Variation in Light Absorption Properties of Mentha aquatica L. as a Function of Leaf Form:...

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Int. J. Plant Sci. 164(1):125–136. 2003.� 2003 by The University of Chicago. All rights reserved.1058-5893/2003/16401-0012$15.00

VARIATION IN LIGHT ABSORPTION PROPERTIES OF MENTHA AQUATICA L. AS AFUNCTION OF LEAF FORM: IMPLICATIONS FOR PLANT GROWTH

Susana Enrıquez1 and Kaj Sand-Jensen

Unidad Academica de Puerto Morelos, Instituto de Ciencias del Mar y Limnologıa, Universidad Nacional Autonomade Mexico, Apdo. Postal 1152, 77500 Cancun (Quintana Roo), Mexico; and Freshwater Biological Laboratory,

University of Copenhagen, Helsingørsgade 51, DK-3400 Hillerød, Denmark

To understand the association between leaf form and leaf optical properties, we examined light absorptionvariations in the leaves of Mentha aquatica L., an amphibious freshwater macrophyte. Specific absorption ofleaves of M. aquatica showed a 7.5-fold variation, decreasing as pigment per unit area increased. This rela-tionship indicates that dispersive samples, such as leaves, although efficient light traps, can also be affectedby the “package effect.” Mentha aquatica leaves, by expanding their biomass (increased specific leaf area[SLA]), improve their light absorption efficiency per unit of both pigment and leaf biomass. Changes in leafbiomass expansion were mainly a result of changes in leaf density, and as a consequence, leaf density appearsto be a better descriptor of light absorption efficiency in M. aquatica leaves than does leaf thickness. Lightabsorption efficiency per unit of leaf biomass was also enhanced by increasing pigment content. Our resultsindicate that M. aquatica produces two types of leaves: (1) thin, less dense, and highly pigmented leaves and(2) thick, denser, and low pigmented leaves. The first type shows higher light absorption efficiency per unitof leaf biomass, which may allow the plant to achieve a better carbon balance under light limitation. Thesecond type shows lower light absorption efficiency per unit of leaf biomass. Although it is unclear whetherthis reduction affects plant performance, a reduction in net carbon income per unit of absorbed photon mayresult in a reduction in the specific plant growth rate (RGR). Understanding the association between leaf formand the ability of leaf biomass to absorb light provides a mechanistic explanation for the empirical relationshipfound repeatedly in the literature between RGR and SLA. Our results offer a quantitative basis to explainpart of the association between biomass expansion, pigment investment, and plant growth.

Keywords: light absorption, package effect, specific absorption, specific leaf area, leaf thickness, leaf accli-mation, relative growth rate.

Introduction

In comparison to unicellular phytoplankton, there is a lackof quantitative descriptions of light absorption efficiencies ofmulticellular tissues, probably because of the complexity oflight absorption in highly dispersive media such as leaves. Con-sidering the broad repertoire of photosynthetic tissue anato-mies in multicellular organisms, from thalli of macroalgae toleaves and photosynthetic stems of flowering plants, it is highlyprobable that heterogeneous absorption within the tissue (Vo-gelmann and Bjørn 1984; Vogelmann et al. 1991, 1996) variesbecause of widely different internal anatomies. As a conse-quence, light absorption efficiency of photosynthetic pigmentsmay display a wide variability among tissue anatomies, evenassuming that leaves often absorb around a constant value of84% of incident light (Gabrielsen 1948). The magnitude andvariability of pigment self-shading for multicellular structureshave not yet been evaluated. Leaves are able to counterbalancepigment self-shading by developing palisade cells that facilitatethe penetration of light into the leaf (Vogelmann et al. 1996).

1 Author for correspondence; fax 52-99-887-10138; e-mail [email protected].

Manuscript received April 2001; revised manuscript received August 2002.

Differences in pigment distribution within the tissue (Terashi-ma and Saeki 1983; Bornman et al. 1991; Vogelmann et al.1996; Evans 1998) may result in significant differences in pig-ment light-absorbing efficiency. At the same time, multicellulartissues are highly scattering optical structures because of thepresence of refractive surfaces within the tissue, such as celllayer boundaries and intercellular air spaces, which are ableto enhance light absorption by increasing optical path lengthb (Fukshansky 1981; Terashima and Saeki 1983; Richter andFukshansky 1996a, 1996b, 1998; Vogelmann et al. 1996). Yet,the question that still needs to be resolved is how the variabilityin leaf morphology affects light absorption capacity and pig-ment light absorption efficiency. The characterization of thismechanistic relationship between leaf form and function maycontribute to understanding the adaptive significance of certainleaf form descriptors.

Light-absorbing pigments are located within organelles(plastids), which are distributed in cells and tissues. Pigmentswithin cells and tissues absorb less light per unit of pigmentthan the same quantity of pigment dispersed in solution. Thisreduction in pigment light absorption efficiency because ofpigment self-shading is referred to as the “package effect”(Kirk 1994). Theoretical evaluations as well as empirical mea-surements of phytoplankton indicate that the package effect

126 INTERNATIONAL JOURNAL OF PLANT SCIENCES

is stronger at the peaks of maximum absorption (Duysens1956; Kirk 1975, 1976, 1994; Geider and Osborne 1987) andthat the magnitude of the package effect depends on cell sizeand intracellular pigment concentration (Duysens 1956; Kirk1975, 1976, 1994; Morel and Bricaud 1981). To what extenthighly pigmented multicellular structures are affected by thepackage effect, and how leaf form may contribute in regulatinglight absorption efficiency, remain to be examined.

