Trends in Distribution and Size of Stomata in Desert Plants

Item Type Article

Authors Sundberg, Marshall D.

Publisher University of Arizona (Tucson, AZ)

Journal Desert Plants

Rights Copyright © Arizona Board of Regents. The University of Arizona.

Download date 13/05/2018 16:20:21

Link to Item http://hdl.handle.net/10150/554223

154 Desert Plants 7(3) 1985

Trends in Distributionand Size of Stomatain Desert Plants

Marshall D. SundbergUniversity of Wisconsin -Eau Claire

IntroductionStomata are microscopic pores on stems and leaves of

most green land plants which help to regulate gas exchange,particularly carbon dioxide, CO2, and water vapor, H2O.Carbon dioxide is essential for the process of photosyn-thesis. This process not only produces food for the plant andexcess stored food which may be utilized by herbivorousanimals - including mankind, but also produces oxygengas, 02, as a biproduct. Because the aerial portions of a plantare covered by a waxy layer nearly impervious to CO2, thecuticle, this gas enters the plant primarily through thestomates.

Individual living plant cells are often composed of 95% ormore water. Because they are enclosed within the samewaxy cuticle, which is also nearly impermeable to water,the internal air spaces between cells within the plant arenearly saturated with water vapor. As stomates open toadmit CO2 into the plant, H2O is simultaneously lostthrough these same pores. When the plant is growing underconditions of adequate water supply, this trade off of H2Oloss for CO2 gain is not harmful to the plant -in fact it isessential! The loss of water through the stomates, transpi-ration, is the driving force which allows more water anddissolved solutes to be drawn up from the roots through theplant (Raven, Evert & Curtis, 1981). A problem quicklyarises, however, when available water is in short supply.Water lost by transpiration cannot easily be replaced andwater deficits within the plant soon arise. This problem isparticularly severe in arid, xeric, environments; con-sequently desert plants, xerophytes, have evolved a numberof physiological and morphological features to minimizeits effect.

The cells of many desert plants are simply able to toleratelowered water content without injury (Levitt, 1980). Ac-cording to some workers these plants are the only "true"xerophytes. Many xerophytes possess long taproots whichenable them to penetrate to deep reservoirs of ground waterwhile others have extensively branched shallow root sys-tems which are efficient at trapping what minimal precipi-tation occurs (Levitt, 1980). Some desert plants in coastalareas may even trap moisture from fog or dew through theiraerial parts (Gindel, 1970). A large number of xerophytesavoid drought by quickly flowering and producing droughtresistant seeds following a rain. These ephemeral plants dieas subsequent drought becomes more severe but their seedsremain viable for one or more years until the next favorablegrowing season. In a similar fashion, many perennialxerophytes lose their leaves, or even whole shoots as condi-tions become more drier. Some such drought deciduousspecies may produce and shed several crops of leaves peryear as conditions dictate.

The leaves of xerophytes are generally small (Maximov,1929). This not only serves to minimize the surface areaover which transpiration may occur, but it also minimizesheat build up within the tissues (Smith, 1970). The densehairs and spines covering the aerial portions of many desertplants serve a similar function (Juniper and Jeffree, 1983).

For over one hundred years it has also been recognizedthat certain modifications of stomates are characteristic ofxerophytic plants (Haberlandt, 1884). The stomates of mostplants, including many xerophytes, occur at the surface of

Sundberg Stomata in Desert Plants 155

the leaf or stem (Fig. 1B,D), but in other desert plants theymay be sunken beneath the surface (Fig. 1A), or concen-trated in crypts below the surface (Fig. 1C). Likewise thedensity and size of stomates have been implicated asxeromorphic adaptations -here, however, the literature isfull of contradictions.

In 1884, Haberlandt claimed that stomatal densities aredecreased in desert plants. With fewer stomates per unitsurface area there would be less transpiration -a favorableadaptation in a xeric environment. In the same year Volk -ens (1884) stated that there is no correlation between thedensity of stomates and the xeric habitat. In fact in laterstudies he and others claimed that desert plants mayactually have an increased stomatal density (Volkens,1887; Maximov, 1929). The advantage in this is that in-creased transpiration would produce evaporativecooling -also a favorable adaptation in a xeric environ-ment. Although the first school of thought predominatedthrough the middle of this century and the latter predomi-nates today, both are argued in current textbooks of plantphysiology. Hall (1 976), Bidwell ( 1979) and Ting ( 1982)state that stomatal density is decreased while Devlin andWitham (1983) and Noggle and Fritz (1983) state that den-sities are increased in xerophytic plants.

