica vol 50 no 1 pp 15ndash23 2012

[36] G Ke and M J A Werger ldquoDifferent responses to shade ofevergreen and deciduous oak seedlings and the effect of acornsizerdquo Acta Oecologica vol 20 no 6 pp 579ndash586 1999

[37] F Valladares J Chico I Aranda et al ldquoThe greater seedlinghigh-light tolerance of Quercus robur over Fagus sylvatica islinked to a greater physiological plasticityrdquoTreesmdashStructure andFunction vol 16 no 6 pp 395ndash403 2002

[38] G Muller-Stark Biodervisitat und Nachhaltige ForstwirtschaftEcomed Landsberg Germany 1997

[39] A D Peuke C Schraml W Hartung and H RennenbergldquoIdentification of drought-sensitive beech ecotypes by physio-logical parametersrdquoNew Phytologist vol 154 no 2 pp 373ndash3872002


[40] Z Wen Y Ding T Zhao and J Gai ldquoGenetic diversity andpeculiarity of annual wild soybean (G soja Sieb et Zucc) fromvarious eco-regions in ChinardquoTheoretical and Applied Geneticsvol 119 no 2 pp 371ndash381 2009

[41] L Sack P J Grubb and T Maranon ldquoThe functional morphol-ogy of juvenile plants tolerant of strong summer drought inshaded forest understories in southern Spainrdquo Plant Ecologyvol 168 no 1 pp 139ndash163 2003

[42] U Niinemets F Valladares and R Ceulemans ldquoLeaf-levelphenotypic variability and plasticity of invasive Rhododendronponticum and non-invasive Ilex aquifolium co-occurring at twocontrasting European sitesrdquo Plant Cell and Environment vol26 no 6 pp 941ndash956 2003

[43] D Bastlova and J Kvet ldquoPhenotypic plasticity in native pop-ulations of Lythrum salicaria L across geographical gradientbetween- and within-population differencesrdquo in Ecology andManagement of Alien Plant Invasions L Child Ed pp 237ndash247Backhuys Leiden The Netherlands 2003

[44] D Q Thompson R L Stuckey and E B Thompson ldquoSpreadimpact and control of purple loosestrife (Lythrum salicaria) inNorth American wetlandsrdquo US Fish andWildlife Service Fishand Wildlife Research Report 2 Washington DC USA 1987

[45] M M Mendes L C Gazarini and M L Rodrigues ldquoAccli-mation ofMyrtus communis to contrasting Mediterranean lightenvironmentsmdasheffects on structure and chemical compositionof foliage and plant water relationsrdquo Environmental and Experi-mental Botany vol 45 no 2 pp 165ndash178 2001

[46] L Gratani F Covone and W Larcher ldquoLeaf plasticity inresponse to light of three evergreen species of the Mediter-ranean maquisrdquo TreesmdashStructure and Function vol 20 no 5pp 549ndash558 2006

[47] J Oleksyn J Modrzynski M G Tjoelker R ZytkowiakP B Reich and P Karolewski ldquoGrowth and physiology ofPicea abies populations from elevational transects commongarden evidence for altitudinal ecotypes and cold adaptationrdquoFunctional Ecology vol 12 no 4 pp 573ndash590 1998

[48] L Poorter E LianesMMoreno-de lasHeras andMA ZavalaldquoArchitecture of Iberian canopy tree species in relation to wooddensity shade tolerance and climaterdquo Plant Ecology vol 213 no5 pp 707ndash722 2012

[49] M A Zavala J M Espelta and J Retana ldquoConstraints andtrade-offs in Mediterranean plant communities the case ofholm oak-Aleppo pine forestsrdquo Botanical Review vol 66 no 1pp 119ndash149 2000

[50] F J Baquedano F Valladares and F J Castillo ldquoPhenotypicplasticity blurs ecotypic divergence in the response of Quercuscoccifera and Pinus halepensis to water stressrdquo European Journalof Forest Research vol 127 no 6 pp 495ndash506 2008

[51] S Palmroth F Berninger E Nikinmaa J Lloyd P Pulkkinenand P Hari ldquoStructural adaptation rather than water conser-vation was observed in Scots pine over a range of wet to dryclimatesrdquo Oecologia vol 121 no 3 pp 302ndash309 1999

[52] S Nahum M Inbar G Nersquoeman and R Ben-Shlomo ldquoPheno-typic plasticity and gene diversity in Pistacia lentiscus L alongenvironmental gradients in Israelrdquo Tree Genetics and Genomesvol 4 no 4 pp 777ndash785 2008

[53] S E Sultan ldquoAn emerging focus on plant ecological develop-mentrdquo New Phytologist vol 166 no 1 pp 1ndash5 2005

[54] L Gratani R Catoni and L Varone ldquoMorphological anatomi-cal and physiological leaf traits ofQ ilex P latifolia P lentiscusandM communis and their response to Mediterranean climatestress factorsrdquo Botanical Studies vol 54 pp 1ndash12 2013

[55] L Gratani E Fiorentino A Kubova and P Marzi ldquoEffect ofmicroclimate on ecophysiological features of some sclerophyl-lous speciesrdquo Photosynthetica vol 23 pp 230ndash233 1989

[56] L Balaguer E Martınez-Ferri F Valladares et al ldquoPopulationdivergence in the plasticity of the response of Quercus cocciferato the light environmentrdquo Functional Ecology vol 15 no 1 pp124ndash135 2001

[57] A Bonito L Varone and L Gratani ldquoRelationship betweenacorn size and seedling morphological and physiological traitsof Quercus ilex L from different climatesrdquo Photosynthetica vol49 no 1 pp 75ndash86 2011

[58] P Pesoli L Gratani andW Larcher ldquoResponses ofQuercus ilexfrom different provenances to experimentally imposed waterstressrdquo Biologia Plantarum vol 46 no 4 pp 577ndash581 2003

[59] M Barbero R Loisel and P Quezel ldquoBiogeography ecologyand history of Mediterranean Quercus ilex ecosystemsrdquo Vege-tatio vol 99-100 no 1 pp 19ndash34 1992

[60] J Terradas and R Save ldquoThe influence of summer and winterstress and water relationship on the distribution of Quercusilex Lrdquo in Quercus ilex L Ecosystems Function Dynamics andManagement F Romane and J Terradas Eds pp 137ndash145Kluwer Academic Dodrecht The Netherlands 1992