Previous comparative analyses of the variation of light ab-sorption among unicellular and multicellular species have dem-onstrated a strong dependency on different basic descriptorsof the photosynthetic structure. For example, increasing thecross section (cell diameter or tissue thickness) of photosyn-thetic structures (from unicells to leaves) resulted in a reductionof light absorption efficiency per unit of biomass, whereasincreasing pigment content enhanced plant biomass light ab-sorption efficiency (Agustı et al. 1994; Enrıquez et al. 1994).This association between leaf morphology and the ability ofphotosynthetic structures to absorb light has been proposedas a possible mechanism to explain part of the empirical re-lationships found between photosynthetic tissue thickness, orthe closely related descriptor, specific leaf area (1/SLA p leaf

) and (1) interspecific variation in pho-thickness # leaf densitytosynthetic and respiration rates (Enrıquez et al. 1995, 1996)and (2) interspecific variation in relative growth rate (Nielsenet al. 1996).

In this work, we further investigate the association betweenleaf morphology and changes in the ability of leaves to absorblight. The objective was to develop a basic model, based onoptical theory developed for phytoplankton, to examine fun-damental relationships between light absorption and pigmentand leaf biomass packaging of multicellular tissues. As a modelsystem, we utilized an amphibious homophyllous freshwaterspecies, Mentha aquatica L., that has amphistomatous leaves.To compare the intraspecific variability in leaf morphology andlight absorption efficiency, we used pigment biomass, leafthickness, leaf density, and leaf biomass expansion (specificleaf area [SLA]) or leaf biomass packing (described by leafmass per area ) as descriptors of leaf mor-[LMA] p 1/SLAphology; as descriptors of light absorption characteristics, weused absorptance (the fraction of the incident light absorbedby the leaf) and specific absorption coefficients. The specificabsorption coefficient is defined as the effective absorptioncross section, i.e., the effective area exposed per unit pigmentor leaf biomass (mg pigm m�2 and g dM m�2, respectively),and it is calculated as the exponent (extinction coefficient) ofan exponential function, either normalized to pigment contentor leaf biomass.

Because the mechanistic relationship between pigment leafform and light absorption does not need to be proved, weprovide an allometric analysis of the associations between dif-ferent basic leaf form descriptors and light absorption prop-erties of M. aquatica leaves in our work, with the objective ofgaining insight into the adaptive significance of leaf form.Modeling the complexity of the optical properties and of in-ternal multiple scattering within leaves (Richter and Fukshan-sky 1996a, 1996b, 1998) or describing the variation of lightattenuation within the tissue (Terashima and Saeki 1983; Born-man et al. 1991; Vogelmann 1993; Vogelmann et al. 1996;

Evans 1998) associated with changes in internal leaf anatomyare beyond the present objectives of this study.

Material and Methods

Apical sections of young, fast-growing Mentha aquaticaplants were collected from the banks of a Danish stream andpreconditioned in the laboratory for 2 wk. Apical cuttings ofemergent individuals are able to form roots in an alkaline tapwater culture. After the preconditioning period, plants of thesame size and biomass partitioning were selected and mountedindividually, with the roots in 500-cm3 glass containers andthe stems fixed to the lid of the glass container by means ofa molded rubber seal around the stem, placed above the lowestnode. To generate variability in leaf form, pigment, and bio-mass packing in M. aquatica, we grew the plants in hydroponiccultures under various light and nutrient regimes and with theshoots either exposed to the air or submerged. Three levels ofnutrient supply were obtained by using an artificial medium:(1) without nitrogen and phosphorus (low nutrient supply[LN]) and (2) adding to this medium a Hoagland solution ata final concentration of 1% (medium nutrient supply [MN])and (3) 10% (high nutrient supply [HN]). Media were renewedtwice a week, and O2 concentrations in the glass containersduring the dark period were controlled to ensure that they didnot become anoxic. Four replicates per nutrient treatment wereplaced in two 160-L aquaria (12 plants per aquarium) for eachexperiment. The aquaria were illuminated by Osram Fluorafluorescence tubes resulting in a maximum PAR irradiance of100 mmol m�2 s�1. A photoperiod of 14 h : 10 h light : darksimulated summer conditions and a photoperiod of 10 h : 14h light : dark simulated an autumn photoperiod.

Two experiments were performed. In the first experiment,plants were exposed to the summer photoperiod at the max-imum irradiance (HL) and were grown in air or submergedunder the three nutrient levels. Submerged plants were sur-rounded by the same artificial water used to produce the hy-droponics medium (low nutrient). The water in the aquariumwas stirred by a submersible pump and enriched with CO2

from pressurized tanks to 600 mM free CO2 (air saturation 15mM) to alleviate CO2 limitation, and the water was renewedevery second week. In the second experiment, the autumn pho-toperiod was used, with all plants grown in air with the samethree levels of nutrient supply. One aquarium received the high-est irradiance (ML), and the other aquarium was shaded to50% using a black net (LL). Room temperature and humiditywere controlled between 20º and 25ºC and between 45% and65% relative humidity. Plants were harvested after 30 d. Weexamined all ages of healthy and functional leaves on eachshoot to increase the range of variability in leaf morphologyand light absorption.

