research article differential effects of lichens...

Research ArticleDifferential Effects of Lichens versus Liverworts Epiphylls onHost Leaf Traits in the Tropical Montane Rainforest HainanIsland China

Lingyan Zhou1 Fude Liu12 Wenjie Yang1 Hong Liu34 Hongbo Shao5

Zhongsheng Wang1 and Shuqing An1

1 The Laboratory of Forest Ecology and Global Changes School of Life Sciences Nanjing University Nanjing 210093 China2 School of Environmental Science and Safety Engineering Tianjin University of Technology Tianjin 300384 China3Department of Environmental Studies Florida International University Miami FL 33199 USA4Center for Tropical Plant Conservation Fairchild Tropical Botanic Garden Coral Gables Miami FL 33156 USA5 Key Laboratory of Coastal Biology amp Bioresources Utilization Yantai Institute of Coastal Zone Research Chinese Academy of Sciences(CAS) Yantai 264003 China

Correspondence should be addressed to Fude Liu fudeliu2005163com and Hongbo Shao shaohongbochu126com

Received 24 March 2014 Accepted 28 April 2014 Published 4 June 2014

Academic Editor Marian Brestic

Copyright copy 2014 Lingyan Zhou et al 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

Epiphylls widely colonize vascular leaves in moist tropical forests Understanding the effects of epiphylls on leaf traits of host plantsis critical for understanding ecological function of epiphylls A study was conducted in a rain forest to investigate leaf traits of thehost plants Photinia prunifolia colonized with epiphyllous liverworts and foliicolous lichens as well as those of uncolonized leavesOur results found that the colonization of lichens significantly decreased leaf water content (LWC) chlorophyll (Chl) a and a +b content and Chl ab of P prunifolia but increased Chl b content while that of liverworts did not affect them as a whole Thevariations of net photosynthetic rates (119875

119899) among host leaves colonized with different coverage of lichens before or after removal

treatment (a treatment to remove epiphylls from leaf surface) were greater than that colonized with liverworts The full cover oflichens induced an increase of light compensation point (LCP) by 21 and a decrease of light saturation point (LSP) by 54 for theirhost leaves whereas that of liverworts displayed contrary effects Compared with the colonization of liverworts lichens exhibitedmore negative effects on the leaf traits of P prunifolia in different stages of colonizationThe results suggest that the responses of hostleaf traits to epiphylls are affected by the epiphyllous groups and coverage which are also crucial factors in assessing ecofunctionsof epiphylls in tropical forests

1 Introduction

Carbon (C) enters ecosystems via the process of photo-synthesis which is the most important exchange betweenecosystems and the atmosphere [1] Leaf traits link closelywith the photosynthetic characteristics of leaves and affect thecapability of plants to sequestrate C [2ndash4] However leavesof vascular plants are usually covered with epiphylls [5 6] inhumid understory of the tropical forests For example up to40 of the leaf surface was covered by epiphylls in an Aus-tralia tropical rain forest [7] Epiphylls are usually small cryp-togams growing on the upper surfaces of the host leaves [8]

and commonly consist of two dominant visible groupsepiphyllous liverworts and foliicolous lichens (referred to asliverworts and lichens) [9]

The occurrence of epiphylls would induce a series ofsignificant ecological and evolutionary impacts on host plants[10ndash12] due to the physical separation of epiphylls betweenthe leaf surface and the atmosphere Therefore any potentialchange in epiphyllous communities including shifting ofcommunity compositions and alteration of total coverage[13 14] may considerably affect leaf traits of host plantssubsequently In addition compared with vascular plants

Hindawi Publishing Corporatione Scientific World JournalVolume 2014 Article ID 681369 10 pageshttpdxdoiorg1011552014681369

2 The Scientific World Journal

epiphylls are more sensitive to environmental changes owingto their particular structure and physiology [15ndash17] Whetheror not epiphylls exacerbate or mitigate the effects of climatechange on host vascular plants is crucial for understandingecological functions of epiphyllous communities in tropicalforests

Previous studies paid more attention to nitrogen (N)transfer between epiphylls and hosts [9 18ndash22] due to theability of N fixation of epiphylls [23] However how epiphyllsaffect leaf physiological traits is still unclear [13 14] Someresearch has found that epiphylls decreased light radiationand photosynthetic capability of host leaves [24ndash27] whilesome thought that the photoacclimation of host plants couldoffset the negative effects of epiphylls [10 28 29] Theseinconsistencies may result from the diverse composition ofepiphyllous communities and undefined succession stages ofepiphyllous colonization [14] For examples the epiphyllousgroups in Monge-Najera (1989) and Anthony et al (2002)were liverworts and lichens respectively [10 30]

Communities dominated by lichens or liverworts mayinduce different effects on leaf traits of host plants due to theirdiverse structure characteristics [15] and distribution patternson host leaves [14 31] In addition the coverage of epiphyllsgenerally varies largely from sporadic to full cover [25 31] inthe successive process of epiphyllous colonization [7 13 14]which may be also crucial in understanding the roles ofepiphylls on hosts Therefore it is necessary to differentiateeffects of liverworts and lichens on host plants to betterunderstand the exact roles of epiphylls on their host plants

The tropicalMontane rain forests inHainan Island are thelargest and best preserved primary tropical forest in ChinaThe forests harbor diverse epiphylls on the surface of hostleaves in the understory In this study we studied the effectsof liverworts versus lichens with varying degrees of coverson their host tree species Photinia prunifolia in a tropicalMontane forest in Hainan Island We asked the followingquestions (1) Does epiphyllous colonization affect hostrsquos leaftraits (2) Do the effects of epiphyllous groups (liverwortsversus lichens) on hostrsquos leaf traits vary (3) How do theircoverages affect the effects on hostrsquos leaf traits

2 Materials and Methods

21 Study Site and Species The study was conducted in atropical Montane rain forest at the Jianfengling NationalNature Reserve (JNNR) (18∘231015840ndash18∘501015840N 108∘461015840ndash109∘021015840E)which is located in the southwest of Hainan Island ChinaJNNR is dominated by tropical monsoon climate with anaverage air temperature of 245∘C relative humidity of 88and annual sunshine of 1467 h [32] Annual precipitationranges from 1305 to 3662mm with a distinct wet season(May to October) and a dry season (November to April) [32]The monthly temperature and precipitation there had beendescribed by Yang et al [33] Due to the humid environmentapproximately up to 145 leaf area of plants in the understorywas covered with epiphylls (average percentage of leaves withepiphylls times average coverage on leaves) in which more than60 species of epiphyllous liverworts have been identified

(unpublished data) In order to obtain a relatively consistentspecies composition in epiphyllous communities we selectedhost plants within a plot with a diameter of 5 km