[61] H Michaud R Lumaret and F Romane ldquoVariation in thegenetic structure and reproductive biology of holm oak pop-ulationsrdquo Vegetatio vol 99-100 no 1 pp 107ndash113 1992

[62] K Hayashi ldquoGrowth characteristics and silviculture inQuercusmongolica var crispula Blumerdquo in Handbook for HardwoodK Sakaguchi Ed pp 122ndash128 Association For Promotion ofForest Science Tokyo Japan 1985

[63] M Higo ldquoRegeneration behaviors of tree species of secondarystands regenerated on sites disturbed by Typhoon 15 basedon the proportion of advanced regeneration growth rate andseedling density in closedmature standsrdquo Journal of the JapaneseForestry Society vol 76 pp 531ndash539 1994

[64] M-L Navas and E Garnier ldquoPlasticity of whole plant and leaftraits in Rubia peregrina in response to light nutrient and wateravailabilityrdquo Acta Oecologica vol 23 no 6 pp 375ndash383 2002

[65] L Gratani M F Crescente V Drsquoamato C Ricotta A RFrattaroli and G Puglielli ldquoLeaf traits variation in Seslerianitida growing atdifferent altitudes in the Central ApenninesrdquoPhotosynthetica In press

[66] P M S Ashton and G P Berlyn ldquoLeaf adaptations of someShorea species to sun and shaderdquo New Phytologist vol 121 no4 pp 587ndash596 1992

[67] R J N Emery D M Reid and C C Chinnappa ldquoPheno-typic plasticity of stem elongation in two ecotypes of Stellarialongipes the role of ethylene and response to windrdquo Plant Celland Environment vol 17 no 6 pp 691ndash700 1994

[68] M A Molina-Montenegro J Penuelas S Munne-Bosch and JSardans ldquoHigher plasticity in ecophysiological traits enhancesthe performance and invasion success of Taraxacum officinale(dandelion) in alpine environmentsrdquo Biological Invasions vol14 no 1 pp 21ndash33 2012

[69] W Larcher Physiological Plant Ecology Springer Berlin Ger-many 4th edition 2003

[70] P Doughty ldquoTesting the ecological correlates of phenotypicallyplastic traits within a phylogenetic frameworkrdquoActaOecologicavol 16 no 4 pp 519ndash524 1995

[71] K Gotthard and S Nylin ldquoAdaptive plasticity and plasticityas an adaptation a selective review of plasticity in animalmorphology and life historyrdquoOikos vol 74 no 1 pp 3ndash17 1995


[72] S A Cook and M P Johnson ldquoAdaptation to heterogeneousenvironments I Variation in heterophylly in Ranunculus flam-mulardquo Evolution vol 22 pp 496ndash516 1968

[73] T O Haugen and L A Vollestad ldquoPopulation differences inearly life-history traits in graylingrdquo Journal of EvolutionaryBiology vol 13 no 6 pp 897ndash905 2000

[74] C K Ghalambor and T E Martin ldquoComparative manipulationof predation risk in incubating birds reveals variability in theplasticity of responsesrdquoBehavioral Ecology vol 13 no 1 pp 101ndash108 2002

[75] M Pigliucci C J Murren and C D Schlichting ldquoPhenotypicplasticity and evolution by genetic assimilationrdquo Journal ofExperimental Biology vol 209 no 12 pp 2362ndash2367 2006

[76] AWeigelt and P Jolliffe ldquoIndices of plant competitionrdquo Journalof Ecology vol 91 no 5 pp 707ndash720 2003

[77] P E Hulme ldquoPhenotypic plasticity and plant invasions is it allJackrdquo Functional Ecology vol 22 no 1 pp 3ndash7 2008

[78] D Sanchez-Gomez FValladares andMA Zavala ldquoFunctionaltraits and plasticity in response to light in seedlings of fourIberian forest tree speciesrdquo Tree Physiology vol 26 no 11 pp1425ndash1433 2006

[79] H Poorter U Niinemets A Walter F Fiorani and U SchurrldquoA method to construct dose-response curves for a wide rangeof environmental factors and plant traits by means of a meta-analysis of phenotypic datardquo Journal of Experimental Botanyvol 61 no 8 pp 2043ndash2055 2010

[80] D Kuiper and P J C Kuiper ldquoPhenotypic plasticity in a physio-logical perspectiverdquo Acta Oecologica Oecologia Plantarum vol9 pp 43ndash59 1988

[81] F Valladares L Balaguer E Martinez-Ferri E Perez-Coronaand E Manrique ldquoPlasticity instability and canalization Is thephenotypic variation in seedlings of sclerophyll oaks consis-tent with the environmental unpredictability of MediterraneanecosystemsrdquoNew Phytologist vol 156 no 3 pp 457ndash467 2002

[82] U Niinemets and F Valladares ldquoPhotosynthetic acclimation tosimultaneous and interacting environmental stresses along nat-ural light gradients optimality and constraintsrdquo Plant Biologyvol 6 no 3 pp 254ndash268 2004

[83] M Zunzunegui F Ain-Lhout M C D Barradas L Alvarez-Cansino M P Esquivias and F Garcıa Novo ldquoPhysiologicalmorphological and allocation plasticity of a semi-deciduousshrubrdquo Acta Oecologica vol 35 no 3 pp 370ndash379 2009

[84] F S Chapin III K Autumn and F Pugnaire ldquoEvolution ofsuites of traits in response to environmental stressrdquo AmericanNaturalist vol 142 pp S78ndashS92 1993

[85] F Valladares E Martinez-Ferri L Balaguer E Perez-Coronaand EManrique ldquoLow leaf-level response to light and nutrientsin Mediterranean evergreen oaks a conservative resource-usestrategyrdquo New Phytologist vol 148 no 1 pp 79ndash91 2000

[86] J C Crick and J P Grime ldquoMorphological plasticity and min-eral nutrient capture in two herbaceous species of contrastedecologyrdquo New Phytologist vol 107 no 2 pp 403ndash414 1987

[87] N G Dengler ldquoComparative histological basis of sun and shadeleaf dimorphism in Helianthus annuusrdquo Canadian Journal ofBotany vol 58 pp 717ndash730 1980

