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Environmental and Experimental Botany 60 (2007) 458–467
Biophysical and morphological leaf adaptationsto drought and salinity in salt marsh grasses
Brian R. Maricle a,∗, Douglas R. Cobos b, Colin S. Campbell b
a School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USAb Decagon Devices, Inc., 950 NE Nelson Ct. Pullman, WA 99162, USA
Received 6 March 2006; received in revised form 29 November 2006; accepted 20 January 2007
Abstract
Leaf energy budgets were constructed for 13 species of estuarine C4 grasses (Poaceae) to elucidate the biophysical effects of drought andsalinity on the interception and dissipation of solar energy. Spartina alterniflora, S. anglica, S. argentinensis, S. bakeri, S. cynosuroides, S.densiflora, S. foliosa, S. foliosa × S. alterniflora hybrids, S. gracilis, S. patens, S. pectinata, S. spartinae, and Distichlis spicata plants weregrown under controlled soil water potential gradients in a greenhouse. Species were grouped into four major ecological functional types, basedon elevational zonation ranges: low marsh species, middle marsh species, high marsh species, and freshwater species. Different functional typesare adapted to different environmental conditions, and responded differently to reduced water potentials. Latent heat flux decreased similarlyacross species in response to decreasing water potential. Latent heat loss was found to decrease by as much as 65% under decreasing waterpotential, leading to an increase in leaf temperature of up to 4 ◦C. Consequently, radiative and sensible heat losses increased under decreasingwater potential. Sensible heat flux increased as much as 336% under decreasing water potential. Latent heat loss appeared to be an importantmode of temperature regulation in all species, and sensible heat loss appeared to be more important in high marsh species compared to lowmarsh species. High marsh species are characterized by narrower leaves than middle and low marsh species, leading to a smaller boundary layer,and providing higher conductance to sensible heat loss. This may be an adaptation for high marsh species to regulate leaf temperature withoutaccess to large amounts of water for transpirational cooling. Stomatal conductance decreased with decreasing water potential across species: leafconductances to water vapor and CO2 decreased as much as 69% under decreasing water potential. Additionally, oxidative stress appeared toincrease in these plants during times of drought or salinity stress. Ascorbate peroxidase activities increased with decreasing soil water potential,indicating increased cellular reactive oxygen species. High marsh species had higher ascorbate peroxidase activities compared to low marshspecies, indicating higher tolerance to drought- or salinity-induced stresses. It was concluded that different species of marsh grasses are adapted forgrowth in different zones of salt marshes. Adaptations include biophysical, biochemical, and morphological traits that optimize heat exchange withthe environment.© 2007 Elsevier B.V. All rights reserved.
Keywords: Adaptation; Ascorbate peroxidase; Distichlis spicata; Energy balance; Salt stress; Spartina; Water stress
Abbreviations: A, CO2 assimilation rates; APX, ascorbate peroxidase; Ca, ambient concentration of CO2; Ci, intercellular concentration of CO2; cp, specificheat of air; d, characteristic dimension of leaf; D, vapor pressure deficit; es, saturation vapor pressure; E, transpiration; F, view factor (proportion of surroundingsoccupied by an energy source); gCO2 , leaf conductance to CO2; gHa, leaf boundary layer conductance to heat; gHr, gHa + gr; gr, radiative conductance; gs, stomatalconductance; gv, total leaf conductance to water vapor; gva, boundary layer conductance to water vapor; gvs, stomatal conductance to water vapor; H, sensible heatloss; La, longwave radiation emitted from air; Lg, longwave radiation emitted from ground; m, optical air mass; pa, atmospheric air pressure; PPFD, photosyntheticphoton flux density; PSI, photosystem I; R, ideal gas constant; Rabs, total absorbed radiant energy; Rnet, net radiation; s, slope of the saturation mole fraction function;Sb, direct beam of shortwave solar energy; Sd, diffuse shortwave radiation; Spo, solar constant; Sr, reflected shortwave radiation; St, total shortwave radiation; Ta, airtemperature; TL, leaf temperature; Tw, wet bulb temperature; u, wind speed; αs, shortwave absorptivity; αL, longwave absorptivity; γ*, psychrometric constant; ε,longwave emissivity; θ, solar zenith angle; λ, latent heat of vaporization of water; λE, latent heat loss; ρs, shortwave surface reflectance (albedo); σ, Stefan-Boltzmannconstant; τ, atmospheric transmittance; Ψ , water potential; Ψ soil, water potential of soil; Ψ solution, water potential of nutrient solution; ‰, salinity in parts per thousand
∗ Corresponding author. Present address: Department of Biological Sciences, Fort Hays State University, 600 Park St., Hays, KS 67601-4099, USA.Tel.: +1 785 628 5822; fax: +1 785 628 4153.
E-mail address: [email protected] (B.R. Maricle).
0098-8472/$ – see front matter © 2007 Elsevier B.V. All rights reserved.doi:10.1016/j.envexpbot.2007.01.001
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B.R. Maricle et al. / Environmental an
. Introduction
The salinity of sediment porewater is an important environ-ental factor influencing plant growth and species composition
n estuarine salt marshes. Salt ion toxicity has numerous dele-erious effects on plants such as denaturing cytosolic enzymesMunns, 2002) and facilitating the formation of reactive oxy-en species that can damage membranes and proteins (Zhu,001). Like drought stress, increasing soil salinity involves aecrease in soil water potential (Ψ ) (Hasegawa et al., 2000). Sto-ates are sensitive to changes in soil water potential, so stomatal
losure usually accompanies drought and salt stress (Brugnolind Lauteri, 1991). A decrease in stomatal conductance reducesncoming CO2 and thus can reduce photosynthetic rates.