We selected the vascular plants Photinia prunifolia ashost plants in this study for the following reasons Firstly Pprunifolia was a common species with epiphylls at the studysite Secondly the average coverage of epiphylls on thematureleaves of P prunifolia was about 313 which was ideal forsampling purpose Thirdly it was easy to remove epiphyllsfrom coriaceous leaves of P prunifolia for manipulativetreatment Leaves with comparable sizes and locations on thebranches were selected from a large number of labeled leaveswhich had been selected out two years ago when they weretender leaves with no epiphylls We excluded leaves coveredwith mixed epiphyllous community of liverworts and lichensto avoid the interaction effects of the two groups The dom-inant species of lichens on the surface of P prunifolia werePorina chrysophora and P atrocaerulea and the dominantliverworts were Drepanolejeunea spicata Radula acuminataColura acroloba and Leptolejeunea maculata

22 Measurement Using a plastic sheet marked with 2 times2mm2 grids we measured the coverage of epiphylls (com-prised of liverworts or lichens) on leaf surface followingmethods specified in Roskoski (1981) [13]The leaves with 0coverage of epiphylls (uncolonized leaves) were used as thecontrol groups to be compared with leaves colonized by liver-worts or lichens Leaves colonized with liverworts or lichenswere divided into four subgroups according to levels ofcoverage 25 50 75 and 100 (plusmn5 error) respectivelyThe following physical leaf traits were measured leaf massper area (LMA) leaf water content (LWC) and chlorophyll(Chl) content (a and b) We used the method by Linder(1974) and Arnon (1949) for pretreatment and measurementof Chl content respectively [34 35] The contents of Chl a ba + b (mg gminus1) and ab ratios were calculated subsequentlyPhysical leaf trait measurements were replicated 5 times foreach subgroup one replication per tree

Before sampling photosynthetic light-response curves ofthese leaves were examined using the ldquoLight Curverdquo auto-matic program in Li-6400 Portable Photosynthesis System(LI-COR USA) with a 6400-02B RedBlue light sourcechamber (2 times 3 cm) Leaves were allowed 10min to acclimatethe changes of light intensity before measurements whichwere made following photosynthetic photon flux (PPF) 010 20 50 100 200 500 1000 1500 and 2000120583molmminus2 sminus1during 900ndash1200 am when the ambient temperature was20 plusmn 2

∘C and relative humidity ranged from 50 to 70Airflow rate was kept constant at 05 Lminminus1 with 380 plusmn10 120583molmolminus1 CO

2concentrations during themeasurement

In order to determine whether impacts of epiphylls onleaves were temporary epiphylls were removed from thesurface of leaves after photosynthetic measurement usingmethods described by Eze and Berrie (1977) [36] Light-response curves of postremoval leaves were measured usingthe same method two days later after the removal treatment(hereafter preremoval and postremoval were referred to thephotosynthetic traits of leaves covered with epiphylls and

The Scientific World Journal 3

those of epiphylls were removed resp) These measurementswere replicated on 4 leaves from different trees in each sub-group Parameters of photosynthetic light-response curveswhich included respiration rate (119877) maximumnet photosyn-thesis rate (119875max) light compensation point (LCP) and lightsaturation point (LSP) in preremoval and postremoval wereestimated by nonrectangular hyperbola model [37]

119860 =120593119876 + 119860max minus radic(120593119876 + 119860max)

2

minus 4120593119876119896119860max

2119896minus 119877

(1)

where 119860 is net photosynthetic rate 120593 is apparent quantumefficiency 119876 is photosynthetically active radiation 119860max ismaximum net photosynthetic rate 119896 is an angle of photosyn-thesis light curve and 119877 is a dark respiration rate

23 Data Analysis Differences of leaf traits among the fivelevels of coverage (0 25 50 75 and 100) were testedby Tukeyrsquos multiple comparison Studentrsquos 119905-test was used toinvestigate the differences of leaf traits between leaves coveredwith liverworts and lichens The differences of leaf traits inthe same leaves between pre- and postremoval treatmentswere tested by Paired-Samples 119905-test Differences of net pho-tosynthetic rates among light-response curveswere examinedby nonparametric tests (K related samples test) Effects ofepiphyllous groups (liverworts and lichens) coverage (025 50 75 and 100) and removing treatment onphysical traits of P prunifolia leaves were examined usingtwo-way ANOVA or three-way ANOVA

3 Results

31 Physical Leaf Traits of Host Leaves with Different EpiphyllsThe colonization of liverworts did not significantly affect allleaf traits of host (ie leaf mass per area (LMA) leaf watercontent (LWC) chlorophyll content (Chl) and Chl ab ratio)with increasing coverage from 25 to 100 compared to thecontrol group (0 coverage Figure 1) The colonization oflichens significantly decreased LMA only at full coverage(asymp100) compared to the control group while it decreasedChl a and Chl a + b at almost all coverage from 25 to 100except Chl a + b at full coverage (Figures 1(a) 1(c) and1(e)) Lichens significantly decreased LWC and Chl ab andincreased Chl b with increasing coverage when its coveragewas larger than 50 (Figures 1(b) 1(d) and 1(f))

Leaves covered with liverworts exhibited a significantlylower LMA than that in leaves colonized with lichens atcoverage of 50 and 75 but displayed a significantlyhigher one compared to that with lichens at fall coverage(Figure 1(a)) The Chl b of leaves colonized with 75ndash100liverworts was also significantly lower than that colonizedwith lichens (Figure 1(d)) However the LWC and Chl abof leaves covered with liverworts were significantly higherthan that with lichens when the coverage was larger than 50(Figures 1(b) and 1(f)) The Chl a and Chl a + b of leavescolonized with liverworts were all significantly higher thanthese with lichens (Figures 1(c) and 1(e)) The interactions ofthe levels of epiphyllous coverage (0 25 50 75 and100) and groups (liverworts and lichens) were all significant

in LMA LWCChl a Chl b andChl ab (119875 lt 005) except Chla + b (119865 = 132 119875 gt 005) while the main effect of coveragersquoslevels on Chl a + b was significant (119865 = 371 119875 lt 005)(Table 1)

32 Leaf Photosynthesis in Pre- and Postremoval Treat-ments Net photosynthetic rates (119875

119899) of light-response curves

increased from 0 to 500 umol photons mminus2 sminus1 and thenreached a plateau (Figure 2) Except for the leaves colo-nized with 25 liverworts other light-response curves ofP prunifolia leaves (including those colonized by liverwortsand lichens) were all significantly different from those in theuncolonized leaves (119875 lt 005) With increasing coverage ofepiphylls 119875

119899continuously increased from 25 to 75 while

it decreased at 100 coverage (Figures 2(a) and 2(c)) Inpostremoval most curves in leaves colonized by liverwortspreviously were no longer different significantly (119875 gt 005)from those in uncolonized leaves except that in leaveswith 100 liverworts previously (119875 = 0041) In contrastdifferences in 119875

119899between postremoval leaves colonized by

lichens previously and uncolonized leaves were smaller thanthose between preremoval and uncolonized leaves but werestill statistically significant (119875 lt 005) (Figures 2(b) and 2(d))