[88] J H McClendon and G G McMillen ldquoThe control of leafmorphology and the tolerance of shade by woody plantsrdquoBotanical Gazette vol 143 no 1 pp 79ndash83 1982

[89] M P Dale and D R Causton ldquoThe ecophysiology of Veronicachamaedrys V montana and V officinalis I Light quality andlight quantityrdquo Journal of Ecology vol 80 no 3 pp 483ndash4921992

[90] J Kvet J Svoboda andK Fiala ldquoCanopy development in standsof Typha latifolia L and Phragmites communis Trin in SouthMoraviardquo Hidrobiologia vol 10 pp 63ndash75 1969

[91] J R Evans ldquoLeaf anatomy enables more equal access to lightand CO

2

between chloroplastsrdquo New Phytologist vol 143 no 1pp 93ndash104 1999

[92] R B Wylie ldquoPrinciples of foliar organization shown by sun-shade leaves from ten species of deciduous dicotyledonoustreesrdquo American Journal of Botany vol 36 pp 355ndash361 1951

[93] J H McClendon ldquoThe relationship between the thicknessof deciduous leaves and their maximum photosynthetic raterdquoAmerican Journal of Botany vol 49 pp 320ndash322 1962

[94] H K Lichtenthaler C Buschmann M Doll et al ldquoPhotosyn-thetic activity chloroplast ultrastructure and leaf characteris-tics of high-light and low-light plants and of sun and shadeleavesrdquo Photosynthesis Research vol 2 no 2 pp 115ndash141 1981

[95] H K Lichtenthaler G Kuhn U Prenzel and D MeierldquoChlorophyll-protein levels and degree of thylakoid stackingin radish chloroplasts from high-light low-light and bentazon-treated plantsrdquo Physiologia Plantarum vol 56 no 2 pp 183ndash188 1982

[96] J R Evans ldquoPhotosynthesis and nitrogen relationships in leavesof C3

plantsrdquo Oecologia vol 78 no 1 pp 9ndash19 1989[97] K Hikosaka ldquoNitrogen partitioning in the photosynthetic

apparatus of Plantago asiatica leaves grown under differenttemperature and light conditions similarities and differencesbetween temperature and light acclimationrdquo Plant and CellPhysiology vol 46 no 8 pp 1283ndash1290 2005

[98] T Hirose and M J A Werger ldquoMaximizing daily canopyphotosynthesis with respect to the leaf nitrogen allocationpattern in the canopyrdquo Oecologia vol 72 no 4 pp 520ndash5261987

[99] K Yoshimura ldquoIrradiance heterogeneity within crown affectsphotosynthetic capacity and nitrogen distribution of leaves inCedrela sinensisrdquo Plant Cell and Environment vol 33 no 5 pp750ndash758 2010

[100] N P R Anten ldquoModelling canopy photosynthesis using param-eters determined from simple non-destructive measurementsrdquoEcological Research vol 12 no 1 pp 77ndash88 1997

[101] L Sack P J Melcher W H Liu E Middleton and T PardeeldquoHow strong is intracanopy leaf plasticity in temperate decidu-ous treesrdquo American Journal of Botany vol 93 no 6 pp 829ndash839 2006

[102] U Niinemets ldquoA review of light interception in plant standsfrom leaf to canopy in different plant functional types and inspecies with varying shade tolerancerdquo Ecological Research vol25 no 4 pp 693ndash714 2010

[103] H P Meister M M Caldwell J D Tenhunen and O L LangeldquoEcological implications of sunshade-leaf differentiation insclerophyllous canopies assessment by canopy modelingrdquo inPlant Response to Stress Functional Analysis in MediterraneanEcosystems J D Tenhunen F M Catarino O L Lange andW C Oechel Eds pp 401ndash411 Springer Heidelberg Germany1987

[104] U Niinemets and O Kull ldquoStoichiometry of foliar carbonconstituents varies along light gradients in temperate woodycanopies implications for foliagemorphological plasticityrdquoTreePhysiology vol 18 no 7 pp 467ndash479 1998

[105] F Valladares S J Wright E Lasso K Kitajima and R WPearcy ldquoPlastic phenotypic response to light of 16 congenericshrubs from a panamanian rainforestrdquo Ecology vol 81 no 7 pp1925ndash1936 2000


[106] T J Givnish ldquoAdaptive significance of evergreen vs deciduousleaves solving the triple paradoxrdquo Silva Fennica vol 36 no 3pp 703ndash743 2002

[107] L Markesteijn L Poorter and F Bongers ldquoLight-dependentleaf trait variation in 43 tropical dry forest tree speciesrdquoAmerican Journal of Botany vol 94 no 4 pp 515ndash525 2007

[108] T P Wyka J Oleksyn R Zytkowiak P Karolewski A MJagodzinski and P B Reich ldquoResponses of leaf structure andphotosynthetic properties to intra-canopy light gradients acommon garden test with four broadleaf deciduous angiospermand seven evergreen conifer tree speciesrdquoOecologia vol 170 pp11ndash24 2012

[109] L Gratani and I Foti ldquoEstimating forest structure and shadetolerance of the species in a mixed deciduous broad-leavedforest in Abruzzo Italyrdquo Annales Botanici Fennici vol 35 no2 pp 75ndash83 1998

[110] L Gratani ldquoCanopy structure vertical radiation profile andphotosynthetic function in a Quercus ilex evergreen forestrdquoPhotosynthetica vol 33 no 1 pp 139ndash149 1997

[111] R K P Yadav AM Bosabalidis andD Vokou ldquoLeaf structuralfeatures of Mediterranean perennial species plasticity and lifeform specificityrdquo Journal of Biological Research vol 2 pp 21ndash342004

[112] F Valladares and U Niinemets ldquoFeature of complex natureand consequencesrdquo Annual Review of Ecology Evolution andSystematics vol 39 pp 237ndash257 2008

[113] S B Carpenter and N D Smith ldquoA comparative studies of leafthickness among Southern Appalachian hardwoodsrdquo CanadianJournal of Botany vol 59 pp 1393ndash1396 1981

[114] S Strauss-Debenedetti and F A Bazzaz ldquoPlasticity and accli-mation to light in tropical Moraceae of different sucessionalpositionsrdquo Oecologia vol 87 no 3 pp 377ndash387 1991