We measured the thickness of M. aquatica leaves by cuttingand mounting them on microscope slides under an OlympusIMT-2 microscope. Leaf area was measured on a surface areameter (LI-COR, LI-3000), and leaf mass was obtained by dry-ing a known leaf surface area for 24 h at 105ºC. Leaf densitywas calculated by normalizing dry mass to volume, the lattercalculated from the projected surface area and the thicknessof each leaf. Leaf mass per area (LMA) was calculated fromthe measured mass normalized to the projected leaf area. Men-

ENRIQUEZ & SAND-JENSEN—LIGHT ABSORPTION BY MENTHA AQUATICA LEAVES 127

Fig. 1 Light absorption spectra of leaves of Mentha aquatica growingunder low and medium light supplies. The heavy solid line representsleaves grown in the shade (50% of light supply), and the light solid linerepresents leaves grown at 100% light. The dotted line represents theaveraged light absorption spectrum of seven bleached leaves. O.D. p

density.optical

tha aquatica leaves have a single layer of epidermal cells, onelayer of palisade cells, and three layers of spongy mesophyllcells. The volume of the intercellular spaces was highly variableamong treatments (data not shown).

Pigment concentration was measured spectrophotometri-cally on the same fragments used for light absorption mea-surements, following pigment extraction of a homogenizedsuspension in 80% acetone (Dennison 1990). Total caroten-oids and chlorophyll a and b of leaf extracts were calculatedusing the equations of Lichtenthaler and Wellburn (1983). Leafpigment content is expressed per unit of projected surface areaor leaf dry mass. In this study, we included a third descriptorof the amount of pigments calculated per unit of leaf volume.This descriptor is very commonly used to describe pigmentcontent of unicells, but it is rarely used to describe pigmentcontent of multicellular tissues. To avoid confusion amongthese three expressions of the amount of pigment, we decidedto use the terms (1) pigment per unit area (pigmarea) to describepigment mass per unit of surface area, (2) pigment concentra-tion (pigmvol) to describe pigment mass per unit of leaf volume,and (3) pigment content (pigmdM) to describe pigment massper unit of leaf dry mass.

Light absorption was measured using the opal glass tech-nique developed by Shibata (1959) for intact plant leaves. Frag-ments of leaves were mounted between microscope slides in aShimadzu UV-160, a dual-beam scanning spectrophotometercontaining an opal glass unit. Light absorption was measuredat 1-nm intervals between 380 nm and 750 nm (PAR range).We used two descriptors: (1) average light absorption for therange between 400 nm and 700 nm (PAR range) and (2) lightabsorption at 680 nm, which is the peak of chlorophyll a,where there is the lowest interference with other accessorypigments (a more common descriptor for phytoplankton). Thecorrection for nonpigment absorption was done usingbleached/etiolated leaves as a reference in the spectrophotom-eter. Although bleached/etiolated leaf spectra showed no sig-nificant variations among leaf morphologies, we used ableached/etiolated leaf obtained within each treatment as areference. Leaves were bleached by extracting photosyntheticpigments in acetone for 24 h. Shibata’s technique may over-estimate absorptance if residual scattering and backscatteringare significant. The attenuance values (apparent absorbance)obtained were corrected by subtracting absorbance at 750 nmto exclude residual scattering. In our study, absorbance at 750nm was in all measurements very low, confirming low levelsof backscattering and residual scattering. Nevertheless, wemeasured reflectance spectra in the PAR range in a Zeiss self-recording spectrophotometer, DMR 21, equipped with an in-tegrating sphere, ZR 21. We used seven different leaves chosenrandomly among different growth treatments as well as field-growing plants. Leaf reflectance of M. aquatica leaves was low,and so was the variability found among leaves (6.5% � 0.4on average for the PAR range, and at the chlo-3.6% � 0.3rophyll a peak at 680 nm, , ). The corrected ab-x � SE n p 7sorbances were corrected further by subtracting (1) the PARaverage of leaf reflectance to calculate the average PAR ab-sorptance and (2) the value at 680 nm to calculate absorbanceat the chlorophyll a peak. Figure 1 shows two light absorptionspectra of M. aquatica leaves growing under low and medium

light availability. It also shows the averaged light absorptionspectrum of an etiolated leaf.

We express light absorption as absorptance (i.e., fraction oflight absorbed) calculated from measurements of absorbanceusing the equation . We calcu-�absorbanceabsorptance p 1 � 10lated the specific absorption using the exponent in the expo-nential function , according toexp p � ln [1 � absorptance]( )Beer-Lambert law, and normalized this value to either pigmentcontent or leaf dry mass per projected surface area.

The relationships between the variables examined here weredescribed using least squares regression analysis. We also usedmodel 2 regression analysis (RMA) to obtain more reliablescaling coefficient estimates (Niklas 1994). Path analysis (Wil-liams et al. 1990) was used to partition the multiple associa-tions between direct and indirect effects.

Results and Discussion

The leaves of Mentha aquatica varied markedly in structureand composition (fig. 2a, 2b); they also showed plasticity intheir ability to absorb light (fig. 2b). The largest variationswere found in pigment content per unit dry mass (CV p

) and in pigment per unit area ( ). Changes63.94% CV p 44.8%in specific leaf area ( ) were higher (SLA p 1/LMA CV p

) than changes in leaf density ( ) and38.21% CV p 28.35%changes in leaf thickness ( ). The different exper-CV p 19.9%imental growth conditions to which M. aquatica leaves wereexposed produced leaves with broader variation in pigmentcontent and pigment per unit area than in leaf biomass ex-pansion (SLA; fig. 2a, 2b), which is in disagreement with theconclusion by Evans (1998) that growth irradiance alters leafstructure but chlorophyll content per unit area is generallyunaltered. Independently of the nutrient treatment, the thinnestleaves grew in air with the lowest light supply (LL and ML,fig. 2a). Similar leaf morphologies were observed in plants