Even in halophytic salt marsh species, CO2 fixation ratesre sensitive to increasing salinity levels (reviewed by Drake,989). While CO2 fixation rates typically decrease in times ofalt stress, chlorophyll fluorescence analysis has revealed thatight-harvesting processes are not affected by high salinity inome marsh grass species (Nieva et al., 1999). This results insurplus of light energy that is not used in photosynthesis.ithout safe dissipation, this excess light energy can result in
ver-reduction of electron carriers and the subsequent forma-ion of reactive oxygen species (Demmig-Adams and Adams,992). As a result, plant antioxidant systems can also play anmportant role in times of salinity stress (Zhu, 2001). Reducedhotosynthetic production resulting from increased salinity canherefore result from toxic salt ion effects, decreased CO2 fix-tion from closure of stomata, or oxidative stress from reactivexygen species.
Intertidal estuarine zones are inundated with brackish waterwice daily (Pennings and Bertness, 2001), so fluctuating saltevels and fluctuating water potentials are important physicalactors influencing plant productivity in estuaries. However, theffects of soil salinity and drought conditions on the biophysicalnergy budgets of salt marsh grasses remain unknown. Althoughany earlier studies have investigated environmental effects on
nergy budgets of flood-tolerant plants like rice (Homma et al.,999; Campbell et al., 2001; Oue, 2001) or other wetland com-unities (e.g., Bracho and Jose, 1990; Lafleur, 1990; Goodin et
l., 1996; Souch et al., 1998; Jacobs et al., 2002), much less workas been done with halophytes. Previous work has examinedhe importance of latent heat flux (Teal and Kanwisher, 1970)nd effects of water level on marsh energy budgets (Heilman etl., 2000), but no previous studies have measured leaf energyudgets of salt marsh plants over a controlled water potentialradient.
In the present study, we investigated the biophysical effectsf decreasing water potential on energy interception and dis-ipation processes in salt marsh grasses. Leaf energy budgetsere calculated for the estuarine C4 grasses Spartina alterni-ora Loisel., S. anglica C. E. Hubbard, S. argentinensis (Trin.)arodi, S. bakeri Merr., S. cynosuroides (L.) Roth, S. densiflora
rongn., S. foliosa Trin., S. foliosa × S. alterniflora hybrids, S.racilis Trin., S. patens (Aiton) Muhl., S. pectinata Bosc ex Link,. spartinae (Trin.) Merr. ex A.S. Hitchc, and Distichlis spicataL.) Greene under controlled drought and salinity conditions inrses
erimental Botany 60 (2007) 458–467 459
greenhouse. Incoming solar energy was measured and outgo-ng radiative, latent, and sensible heat losses were calculated toxamine the effects of sediment water status on the biophysi-al absorption and dissipation of radiant energy. Additionally,eaf conductances to CO2 were calculated to assess physio-ogical responses of plants to decreasing soil water potential.
e hypothesized that decreased stomatal conductance resultingrom drought or salinity stress would decrease latent heat fluxnd shift that portion of the heat load on radiative and sensibleeat losses. Sensible heat loss may become more important foreaf temperature regulation in plants adapted for growth in high
arsh areas with higher salinity stress and less water available,nd this may cause morphological changes to adapt to theseonditions.
Levels of oxidative stress were also investigated in plants withssays of leaf ascorbate peroxidase (APX). Previous studies haveound CO2 fixation rates in marsh plants to be very sensitiveo increasing salinity (reviewed by Drake, 1989), but the bio-hysical light-harvesting processes are normally not affected byncreasing salinity (e.g., Nieva et al., 1999). When CO2 fixationates are limited relative to light harvesting rates (e.g., underater stress), electron carriers can become over-reduced, and2 can be reduced to the highly reactive O2
− at PSI. Super-xide dismutase oxidizes O2
− and forms H2O2, which APXhen reduces to H2O. This forms the “water–water cycle” inhloroplasts (Asada, 1999) and can become important underonditions where CO2 fixation rates become limited relative toight harvesting rates (Demmig-Adams and Adams, 1992). Aombination of decreased stomatal conductance and increasedxidative stress were expected to decrease photosynthetic CO2onductances and help account for decreased productivity underalt or drought stress.
The group of estuarine grasses tested in this study rep-esents a range of ecological functional types including lowntertidal marsh species (S. alterniflora and S. anglica), middle
arsh species (S. cynosuroides, S. densiflora, S. foliosa, and S.oliosa × S. alterniflora hybrids), high intertidal marsh speciesS. argentinensis, S. bakeri, S. patens, S. spartinae, and D. spi-ata), and inland freshwater species with lower salt toleranceS. gracilis and S. pectinata). These estuarine zones imposeifferent physical conditions on plant life, so an elevationalradient across an intertidal salt marsh contains an assortmentf plant species that encounter different salinity and waterlog-ing regimes in their natural environments. Low intertidal marshpecies are regularly inundated with tides; plants in these areasre adapted to waterlogged sediments with moderate to highalinity (Bertness and Ellison, 1987). In contrast, high intertidalarsh species experience infrequent tidal fluxes. Evaporative
tress is often high in these areas, leading to drier soils oftenontaining higher salinity levels compared to low marsh regionsPennings and Callaway, 1992). Thus high marsh plants aredapted to high salt levels but not chronic waterlogging.