[115] CCMuth andFA Bazzaz ldquoTree canopy displacement at forestgap edgesrdquo Canadian Journal of Forest Research vol 32 no 2pp 247ndash254 2002

[116] F Longuetaud A Piboule H Wernsdorfer and C ColletldquoCrown plasticity reduces inter-tree competition in a mixedbroadleaved forestrdquo European Journal of Forest Research vol132 pp 621ndash634 2013

[117] M H Turnbull ldquoThe effect of light quantity and qualityduring development on the photosynthetic characteristics of sixAustralian rainforest tree speciesrdquo Oecologia vol 87 no 1 pp110ndash117 1991

[118] J Popma F Bongers and M J A Werger ldquoGap-dependenceand leaf characteristics of trees in a tropical lowland rain forestin Mexicordquo Oikos vol 63 no 2 pp 207ndash214 1992

[119] F Valladares S Arrieta I Aranda et al ldquoShade tolerancephotoinhibition sensitivity and phenotypic plasticity of Ilexaquifolium in continental Mediterranean sitesrdquo Tree Physiologyvol 25 no 8 pp 1041ndash1052 2005

[120] R Catoni L Gratani and L Varone ldquoPhysiological morpho-logical and anatomical trait variations betweenwinter and sum-mer leaves of Cistus speciesrdquo Flora Morphology DistributionFunctional Ecology of Plants vol 207 pp 442ndash449 2012

[121] A F M van Hees ldquoGrowth and morphology of pedunculateoak (Quercus robur L) and beech (Fagus sylvatica L) seedlingsin relation to shading and droughtrdquo Annales des SciencesForestieres vol 54 no 1 pp 9ndash18 1997

[122] H Ishii and S Asano ldquoThe role of crown architecture leafphenology and photosynthetic activity in promoting comple-mentary use of light among coexisting species in temperateforestsrdquo Ecological Research vol 25 no 4 pp 715ndash722 2010

[123] A M Barton ldquoFactors controlling plant distributions droughtcompetition and fire in montane pines in Arizonardquo EcologicalMonographs vol 63 no 4 pp 367ndash397 1993

[124] J Martınez-Vilalta and J Pinol ldquoDrought-induced mortalityandhydraulic architecture in pine populations of theNE IberianPeninsulardquo Forest Ecology andManagement vol 161 no 1ndash3 pp247ndash256 2002

[125] M A Zavala J M Espelta J Caspersen and J RetanaldquoInterspecific differences in sapling performance with respectto light and aridity gradients inmediterranean pine-oak forestsimplications for species coexistencerdquoCanadian Journal of ForestResearch vol 41 no 7 pp 1432ndash1444 2011

[126] M Kitao T T Lei T Koike H Tobita and Y MaruyamaldquoSusceptibility to photoinhibition of three deciduous broadleaftree species with different successional traits raised undervarious light regimesrdquo Plant Cell and Environment vol 23 no1 pp 81ndash89 2000

[127] S S Mulkey and R W Pearcy ldquoInteractions between accli-mation and photoinhibition of photosynthesis of a tropicalforest understory herb Alocasia macrorrhiza during simulatedcanopy gap formationrdquo Functional Ecology vol 6 pp 719ndash7291992

[128] C B Osmond ldquoWhat is photoinhibition Some insights fromcomparison of shade and sun plantsrdquo in Photoinhibition ofPhotosynthesis from Molecular Mechanisms to the Field NR Baker and J R Bowyer Eds pp 1ndash24 BIOS ScientificPublishers Lancaster UK 1994

[129] T Koike M Kitao Y Maruyama S Mori and T T Lei ldquoLeafmorphology and photosynthetic adjustments among deciduousbroad-leaved trees within the vertical canopy profilerdquo TreePhysiology vol 21 no 12-13 pp 951ndash958 2001

[130] T Koike ldquoPhotosynthetic responses to light intensity of decid-uous broad-leaved tree seedlings raised under various artificialshaderdquo Environmental Control in Biology vol 24 pp 51ndash581986

[131] N C Vance and J B Zaerr ldquoInfluence of drought stress and lowirradiance on plant water relations and structural constituentsin needles of Pinus ponderosa seedlingsrdquo Tree Physiology vol 8pp 175ndash184 1991

[132] S H Janse-Ten Klooster E J P Thomas and F J SterckldquoExplaining interspecific differences in sapling growth andshade tolerance in temperate forestsrdquo Journal of Ecology vol 95no 6 pp 1250ndash1260 2007

[133] T J Kawecki and D Ebert ldquoConceptual issues in local adapta-tionrdquo Ecology Letters vol 7 no 12 pp 1225ndash1241 2004

[134] O Savolainen T Pyhajarvi and T Knurr ldquoGene flow and localadaptation in forest treesrdquo Annual Review of Ecology Evolutionand Systematics vol 37 pp 595ndash619 2007

[135] K M Hufford and S J Mazer ldquoPlant ecotypes genetic differ-entiation in the age of ecological restorationrdquo Trends in Ecologyand Evolution vol 18 no 3 pp 147ndash155 2003

[136] M C Grant and J B Mitton ldquoGenetic differentiation amonggrowth forms of Engelmann spruce and subalpine fir at treelinerdquo Arctic Antarctic and Alpine Research vol 9 pp 259ndash2631977

[137] J B Mitton Y B Linhart J L Hamrick and J S BeckmanldquoObservations on the genetic structure and mating system ofponderosa pine in the Colorado front rangerdquo Theoretical andApplied Genetics vol 51 no 1 pp 5ndash13 1977

[138] C K Kelly M W Chase A de Bruijn M F Fay and FI Woodward ldquoTemperature-based population segregation inbirchrdquo Ecology Letters vol 6 no 2 pp 87ndash89 2003


[139] B C Bongarten and R O Teskey ldquoWater relations of loblollypine seedlings from diverse geographic originsrdquo Tree Physiol-ogy vol 1 pp 265ndash276 1986

[140] R Y Soolanayakanahally R D Guy S N Silim E C Drewesand W R Schroeder ldquoEnhanced assimilation rate and wateruse efficiency with latitude through increased photosyntheticcapacity and internal conductance in balsam poplar (Populusbalsamifera L)rdquo Plant Cell and Environment vol 32 no 12 pp1821ndash1832 2009