Fig. 2 a–c, of leaf form descriptors of Mentha aquatica grown in hydroponic cultures under different environmental conditions:Average � SEleaf thickness, mm (a); leaf density, g dM dm�3 (b); and leaf mass per area, g dM m�2 (c). d–f, of leaf absorptance and pigmentAverage � SEinvestment of M. aquatica grown in hydroponic cultures under different environmental conditions: leaf absorptance (d); pigment per unit area, mgpigm m�2 (e); and pigment content, mg pigm g dM�1 (f ). LH, MN, and HN denote low, medium, and high nutrient supply; LL refers to the lowerlight supply (50% of shading) and the shorter photoperiod (10 h : 14 h light : dark); ML refers to the maximum light supply (100 mmol m�2 s�1)and the shorter photoperiod (10 h : 14 h light : dark); HL refers to the maximum light supply (100 mmol m�2 s�1) and the longest photoperiod (14h : 10 h light : dark); Water refers to plants growing submerged at the maximum light supply (100 mmol m�2 s�1) and the longer photoperiod (14h : 10 h light : dark).

growing in air under the highest light regime with the highestnutrient availability (HL and HN, fig. 2a). Submerged plantsproduced the thickest leaves with the lowest pigment content(fig. 2a, 2b). Light absorption properties of M. aquatica leavesalso varied broadly as a function of pigment content and leafmorphology. Leaves absorbed between 50% and 80% of theincident light across the PAR range (fig. 2b). Differences inlight absorption were stronger among leaves grown under dif-ferent nutrient treatments than under different irradiances

(ANOVA showed significant differences among nutrient treat-ments [F-test, ]; differences were not significantP ! 0.001among light treatments [F-test, ]). Leaves grown in air,P 1 0.05low nutrients, and the highest light supply (HL) showed thelowest absorptance values (fig. 2b). However, submergedleaves grown under low nutrient supply (LN), which showed0.6 times lower pigment content (fig. 2b) than leaves grownin air under the same irradiance (HL) and nutrient regimes(LN), were able to collect 1.16 times more light. Both light-


Table 1

Pearson Correlation between Light Absorption Descriptors and Leaf Traits

Log absorptancePAR average Log ∗apigm Log ∗aM avg

Log pigmentdensity

Log pigmentcontent

Log leafdensity

Log leafthickness

Log (m2 mg pigm�1)∗apigm �0.04 1Log (m2 g dM�1)∗aM avg 0.44∗ �0.24∗ 1Log pigment per unit area (mg pigm m�2) 0.43∗ �0.92∗ 0.38∗ 1Log pigment content (mg pigm g dM�1) 0.30 �0.79∗ 0.78∗ 0.83∗ 1Log leaf density (g dM dm�3) �0.06 0.18 �0.83∗ �0.19 �0.64∗ 1Log leaf thickness (mm) 0.10 0.22 �0.61∗ �0.15 �0.53∗ 0.35∗ 1Log leaf mass per area (g dM m�2) �0.01 0.25∗ �0.90∗ �0.23 �0.73∗ 0.89∗ 0.73∗

Log absorptanceat 680 nm Log ∗achla Log ∗aM 680

Log chladensity

Log chlacontent

Log leafdensity

Log leafthickness

Log (m2 mg chla�1)∗achla �0.20 1Log (g dM m�2)∗aM 680 0.74∗ �0.15 1Log chlorophyll a per unit area (mg chla m�2) 0.51∗ �0.94∗ 0.39∗ 1Log chlorophyll a content (mg chla g dM�1) 0.65∗ �0.72∗ 0.79∗ 0.86∗ 1Log leaf density (g dM dm�3) �0.49∗ 0.06 �0.87∗ �0.23 �0.64∗ 1Log leaf thickness (mm) �0.31∗ 0.06 �0.68∗ �0.16 �0.51∗ 0.35∗ 1Log LMA (g dM m�2) �0.52∗ 0.09 �0.96∗ �0.26 ∗ �0.72∗ 0.89∗ 0.73∗

Note. The upper half shows averages for the entire 400–700 PAR range. The lower half shows measurements at 680 nm.∗ Significant coefficients ( ).P ! 0.05

specific coefficients (normalized to either pigment mass or drymass) showed larger differences among treatments than leafabsorptance. The highest pigment efficiency in light absorptionwas shown by leaves grown under low nutrient supply, andthe highest biomass-specific efficiency was shown by leavesgrown in air under conditions of low light and maximumnutrient availability (data not shown).

When we examined all the variability displayed by M. aqua-tica leaves from all treatments as a function of pigment perunit area (pigmarea), we found a weak, though significant, re-lationship between absorptance and pigment per unit area (ta-ble 1). At low pigment per unit area values, some leaves ab-sorbed ca. 50% of the incident PAR, while others absorbedabove 70% (fig. 3). These large differences in leaf absorptanceindicate that there are differences among leaves in pigment andbiomass absorption efficiency due to variation in leaf mor-phology, probably resulting from changes in pigment distri-bution within the leaf and internal leaf anatomy. Using twodescriptors, average light absorption across the PAR range ver-sus total pigment ( ) per unit area andchlorophyll + carotenoidslight absorption at 680 nm versus chlorophyll a per unit area,we examined the variation of light absorption efficiency perunit of pigment and leaf mass. First, we examined the asso-ciation between changes in pigment per unit area and lightabsorption efficiency per unit of pigment to analyze the effectof leaf morphology on light absorption properties of M. aqua-tica leaves.