The apparent contradiction in the current literature wasthe stimulus for a preliminary study undertaken by a stu-dent and myself (Strobel and Sundberg, 1984). The results ofthis study suggested that succulent and non -succulentxerophytes evolved different stomatal strategies to dealwith water stress. In the study described here a much largernumber of desert plants, growing under natural conditions,were examined to test our preliminary results.

Materials and MethodsField collections and laboratory examination was done at

the Desert Botanical Garden, Phoenix, AZ, during the firsttwo weeks of January, 1984. A total of 134 species, repre-senting 19 desert lifeforms (Crosswhite and Crosswhite,1984), were examined. Of these the stems and/or leaves of56 were succulent or semiscculent while those of 81 werenonsucculent (The leaves and stems of Ascelepias sub -ulata, Caralluma frerei and Pedilanthus sp. were treatedseparately).

A total of five tissue samples for each species were col-lected from fully sunlit plants. The number of stomates percalibrated field of view was determined from peels or freshparadermal sections of each sample. The average stomatallength was calculated from a sample of ten randomlyselected stomates measured with an ocular micrometer.Both surfaces of each leaf were examined. Photomicro-graphs were made of all fresh sections.

In those cases where counts and/or measurements couldnot be made directly (eg. Hesperaloe, Canotia, Casuarinaand Grewia) specimens were fixed in FAA and later em-bedded in paraffin, sectioned, and examined morphometri-cally as described previously (Strobel and Sundberg, 1984).Statistics were computed on an Apple IIe microcomputerusing biometry programs developed by Dr. Dwight Kincaid,Lehman College, City University of New York.

Materials for SEM were fixed in 10% acrolein, washed intwo changes of H2O and dehydratd in DMP ( Posteck and

Tucker, 1976). Following dehydration the tissue wasbrought through two changes of absolute acetone, onechange of amyl acetate and critical point dried. The speci-mens were gold coated with a Denton sputter coater andexamined with an ISI -Super I scanning electron micros-cope.

Results and DiscussionAn examination of the photomicrographs in Figure 2, all

taken at the same magnification, quickly suggests thatstomata of xerophytes may be either widely separated ordensely distributed over the surface of the plant. Further-more, the size of the stomatal opening may vary widely.The impression is that densely distributed stomates aregenerally smaller while widely distributed stomates aregenerally larger.

Our original suggestion (Strobel and Sundberg, 1984) wasthat low stomatal frequencies are associated with succu-lent tissues while high stomatal frequencies are associatdwith non -succulents. To test this hypothesis the mean fre-quencies for all succulents were calculated and comparedto similar values for all non- succulents. These data arepresented graphically in Figure 3. The average value fornon- succulents is 165.03mm-2 while the average for suc-culents is 32.64mm-2. Stomatal values in most plants rangefrom about 100 to 300mm-2, therefore succulents arecharacterized by a reduced number of stomates per unitsurface area. These desert plants reduce water loss by re-ducing the number of stomates through which water maytranspire. This is in agreement with actual transpirationstudies which have been done on succulent plants (Black etal., 1976; Stocker, 1976; Kluge & Ting, 1978). An interest-ing peculiarity in this regard is that the rate of transpirationin succulents is highest at night during periods of waterstress (Kluge & Ting, 1978). Most, if not all, desert succu-lents are CAM plants (Crosswhite, 1984), therefore therelatively few stomates are open predominantly at night.Carbon dioxide is fixed into organic acids and stored withinthe cells. During the following day these acids provide aCO2 source for photosynthesis while the stomates remainclosed, thus reducing H2O loss.

Associated with the low density of stomates in succu-lents is their relatively large size (Fig. 1B,D; 2A). The largeopen area of individual stomatal aperatures would tend tocounter the overall area decrease in stomatal area, per unitsurface area, caused by deceased density. In this waymaximum gas exchange occurs when the stomates areopen. Furthermore, Ting and Szarek (1975) have argued thatbecause of the generally round shape of the transpiringsurface of succulents, another factor, boundary layer resis-tance, is greater than the resistance to gas diffusion pro-vided by stomates. The result is that the large stomata ofsucculents are effective at regulating gas exchange overtheir entire range of apertures, a phenomenon noted byKluge (1976).