This study was conducted to examine the biophysical
esponses of salt marsh plants to increasing drought and salttress. The results of this study are expected to be of broad inter-st because many plants are confronted with drought or salttress (low Ψ ) during part of their life. Historically, over 25% of
460 B.R. Maricle et al. / Environmental and Exp
Table 1The plant species included in the study. Shown is the approximate ecologicalfunctional type of each species, after Mobberley (1956) and other sources asstated, and where each was collected
Species Ecologicalfunctional type
Collected from
Spartina alterniflora Low marsha,b,c Willapa Bay, WashingtonSpartina anglica Low marshd,b Puget Sound, WashingtonSpartina argentinensis High marsh ArgentinaSpartina bakeri High marsh Sapelo Island, GeorgiaSpartina cynosuroides Middle marshe,f Sapelo Island, GeorgiaSpartina densiflora Middle marshg Odeil Salt marshes, SW SpainSpartina foliosa Middle marshh,i San Francisco Bay, CaliforniaS. alterniflora x S. Middle marshi,j San Francisco Bay, Californiafoliosa F1 hybridSpartina gracilis Inland freshwater Grant County, WashingtonSpartina patens High marshc,k Gulf Coast, NW FloridaSpartina pectinata Inland freshwaterk Butler County, NebraskaSpartina spartinae High marsh Galveston Bay, TexasDistichlis spicata High marshh,k Puget Sound, Washington
a McKee and Patrick, 1988.b Sayce and Mumford, 1990.c Bertness, 1991.d Frenkel, 1987.e Odum and Fanning, 1973.f Higinbotham et al., 2004.g Castillo et al., 2000.h Zedler et al., 1999.i
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Ayres et al., 2004.j Maricle, personal observation.k Nova Scotia Museum of Natural History, 1996.
.S. soils are prone to drought conditions and 40.8% of insur-nce claims for crop loss in the U.S. result from drought (Boyer,982). Additionally, almost half the irrigated land and 20% of theorld’s cultivated lands are subjected to some degree of salin-
ty (Zhu, 2001). Adaptations of plants that naturally tolerate lowater potentials are clearly important when considering primaryroductivity in many estuarine and agricultural systems.
. Materials and methods
.1. Plant material and growing conditions
Experimental plants were collected from the field sites listedn Table 1 and were subsequently maintained and tested underreenhouse conditions. Field plants were broken apart andillers were potted individually in a 50/50 (v/v) sand/potting
wac
able 2olution and soil water potentials (Ψ ) of all waterlogging and salinity treatments used
dentified by salinity (‰) and “flooded” or “drained” soil conditions
utrient solution salinity (‰) Ψ solution (MPa)
0‰ −0.034 ± 0.12 (6)0‰ −0.87 ± 0.07 (6)0‰ −1.59 ± 0.04 (6)0‰ −2.38 ± 0.04 (6)0‰ −3.05 ± 0.10 (6)
erimental Botany 60 (2007) 458–467
oil mixture. All plants were watered sparingly twice weeklyith modified Hoagland nutrient solution (Epstein, 1972).reenhouse conditions consisted of natural lighting (averagePFD was 1280 �mol m−2 s−1 and average radiant energy was80 W m−2 at midday) with 26 ◦C daytime temperatures and8 ◦C at night.
Plants were randomized between treatments (drained vs.ooded soil conditions; 0 to 40‰ salt) and allowed 30 days tocclimate to growing conditions before initiating the experiment.welve pots were placed into each tub in an unbalanced blockesign; at least five tubs were used for each treatment. Floodedreatment plants were submerged to a level 2 cm above the soilurface (about 12 L) and the water was completely replacedeekly. During the acclimation period, salinity levels were
ncreased incrementally (10‰ per week) until flooded treat-ents included 0, 10, 20, 30, and 40‰ salt (Instant Ocean salts;quarium Systems, Mentor, OH). Drained treatment plants
epresented droughted conditions. These plants were wateredparingly twice a week with water containing 0 or 10‰ salt;he surface soil in drained treatment plants became slightly dryetween waterings. Once proper salinity levels were reached,lants grew at least 30 days in their respective treatment beforeesting. The freshwater species S. gracilis and S. pectinata wereuite sensitive to salt, and most of these plants died in treat-ents with at least 20‰ salt. This led to small sample sizes
n = l) for the “freshwater” functional type in the 40‰ treatment,nd n = 3–6 in all other salinity levels > 0‰ in the “freshwater”unctional type. The statistical model was therefore not able toompare 40‰ salinity freshwater plants with other species orreatments. The other three species groupings had substantiallyarger sample sizes across treatments (n = 9–91).