Light Absorption Efficiency of Pigments

Pigment-specific absorption ( ) of M. aquatica leaves∗apigm

showed a highly significant and negative correlation with pig-ment per unit area (table 1). Pigment light absorption efficiencyfor the entire PAR range and chlorophyll a absorption effi-ciency for the peak at 680 nm ( ) decreased as total pigment∗achla

and chlorophyll a per unit area, respectively, increased. Theserelations are described by the following equations:

∗loga p �2.85 � 0.03 � 0.83pigm

� 0.04 logpigment per unit area,

∗loga p �2.55 � 0.03 � 0.80chla

� 0.03 logchlorophyll a per unit area,

with , , , , and2R p 0.85 n p 74 P ! 0.0001 SE p 0.076 F pfor the first equation and , ,2409 R p 0.89 n p 74 P !

, , and for the second equation.0.0001 SE p 0.065 F p 573These results indicate that pigment efficiency decreases non-

linearly (scaling coefficients are �0.90 for and �0.85 for∗apigm

after correction by RMA regression analysis; Niklas 1994)∗achla

as the amount of pigment per unit of leaf-projected area in-creases (fig. 4). Yet, M. aquatica leaves are affected by thepackage effect. Estimates for M. aquatica leaves of photon pathlength (b) at the 680 chlorophyll a peak following the methodof Ruhle and Wild (1979; i.e., comparison between the ab-sorption values of photosynthetic pigments in vivo and thoseof the extracted pigments) varied between 0.617 and 1.273.These values confirmed the amplification effect of multiplescattering on M. aquatica absorptance for some leaves, whileother leaves showed less pigment absorption efficiency thanthe solution of extracted pigments. The ability of increasingphoton path length (b) does not counterbalance the loss ofchlorophyll a light absorption efficiency because of the packageeffect. Optical theory developed for unicellular algae has de-scribed a nonlinear relationship between the relative opticallength (the product of intracellular chlorophyll a content, Ci,times the cell diameter, d) and the specific absorption coefficient(i.e., effective pigment absorption cross section; Geider andOsborne 1992; Kirk 1994). The novel conclusion provided by


Fig. 3 Relationships between leaf absorptance at 400–700 nm andtotal pigment per unit area (normalized to projected surface area) andleaf absorptance at 680 nm and chlorophyll a density (normalized toprojected surface area) of leaves of Mentha aquatica.

Fig. 4 Relationships between specific absorptance (based on totalpigment) at 400–700 nm and total pigment per unit area (normalizedto projected surface area) and specific absorptance (normalized to chlo-rophyll a) at 680 nm and chlorophyll a density (normalized to projectedsurface area) of leaves of Mentha aquatica.

our model system based on M. aquatica leaf plasticity is thatleaves, although very efficient light traps (they increase lightabsorption through multiple scattering and heterogeneous ab-sorption within the tissue), can also be affected by the packageeffect.

Optical theory predicts that pigment-specific absorption de-pends on cell size (a function of cell diameter) and intracellularpigment concentration (pigment biomass per unit of cell vol-ume) (Duysens 1956; Kirk 1975, 1976, 1994; Morel and Bri-caud 1981). The equivalent leaf descriptors for intracellularchlorophyll a content (Ci) and cell diameter are pigment con-centration of leaves (g pigm m�3) and leaf thickness (m), re-spectively. Pigment per unit area (g pigm m�2) is also the prod-uct of pigment concentration (g pigm m�3) and leaf thickness(m). We found no relation between leaf thickness and pigment-specific absorption ( ; table 1). Nevertheless, despiteP 1 0.05the apparent lack of such an association, multiple least squaresregression showed a significant coefficient for leaf thickness(table 2; t-test, ). The effect of total pigment con-P ! 0.0001centration (pigmvol) and chlorophyll a concentration (chlavol)on pigment-specific absorption was similar (table 2). Leafthickness showed a stronger effect in reducing the light ab-sorption efficiency of chlorophyll a than it did for total pigmentcontent efficiency (leaf thickness coefficient was �0.63 for total

pigment content efficiency, whereas it was �0.91 for chloro-phyll a–specific absorption; table 2). We conclude, therefore,that increasing both pigment concentration (pigmvol) and leafthickness results in increased pigment self-shading within M.aquatica leaves, analogous to what has been described for uni-cellular algae. Pigment “packaging,” or the magnitude of pig-ment self-shading within M. aquatica leaves, is mainly asso-ciated with increasing total pigment concentration; however,leaf thickness and chlorophyll a concentration equally con-tribute to the variation of chlorophyll a self-shading.

Pigment concentration (pigmvol) is not a usual leaf descriptorfor multicellular tissues. Variation of pigment concentration (gpigm m�3) may result from changes in pigment content(pigmdM, g pigm leaf dry mass �1) and/or changes in leaf density(leaf dry mass m�3). To evaluate the contribution of both de-scriptors and to predict pigment-specific absorption, we sub-stituted pigment concentration with pigment content and leafdensity into the model. Multiple regression analysis showedsignificant negative effects for both parameters (table 2; t-test,

), though the Pearson correlation did not show sig-P ! 0.0001nificant association between leaf density and pigment-specificabsorption ( ; table 1). We conclude from the equationsP 1 0.05shown in table 2 that pigment content (pigmdM), leaf thickness,and leaf density contribute to “pack” photosynthetic pigmentswithin M. aquatica leaves. The effect of pigment content and


Table 2

Statistics and Significant Slopes (�SE) of the Independent Variables Used in the Multiple LeastRegression Equations between Descriptors of Light Absorption and Leaf Traits

