Carbon balance, productivity, and water use of cold-winter ... et al 1977.pdf · Leaf areas were determined with a photoelectric planimeter (Caldwell and Moore, 1971). As part of

Oecologia (Berl.) 29, 275-300 (1977) Oecologia �9 by Springer-Verlag 1977

Carbon Balance, Productivity, and Water Use of Cold-Winter Desert Shrub Communities Dominated by C3 and C4 Species

Martyn M. Caldwell*, Richard S. White**, Russell T. Moore***, and L.B. Camp Department of Range Science and the Ecology Center, Utah State University, Logan, UT 84322, USA

Summary. Common generalizations concerning the ecologic significance of C4 photosynthesis were tested in a study of plant gas exchange, productivity, carbon balance, and water use in monospecific communities of C3 and C4 salt desert shrubs. Contrary to expectations, few of the hypotheses concerning the performance of C4 species were supported. Like the C3 species, Ceratoides Ianata, the C4 shrub, Atriplex confertifolia, initiated growth and photosynthetic activity in the cool spring months and also exhibited maximum photosynthetic rates at this time of year. To compete success- fully with C3 species, Atriplex may have been forced to evolve the capacity for photosynthesis at low temperatures prevalent during the spring when moisture is most abundant. Maximum photosynthetic rates of Atriplex were lower than those of the C3 species. This was compensated by a prolonged period of low photosynthetic activity in the dry late summer months while Ceratoides became largely inactive. However, the annual photosynthetic carbon fixation per ground area was about the same in these two communities composed of C3 and C4 shrubs. The C4 species did not exhibit greater leaf diffusion resistance than the C3 species. The photosynthesis/transpiration ratios of the two species were about the same during the period of maximum photosynthetic rates in the spring. During the warm summer months the C , species did have superior photosynthesis/transpiration ratios. Yet, since Ceratoides completed a somewhat greater proportion of its annual carbon fixation earlier in the season, the ratio of annual carbon fixation/transpiratory water loss in the two communities was about the same. Atriplex did incorporate a greater percentage of the annual carbon fixation into biomass production than did Ceratoides. However, this is considered to be a reflection

* To whom offprint requests should be sent ** Present address." U.S. Range Livestock Experiment Station, Agricultural Research Service, Miles City, MO, USA *** Present address: Ecology Consultants, Inc., Fort Collins, CO, USA

276 M.M. Caldwell et al.

of properties apart from the C4 photosynthetic pathway. Both species displayed a heavy commitment of carbon to the belowground system, and only about half of the annual moisture resource was utilized in both communities.

Introduction

Physiologic mechanisms and attributes of the C4 photosynthetic pathway have been well elucidated during the past decade (Hatch and Osmond, 1976). Yet an understanding of the ecologic import of this specialized photosynthetic pathway is still largely dependent upon generalizations from physiologic studies concerning characteristics such as impressive rates of net photosynthesis under conditions of high irradiance and warm temperatures (Black, 1973).

The essential physiologic characteristics that might confer adaptive advantage for C4 species include an initial carboxylation in mesophyll cells by phosphoenol- pyruvate carboxylase, an enzyme with particularly high affinity for CO2, and a subsequent decarboxylation in the thick-walled bundle sheath cells that act as a CO2-concentrating mechanism providing a rich CO2 environment for fixation by ribulosebiphosphate carboxylase with a minimum photorespiratory carbon loss. Thus, the benefits of C4 photosynthesis would be primarily the result of a favorable cellular environment for efficient carbon fixation by the Calvin- Benson enzymes combined with the capacity for effective CO2 carboxylation in mesophyll cells, even when leaf intercellular CO2 concentrations might be low due to partial stomatal occlusion (Bj6rkman, 1975; Hatch and Osmond, 1976). The greatest advantage of this pathway in permitting efficient photosynthesis while curbing water loss with greater stomatal diffusion resistance would appear to exist in environments in which there are water constraints and, at the same time, factors such as irradiance and low temperatures are not limiting. Indeed, most C4 species are found in warm arid environments, particularly at tropical latitudes.

Even in cooler temperate environments C4 photosynthesis should also provide some margin of selective advantage for species in water-limited areas. Although C4 species in many agronomic situations do exhibit both high productivity and favorable water use efficiency for growth (Black, 1973), a synoptic view of species in nonagricultural systems does not reveal any particular correla- tion between photosynthetic pathways and productivity (Caldwell, 1975). How- ever, seldom can suitable comparisons be made in which species of similar life forms possess different photosynthetic pathways and yet exist in truly comparable environments. Two prominent shrubs of the North American Great Basin, Atriplex confertifolia (Torr. and Frem.) S. Wats., C4, and Ceratoides lanata (Pursh) J.T. Howell, C3, present such an opportunity. These species occur either in mixed communities or in nearly monospecific stands in close proximity in sites of both comparable microenvironment and soils. These species are most abundant in the salt desert shrublands of the Intermountain West of the United States (Branson et al., 1967), but range from Mexico to Canada and are associates of shrublands and grasslands throughout western North

Carbon Balance and Water Use of C3 and C 4 Shrubs 277

America, especially on dry halomorphic soils. The shrublands of the Great Basin constitute an important winter grazing resource.