.2. Water potential measurements
A vapor pressure osmometer (model 5500; Wescor, Inc.,ogan, UT) was used to measure osmolality (mmol kg−1) ofutrient solutions (Ball and Oosterhuis, 2005). 10 �L samplesrom six replicate mixings were measured for each salinity levelrior to addition to plants, and Ψ was calculated using the Van’toff relation:
−1
here R is the ideal gas constant (0.00831 MPa kg mol−1 K−1)nd T is temperature (K) (Nobel, 1983). Solution Ψ was veryonsistent between mixings (Table 2).
in the study. Shown is the mean ± S.D. (n) for each treatment. Treatments are
Treatment Ψ soil (MPa)
0‰ flooded −0.195 ± 0.081 (21)0‰ drained −0.69 ± 0.28 (26)10‰ flooded −0.98 ± 0.06 (12)20‰ flooded −1.66 ± 0.07 (12)30‰ flooded −2.34 ± 0.06 (12)40‰ flooded −3.11 ± 0.20 (9)10‰ drained −5.03 ± 1.87(8)
B.R. Maricle et al. / Environmental and Exp
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ig. 1. The water potential (Ψ ) of soils in 0‰ drained treatments at surfaceblack circles) and rooting depth (open circles). Bars indicate ± S.E. (n = 4–6).
Soil water potentials were measured for plants in all treat-ents using a WP4 Dew Point Potentiometer (Decagon Devices,
nc., Pullman, WA). Soil Ψ was measured at the surface and atooting depths (4–5 cm) in 4–6 pots from each of two tubs perreatment following two separate watering events. Soil Ψ wasery consistent between pots for flooded treatments (Table 2).rained treatment plants were slightly more variable between
ndividuals. Surface Ψ was quite variable between waterings inrained treatment plants, but Ψ at rooting depth remained nearlyonstant (Fig. 1).
.3. Leaf energy budget calculations
Leaf energy budgets were constructed for three populationsf greenhouse plants. Measurements were made on each planturing mid-day hours on clear days on 8 April to 16 April004, 23 May to 4 June 2005, and 24 August to 13 Septem-er 2005. A standard sling psychrometer (model #1328; Taylorrecision products; Oak Brook, IL) was used to measure dryulb (Ta) and wet bulb temperatures (Tw), and temperatures ofhe greenhouse walls and floor were measured with an infraredhermometer (Raytek Raynger ST; Total Temperature Instru-
entation, Inc.; Williston, VT). Wind speed (u) was measuredith a Traceable® hot wire anemometer (Control Company;riendswood, TX). Stomatal conductance (gs) was measuredith an LI-1600 steady state porometer (LI-COR Inc., Lincoln,E) and leaf temperature (TL) was measured for each plant withfine-wire thermocouple inside the porometer leaf chamber.
otal incoming shortwave radiant energy (St) was measured withn LI-200 cosine-corrected pyranometer (LI-COR Inc., Lincoln,E). Diffuse shortwave energy (Sd) was calculated after Liu and
ordan (1960) as:
(W m−2) = 0.3(1 − τm)S cos θ (2)
d pohere τ is atmospheric transmittance (taken to be 0.7 on a clearay; Campbell and Norman, 1998), θ is the solar zenith angle,po is the solar constant (1360 W m−2), and m is the optical airass, calculated after Campbell and Norman (1998) as:
g
wdm
erimental Botany 60 (2007) 458–467 461
(unitless) = pa
(101.3 kPa)(cos θ)(3)
here pa is atmospheric pressure (in kPa). Reflected shortwaveadiation (Sr) was calculated as:
r(W m−2) = ρs(St) (4)
here ρs is the shortwave surface reflectance (albedo), measuredo be 0.166 in the greenhouse.
The direct beam of solar energy (Sb) was calculated afterampbell and Norman (1998) as:
b(W m−2) = St − Sd (5)
Total absorbed radiant energy (Rabs) was then calculated,odified from Campbell and Norman (1998) as:
abs(W m−2) = αs(FbSb + FdSd + FrSr) + αL(FaLa + FgLg)
(6)
here αs and αL are absorptivities of plant leaves in the short-ave and longwave ranges; αs was estimated from pyranometereasurements of incident, transmitted, and reflected radiation
rom plant leaves, and αL was taken to be 0.97 (Campbell andorman, 1998). The “F” terms represent the appropriate view
actor for each component: Fb is 0.5, Fd is 1.0, and Fr, Fa, andg are each 0.5. La and Lg are longwave radiation emitted from
he atmosphere and ground, calculated as:
(W m−2) = εσT 4 (7)
here ε is the longwave emissivity of the object (taken to be 0.90or concrete and 0.93 for glass; Campbell and Norman, 1998),
is the Stefan-Boltzmann constant (5.67 × 10−8 W m−2 K−4),nd T is the temperature of the object (K). Net radiation was thenound by subtracting the outgoing radiative (longwave) radiationrom each plant:
net(W m−2) = Rabs − εLσT 4L (8)
here εL is the emissivity of the leaf (taken to be 0.97; Campbellnd Norman, 1998), and TL is leaf temperature (K). The com-lete energy budget was then found by subtracting sensible andatent heat lost:
net − H − λE = 0 (W m−2) (9)
ith an experimental error rate of 2.91%. In the above equation,is sensible heat flux and λE is latent heat loss (Campbell andorman, 1998). Sensible heat flux was calculated as:
(W m−2) = cpgHa(TL − Ta) (10)
here cp is the specific heat of air (29.3 J mol−1 ◦C−1) and gHas the leaf boundary layer conductance to heat, calculated as:
Ha(mol m−2s−1) = (0.135)
√u
(11)
dhere u is the wind speed (m s−1) and d is the characteristicimension of the leaf (m), found by multiplying 0.72 by theaximum width of the plant leaf (Campbell and Norman, 1998).