In contrast to succulents, the stomatal densities of non -succulents fall mostly within the typical range of moremesophytic plants and actually include some of the higheststomatal densities recorded. In the present study such highvalues included 580mm -2 (Buddleja saligna ), 523 mm -2(Guaiacum coulteri), 457mm-2 (Pithecellobium flexi-

156 Desert Plants 7(3)

Figure 1. Locations of stomata in desert plants relative tothe plant surface. A: Canotia holacantha (X1 000). B: Opun-tia Ficus -indica (X400), C: Nerium oleander (X700). D:Stapelia nobilis (X1000). Stomata are located at the surface(B) or even slightly elevated (D) in most succulents. Inmany non -succulents they are sunken in chambers belowthe surface. (A) or concentrated in subsurface crypts (C)[see arrows].

Figure 2. Relative size and density of stomates on leaves ofdesert plants. A: Cereus peruvianus. B: Lycium fremontii.C: Aloinopsis. D: Pithecellobium flexicaule. Magnifica-tion 1250x.

caule), and 440mM-2 (Ambrosia deltoidea). With such highnumbers of stomata per unit area one would expect that thesize of individual stomata would be smaller to effectivelyreduce the total transpiring area. This is to some degree true(Fig. 4), but the range of sizes is considerably smaller thanwould be expected based on the size /density relationshipfound in succulents. As a result it may be predicted thattranspiration rates in non -succulent desert plants will behigh. Many non -succulent xerophytes in fact have highrates of transpiration which often increases with increasingwater stress! Such an apparently contradictory situation

1985

200

I00

(I)

Et

ci]

MEAN VALUES

20

I0

Figure 3. Average stomatal density and stomatal length ofsucculent and non -succulent desert plants. Circles repre-sent non -succulents, squares represent succulents. Thestandard errors of the means are indicated by the verticalbars.

was noted by Maximov (1929) and has been subsequentlyreaffirmed by others (Ehrler, 1975; Stocker, 1976).

The adaptive advantage of high rates of water loss inthese xerophytes is to reduce tissue temperature byevaporative cooling. Unlike succulents, whose cells areable to tolerate very high daytime temperatures, a majorproblem of non -succulent xerophytes is to avoid heatbuildup in the tissues (Levitt, 1980). Evaporative cooling,due to high :rates of transpiration, can actually depressinternal tissue temperatures below that of the surroundingair (Levitt, 1980).

Ting and Szarek (1975) have noted that in the relativelyflat leaves of non -succulents, the resistance to diffusion,due to the boundary layer of air around the leaf, actuallybecomes more important than stomatal resistance by thetime the stomates are half open. Maximum gas exchange,therefore, will occur not with few, relatively large stomata,but rather with many smaller stomates. Although an indi-vidual small stomate will be less efficient at allowing gasexchange per unit pore area than an individual large sto-mate, a considerably larger number of small stomates maybe packed into a unit leaf area thus providing for greatertotal transpiration and consequently greater evaporativecooling potential.

Sundberg

NON-SUCCULENT

I 1 I

I00 200 300 400STOMATAL DENSITY (mm-2)

Figure 4. Regression lines for stomate length on stomataldensity in succulent and non -succulent desert plants. Suc-culents, y = 17.70 - 0.02x. The slopes of the regressionlines are significantly different.

ConclusionsIt is apparent from the data presented above that two

distinct stomatal strategies have evolved in desert plants:relatively large, infrequent stomates on the surface of suc-culents and smaller, more numerous stomates on the sur-face of non -succulents. In each case the stomatal size andfrequency provides an adaptive advantage to plants of aparticular life form. The large stomates provide for maxi-mum gas exchange at night in succulent CAM plants whiletheir infrequent occurrence helps to minimize water lossduring the day when the stomata are usually closed. Thefrequent, small stomates of non -succulents allow for highdaytime transpiration rates, therefore cooler tissue temp-eratures.

The results of this study also clarify the contradictorydescriptions of stomatal frequency found in the literature,and referred to at the beginning of this paper. Both increasedand decreased stomatal frequencies are found in desertplants- depending on their life form. Authors must becareful to specify if by xerophytic plant they are referring tosucculents, non -succulents, or all xerophytes.

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