Epiphylls showed a negligible effect on total respirationrate (119877) of leaves colonized with epiphylls in preremoval(left panel Figure 3(a)) but the treatment of removingepiphylls resulted in a significant variation of 119877 in mostleaves of P prunifolia particularly for those with 25ndash75 liverworts exhibited significant higher 119877 (119875 lt 005)compared with uncolonized leaves Leaves colonized with100 lichens had a significantly higher 119877 (119875 = 0040) inpostremoval comparedwith those in preremoval (right panelFigure 3(a)) With the exception of that in coverage andremoval interactions among epiphyllous groups coverageand treatment of removal (removal) were all significant in119877 of P prunifolia leaves (Table 2) Epiphyll colonization didnot affect the maximum net photosynthesis rates (119875max) ofhost leaves in general (119875 gt 005 Figure 3(b)) except that ofleaveswith 50 lichens in preremoval with a higher119875max (119875 =0042) in spite of the corresponding photosynthetic photonflux for 119875max that was different (Figure 2) The interaction ofcoverage and removal was significant in 119875max

The leaves of P prunifolia colonized with lichens exhib-ited a significant higher light compensation point (LCP) at100 coverage (116 120583mol mminus2sminus1) than that of uncolonizedleaves (76 120583molmminus2 sminus1) In contrast the LCP of leavescolonized with 100 liverworts exhibited a significant lowerone contrarily (left panel Figure 3(a)) The difference in LCPbetween leaves colonized with lichens and liverworts becamesignificant when the coverage is large enough (75ndash100119875 lt 005) In contrast it was only significant at full coverageof epiphylls after removal (119875 = 0048) The interactionof epiphyllous groups and coverage was significant on LCP(Table 2)

In preremoval the difference in light saturation point(LSP) between leaves colonized with lichens and liverwortswas also significant when the coverage was 100 Remov-ing treatment expanded the difference between epiphyllousgroups in postremoval at full coverage and exhibited contrary


160

140

120

100

80

60

40

20

0

a aa

blowast

lowast

a

lowast

LMA

(g m

minus2)

(a)

a ab bc

c

lowastlowast

lowast

100

80

60

40

20

0

LWC

()

(b)

5

4

3

2

1

0

a

lowastb lowastb lowastb lowastb

Chl a

(mg g

minus1)

(c)

20

15

10

05

00

lowastlowastab

b

ba

a

b

Chl b

(mg g

minus1)

(d)

6

4

2

00

25 50 75 100

Coverage ()

a

blowastblowast ablowastblowast

Leaves colonized with lichensLeaves colonized with liverworts

Chl a+

b (m

g gminus1)

(e)

3

2

1

0

Chl a

b

0 25 50 75 100

Coverage ()

aab

blowastcblowast

clowast


(f)

Figure 1 Physical leaf traits of Photinia prunifolia colonized with lichens and liverworts at different coverages (0 25 50 75 and 100)(a) Leaf mass per area (LMA) (gmminus2) (b) leaf water content (LWC) () (c) concentration of chlorophyll a (Chl a) (mg gminus1) (d) concentrationof chlorophyll b (Chl b) (mg gminus1) (e) concentration of chlorophyll a + b (Chl a + b) (mg gminus1) and (f) chlorophyll ab ratio (Chl ab) (meanplusmn 1 SE) (119899 = 5) Different lowercase letters above the bars indicate the differences of physical leaf traits among leaves colonized with lichensthe symbol lowastindicates the difference between leaves colonized with liverworts and lichens (119875 lt 005)

effects on LSP between leaves colonized with liverwortsand lichens In postremoval the LSP of leaves colonizedwith liverworts previously increased with an increasingdegree of coverage and was significantly different from theuncolonized leaves at 75 and 100 coverage (Figure 3(d))

Full coverage of lichens decreased LSP of leaves by 54while that of liverworts increased LSP of leaves by 43The interactions of epiphyllous groups and coverage groupsand removal were significant in LSP of P prunifolia leaves(Table 2)


0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1

PPF (120583mol photons mminus2 sminus1)

Pn

(120583m

olCO

2mminus2

sminus1)

(a)

0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(b)

0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(c)

0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(d)

Figure 2 Photosynthetic light-response curves of leaves of Photinia prunifolia colonized with liverworts (a and b) or lichens (c and d) pre-(a and c) versus postremoval (b and d) (mean plusmn 1 SE) (119899 = 4)

Table 1 Effects (119865 value) of epiphyllous coverage (coverage 0 25 50 75 and 100) and epiphyllous groups (groups liverworts andlichens) on the leaf traits leaf mass per area (LMA) leaf water content (LWC) concentration of chlorophyll a (Chl a) Chl b Chl a + b andChl ab of Photinia prunifolia in JNNR

df LMA LWC Chl a Chl b Chl a + b Chl abCoverage 4 862lowastlowastlowast 301lowast 498lowastlowast 267lowast 371lowast 155ns

Groups 1 209ns 151lowastlowastlowast 309lowastlowastlowast 594lowast 352ns 190lowastlowastlowast

Coverage times groups 4 546lowastlowast 317lowast 555lowastlowast 303lowast 132ns 601lowastlowastlowast

119875 lt 005 lowastlowast119875 lt 001 lowastlowastlowast119875 lt 0001 nsNot significant

4 Discussion

41 Effects of Epiphylls on the Physical Leaf Traits of Pprunifolia In tropical rain forest light is one of the mostimportant limitation affecting plant growth [2] especially

in the understory which received only 05ndash50 of thesunlight [12] Thus the wide distribution of epiphylls maymake the low-light condition worse for hosts there [10 36]Host leaves are assumed to modify a series of physical traitsin some extent to acclimate the colonization of epiphylls [30]


Preremoval Postremoval

100

75

50

25

0

Cov

erag

e (

)

04 0402 0200

Alowast

Alowast

Ablowast

Ablowast

a

aa

b

blowastB

B

aB

aB

a


R (120583mol CO2 mminus2 sminus1)

(a)

100

75

50

25

0

Cov

erag

e (

)

4 2 0 2 4

b

lowast

a

a

a

a


Pmax (120583mol CO2 mminus2 sminus1)


(b)

100

75

50

25

0

Cov

erag

e (

)


20 10 0 10 20

aa

aa

aa

a

a

a

a

Ab AbB bB

LCP (120583mol mminus2 sminus1)


(c)

100

75

50

25

0

Cov

erag

e (

)


lowastlowast

a

a

a

a aa

aa

aa

aa

AA bbB bB

600 3000300 600

LSP (120583mol mminus2 sminus1)


(d)

Figure 3 Estimated photosynthetic parameters of Photinia prunifolia colonized with lichens and liverworts pre- versus postremoval (meanplusmn1 SE) (119899 = 4) (a) Respiration rate (119877) (b)maximum rates of photosynthesis (119875max) (c) light compensation point (LCP) and (d) light saturationpoint (LSP)The symbol lowastindicates the difference of photosynthetic parameters between pre- and postremoval treatment different small andcapital letters near the bars indicate the differences among leaves with different coverage and between leaves colonized with liverworts andlichens (119875 lt 005)