[141] J A Ramırez-Valiente F Valladares L Gil and I ArandaldquoPopulation differences in juvenile survival under increasingdrought are mediated by seed size in cork oak (Quercus suberL)rdquo Forest Ecology and Management vol 257 no 8 pp 1676ndash1683 2009

[142] L Gratani and M Amadori ldquoPost-fire resprouting of shrubbyspecies in Mediterranean maquisrdquo Vegetatio vol 96 no 2 pp137ndash143 1991

[143] W Larcher C Kainmuller and J Wagner ldquoSurvival typesof high mountain plants under extreme temperaturesrdquo FloraMorphology Distribution Functional Ecology of Plants vol 205no 1 pp 3ndash18 2010

[144] D Nogues-Bravo M B Araujo M P Errea and J P Martınez-Rica ldquoExposure of globalmountain systems to climatewarmingduring the 21st Centuryrdquo Global Environmental Change vol 17no 3-4 pp 420ndash428 2007

[145] W Thuiller S Lavorel M B Araujo M T Sykes and I CPrentice ldquoClimate change threats to plant diversity in EuroperdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 102 no 23 pp 8245ndash8250 2005

[146] R Engler C F Randin W Thuiller et al ldquo21st century climatechange threatens mountain flora unequally across EuroperdquoGlobal Change Biology vol 17 no 7 pp 2330ndash2341 2011

[147] T Dirnbock F Essl and W Rabitsch ldquoDisproportional riskfor habitat loss of high-altitude endemic species under climatechangerdquoGlobal Change Biology vol 17 no 2 pp 990ndash996 2011

[148] O Savolainen F Bokma R Garcıa-Gil P Komulainen andT Repo ldquoGenetic variation in cessation of growth and frosthardiness and consequences for adaptation of Pinus sylvestristo climatic changesrdquo Forest Ecology and Management vol 197no 1ndash3 pp 79ndash89 2004

[149] A S Jump and J Penuelas ldquoRunning to stand still adaptationand the response of plants to rapid climate changerdquo EcologyLetters vol 8 no 9 pp 1010ndash1020 2005

[150] H Pauli M Gottfried and G Grabherr ldquoEffect of climatechange on the alpine and nival vegetation of the Alpsrdquo Journalof Mountain Ecology vol 7 pp 9ndash12 2003

[151] M Lindner M Maroschek S Netherer et al ldquoClimate changeimpacts adaptive capacity and vulnerability of European forestecosystemsrdquo Forest Ecology andManagement vol 259 no 4 pp698ndash709 2010

[152] J F Scheepens E S Frei and J Stocklin ldquoGenotypic and envi-ronmental variation in specific leaf area in a widespread Alpineplant after transplantation to different altitudesrdquoOecologia vol164 no 1 pp 141ndash150 2010

[153] A M Davidson M Jennions and A B Nicotra ldquoDo invasivespecies show higher phenotypic plasticity than native speciesand if so is it adaptive A meta-analysisrdquo Ecology Letters vol14 no 4 pp 419ndash431 2011

[154] S L Chown S Slabber M A McGeoch C Janion andH P Leinaas ldquoPhenotypic plasticity mediates climate change

responses among invasive and indigenous arthropodsrdquoProceed-ings of the Royal Society B Biological Sciences vol 274 no 1625pp 2531ndash2537 2007

[155] J S Dukes ldquoTomorrowrsquos plant communities different buthowrdquo New Phytologist vol 176 no 2 pp 235ndash237 2007

[156] S C H Barrett and B J Richardson ldquoGenetic attributes ofinvading speciesrdquo in Ecology of Biological Invasions R HGroves and J J Burdon Eds pp 21ndash33 1986

[157] J Antonovics ldquoThe nature of limits to natural selectionrdquoAnnalsof the Missouri Botanical Garden vol 63 pp 224ndash247 1976

[158] S C H Barrett ldquoGenetic variation in weedsrdquo in BiologicalControl of Weeds with Plant Pathogens R Charudattan and HWalker Eds pp 73ndash98 John Wiley amp Sons New York NYUSA 1982

[159] K J Rice and R N Mack ldquoEcological genetics of BromustectorummdashII Intraspecific variation in phenotypic plasticityrdquoOecologia vol 88 no 1 pp 84ndash90 1991

[160] R J Abbott ldquoPlant invasions interspecific hybridization andthe evolution of new plant taxardquo Trends in Ecology and Evolu-tion vol 7 no 12 pp 401ndash405 1992

[161] D G Williams and R A Black ldquoPhenotypic variation in con-trasting temperature environments growth and photosynthesisin Pennisetum setaceum from different altitudes on HawaiirdquoFunctional Ecology vol 7 no 5 pp 623ndash633 1993

[162] L Z Durand and G Goldstein ldquoPhoto-synthesis photoinhibi-tion and nitrogen use efficiency in native and invasive tree fernsin Hawaiirdquo Oecologia vol 126 no 3 pp 345ndash354 2001

[163] D G Williams R N Mack and R A Black ldquoEcophysiologyof introduced Pennisetum setaceum on Hawaii the role ofphenotypic plasticityrdquo Ecology vol 76 no 5 pp 1569ndash15801995

[164] O K Atkin B R Loveys L J Atkinson and T L PonsldquoPhenotypic plasticity and growth temperature understandinginterspecific variabilityrdquo inMeeting on Phenotypic Plasticity andthe Changing Environment Held at the Society for ExperimentalBiology Plant Frontiers Meeting pp 267ndash281 Sheffield UK2005

[165] P J Yeh and T D Price ldquoAdaptive phenotypic plasticity andthe successful colonization of a novel environmentrdquo AmericanNaturalist vol 164 no 4 pp 531ndash542 2004

[166] J L Funk ldquoDifferences in plasticity between invasive and nativeplants froma low resource environmentrdquo Journal of Ecology vol96 no 6 pp 1162ndash1173 2008

[167] S Lavergne and J Molofsky ldquoIncreased genetic variation andevolutionary potential drive the success of an invasive grassrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 104 no 10 pp 3883ndash3888 2007

[168] R E Drenovsky B J Grewell C M DrsquoAntonio et al ldquoAfunctional trait perspective on plant invasionsrdquo Annals ofBotany vol 110 pp 141ndash153 2012