Y and X Log–log slope R2 n SE F

:∗apigm

Leaf thickness (mm) �0.58 � 0.12Pigment concentration (mg pigm dm�3) �0.80 � 0.04 0.84 74 0.077 199

:∗achla

Leaf thickness (mm) �1.00 � 0.1Chlorophyll a concentration (mg chla dm�3) �0.80 � 0.03 0.89 74 0.065 288

:∗apigm

Leaf density (g dM dm�3) �0.87 � 0.09Leaf thickness (mm) �0.63 � 0.13Pigment content (mg pigm g dM�1) �0.83 � 0.04 0.85 74 0.075 140

:∗achla

Leaf density (g dM dm�3) �1.04 � 0.08Leaf thickness (mm) �0.91 � 0.1Chlorophyll a content (mg chla g dM�1) �0.82 � 0.03 0.90 74 0.060 226

:∗apigm

Leaf mass per area (g dM m�2) �0.81 � 0.08Pigment content (mg pigm g dM�1) �0.84 � 0.04 0.85 74 0.076 205

:∗achla

Leaf mass per area (g dM m�2) �1.03 � 0.06Chlorophyll a content (mg chl a g dM�1) �0.84 � 0.05 0.91 74 0.057 375

Note. apigm represents the specific absorption for the 400–700 PAR range, and achla represents the specific absorption for thechlorophyll a peak at 680 nm.

leaf density on the variation of total pigment-specific absorp-tion is stronger than that of leaf thickness. Ruhle and Wild(1979) found that increased leaf thickness enlarges photonpath length (b) and consequently increases the probability thata photon is absorbed (Vogelmann 1993). These opposing ef-fects of leaf thickness on leaf absorptance (pigment packingvs. photon path length enlargement) may explain the lowercontribution of leaf thickness in reducing total pigment-specificabsorption. Nevertheless, the three descriptors have equal im-portance in reducing chlorophyll a–specific absorption at 680nm.

The product of leaf thickness and leaf density is leaf massper area (LMA; gdM m�2), which describes the degree of over-lapping or packing of leaf biomass (amount of leaf biomassdisplayed per unit of projected area). LMA and pigment con-tent (pigmdM) were suitable descriptors of pigment-specific ab-sorption (table 2). Multiple regression analysis showed thatincreasing biomass packing (LMA) resulted in a stronger re-duction of chlorophyll a efficiency in absorbing light than totalpigment efficiency (stronger chlorophyll a self-shading). Thedependence between light absorption efficiency per unit of pig-ment and SLA has been examined previously by Evans (1998),who concluded that there is no effect of SLA on the ability ofleaves to absorb light per unit of chlorophyll. This conclusionwas based on the analysis of the relationship between SLA andan absorptance error. That absorptance error was calculatedfrom the difference between measured leaf absorptance and apredicted empirical value calculated from a function that de-scribes the relation between leaf absorptance and chlorophyllcontent per unit area. The absorptance error only describesthe goodness of fit of the data set used for the function em-ployed, but it does not reflect the light absorption efficiencyper unit of chlorophyll. The efficiency of pigments in absorbing

light (i.e., effective pigment absorption cross section) is de-scribed by its specific absorption (Kirk 1994). The use of apoor descriptor for the specific absorption seriously compro-mises the conclusion of Evans. Furthermore, the associationbetween SLA and pigment-specific absorption examined in ourwork includes only the variation in leaf morphology and lightabsorption properties displayed by a single species, minimizingthe optical uncertainty inherent in the comparison of specieswith different internal leaf anatomies.

Light Absorption Efficiency of Leaf Biomass

To quantify leaf biomass efficiency in absorbing light, weused mass-specific absorption. As noted by Falkowski et al.(1985) and Ramus (1990), mass-specific absorption is a math-ematical construct, because biomass (excluding pigments) hasno real absorption cross section. Nevertheless, it is a usefulparameter for comparison of light-capture efficiencies becauseit reflects the energy return per unit tissue produced and mayreflect the potential carbon turnover of the plants (Ramus1990; Agustı et al 1994; Enrıquez et al. 1994). The light ab-sorption efficiency per unit of leaf mass of M. aquatica showeda weak, though significant and positive, relationship with pig-ment per unit area (table 1; ). When we separatedP ! 0.001pigment per unit area into the three leaf descriptors used for-merly (leaf thickness, leaf density, and pigment content,pigmdM), we found strong Pearson correlation coefficients be-tween them and mass-specific absorption (table 1). Changesin LMA accounted for the major fraction of the variability inmass-specific absorption (81% of the PAR and 90% at thechla peak at 680 nm; fig. 5). RMA regression analysis showednonlinear coefficients for LMA (�1.11 for the PAR absorptionand �1.30 for the 680 nm peak absorption). This result in-


Fig. 5 Relationships between mass-specific absorptance (normalizedto mass) and leaf mass per area at 400–700 nm and at 680 nm of leavesof Mentha aquatica.

dicates that leaves with high biomass packing (thick and denseleaves with high LMA) suffer proportionally stronger reduc-tion in their efficiency to absorb light per unit of leaf biomassthan highly “expanded” leaves (thin and less dense with highSLA).