As a composite parameter associated with a suite of structuraltraits leaf mass per area (LMA) can be understood as anindex of leaf-level cost for light interception of host leavesand an important indicator of plant strategies [38 39] In thisstudy colonization of liverworts did not induce significantchanges in hostrsquos LMA overall while leaves with full coverageof lichens exhibited the lowest LMA In addition the leavescolonized with liverworts exhibited a significantly lowerLMA than that with lichens at coverage of 50 and 75respectively (Figure 1(a)) In general leaves possessed a lowerLMA adapted to the low-light condition much better thanthat with a higher one [40 41] Therefore the host leaves

coveredwith liverworts (50ndash75)may bemore competitivethan that with lichens especially under the increased shadingcondition [16] However leaves colonized with 100 lichensdecreased LMA significantly by 186 compared with that inuncovered leaves which may be attributed to the decline ofphotosynthetic output in mesophyll tissue due to the densecoverage of lichens [12 42]

Lichens colonization on leaves of P prunifolia also dis-played a significantly negative effect on leaf water content(LWC) when the coverage was larger than 50 (Figure 1(b))while the colonization of liverworts exhibited no effecton hostrsquos LWC at any coverage Although some epiphylls


Table 2 Effects of epiphyllous coverage (0 25 50 75 and 100) epiphyllous groups (groups liverworts and lichens) and treatmentof removal (preremoval and postremoval) on photosynthetic parameters respiration rate (119877) maximum rates of photosynthesis (119875max) lightcompensation point (LCP) and light saturation point (LSP) of Photinia prunifolia in JNNR

Source df 119877 119875max LCP LSPGroups 1 088ns 386ns 206lowastlowastlowast 160lowastlowastlowast

Coverage 4 168ns 185lowastlowastlowast 0556ns 102lowastlowastlowast

Removal 1 846lowastlowast 291lowastlowastlowast 0120ns 114ns

Groups times coverage 4 290lowast 120ns 665lowastlowastlowast 186lowastlowastlowast

Coverage times removal 4 160ns 591lowastlowastlowast 0566ns 232ns

Groups times removal 1 834lowastlowast 215ns 115ns 649lowast

Groups times coverage times removal 4 570lowastlowastlowast 205ns 0239ns 231nslowast


(including lichens and liverworts) growing between thecuticle and epidermis had been indicated to absorb waterfrom their hosts during periods of drought [8 12 16] theLWC of host leaves would not decline significantly unless thewater transport of host plants was depressed by colonizationof epiphylls [43] Although both lichens and liverworts arepoikilohydric the former are more likely to occur in dryhabitat than the latter [44] This physiological drought ofhost leaves resulted from lichens colonization that may makelichens more competitive over liverworts and accelerate thesenescence of host leaves accordingly [8 25] Thereforethe lowest LWC of leaves colonized with 100 lichens alsosupported the assumption that the leaves colonized with fullcover of lichens may be ready for shedding [45]

Changes of chlorophyll contents in host leaves in responseto epiphyllous colonization are crucial topics related tothe acclimation of hosts to epiphyllous colonization [3646 47] The colonization of lichens significantly decreasedchlorophyll content (Chl) a a + b and ab (Figures 1(c) 1(e)and 1(f)) but increased Chl b in host leaves of P prunifolia(Figure 1(d)) while the colonization of liverworts inducedno changes of them even at full coverage (Figures 1(c)ndash1(f)) Combined with the change in LMA lichensrsquo effecton total chlorophyll content (120583g Chl cm2) of P prunifoliawas comparable with the results from Anthony et al (2002)[10] Lichens colonized on the leaves commonly are thoughtto prefer the habitat with higher light relative to liverworts[48]Their absorptance spectra were also demonstrated to besimilar to those of host leaves [10 16] while most epiphyllousliverworts possessed lower Chl ab ratio with higher levelsof Chl b and were adapted to low-light intensities betterthan did lichens [44] Therefore relative to light competitionbetween liverworts and host leaves the light competitionbetween lichens and hosts would be more significant whichthus inducedmoremodification in hostrsquos chlorophyll such asdecreased Chl ab (Figure 1(f)) [28 29]

42 Effects of Epiphylls on Photosynthesis of Host LeavesBecause of the independent photosynthetic capacity of liver-worts and photobionts from lichens [15 16 49] the coatingof epiphylls had been considered widely to affect the pho-tosynthetic efficiency of host leaves [10 13 36] With theexception of leaves colonized with 25 liverworts and full

epiphylls rates of C assimilation per unit leaf area colonizedwith epiphylls were all higher than that in single uncoveredleaves of P prunifolia (Figures 2(a) and 2(c)) Combinedwith the well-known contribution of epiphylls for N-fixationfor host leaves [9 18 22] the colonization of epiphyllsmay increase the photosynthetic efficiency in communitylevel at some extent Although there is a general perceptionthat both lichens and liverworts have low photosyntheticrates compared to their host vascular plants [15] the largerdiversity of photosynthetic rates (119875

119899) induced by increasing

of lichens coverage implied a relative higher rate of lichenscompared with that of liverworts (Figures 2(a) and 2(c))

However the respiration rate (119877) and maximum netphotosynthesis rates (119875max) of leaves with coating of lichensand liverworts did not show the expected increase as theirlarger intragroup variance in the same level of coverageexcepted for the larger 119875max in leaves covered with 50lichens (Figures 3(a) and 3(b) left panels) This negligiblecontribution of epiphylls to total 119877 and 119875max was similarwith that of lichens on host plants (Calamus australis) inAnthony et al (2002) [10] The full coverage of both lichensand liverworts induced some interesting changes of lightcompensation point (LCP) and light saturation point (LSP)(Figures 3(c) and 3(d) left panels)The full coverage of lichensinduced an increased LCP but a decreased LSP of P prunifolialeaves which was inconsistent with general traits of plants inshading condition [50 51] whereas leaves covered with denseliverworts were characterized by a decreased LCP contrarilyThe dense coverage of liverworts advanced their hostsrsquo shadetolerance [52] but without any significant impacts on theirphysical leaf traits compared with that in uncolonized leaves(Figure 1)

By removing epiphylls on host leaves the effects ofepiphylls to light-response curves were eliminated inpostremoval however remained differences among bareleaves colonized with lichens previously were still larger thanthat with liverworts previously (Figure 2) The progressivecolonization of lichens leaded tomore accumulated effects ontheir hostrsquos photosynthetic capacity which may concurrentlyoccur with lichen-induced changes of physical leaf traits wediscussed above (Figure 1) However the significant increasesof respiration rate (119877) in some leaves induced by removaltreatment were unexpected (Figure 3(a) right panel)


The removal of dense lichen-induced increment of 119877 inbare leaves may be attributed to the relative larger leaf area(the same as the area of leaf chamber) disturbed by removaltreatment [53] Leaves colonized with full lichens andliverworts before still exhibited an increased and a decreasedLCP respectively after removal treatment (Figure 3(c) rightpanel) which also demonstrated that the lower LCP in thelatter was one of acclimated leaf traits but not the temporarycontribution from liverworts [14 22] The effects of removaltreatment on LSP in leaves with full epiphylls were contrarilybetween that with full lichens and liverworts (Figure 3(d)right panel) The decreased LSP (by lichens) may preventtheir leaves from utilizing sunflecks which are commonlyhigher irradiances and important sources of photosyntheticphoton flux (PPF) in the understory of tropical forestswhereas the increased LSP (by liverworts) may advance thiscapability to absorb them [51 54]