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62 B.R. Maricle et al. / Environmental an
atent heat flux (λE) was found using the Penman-Monteithquation (Monteith, 1965):
Eleaf(W m−2) = s(Rabs − εLσT 4a ) + γ∗λgvD/Pa
s + γ∗ (12)
here gv is leaf conductance to water vapor, Ta is in K, D is theapor pressure deficit (kPa), pa is atmospheric pressure (kPa), ss the slope of the saturation mole fraction function, and γ* ishe psychrometric constant, calculated as:
(◦C−1) = (17.502)(265.5 ◦C)(es)
(pa)(265.5 ◦C + Ta)2 (13)
∗(◦C−1) = cp/λ × gHr
gv(14)
here λ is the latent heat of vaporization of water44,000 J mol−1), es is the saturation vapor pressure at theeasured air temperature, and gHr = gHa + gr (Campbell andorman, 1998). Radiative conductance (gr) was calculated as:
r(mol m−2s−1) = 4εLσT 3a
cp(15)
here Ta is in K (Campbell and Norman, 1998). Leaf conduc-ance to water vapor (gv) is the sum of boundary layer andtomatal resistances and was calculated as:
v(mol m−2s−1) = 1
1/gvs + 1/gva(16)
here gvs is stomatal conductance to water vapor measured withhe LI-1600 porometer and gva is the boundary layer conduc-ance to water vapor, calculated after Campbell and Norman1998):
va(mol m−2s−1) = (0.147)
√u
d(17)
eaf conductance to CO2 was calculated after Salisbury andoss (1992):
CO2 = 0.625gv (18)
gCO2 measures allow researchers to calculate CO2 assimila-ion rates (A) with simple models, e.g., A = gCO2 (Ca − Ci), where
a and Ci are ambient and intercellular concentrations of CO2Salisbury and Ross, 1992). Since CO2 levels within the green-ouse were likely not equal to ambient, we present only gCO2
nd not A.
.4. Leaf ascorbate peroxidase assays
Following energy budget measurements, plant leaves werearvested and flash-frozen in liquid nitrogen. Assays of thentioxidant enzyme ascorbate peroxidase (APX) were later per-ormed spectrophometrically after Nakano and Asada (1981).eaf samples stored at −80 ◦C were ground with a mortar and
estle in 10 mL g−1 cold extraction buffer, containing 50 mMris (pH 7.0) with 5 mM MgCl2, 2 mM cysteine hydrochloride,nd 2% w/v PVP-40. The resulting mixture was centrifugedt 15,000 × g for 5 min at 4 ◦C. The supernatant was assayed(piP
erimental Botany 60 (2007) 458–467
or APX activity at 25 ◦C. 10 �L aliquots of the extract super-atant were added to 0.980 mL of a reaction mixture containing0 mM KH2PO4, 0.5 mM ascorbate, and 0.1 mM EDTA (pH.0). Background rates of ascorbate reduction were calculated inhe presence of enzyme extract but in the absence of H2O2. Theeaction was initiated with the addition of 10 �L 10 mM H2O2final concentration = 0.1 mM). Enzyme activity was determineds a decrease in ascorbate, measured as a decrease in absorbancet 290 nm, using an extinction coefficient of 2.8 mM−1 cm−1
Nakano and Asada, 1981). APX activities were corrected forackground rates of ascorbate reduction and standardized to gresh leaf weight.
.5. Statistical analyses
Statistical analyses were performed using two-factor (speciesnd treatment) analysis of variance (proc mixed; SAS version.0, 2001 SAS Institute Inc., Cary, NC;α = 0.05). In these modelspecies were grouped by ecological functional type and blockedy the three populations and the 76 tubs involved in the study.
. Results
.1. Effects of decreasing water potential
Increasing salinity and increasing soil dryness both decreasedoil water potential (Ψ ) and both had similar effects on plantnergy budgets in this study. The soil in drained treatment plantsecame slightly dry between waterings (Fig. 1), thus reducinghe matric potential of the soil (Salisbury and Ross, 1992). Plantsrowing in the 10‰ salt drained treatment experienced the mostevere water stress from a combination of the low matric poten-ials of dry soils and low osmotic potentials characteristic ofaline soils (Table 2). In contrast to the drained treatments, theoil in flooded treatment plants remained saturated throughouthe experiment. Therefore, the matric potential of these soilsemained at zero. The stepwise increase in treatment salinityesulted in a corresponding decrease in soil osmotic potentialTable 2). Consequently, both drought and saline conditionsesult in decreased soil Ψ , with an additive effect in the 10‰alt drained treatment.