Multiple linear regression analysis provided only a slightimprovement in the relationship between LMA and the mass-specific absorption. Nevertheless, we present the equations be-low because they show a small, but significant and positive,effect of pigment content on mass-specific absorption:

∗loga p �2.59 � 0.17 + 0.16M avg

� 0.04 logpigment content

� 0.80 � 0.08 logLMA

( , , , , );2R p 0.84 n p 73 P ! 0.0001 SE p 0.076 F p 191

∗loga p �2.98 � 0.13 + 0.15M 680

� 0.03 logchlorophyll a content

� 1.06 � 0.06 logLMA

( , , , , ).2R p 0.93 n p 73 P ! 0.0001 SE p 0.057 F p 506Each leaf descriptor showed a significant coefficient in the

multiple regression equations (t-test, , data notP ! 0.0001shown). Leaf density showed the strongest effect on thevariation of mass-specific efficiency (leaf density

, ;coefficient p �0.86 � 0.09 P ! 0.0001 leaf thickness, ) for light absorption.coefficient p �0.61 � 0.01 P ! 0.0001

Both effects were similar at the chlorophyll a absorption peak( , ;leaf density coefficient p �1.07 � 0.07 P ! 0.0001 leaf

, ). In sum-thickness coefficient p �0.96 � 0.09 P ! 0.0001mary, increased biomass packing (increased leaf thickness and/or increased leaf density) results in a reduction of light ab-sorption efficiency of leaf biomass, but an increment ofpigment content slightly offsets this tendency. Leaf density isthe parameter most strongly associated with the reduction oflight absorption efficiency of leaf biomass across the PARrange. However, leaf thickness and density were equally im-portant at the chlorophyll a absorption peak.

Colinearity between the Three Leaf Descriptors

The three leaf morphological descriptors used in this com-parison—leaf thickness, leaf density, and pigment content—areintercorrelated (table 1). Highly pigmented leaves tend to bethin and of low density, while thick leaves tend to be denserand to have lower pigment content. This colinearity affectstheir individual relation with both pigment- and mass-specificabsorption. We used path analysis in an attempt to distinguishbetween direct and indirect effects (Williams et al. 1990) andfound significant direct effects for each leaf descriptor on thevariation of pigment- and mass-specific absorption (fig. 6; pathanalysis data for mass-specific absorption are not shown). Pig-ment content and leaf density were the main factors associatedwith the variation in pigment-specific absorption (fig. 6) andmass-specific absorption, respectively. The indirect effects re-sulting from the colinearity between leaf thickness, leaf density,and pigment content led to (1) an absence of a correlation forboth leaf thickness and leaf density with pigment-specific ab-sorption (Pearson correlation coefficients, ; table 1; fig.P 1 0.056) and (2) an overestimation of the Pearson correlation coef-ficients with mass-specific absorption (table 1). Therefore, pathanalysis showed a direct and negative association between leafdensity and leaf thickness with pigment-specific absorption.The reduction in the effective absorption cross section (i.e.,higher-pigment self-shading) shown by pigments within thickand dense leaves is counterbalanced by a reduction in pigmentcontent. However, highly pigmented leaves exhibit less reduc-tion in pigment effective absorption cross section because theytend to be thinner and less dense (higher leaf-biomass expan-sion, high SLA or low LMA). Path analysis also showed adirect and positive effect of pigment content on the variationof mass-specific absorption as well as a strong and negativedirect effect of leaf thickness and leaf density. Thick and denseleaves of M. aquatica will experience a high reduction in mass-specific absorption because they tend to have lower pigmentcontent. Highly pigmented leaves will be very efficient in ab-sorbing light per unit of mass because of their higher “biomassexpansion” (lower density and thickness).


Fig. 6 Path diagrams describing the structure of the relationship between specific absorption (average along the PAR range, , and at the∗apigm

clorophyll a peak, ) and leaf density, leaf thickness, and pigment or chlorophyll a content. Numbers in bold type show the Pearson correlation∗achla

coefficients among the variables. Pearson correlations between the specific absorptions and leaf descriptors have been separated into direct andindirect effects. We show the fraction of the association explained by each effect. Indirect effects are attributable to indirect relationships to othervariables (Williams et al. 1990).

Implications of Leaf Morphological Variation onMentha aquatica Acclimation

Considering only the differences among leaves in their abilityto capture light, and assuming a similar ability to fix CO2, wefind that thin, low-density, highly pigmented leaves of M. aqua-tica may allow the plant to achieve better net carbon incomeper unit of absorbed photon because they display higher lightabsorption efficiencies per unit of carbon or dry mass thanthick, dense, less pigmented leaves. Consequently, the devel-opment of (1) thin, low-density, highly pigmented leaves mayoptimize plant growth under light limitation, while the devel-opment of (2) thick, dense, less pigmented leaves may lead toa reduction in plant specific growth rate (RGR). We confirmedboth assumptions by examining the variation in LMA andrelative growth rates (RGR) displayed by M. aquatica in ourexperiments. Plants grown under low and medium light treat-ments (LL and ML) showed low leaf biomass packing (lowLMA) irrespective of their nutrient treatment (fig. 7b). Theseplants also showed the lowest RGR (fig. 7a), indicating growthlimitations resulting from their low light income. Plants grownunder optimal nutrient supply (HN) and high light (HL)

showed the highest growth rates (fig. 7a) and low leaf biomasspacking (fig. 7b). We found a strong and negative relationshipbetween LMA and RGR ( , ) for ther p �0.78 P ! 0.0001plants grown under high light supply (HL) and the three dif-ferent nutrient treatments (LN, MN, and HN), in both air andwater. The association between LMA, or its inverse, SLA, andrelative growth rate has been repeatedly described in the lit-erature (Odum et al. 1958; Littler and Murray 1974; Littlerand Littler 1980; Poorter 1989; Poorter and Remkes 1989;Nielsen and Sand-Jensen 1990; Lambers and Poorter 1992;Kirk 1994; Nielsen et al. 1996; Reich et al. 1997). However,these comparative works, which differ in the taxonomic groupexamined or in the diversity of species considered, cannot pro-vide an explanation for the mechanism behind the empiricalassociation described. Our work provides such a mechanisticexplanation, describing the quantitative bases of the relationbetween the degree of biomass-packing expansion and the var-iation in leaf ability to absorb light. It is important to considerthat the association between LMA and relative growth rate isnot only dependent on light absorption processes. Maximumphotosynthetic rate depends on Rubisco concentration, which