43 Advantage of Liverworts in Epiphyllous Community Therelations between liverworts and lichens on phyllosphere areknown as competitions in which liverworts are generallypreponderant and overgrow its opponent (lichens) [14 1655] For the host plants (P prunifolia) we selected in thisstudy lichensrsquo colonization had induced much more negativeimpacts on their physical leaf traits (Figure 1) as well ascorrelated photosynthetic parameters (eg LCP and LSPFigure 3) compared to that of liverworts In long termcoevolution between epiphylls and host plants epiphyllousgroup (liverworts) exhibited less disadvantageous effects onhosts that may possess more predominance in epiphyllouscommunity [14] unless environmental changes favoringlichens competition

In epiphyllous community liverworts commonly requiremore proportion of available water than lichens [12] Thusonce available water in environment decreased excessivewater loss during drought periods in the understory oftropical rain forest may depress the advantage of liverwortsin the competition with lichens [16] Increasing frequencyof drought and duration of heat waves may similarly inducemore wide distribution of lichens [56 57] Thereby currentstructure of epiphyllous community including ratios ofliverworts and lichens and total coverage on vascular plantsmay shift to some extent in responding to these new ratios ofavailable water and energy [58]

5 Conclusion and Prospect

In this study the effects of epiphylls on host plants werefocused on aspects of physical and photosynthetic leaf traitsLichens colonization (especially at full coverage) significantlydecreased leaf water content (LWC) chlorophyll (Chl) a anda + b content and Chl ab of P prunifolia but increasedChl b content while liverworts did not affect them as awhole (Figure 1) The variations of photosynthetic rates (119875

119899)

among host leaves induced by lichens before or after removaltreatment were all larger than liverworts (Figure 2) The fullcoverage of lichens even induced an increased LCP but adecreased LSP of P prunifolia leaves while that of liverworts

exhibited a contrary effect Our results suggested that theeffects of epiphyllous communities dominated by lichens orliverworts on host leaves had differentiated effects Comparedwith liverworts lichens colonization exhibited more adverseeffects on their hostrsquos leaf traits The coverage of epiphylls is acritical factor for determining the roles of epiphylls for hostleaves after all the vital effects on hosts only occur at largestcoverage

In natural understory of tropical rain forest with col-onization of epiphylls on phyllosphere some symbioticorganisms with epiphylls provide the host leaf protectionagainst herbivores and pathogens as well as the newly fixednitrogen The exact relationship between epiphylls and hostplants is much more complicated than the modification ofleaf traits Furthermore the advantage of liverworts relativeto lichens exhibited in affecting hostrsquos leaf traits may shiftwith current environmental changes as their environmentalsensitivity and ecological fragility More studies are neededto examine the ecophysiology of epiphylls particularly underthe background of climate change

Conflict of Interests

There is no conflict of interests regarding the publication ofthis paper

Acknowledgments

The authors are deeply indebted to Professor Yide Li for hishelp in sampling This study was supported by the SpecialResearch Program for Public-welfare Forestry (200804001)the General Program (30970512 30570298) and the Key Pro-gram (30430570) of National Natural Sciences Foundation ofChina

References

[1] O L Lange W Beyschlag and J D Tenhumen ldquoControl of leafcarbon assimilation-input of chemical energy into ecosystemsrdquoin Potentials and Limiatations of Ecosystem Analysis E DSchulze and H Zwlfer Eds pp 149ndash163 Springer BerlinGermany 1987

[2] L Poorter ldquoGrowth responses of 15 rain-forest tree species toa light gradient the relative importance of morphological andphysiological traitsrdquo Functional Ecology vol 13 no 3 pp 396ndash410 1999

[3] D M A Rozendaal V Hurtado and L Poorter ldquoPlasticityin leaf traits of 38 tropical tree species in response to lightrelationships with light demand and adult staturerdquo FunctionalEcology vol 20 no 2 pp 207ndash216 2006

[4] A Trewavas ldquoWhat is plant behaviourrdquo Plant Cell and Envi-ronment vol 32 no 6 pp 606ndash616 2009

[5] R Lucking Additions and Corrections to the Knowledge ofthe Foliicolous Lichen Flora of Costa Rica The Family Gom-phillaceae J Cramer Berlin Germany 1997

[6] R Lucking ldquoEcology of foliicolous lichens at the ldquoBotar-ramardquo trail (Costa Rica) a neotropical rainforest IV Speciesassociations their salient features and their dependence onenvironmental variablesrdquo The Lichenologist vol 31 no 3 pp269ndash289 1999


[7] J S Rogers E Clark G Cirvilleri and S E Lindow ldquoCloningand characterization of genes conferring copper resistance inepiphytic ice nucleation-active Pseudomonas syringae strainsrdquoPhytopathology vol 84 no 9 pp 891ndash897 1994

[8] G K Berrie and J M O Eze ldquoThe relationship between anepiphyllous liverwort and host leavesrdquoAnnals of Botany vol 39no 4 pp 955ndash963 1975

[9] B L Bentley and E J Carpenter ldquoDirect transfer of newly-fixednitrogen from free-living epiphyllous microorganisms to theirhost plantrdquo Oecologia vol 63 no 1 pp 52ndash56 1984

[10] P A Anthony J A M Holtum and B R Jackes ldquoShadeacclimation of rainforest leaves to colonization by lichensrdquoFunctional Ecology vol 16 no 6 pp 808ndash816 2002

[11] P D Coley and T A Kursar ldquoAnti-herbivore defenses of youngtropical leaves physiological constraints and ecological trade-offsrdquo in Tropical Forest Plant Ecophysiology S S Mulkey R LChazdon and A P Smith Eds pp 305ndash336 Springer NewYork NY USA 1996

[12] P D Coley T A Kursar and J L Machado ldquoColonization oftropical rain-forest leaves by epiphyllsmdasheffects of site and hostplant leaf lifetimerdquo Ecology vol 74 no 2 pp 619ndash623 1993

[13] J P Roskoski ldquoEpiphyll dynamics of a tropical understoryrdquoOikos vol 37 no 2 pp 252ndash256 1981

[14] L -Y Zhou Z -S Wang S -N Chen et al ldquoAdvances inresearches on ecological epiphyllsrdquo Chinese Journal of PlantEcology vol 33 no 5 pp 993ndash1002 2009

[15] T Green andO Lange ldquoPhotosynthesis in poikilohydric plantsa comparison of lichens and bryophytesrdquo in Ecophysiology ofPhotosynthesis pp 319ndash341 Springer NewYork NYUSA 1994

[16] A Pinokiyo K P Singh and J S Singh ldquoLeaf-colonizinglichens their diversity ecology and future prospectsrdquo CurrentScience vol 90 no 4 pp 509ndash518 2006

[17] T Pocs ldquoEpiphyllous liverwort diversity at worldwide level andits threat and conservationrdquoAnales del Instituto de Biologıa SerieBotanica vol 67 no 1 pp 109ndash127 2009