[169] O Godoy A Saldana N Fuentes F Valladares and E GianolildquoForests are not immune to plant invasions phenotypic plas-ticity and local adaptation allow Prunella vulgaris to colonize atemperate evergreen rainforestrdquo Biological Invasions vol 13 no7 pp 1615ndash1625 2011

[170] S J DeWalt J S Denslow and J L Hamrick ldquoBiomass allo-cation growth and photosynthesis of genotypes from nativeand introduced ranges of the tropical shrub Clidemia hirtardquoOecologia vol 138 no 4 pp 521ndash531 2004

[171] P Poot and H Lambers ldquoShallow-soil endemics adaptiveadvantages and constraints of a specialized root-system mor-phologyrdquo New Phytologist vol 178 no 2 pp 371ndash381 2008


[172] G-RWalther E Post P Convey et al ldquoEcological responses torecent climate changerdquo Nature vol 416 no 6879 pp 389ndash3952002

[173] A Menzel T H Sparks N Estrella et al ldquoEuropean phenolog-ical response to climate change matches the warming patternrdquoGlobal Change Biology vol 12 pp 1ndash8 2006

[174] Y Vitasse C C Bresson A Kremer RMichalet and S DelzonldquoQuantifying phenological plasticity to temperature in twotemperate tree speciesrdquo Functional Ecology vol 24 no 6 pp1211ndash1218 2010

[175] M Desponts and J P Simon ldquoStructure et variabilite genetiquede populations drsquoepinettes noires (Picea mariana (Mill) BSP)dans la zone hemiarctique du Nouveau- Quebecrdquo CanadianJournal of Forest Research vol 17 pp 1006ndash1012 1987

[176] F Villani S Benedettelli M Paciucci M Cherubini andM Pigliucci ldquoGenetic variation and differentiation betweennatural populations or chestnust (Castanea sativa Mill) fromItalyrdquo in Biochemical Markers in the Population Genetics ofForest Trees H H Hattemer S Fineschi F Cannata and ME Malvolti Eds pp 91ndash103 SPB Acadamic The Hague TheNetherlands 1991

[177] S Richter T Kipfer TWohlgemuth C C Guerrero J Ghazouland B Moser ldquoPhenotypic plasticity facilitates resistance toclimate change in a highly variable environmentrdquoOecologia vol169 no 1 pp 269ndash279 2012

[178] A B Nicotra O K Atkin S P Bonser et al ldquoPlant phenotypicplasticity in a changing climaterdquo Trends in Plant Science vol 15no 12 pp 684ndash692 2010

[179] I K Dawson A Lengkeek J C Weber and R JamnadassldquoManaging genetic variation in tropical trees Linking knowl-edge with action in agroforestry ecosystems for improvedconservation and enhanced livelihoodsrdquo Biodiversity and Con-servation vol 18 no 4 pp 969ndash986 2009

[180] J R Etterson and R G Shaw ldquoConstraint to adaptive evolutionin response to global warmingrdquo Science vol 294 no 5540 pp151ndash154 2001

[181] S M Scheiner ldquoThe genetics of phenotypic plasticity VIIEvolution in a spatially-structured environmentrdquo Journal ofEvolutionary Biology vol 11 no 3 pp 303ndash320 1998

[182] G G Simpson ldquoThe Baldwin effectrdquo Evolution vol 7 pp 110ndash117 1953

[183] M Pigliucci and C J Murren ldquoGenetic assimilation and apossible evolutionary paradox can macroevolution sometimesbe so fast as to pass us byrdquo Evolution vol 57 no 7 pp 1455ndash1464 2003

[184] C Wellstein S Chelli G Campetella et al ldquoIntraspecificphenotypic variability of plant functional traits in contrastingmountain grassland habitatsrdquo Biodiversity and Conservationvol 22 pp 2353ndash2374 2013

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of


Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology


Molecular Biology International

GenomicsInternational Journal of


The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014


BioinformaticsAdvances in

Marine BiologyJournal of



Signal TransductionJournal of


BioMed Research International

Evolutionary BiologyInternational Journal of



Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014


Genetics Research International


Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational



Enzyme Research



Microbiology


Table 1 List of thementioned species and corresponding references

Species ReferencesAbies alba [27]Acer pseudoplatanus [27]Acer saccharum [28]Betula papyrifera [28]Campanula thyrsoides [29]Coffea arabica [30 31]Corylus avellana [32ndash34]Crepis pygmaea subsp pygmaea [35]Cyclobalanopsis multinervis [36]Epilobium fleischeri [29]Fagus sylvatica [27 37ndash39]Fraxinus excelsior [32ndash34]Geum reptans [29]Glycine max [40]Glycine soja [40]Hedera helix [41]Ilex aquifolium [42]Isatis apennina [35]Lythrum salicaria [43 44]Myrtus communis [45]Ostrya virginiana [28]Phillyrea latifolia [41 46]Picea abies [27 47]Pinus halepensis [48ndash50]Pinus nigra [48]Pinus pinaster [48]Pinus pinea [48]Pinus sylvestris [48 51]Pinus uncinata [48]Pistacia lentiscus [46 52ndash55]Poa alpina [29]Populus tremula [32 33]Populus tremuloides [28]Quercus aliena var acutiserrata [36]Quercus coccifera [50 56]Quercus faginea [48]Quercus ilex [19 46 48 55 57ndash61]Quercus mongolica var crispula [62 63]Quercus petraea [48]Quercus pyrenaica [48]Quercus robur [48]Quercus suber [48]Rhododendron ponticum [42]Rubia peregrina [41 64]Ruscus aculeatus [41]Sesleria nitida [65]Shorea disticha [66]Shorea trapezifolia [66]Shorea worthingtonii [66]

Table 1 Continued

Species ReferencesSmilax aspera [41]Stellaria longipes [67]Taraxacum officinale [68]Tilia cordata [32ndash34]Viburnum tinus [41]

viewing the phenotype as an integrated function of growthmorphology life history and physiology [22] The timingof plant development can itself be plastic [23] and manyphenotypic responses to environmental stress factors may bethe consequence of growth reduction due to resource limi-tations [24 25] Differences among species and populationsmay reflect different selective pressures on plasticity differentlimitations acting upon the maximization of plasticity or acombination of both [26] The potential plastic response ofa given trait may be large but the observed plasticity maybe lowered by resource limitations or environmental stressfactors [14]