Leaf shortwave absorptivities (αs) ranged from 0.62 to.70 across species (data not shown). There were no differ-nces in αs between treatments or species (ANOVA, p > 0.126;ata not shown). Absorbed radiation (Rabs) did not differetween treatments (ANOVA, p = 0.924) or species group-ngs (ANOVA, p = 0.103). Mean Rabs ranged from 572.4 to62.4 W m−2 (Fig. 2a); variations in Rabs reflect changingime-of-day conditions between individual measurements. Netadiation (Rnet) was found by subtracting leaf radiative energyrom Rabs (Eq. (8)). Therefore, plants with higher leaf tempera-ures had a correspondingly lower Rnet. Mean Rnet ranged from9.2 to 208.9 W m−2 across treatments and species groupings
Fig. 2b) and did not differ between species groupings (ANOVA,= 0.786). While variations in Rnet reflect the random variationsn Rabs, some differences between treatments were apparent.lants under drained soil conditions and higher salinities tended
B.R. Maricle et al. / Environmental and Experimental Botany 60 (2007) 458–467 463
Fig. 2. The effect of soil Ψ on (a) total leaf absorbed shortwave radiation (Rabs)and (b) leaf net radiation (Rnet). Bars indicate ± S.E. (n = 3–91). Species aregΨ
s
tdttd
Fabl
Fig. 4. The effect of decreasing soil Ψ on leaf conductance to water vapor (gv)and leaf CO conductance (g ). Bars indicate ± S.E. (n = 3–91). Species arega
bp
1omntΨ
(m
rouped by ecological functional type. Treatments are arranged by decreasing: the number for each treatment category (0 through 40) refers to treatment
alinity (‰) and “DR” or “FL” refers to drained or flooded soil conditions.
o have the lowest Rnet values. Rnet significantly decreased with
ecreasing Ψ (ANOVA, p < 0.001), resulting from increased leafemperature (TL) in low Ψ treatments. Mean TL ranged from 25.9o 30.4 ◦C across treatments and species groupings (Fig. 3a). TLid not differ between species groupings (ANOVA, p = 0.398)ig. 3. The effect of soil Ψ on (a) leaf temperature (Tleaf) and (b) leaf char-cteristic dimension (d). Bars indicate ± S.E. (n = 3–91). Species are groupedy ecological functional type; treatments are arranged by decreasing Ψ and areabeled as in Fig. 2.
dslmbd(Tdrsds
fsMt
(Ψ
st
a0nsA
2 CO2
rouped by ecological functional type; treatments are arranged by decreasing Ψ
nd are labeled as in Fig. 2.
ut became significantly higher with decreasing Ψ (ANOVA,< 0.001), increasing by as much as 4 ◦C.
Mean leaf characteristic dimension (d) ranged from 3.8 to0.9 mm (Fig. 3b) and was significantly different between eachf the four species groupings (high marsh < fresh water < lowarsh < middle marsh; ANOVA, p < 0.001). Although not sig-
ificantly different between treatments (ANOVA, p = 0.265),here appeared to be trends of d decreasing under decreasing
(Fig. 3b), either as a gradual decline with decreasing Ψ
high marsh and fresh water) or as a threshold response (middlearsh).Increasing soil dryness had a large effect on stomatal con-
uctance (gs) and related parameters (gv, gCO2 , and λE) in allpecies. Mean gs measures ranged from 49 mmol m−2 s−1 inow Ψ treatments up to 206 mmol m−2 s−1 in high Ψ treat-ents (data not shown). There were no significant differences
etween species groupings (ANOVA, p = 0.403), but largeifferences were observed between treatments in all speciesANOVA, p < 0.001), suggesting similar effects across species.he decreased gs resulting from decreasing Ψ led to consequentecreased leaf vapor conductance (gv) across species. Mean gvanged from 0.046 to 0.173 mol m−2 s−1 across treatments andpecies groupings (Fig. 4). In a manner similar to gs, gv did notiffer between species groupings (ANOVA, p = 0.210) but wastrongly reduced at low Ψ (ANOVA, p < 0.001).
Rates of latent heat loss (λE) were not significantly dif-erent between species groups (ANOVA, p = 0.671) but weretrongly affected by decreasing soil Ψ (ANOVA, p < 0.001).
ean λE ranged from 61.4 W m−2 in water stressed plants upo 175.4 W m−2 in moderate salinity plants (Fig. 5a).
Mean H ranged from 14.5 to 100.6 W m−2 across treatmentsFig. 5b). H became significantly higher with decreasing soil
(ANOVA, p = 0.001). The high marsh species in this studyhowed significantly higher rates of sensible heat loss comparedo middle and low marsh species (ANOVA, p = 0.030).
The relation of sensible to latent heat losses is often expresseds the Bowen ratio (H/λE). Mean Bowen ratios ranged from.11 to 2.05 in the present study (Fig. 6). Bowen ratios did
ot differ between species groupings (ANOVA, p = 0.263) butignificantly increased with decreasing Ψ (ANOVA, p < 0.001).significant treatment/species grouping interaction (p = 0.022)
464 B.R. Maricle et al. / Environmental and Experimental Botany 60 (2007) 458–467
Fig. 5. The effect of decreasing soil Ψ on (a) latent heat flux of leaves (λE) and(ga
is
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Fig. 7. The effect of decreasing soil Ψ on leaf ascorbate peroxidase (APX)activities. Bars indicate ± S.E. (n = 3–15). Species are grouped by ecologicalfF
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4
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sfv(
b) sensible heat loss by leaves (H). Bars indicate ± S.E. (n = 3–91). Species arerouped by ecological functional type; treatments are arranged by decreasing Ψ
nd are labeled as in Fig. 2.
ndicated increasing Bowen ratios with salinity in the marshpecies.