[18] B L Bentley ldquoNitrogen fixation by epiphylls in a tropicalrainforestrdquo Annals of the Missouri Botanical Garden vol 74 no2 pp 234ndash241 1987

[19] B L Bentley and E J Carpenter ldquoEffects of desiccation andrehydration on nitrogen fixation by epiphylls in a tropicalrainforestrdquoMicrobial Ecology vol 6 no 2 pp 109ndash113 1980

[20] E Freiberg ldquoMicroclimatic parameters influencing nitrogenfixation in the phyllosphere in a Costa Rican premontane rainforestrdquo Oecologia vol 117 no 1-2 pp 9ndash18 1998

[21] K Palmqvist and L Dahlman ldquoResponses of the green algalfoliose lichen Platismatia glauca to increased nitrogen supplyrdquoNew Phytologist vol 171 no 2 pp 343ndash356 2006

[22] W Wanek and K Portl ldquoPhyllosphere nitrogen relationsreciprocal transfer of nitrogen between epiphyllous liverwortsand host plants in the understorey of a lowland tropical wetforest in Costa Ricardquo New Phytologist vol 166 no 2 pp 577ndash588 2005

[23] J P Roskoski ldquoN2fixation (C

2H2reduction) by epiphylls on

coffee Coffea arabicardquoMicrobial Ecology vol 6 no 4 pp 349ndash355 1980

[24] R L Chazdon and N Fetcher ldquoPhotosynthetic light environ-ments in a lowland tropical rain forest in Costa Ricardquo Journal ofEcology vol 72 no 2 pp 553ndash564 1984

[25] D B Clark D A Clark andM H Grayum ldquoLeaf demographyof a neotropical rain forest cycad Zamia skinneri (Zamiaceae)rdquoThe American Journal of Botany vol 79 no 1 pp 28ndash33 1992

[26] S F Oberbauer D A Clark D B Clark and M QuesadaldquoComparative-analysis of photosynthetic light environmentswithin the crowns of juvenile rain-forest treesrdquo Tree Physiologyvol 5 no 1 pp 13ndash23 1989

[27] S F Oberbauer D B Clark and M Quesada ldquoCrown lightenvironments of saplings of two species of rain forest emergenttreesrdquo Oecologia vol 75 no 2 pp 207ndash212 1988

[28] R L Chazdon R W Pearcy D W Lee and N Fetcher ldquoPho-tosynthetic responses of tropical forest plants to contrastinglight environmentsrdquo in Tropical Forest Plant Ecophysiology S SMulkey R L Chazdon andA P Smith Eds pp 5ndash55 SpringerNew York NY USA 1996

[29] H Lambers F S Chapin and T L Pons Plant PhysiologicalEcology Springer New York NY USA 1998

[30] J Monge-Najera ldquoThe relationship of epiphyllous liverwortswith leaf characteristics and light in Monte Verde Costa RicardquoCryptogamie Bryologie vol 10 no 4 pp 345ndash352 1989

[31] M Sonnleitner S Dullinger W Wanek and H ZechmeisterldquoMicroclimatic patterns correlate with the distribution of epi-phyllous bryophytes in a tropical lowland rain forest in CostaRicardquo Journal of Tropical Ecology vol 25 no 3 pp 321ndash3302009

[32] Z Zhou Y-D Li M-X Lin et al ldquoChange characteristics ofthermal factors in tropical mountain rainforest area of Jianfen-gling Hainan Island in 1980ndash2005rdquo Chinese Journal of Ecologyvol 28 no 6 pp 1006ndash1012 2009

[33] W Yang F Liu L Zhou S Zhang and S An ldquoGrowth andphotosynthetic responses of Canarium pimela and Nepheliumtopengii seedlings to a light gradientrdquo Agroforestry Systems vol87 no 3 pp 507ndash516 2013

[34] D I Arnon ldquoCopper enzymes in isolated chloroplastsmdashpolyphenoloxidase in beta-vulgarisrdquo Plant Physiology vol 24no 1 pp 1ndash15 1949

[35] S Linder ldquoA proposal for the use of standardised methods forchlorophyll determination in ecological and ecophysiologicalinvestigationsrdquo Physiologia Plantarum vol 32 no 2 pp 154ndash156 1974

[36] J M O Eze and G K Berrie ldquoFurther investigations into thephysiological relationship between an Epiphyllous Liverwortand its host leavesrdquo Annals of Botany vol 41 no 2 pp 351ndash3581977

[37] J L Prioul and P Chartier ldquoPartitioning of transfer andcarboxylation components of intracellular resistance to photo-synthetic CO

2fixation a critical analysis of the methods usedrdquo

Annals of Botany vol 41 no 174 pp 789ndash800 1977[38] I Klein T M Dejong S A Weinbaum and T T Muraoka

ldquoSpecific leaf weight and nitrogen allocation responses to lightexposure within Walnut treesrdquo Hortscience vol 26 no 2 pp183ndash185 1991

[39] H Poorter U Niinemets L Poorter I J Wright and R VillarldquoCauses and consequences of variation in leaf mass per area(LMA) a meta-analysisrdquo New Phytologist vol 182 no 3 pp565ndash588 2009

[40] U Niinemets ldquoRole of foliar nitrogen in light harvesting andshade tolerance of four temperate deciduous woody speciesrdquoFunctional Ecology vol 11 no 4 pp 518ndash531 1997

[41] M B Walters E L Kruger and P B Reich ldquoGrowth biomassdistribution andCO

2exchange of northern hardwood seedlings

in high and low light relationships with successional status andshade tolerancerdquo Oecologia vol 94 no 1 pp 7ndash16 1993


[42] RW Rogers and A Barnes ldquoLeaf demography of the rainforestshrubWilkiea macrophylla and its implications for the ecologyof foliicolous lichensrdquo Australian Journal of Ecology vol 11 no4 pp 341ndash345 1986

[43] C T Ivey and N Desilva ldquoA test of the function of drip tipsrdquoBiotropica vol 33 no 1 pp 188ndash191 2001

[44] M Marschall and M C F Proctor ldquoAre bryophytes shadeplants Photosynthetic light responses and proportions ofchlorophyll a chlorophyll b and total carotenoidsrdquo Annals ofBotany vol 94 no 4 pp 593ndash603 2004

[45] P W Richards The Tropical Rain Forest An Ecological StudyCambridge University Press Cambridge UK 1952

[46] R Lucking andA Bernecker-Lucking ldquoDrip-tips do not impairthe development of epiphyllous rain-forest lichen communi-tiesrdquo Journal of Tropical Ecology vol 21 no 2 pp 171ndash177 2005

[47] M Toomey D Roberts and B Nelson ldquoThe influence ofepiphylls on remote sensing of humid forestsrdquo Remote Sensingof Environment vol 113 no 8 pp 1787ndash1798 2009

[48] P D Coley and T A Kursar ldquoCauses and consequences ofepiphyll colonizationrdquo in Tropical Forest Plant Ecophysiology SS Mulkey R L Chazdon and A P Smith Eds pp 337ndash362Springer New York NY USA 1996