The particular way by which a genotype varies in itsexpression across a range of environments can be describedby a reaction norm which is genetically determined [69]The reaction norm for any specific trait of a genotype canbe visualized as a line or a curve on a two-dimensionalplot of the environmental value versus the phenotypic value(Figure 1) Phenotypic plasticity can be visualized as a changein the slope of the reaction norm between ancestral andderived populations or species [70 71] Such change hasbeen shown to occur in nature between species subjectedto different selection pressures [72ndash74] Plasticity is whatmakes the appearance of an environmentally induced novelphenotype possible and a process of selection on the expres-sion of such phenotype in a new environment may end upldquofixingrdquo (genetically assimilating) it by altering the shape ofthe reaction norm [75] Thus plasticity could facilitate theexpression of relatively well-adapted phenotypes under novelconditions (eg after migration to new geographical areas)improving the performance of the population and resulting inthe genetic assimilation of the trait in the new environmentThis has the potential to explain a variety of evolutionaryecological processes [14 75]

Indexes can facilitate comparison of different studies [7677] set of species or populations within a given speciesby considering experimental data in research on plasticity[19 56 57] However at least 17 different indexes have beenemployed as a measure of the phenotypic plasticity but canbe flawed and applied in different ways Most of them cannotbe standardized across traits or compared among differentspecies [78] complicating comparison among studies [3 79]Moreover measures of phenotypic plasticity are stronglyrelated to the context and may not be comparable acrossdifferent studies where different gradients andor specieshave been used [77] Since information about plasticity isstructured in a way that makes it difficult for quantitative andcomparative analysis Poorter et al [79] proposed a methodto fill this gap by building a large database which currently


000005010015020025030035040

000

050

100

150

200

250

000050100150200250300350400

Air temperature

LA (m

2)

LMA

(Kg m

minus2)

T1 T2 T3




P lentiscusS aspera

Chlab
















4 Shade Tolerance



000510152025303540


0020406080

100120140

00051015202530


LMA 041 028 024SLA 041 029 024









ChlCar 032 032 042016 015 008044 043 051



WUE 086 092 085PNUE 092 095 093

014 012 010Mean value 071 070 069





PNU

E (120583

mol

gminus1

sminus1)

Chlab

Chl a + b

Chl ab

N

ChlN

PNgs

Ψm

N (m

g gminus1)


119904


119898

) are shown






Shade-tolerant




Intermediate







2) exchange









5 Ecotypes





Plasticity index A

A

B

B

C

C


073 073 067073 079 077

E 084 084 082WUE 088 087 082

089 093 093


LA 024 027 033DM 019 040 032SLA 015 027 015LMA 015 027 015LTD 021 032 015


PN

gs

Ψpd

0

50

100

150

200

0

25

50

75

100

0

50

100

150

200

0

25

50

75

100

0

50

100

150

200

0

25

50

75

100

T(∘

C)T

(∘C)

T(∘

C)

T

T

T

A

BC

R(m

m)

R(m

m)

R(m

m)

R

R

R





119873















LA 020 119875119873

063DM 039 119892

119904

065LMA 038 119877 053LTD 042 WUE 036

Ψ119898

073Chl 031RWC 021119875119892


Isatis apennina

LA 025 119875119873

042DM 032 119892

119904

048LMA 030 119877 072LTD 033 WUE 026

Ψ119898

048Chl 017RWC 015119875119892


Sesleria nitida



119904











119892) leaf







8 Conclusions







References































































































2











































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


000005010015020025030035040

000

050

100

150

200

250

000050100150200250300350400

Air temperature

LA (m

2)

LMA

(Kg m

minus2)

T1 T2 T3




P lentiscusS aspera

Chlab
















4 Shade Tolerance



000510152025303540


0020406080

100120140

00051015202530


LMA 041 028 024SLA 041 029 024









ChlCar 032 032 042016 015 008044 043 051



WUE 086 092 085PNUE 092 095 093

014 012 010Mean value 071 070 069





PNU

E (120583

mol

gminus1

sminus1)

Chlab

Chl a + b

Chl ab

N

ChlN

PNgs

Ψm

N (m

g gminus1)


119904


119898

) are shown






Shade-tolerant




Intermediate







2) exchange









5 Ecotypes





Plasticity index A

A

B

B

C

C


073 073 067073 079 077

E 084 084 082WUE 088 087 082

089 093 093


LA 024 027 033DM 019 040 032SLA 015 027 015LMA 015 027 015LTD 021 032 015


PN

gs

Ψpd

0

50

100

150

200

0

25

50

75

100

0

50

100

150

200

0

25

50

75

100

0

50

100

150

200

0

25

50

75

100

T(∘

C)T

(∘C)

T(∘

C)

T

T

T

A

BC

R(m

m)

R(m

m)

R(m

m)

R

R

R





119873















LA 020 119875119873

063DM 039 119892

119904

065LMA 038 119877 053LTD 042 WUE 036

Ψ119898

073Chl 031RWC 021119875119892


Isatis apennina

LA 025 119875119873

042DM 032 119892

119904

048LMA 030 119877 072LTD 033 WUE 026

Ψ119898

048Chl 017RWC 015119875119892


Sesleria nitida



119904











119892) leaf







8 Conclusions







References































































































2











































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology











4 Shade Tolerance



000510152025303540


0020406080

100120140

00051015202530


LMA 041 028 024SLA 041 029 024









ChlCar 032 032 042016 015 008044 043 051



WUE 086 092 085PNUE 092 095 093

014 012 010Mean value 071 070 069





PNU

E (120583

mol

gminus1

sminus1)

Chlab

Chl a + b

Chl ab

N

ChlN

PNgs

Ψm

N (m

g gminus1)


119904


119898

) are shown






Shade-tolerant




Intermediate







2) exchange









5 Ecotypes





Plasticity index A

A

B

B

C

C


073 073 067073 079 077

E 084 084 082WUE 088 087 082

089 093 093


LA 024 027 033DM 019 040 032SLA 015 027 015LMA 015 027 015LTD 021 032 015


PN

gs

Ψpd

0

50

100

150

200

0

25

50

75

100

0

50

100

150

200

0

25

50

75

100

0

50

100

150

200

0

25

50

75

100

T(∘

C)T

(∘C)