.2. Oxidative stress
Mean leaf APX activities ranged from 10.2 �mol g−1 min−1
n 10‰ salinity flooded low marsh plants up to9.6 �mol g−1 min−1 in 40‰ salinity flooded high marshlants (Fig. 7). There was a significant interaction betweenreatment and species grouping in APX activity (ANOVA,< 0.001). The middle and high marsh species significantly
ncreased APX activities in response to decreasing Ψ (ANOVA,≤ 0.044), while the fresh water and low marsh species did not
ANOVA, p ≥ 0.580). Additionally, APX activities in the higharsh species were significantly higher compared to all other
pecies groupings (ANOVA, p < 0.001).
ig. 6. The effect of decreasing soil Ψ on leaf Bowen ratios (H/λE). Barsndicate ± S.E. (n = 3–91). Species are grouped by ecological functional type;reatments are arranged by decreasing Ψ and are labeled as in Fig. 2.
tpasiSlab
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unctional type; treatments are arranged by decreasing Ψ and are labeled as inig. 2.
. Discussion
.1. Effects of decreasing water potential
Environmental conditions vary across intertidal zones in saltarshes. Plants in low intertidal marsh settings are subjected to
requent tidal inundations with brackish water. In contrast, plantsn high marsh settings often experience dried soils between infre-uent inundations, leading to elevated soil salinities and lowater potentials. Survival in these sediments requires mecha-isms to maintain adequate water relations as well as a properalance of interception and dissipation of solar energy. Theesults of this study indicate that many salt marsh species aredapted to the prevailing conditions in their specific zone of thealt marsh by variations in leaf biophysics, biochemistry, andorphology.Incoming solar radiation was efficiently absorbed by all
pecies in the study. Leaf shortwave absorptivities (αs) rangedrom 0.62 to 0.70 and were slightly higher than expected αsalues for C3 inland plants reported by Campbell and Norman1998). The thick, dark leaves of C4 Spartina species may helpo intercept more solar radiation compared to other herbaceouslants that may not be adapted to high light environments thatre typical in salt marshes. While some plants appeared to sufferalinity-induced bleaching of leaves at high salinity, this increasen transmissivity did not lead to differences between treatments.alt crystals were secreted on leaves under salinity treatments,
eading to increased reflectance that apparently overshadowedny bleaching effects. Thus, there were no differences in αsetween treatments or species.
Since the plants in this study were grown under identical con-itions, all received equal amounts of radiant energy. Plants atigh water potential (high Ψ ; flooded soil, low salt) lost moreeat via latent cooling than plants at low Ψ (drained soil, highalt). Plants at low Ψ tended to lose more energy via radiative andensible pathways than plants at high Ψ . During times of watertress, transpiration rates decreased, leading to decreased rates of
atent cooling. With decreased latent cooling during water stress,eaf temperatures were noted to increase by as much as 4 ◦C,eading to increased radiative and sensible heat losses. Mean TL
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B.R. Maricle et al. / Environmental an
anged from 25.9 to 30.4 ◦C across treatments and species group-ngs (Fig. 3a), similar to measurements of Spartina alterniflorand S. patens leaves by Teal and Kanwisher (1970). Interest-ngly, the lowest leaf temperatures were observed in moderatealinity treatments (usually 10‰ flooded treatments), likely dueo high rates of latent cooling. Mean λE ranged from 61.4 W m−2
n water stressed plants up to 175.4 W m−2 in moderate salin-ty plants (Fig. 5a). These measurements are slightly lower than
aximum values reported by Jacobs et al. (2002) for a prairieetland and Teal and Kanwisher (1970) for S. alterniflora and. patens in field settings. These differences are likely due to theonditions under which measurements were taken. The green-ouse conditions in the present study had a lower radiation loadhan the field sites used by Jacobs et al. (2002) and Teal andanwisher (1970). A higher radiation load under similar tem-eratures likely led to increased rates of latent heat flux in thesetudies (Eq. (12)) compared to the present study.
Latent cooling appeared to be similar across all ecologicalunctional types, but sensible heat loss (H) became more impor-ant in water-stressed high marsh species compared to low marshpecies. Plants with low transpiration rates in low Ψ treatmentsay be adapted to tolerate higher leaf temperatures in times
f low latent heat loss. Indeed, rates of latent heat loss comple-ented rates of H for many plants in this study. Leaf dimensions
an be important when considering leaf boundary layer conduc-ances to heat (gHa; Eq. (11)) and water vapor (gva; Eq. (17)).
ean H ranged from 14.5 to 100.6 W m−2 across treatmentsFig. 5b). These measurements are slightly lower than valueseported by Jacobs et al. (2002) for a prairie wetland but similaro the values of Teal and Kanwisher (1970) for S. alterniflorand S. patens in field settings. H is proportional to the differencen temperature between leaf and air (Eq. (10); Campbell andorman, 1998), and increased with decreasing soil Ψ . Similarly,ouch et al. (1998) found H to increase with drying soil con-itions on lakeshore communities. Additionally, the high marshpecies in this study showed significantly higher rates of sensi-le heat loss compared to middle and low marsh species. Higharsh conditions usually involve high salinity regimes and dry
oil between infrequent tidal fluxes. Therefore, plants adaptedo life in these conditions may be adapted to withstand highereaf temperatures, allowing higher rates of sensible heat flux toonserve water in times of low latent cooling. The high-marshpecies have narrow leaves (Fig. 3b) that help to increase con-uctance to heat loss (gHa; Eq. (11)) and therefore help increase
(Eq. (10)). Narrow leaves also increase the conductance toater loss (Eq. (17)), but many similar plants are noted to curl
eaves or orient leaves paraheliotropically to reduce water lossHeckathorn and DeLucia, 1991).