[49] G Zotz and K Winter ldquoPhotosynthesis and carbon gain of thelichen Leptogium azureum in a lowland tropical forestrdquo Floravol 189 no 2 pp 179ndash186 1994

[50] R Bohning and C A Burnside ldquoThe effect of light intensityon rate of apparent photosynthesis in leaves of sun and shadeplantsrdquoThe American Journal of Botany vol 43 no 8 pp 557ndash561 1956

[51] K Kitajima ldquoRelative importance of photosynthetic traits andallocation patterns as correlates of seedling shade tolerance of13 tropical treesrdquo Oecologia vol 98 no 3-4 pp 419ndash428 1994

[52] J M Craine and P B Reich ldquoLeaf-level light compensationpoints in shade-tolerant woody seedlingsrdquoNew Phytologist vol166 no 3 pp 710ndash713 2005

[53] M Ribas-Carbo N L Taylor L Giles et al ldquoEffects of waterstress on respiration in soybean leavesrdquo Plant Physiology vol139 no 1 pp 466ndash473 2005

[54] R L Chazdon and R W Pearcy ldquoThe importance of sunflecksfor forest understory plantsrdquo BioScience vol 41 no 11 pp 760ndash766 1991

[55] S Olarinmoye ldquoEcology of epiphyllous liverworts growth inthree natural habitats in Western Nigeriardquo Journal of Bryologyvol 8 no 2 pp 275ndash289 1974

[56] C J Ellis B J Coppins and T P Dawson ldquoPredicted responseof the lichen epiphyte Lecanora populicola to climate changescenarios in a clean-air region of Northern Britainrdquo BiologicalConservation vol 135 no 3 pp 396ndash404 2007

[57] C J Ellis R Yahr and B J Coppins ldquoLocal extent of old-growthwoodland modifies epiphyte response to climate changerdquo Jour-nal of Biogeography vol 36 no 2 pp 302ndash313 2009

[58] N L Stephenson ldquoClimatic control of vegetation distributionthe role of the water balancerdquoThe American Naturalist vol 135no 5 pp 649ndash670 1990

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


epiphylls are more sensitive to environmental changes owingto their particular structure and physiology [15ndash17] Whetheror not epiphylls exacerbate or mitigate the effects of climatechange on host vascular plants is crucial for understandingecological functions of epiphyllous communities in tropicalforests

Previous studies paid more attention to nitrogen (N)transfer between epiphylls and hosts [9 18ndash22] due to theability of N fixation of epiphylls [23] However how epiphyllsaffect leaf physiological traits is still unclear [13 14] Someresearch has found that epiphylls decreased light radiationand photosynthetic capability of host leaves [24ndash27] whilesome thought that the photoacclimation of host plants couldoffset the negative effects of epiphylls [10 28 29] Theseinconsistencies may result from the diverse composition ofepiphyllous communities and undefined succession stages ofepiphyllous colonization [14] For examples the epiphyllousgroups in Monge-Najera (1989) and Anthony et al (2002)were liverworts and lichens respectively [10 30]

Communities dominated by lichens or liverworts mayinduce different effects on leaf traits of host plants due to theirdiverse structure characteristics [15] and distribution patternson host leaves [14 31] In addition the coverage of epiphyllsgenerally varies largely from sporadic to full cover [25 31] inthe successive process of epiphyllous colonization [7 13 14]which may be also crucial in understanding the roles ofepiphylls on hosts Therefore it is necessary to differentiateeffects of liverworts and lichens on host plants to betterunderstand the exact roles of epiphylls on their host plants

The tropicalMontane rain forests inHainan Island are thelargest and best preserved primary tropical forest in ChinaThe forests harbor diverse epiphylls on the surface of hostleaves in the understory In this study we studied the effectsof liverworts versus lichens with varying degrees of coverson their host tree species Photinia prunifolia in a tropicalMontane forest in Hainan Island We asked the followingquestions (1) Does epiphyllous colonization affect hostrsquos leaftraits (2) Do the effects of epiphyllous groups (liverwortsversus lichens) on hostrsquos leaf traits vary (3) How do theircoverages affect the effects on hostrsquos leaf traits

2 Materials and Methods

21 Study Site and Species The study was conducted in atropical Montane rain forest at the Jianfengling NationalNature Reserve (JNNR) (18∘231015840ndash18∘501015840N 108∘461015840ndash109∘021015840E)which is located in the southwest of Hainan Island ChinaJNNR is dominated by tropical monsoon climate with anaverage air temperature of 245∘C relative humidity of 88and annual sunshine of 1467 h [32] Annual precipitationranges from 1305 to 3662mm with a distinct wet season(May to October) and a dry season (November to April) [32]The monthly temperature and precipitation there had beendescribed by Yang et al [33] Due to the humid environmentapproximately up to 145 leaf area of plants in the understorywas covered with epiphylls (average percentage of leaves withepiphylls times average coverage on leaves) in which more than60 species of epiphyllous liverworts have been identified

(unpublished data) In order to obtain a relatively consistentspecies composition in epiphyllous communities we selectedhost plants within a plot with a diameter of 5 km

We selected the vascular plants Photinia prunifolia ashost plants in this study for the following reasons Firstly Pprunifolia was a common species with epiphylls at the studysite Secondly the average coverage of epiphylls on thematureleaves of P prunifolia was about 313 which was ideal forsampling purpose Thirdly it was easy to remove epiphyllsfrom coriaceous leaves of P prunifolia for manipulativetreatment Leaves with comparable sizes and locations on thebranches were selected from a large number of labeled leaveswhich had been selected out two years ago when they weretender leaves with no epiphylls We excluded leaves coveredwith mixed epiphyllous community of liverworts and lichensto avoid the interaction effects of the two groups The dom-inant species of lichens on the surface of P prunifolia werePorina chrysophora and P atrocaerulea and the dominantliverworts were Drepanolejeunea spicata Radula acuminataColura acroloba and Leptolejeunea maculata

22 Measurement Using a plastic sheet marked with 2 times2mm2 grids we measured the coverage of epiphylls (com-prised of liverworts or lichens) on leaf surface followingmethods specified in Roskoski (1981) [13]The leaves with 0coverage of epiphylls (uncolonized leaves) were used as thecontrol groups to be compared with leaves colonized by liver-worts or lichens Leaves colonized with liverworts or lichenswere divided into four subgroups according to levels ofcoverage 25 50 75 and 100 (plusmn5 error) respectivelyThe following physical leaf traits were measured leaf massper area (LMA) leaf water content (LWC) and chlorophyll(Chl) content (a and b) We used the method by Linder(1974) and Arnon (1949) for pretreatment and measurementof Chl content respectively [34 35] The contents of Chl a ba + b (mg gminus1) and ab ratios were calculated subsequentlyPhysical leaf trait measurements were replicated 5 times foreach subgroup one replication per tree