Fig. 7 a, Relative growth rate (RGR) of Mentha aquatica grown inhydroponic cultures under different environmental conditions. LH, MN,and HN denote low, medium, and high nutrient supply; LL refers tothe lower light supply (50% of shading) and the shorter photoperiod(10 h : 14 h light : dark); ML refers to the maximum light supply (100mmol m�2 s�1) and the shorter photoperiod (10 h : 14 h light : dark);HL refers to the maximum light supply (100 mmol m�2 s�1) and thelongest photoperiod (14 h : 10 h light : dark); Water refers to plantsgrowing submerged at the maximum light supply (100 mmol m�2 s�1)and the longer photoperiod (14 h : 10 h light : dark). b, Relationshipbetween relative growth rates (RGR) and leaf biomass packing (LMA)of M. aquatica grown in hydroponic cultures under different environ-mental conditions. Circles refer to the lowest nutrient supply (LN), tri-angles refer to the medium nutrient supply (MN), and squares refer tothe highest nutrient supply (HN). Symbols are filled with the same pat-tern shown in a.

may affect variation in LMA. At the same time, maximumphotosynthetic rate is regulated by CO2 availability, which de-pends, for C3 plants such as M. aquatica, on CO2 uptake. Lloydet al. (1992) showed that differences among species in CO2

diffusion explain the variability found in CO2 assimilationrates despite having similar levels of Rubisco and electrontransport capacity. A mechanistic relation between internal leafstructure and photosynthetic carbon dioxide diffusion has been

proposed (Nobel 1983; Parkhurst 1986). The conclusions of-fered so far have emphasized the primary importance of CO2

diffusion to explain the adaptive significance of internal leafstructure, especially the differentiation between palisade andspongy mesophyll tissues, without minimizing the relevance ofother lesser-known factors such as light. Single parameters pro-posed by Nobel (1983) as optimizing photosynthetic ratesthrough improving internal conductance for CO2 diffusionfrom stomatal cavity to chloroplasts (e.g., cell surface area,volume of intercellular spaces, or chlorophyll content per areaor volume) may also optimize photosynthesis through en-hancing leaf light absorption within the tissue. Plant growthintegrates multiple levels of plant complexity; therefore, itsregulation is not dependent on a single mechanism but onmultiple factors. Photosynthetic carbon assimilation relies ba-sically on two processes: the ability of the photosynthetic struc-ture to capture light and the efficiency of the photosyntheticprocesses to transform such absorbed energy into assimilatedcarbon. Any variation in leaf form that results in an increasein leaf ability to absorb light and, therefore, causes an increasein photosynthetic carbon assimilation will be of primary im-portance in improving plant growth and survival. Menthaaquatica leaves may enhance absorptance by increasing leafthickness or increasing pigment content. Plants grown undernutrient limitation may reduce investment in pigment-proteincomplexes without significantly reducing photon collection byproducing thicker leaves. At the same time, thicker leaves mayalso maintain a higher amount of chloroplasts under lowerirradiance levels, reducing photoinhibition and photodamagelosses. Therefore, thick, dense, less pigmented leaves wouldenhance plant performance under suboptimal environmentalconditions, reducing Photosystem II excitation pressure by in-creasing chloroplasts’ self-shading (Terashima and Saeki 1983;Bornman et al. 1991; Vogelmann 1993; Vogelmann et al. 1996;Evans 1998). Conversely, thin, low-density, highly pigmentedleaves would be produced under light limitation to reduce self-shading and maximize light collection. However, under opti-mal conditions, highly pigmented leaves may support higherphotosynthetic rates per unit biomass for the same Rubiscoconcentration by being thinner. Thinner leaves also may main-tain higher rates of CO2 supply, reducing photosynthesis car-bon limitation at saturating irradiances. The development ofthin, low-density, highly pigmented leaves under optimalgrowth conditions may enhance plant performance (i.e., RGR).

The evaluation of the relative importance of CO2 uptake orlight absorption (among other processes) to explain the mech-anistic association between leaf form and function is beyondthe objective of this work. It may be possible that the relativeimportance of light absorption versus CO2 uptake varies ac-cording to the environmental conditions. For instance, the ef-fect of light may dominate under subsaturating light condi-tions, while CO2 uptake may be more important to explainleaf acclimation to high light availability. Our work contributesto an understanding of the mechanistic association betweenplant form and plant function, offering new insights relatedto light absorption processes. Further work is needed to fullyunderstand the association between leaf morphology and in-trinsic functional plant traits such as maximum photosyntheticcapacity, leaf life span, and relative growth rate.


Acknowledgments

This research was funded by grants from the Danish Re-search Academy to S. Enrıquez and the Danish Natural ScienceResearch Council to K. Sand-Jensen. S. Enrıquez was also sup-

ported by a postdoctoral EU fellowship (ERBCHBICT941787) within the Human Capital and Mobility program.We thank Professor R. Trench, Dr. R. Iglesias-Prieto, Dr. A.T. Banaszak, and Dr. E. Garnier for their useful comments onthe manuscript.

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