Leaf size, best represented by characteristic dimension (d), isherefore of interest when considering responses of plants to con-itions that increase TL. Growth of many plants became stuntednder low Ψ conditions, which may indicate sensitivity, but maylso provide increased ability to dissipate heat. Significantly
ncreasing Bowen ratios in the middle and high marsh speciesuggest these species are adapted to tolerate higher leaf temper-tures, resulting in higher rates of sensible heat loss, comparedo the freshwater species.mλ
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erimental Botany 60 (2007) 458–467 465
Mean stomatal conductance (gs) measures ranged from9 mmol m−2 s−1 in low Ψ treatments up to 206 mmol m−2 s−1
n high Ψ treatments, similar to results published for S. pectinatay Heckathorn and DeLucia (1991). The decreased leaf vaporonductance with decreased Ψ also resulted in a decreased leafonductance to CO2 (gCO2 ; Fig. 4). This will lead to a decreasen CO2 assimilation rates (A), consistent with observations ofecreased photosynthetic rates under salinity in many other saltarsh species (reviewed by Drake, 1989). If one assumed ambi-
nt CO2 concentrations of 370 ppm and Ci/Ca ratios 0.27–0.36Henderson et al., 1998), values for A in this study would beery similar to previously published measures of CO2 uptakey S. pectinata under salinity stress (Heckathorn and DeLucia,991).
It appears that energy may be gained and lost by differenteans with the onset of drought or salinity stress in marsh halo-
hytes. The results of this study suggest both drought and salinityave similar effects on marsh halophytes. Moreover, none ofhese results may be directly attributable to salt ion toxicity.n these marsh halophytes, the major influence of salt appearso be lowering soil Ψ , although increasing APX activities mayndicate oxidative stress also contributes to decreased marsh pro-uction with increasing salinity. However, stomatal conductanceFig. 4) and λE (Fig. 5) were lower in drained treatment plantsboth 0‰ and 10‰ salinity treatments) than would be expectedolely from a Ψ gradient. Environmental factors in additiono Ψ may exist in drained soil conditions that may yet needo be addressed. The role of toxic ion effects in these salinityreatments may be an interesting area for future investigation.
.2. Oxidative stress
In the present study, leaf APX activities ranged from0.2 �mol g−1 min−1 in 10‰ salinity flooded low marsh plantsp to 29.6 �mol g−1 min−1 in 40‰ salinity flooded high marshlants (Fig. 7). These values are lower than APX activities pub-ished previously for cotton (Gossett et al., 1996), tomato speciesShalata et al., 2001), and lotus (Ushimaru et al., 2001), but moreimilar to values published for potato (Benavides et al., 2000),aize (Jahnke et al., 1991), and rice (Lee et al., 2001). Previous
tudies have shown APX activities to increase with increasingalinity in rice (Lee et al., 2001) and the salt-tolerant tomatopecies Lycopersicon pennellii (Shalata et al., 2001; Mittova etl., 2004). In the present study, APX activities were found toncrease in the middle and high marsh species groupings. Thisndicates increasing salt or drought stress led to over-reductionf photosynthetic electron carriers, leading to the formation ofeactive oxygen species (Asada, 1999). High antioxidant activ-ties may be one way high marsh species are adapted for theighly saline conditions found in high marsh areas.
. Conclusions
The marsh plants in this study appeared to perform best underoderate salinity levels (10–20‰). Stomatal conductance andE were at their highest and TL was at its lowest under moderatealinity. Additionally, maximum growth occurred at 10–20‰
4 d Exp
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66 B.R. Maricle et al. / Environmental an
alinity (data not shown). Many of the effects of salt on plantsome as a result of water stress. Tolerance to saline soils appearso be due in part to specific biophysical, morphological, andiochemical adaptations in plants. The narrow leaves charac-eristic of high marsh species may be an adaptation to helpegulate leaf temperature in times of low latent cooling. Fur-her work may be needed to characterize changes in halophyteeaf size in response to environmental salinity. Additionally, theigh marsh species had higher APX activities compared to thether species in the study, indicating an increased ability to resistxidative stress. These strategies may be adaptations for plantrowth in the highly saline upper marsh zones. This indicateshat salt marsh Spartina and Distichlis species are highly tol-rant of saline soils, since growth is enhanced under moderatealinity (Greenway and Munns, 1980).
cknowledgments
The authors thank Chuck Cody for greenhouse assistance;enny Cartwright for use of equipment; Paul Rabie for help with
tatistics; Kim Patten, Sally Hacker, Eric Hellquist, M. Enriqueigueroa, Heather Davis, Debra Ayres, Eric Roalson, Steve Pen-ings, and Renae Maricle for providing plants; Al Black forelpful comments on the manuscript; and Janelle Maricle forelp with plant measurements. This project was partially fundedy the Betty W. Higinbotham Trust and NSF DEB-0508833 toRM.
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