Before sampling photosynthetic light-response curves ofthese leaves were examined using the ldquoLight Curverdquo auto-matic program in Li-6400 Portable Photosynthesis System(LI-COR USA) with a 6400-02B RedBlue light sourcechamber (2 times 3 cm) Leaves were allowed 10min to acclimatethe changes of light intensity before measurements whichwere made following photosynthetic photon flux (PPF) 010 20 50 100 200 500 1000 1500 and 2000120583molmminus2 sminus1during 900ndash1200 am when the ambient temperature was20 plusmn 2

∘C and relative humidity ranged from 50 to 70Airflow rate was kept constant at 05 Lminminus1 with 380 plusmn10 120583molmolminus1 CO

2concentrations during themeasurement

In order to determine whether impacts of epiphylls onleaves were temporary epiphylls were removed from thesurface of leaves after photosynthetic measurement usingmethods described by Eze and Berrie (1977) [36] Light-response curves of postremoval leaves were measured usingthe same method two days later after the removal treatment(hereafter preremoval and postremoval were referred to thephotosynthetic traits of leaves covered with epiphylls and




2

minus 4120593119876119896119860max

2119896minus 119877

(1)



3 Results















160

140

120

100

80

60

40

20

0

a aa

blowast

lowast

a

lowast

LMA

(g m

minus2)

(a)

a ab bc

c

lowastlowast

lowast

100

80

60

40

20

0

LWC

()

(b)

5

4

3

2

1

0

a


Chl a

(mg g

minus1)

(c)

20

15

10

05

00

lowastlowastab

b

ba

a

b

Chl b

(mg g

minus1)

(d)

6

4

2

00

25 50 75 100

Coverage ()

a



Chl a+

b (m

g gminus1)

(e)

3

2

1

0

Chl a

b

0 25 50 75 100

Coverage ()

aab

blowastcblowast

clowast


(f)





0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(a)

0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(b)

0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(c)

0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(d)







4 Discussion





100

75

50

25

0

Cov

erag

e (

)

04 0402 0200

Alowast

Alowast

Ablowast

Ablowast

a

aa

b

blowastB

B

aB

aB

a



(a)

100

75

50

25

0

Cov

erag

e (

)

4 2 0 2 4

b

lowast

a

a

a

a




(b)

100

75

50

25

0

Cov

erag

e (

)


20 10 0 10 20

aa

aa

aa

a

a

a

a

Ab AbB bB



(c)

100

75

50

25

0

Cov

erag

e (

)


lowastlowast

a

a

a

a aa

aa

aa

aa

AA bbB bB

600 3000300 600



(d)





























119899)






Acknowledgments


References










































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology




2

minus 4120593119876119896119860max

2119896minus 119877

(1)



3 Results















160

140

120

100

80

60

40

20

0

a aa

blowast

lowast

a

lowast

LMA

(g m

minus2)

(a)

a ab bc

c

lowastlowast

lowast

100

80

60

40

20

0

LWC

()

(b)

5

4

3

2

1

0

a


Chl a

(mg g

minus1)

(c)

20

15

10

05

00

lowastlowastab

b

ba

a

b

Chl b

(mg g

minus1)

(d)

6

4

2

00

25 50 75 100

Coverage ()

a



Chl a+

b (m

g gminus1)

(e)

3

2

1

0

Chl a

b

0 25 50 75 100

Coverage ()

aab

blowastcblowast

clowast


(f)





0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(a)

0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(b)

0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(c)

0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(d)







4 Discussion





100

75

50

25

0

Cov

erag

e (

)

04 0402 0200

Alowast

Alowast

Ablowast

Ablowast

a

aa

b

blowastB

B

aB

aB

a



(a)

100

75

50

25

0

Cov

erag

e (

)

4 2 0 2 4

b

lowast

a

a

a

a




(b)

100

75

50

25

0

Cov

erag

e (

)


20 10 0 10 20

aa

aa

aa

a

a

a

a

Ab AbB bB



(c)

100

75

50

25

0

Cov

erag

e (

)


lowastlowast

a

a

a

a aa

aa

aa

aa

AA bbB bB

600 3000300 600



(d)





























119899)






Acknowledgments


References










































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


160

140

120

100

80

60

40

20

0

a aa

blowast

lowast

a

lowast

LMA

(g m

minus2)

(a)

a ab bc

c

lowastlowast

lowast

100

80

60

40

20

0

LWC

()

(b)

5

4

3

2

1

0

a


Chl a

(mg g

minus1)

(c)

20

15

10

05

00

lowastlowastab

b

ba

a

b

Chl b

(mg g

minus1)

(d)

6

4

2

00

25 50 75 100

Coverage ()

a



Chl a+

b (m

g gminus1)

(e)

3

2

1

0

Chl a

b

0 25 50 75 100

Coverage ()

aab

blowastcblowast

clowast


(f)





0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(a)

0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(b)

0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(c)

0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(d)







4 Discussion





100

75

50

25

0

Cov

erag

e (

)

04 0402 0200

Alowast

Alowast

Ablowast

Ablowast

a

aa

b

blowastB

B

aB

aB

a



(a)

100

75

50

25

0

Cov

erag

e (

)

4 2 0 2 4

b

lowast

a

a

a

a




(b)

100

75

50

25

0

Cov

erag

e (

)


20 10 0 10 20

aa

aa

aa

a

a

a

a

Ab AbB bB



(c)

100

75

50

25

0

Cov

erag

e (

)


lowastlowast

a

a

a

a aa

aa

aa

aa

AA bbB bB

600 3000300 600



(d)





























119899)






Acknowledgments


References










































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(a)

0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(b)

0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(c)

0 500 1000 1500 2000

02550

75100

0

1

2

3

4

minus1


Pn

(120583m

olCO

2mminus2

sminus1)

(d)







4 Discussion





100

75

50

25

0

Cov

erag

e (

)

04 0402 0200

Alowast

Alowast

Ablowast

Ablowast

a

aa

b

blowastB

B

aB

aB

a



(a)

100

75

50

25

0

Cov

erag

e (

)

4 2 0 2 4

b

lowast

a

a

a

a




(b)

100

75

50

25

0

Cov

erag

e (

)


20 10 0 10 20

aa

aa

aa

a

a

a

a

Ab AbB bB



(c)

100

75

50

25

0

Cov

erag

e (

)


lowastlowast

a

a

a

a aa

aa

aa

aa

AA bbB bB

600 3000300 600



(d)





























119899)






Acknowledgments


References










































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology



100

75

50

25

0

Cov

erag

e (

)

04 0402 0200

Alowast

Alowast

Ablowast

Ablowast

a

aa

b

blowastB

B

aB

aB

a



(a)

100

75

50

25

0

Cov

erag

e (

)

4 2 0 2 4

b

lowast

a

a

a

a




(b)

100

75

50

25

0

Cov

erag

e (

)


20 10 0 10 20

aa

aa

aa

a

a

a

a

Ab AbB bB



(c)

100

75

50

25

0

Cov

erag

e (

)


lowastlowast

a

a

a

a aa

aa

aa

aa

AA bbB bB

600 3000300 600



(d)





























119899)






Acknowledgments


References










































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

























119899)






Acknowledgments


References










































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology




































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

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