T(∘

C)

T

T

T

A

BC

R(m

m)

R(m

m)

R(m

m)

R

R

R





119873















LA 020 119875119873

063DM 039 119892

119904

065LMA 038 119877 053LTD 042 WUE 036

Ψ119898

073Chl 031RWC 021119875119892


Isatis apennina

LA 025 119875119873

042DM 032 119892

119904

048LMA 030 119877 072LTD 033 WUE 026

Ψ119898

048Chl 017RWC 015119875119892


Sesleria nitida



119904











119892) leaf







8 Conclusions







References































































































2











































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


000510152025303540


0020406080

100120140

00051015202530


LMA 041 028 024SLA 041 029 024









ChlCar 032 032 042016 015 008044 043 051



WUE 086 092 085PNUE 092 095 093

014 012 010Mean value 071 070 069





PNU

E (120583

mol

gminus1

sminus1)

Chlab

Chl a + b

Chl ab

N

ChlN

PNgs

Ψm

N (m

g gminus1)


119904


119898

) are shown






Shade-tolerant




Intermediate







2) exchange









5 Ecotypes





Plasticity index A

A

B

B

C

C


073 073 067073 079 077

E 084 084 082WUE 088 087 082

089 093 093


LA 024 027 033DM 019 040 032SLA 015 027 015LMA 015 027 015LTD 021 032 015


PN

gs

Ψpd

0

50

100

150

200

0

25

50

75

100

0

50

100

150

200

0

25

50

75

100

0

50

100

150

200

0

25

50

75

100

T(∘

C)T

(∘C)

T(∘

C)

T

T

T

A

BC

R(m

m)

R(m

m)

R(m

m)

R

R

R





119873















LA 020 119875119873

063DM 039 119892

119904

065LMA 038 119877 053LTD 042 WUE 036

Ψ119898

073Chl 031RWC 021119875119892


Isatis apennina

LA 025 119875119873

042DM 032 119892

119904

048LMA 030 119877 072LTD 033 WUE 026

Ψ119898

048Chl 017RWC 015119875119892


Sesleria nitida



119904











119892) leaf







8 Conclusions







References































































































2











































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology




Shade-tolerant




Intermediate







2) exchange









5 Ecotypes





Plasticity index A

A

B

B

C

C


073 073 067073 079 077

E 084 084 082WUE 088 087 082

089 093 093


LA 024 027 033DM 019 040 032SLA 015 027 015LMA 015 027 015LTD 021 032 015


PN

gs

Ψpd

0

50

100

150

200

0

25

50

75

100

0

50

100

150

200

0

25

50

75

100

0

50

100

150

200

0

25

50

75

100

T(∘

C)T

(∘C)

T(∘

C)

T

T

T

A

BC

R(m

m)

R(m

m)

R(m

m)

R

R

R





119873















LA 020 119875119873

063DM 039 119892

119904

065LMA 038 119877 053LTD 042 WUE 036

Ψ119898

073Chl 031RWC 021119875119892


Isatis apennina

LA 025 119875119873

042DM 032 119892

119904

048LMA 030 119877 072LTD 033 WUE 026

Ψ119898

048Chl 017RWC 015119875119892


Sesleria nitida



119904











119892) leaf







8 Conclusions







References































































































2











































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology





5 Ecotypes





Plasticity index A

A

B

B

C

C


073 073 067073 079 077

E 084 084 082WUE 088 087 082

089 093 093


LA 024 027 033DM 019 040 032SLA 015 027 015LMA 015 027 015LTD 021 032 015


PN

gs

Ψpd

0

50

100

150

200

0

25

50

75

100

0

50

100

150

200

0

25

50

75

100

0

50

100

150

200

0

25

50

75

100

T(∘

C)T

(∘C)

T(∘

C)

T

T

T

A

BC

R(m

m)

R(m

m)

R(m

m)

R

R

R





119873















LA 020 119875119873

063DM 039 119892

119904

065LMA 038 119877 053LTD 042 WUE 036

Ψ119898

073Chl 031RWC 021119875119892


Isatis apennina

LA 025 119875119873

042DM 032 119892

119904

048LMA 030 119877 072LTD 033 WUE 026

Ψ119898

048Chl 017RWC 015119875119892


Sesleria nitida



119904











119892) leaf







8 Conclusions







References































































































2











































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


Plasticity index A

A

B

B

C

C


073 073 067073 079 077

E 084 084 082WUE 088 087 082

089 093 093


LA 024 027 033DM 019 040 032SLA 015 027 015LMA 015 027 015LTD 021 032 015


PN

gs

Ψpd

0

50

100

150

200

0

25

50

75

100

0

50

100

150

200

0

25

50

75

100

0

50

100

150

200

0

25

50

75

100

T(∘

C)T

(∘C)

T(∘

C)

T

T

T

A

BC

R(m

m)

R(m

m)

R(m

m)

R

R

R





119873















LA 020 119875119873

063DM 039 119892

119904

065LMA 038 119877 053LTD 042 WUE 036

Ψ119898

073Chl 031RWC 021119875119892


Isatis apennina

LA 025 119875119873

042DM 032 119892

119904

048LMA 030 119877 072LTD 033 WUE 026

Ψ119898

048Chl 017RWC 015119875119892


Sesleria nitida



119904











119892) leaf







8 Conclusions







References































































































2











































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology













LA 020 119875119873

063DM 039 119892

119904

065LMA 038 119877 053LTD 042 WUE 036

Ψ119898

073Chl 031RWC 021119875119892


Isatis apennina

LA 025 119875119873

042DM 032 119892

119904

048LMA 030 119877 072LTD 033 WUE 026

Ψ119898

048Chl 017RWC 015119875119892


Sesleria nitida



119904











119892) leaf







8 Conclusions







References































































































2











































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology



8 Conclusions







References































































































2











































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology





























































































2











































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology



























































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

Plant Phenotypic Plasticity in Response to …themodern.farm/studies/Plant Phenotypic Plasticity in...

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Transcript of Plant Phenotypic Plasticity in Response to …themodern.farm/studies/Plant Phenotypic Plasticity in...