In a somewhat broader perspective, both C~ and C3 species are well represented in the flora of the Great Basin. Yet these C4 and C3 species do not necessarily segregate along environmental gradients of latitude or salinity. Thus, this region is of particular interest as a stage for gauging the success of the C4 pathway in a temperate region.

A study of primary production processes in the U.S. International Biological Program Desert Biome afforded the opportunity to test several common generalizations concerning performance of Ca and C4 species at the community level. Physiologic characteristics generally attributed to Ca and C4 species would suggest the following hypotheses:

1. The C4 species should not only exhibit higher rates of net photosynthesis per unit foliage mass, but this should also be reflected in greater carbon fixation on a ground area basis and greater biomass production in the community dominated by the C4 species.

2. Because C~ species characteristically exhibit high temperature optima for photosynthesis and effectively utilize high irradiance, in temperate environments one would expect the C4 species to delay growth and photosynthetic activity until the warmest period of the year when solar irradiance would also be highest, while the Ca species might initiate growth and photosynthetic activity in the early spring.

3. Because C4 species can still effectively conduct photosynthesis at low intercellular CO2 concentrations, which would result from partial stomatal clo- sure, one would expect these plants to take advantage of this property and partially occlude their stomates to curtail water loss. Thus, under field conditions they should exhibit higher stomatal diffusion resistance than their C3 counterparts under similar environmental conditions.

4. Associated with the higher stomatal diffusion resistance and greater effi- cacy of photosynthesis, foliage of C4 plants should exhibit higher ratios of net photosynthesis/transpiration than that of Ca species under similar environmental conditions in the field. This property should also be reflected in greater carbon fixation at the community level in relation to the annual transpiratory water loss, and greater community biomass production in relation to water use by the stand than would be the case for the Ca species.

5. More favorable photosynthesis/transpiration ratios may also enable the C4 species to allocate less energy to the root system and support more aboveground biomass at a given site.

Apart from attributes of these species specifically related to photosynthetic pathways and gas exchange characteristics, it was also a goal of this study to determine the general allocation of fixed carbon to the turnover and productivity of the above- and belowground biomass, to assess respiratory and other losses of carbon at the community level, and to evaluate the utilization of the annual moisture resource by these communities.

Results of this study do not support most of the hypotheses posed and suggest that caution is warranted in generalizing about the ecologic significance of C4 photosynthesis in temperate environments.


Study Area

This study was conducted in Curlew Valley of nor thwestern U t a h (41o52 , N, 113o5 , W, 1350 m elev.) in a b road lacustr ine valley occupied by the nor the rn a rm of Lake Bonnevil le dur ing the Pleistocene epoch. Soils are generally homo- geneous and texture varies only from silt loam to sandy loam through the upper 2 m of the profile. In the areas where Atriplex confertifolia and Ceratoides lanata occur, either in mixed or monospecif ic stands, soils are ha lomorphic , and up to 35 bars osmotic potent ia l have been demons t ra ted in these soils unde r field condi t ions (Moore and Caldwell, 1972). Thus, the soil salinity accen- tuates the aridity of this site. Chemical and physical characteristics of soils of these sites are described by Gates et al. (1956) and Mitchell et al. (1966). They concluded that soil profiles under the Atriplex and Ceratoides stands, as well as those unde r stands where these species occur together, were essentially identical.

The salient features of the climate of this area are summar ized in Figure 1. The mean annua l t empera ture is decidedly cool, i.e., 7.1~ yet dur ing summer mon ths average daily m a x i m u m temperatures are high (32~ The progression of soil mois ture con ten t at several depths in the profile, a long with precipi ta t ion from March to October, is depicted for 1970 in Figure 2. Precipi ta t ion dur ing 1970 was only 9% greater than the long- term average.

Methods

Plant Gas Exchange

Net photosynthesis, transpiration, and dark respiration were measured in the field from April through early October, 1970, using a modified Siemens Co. gas exchange system (Koch et al., 1971; Moore, 1971; White, 1976). For logistic reasons measurements were taken where Atriplex confertifolia and Ceratoides lanata occur in a mixed stand. During this 7-month period, measurements were taken on 45 Atriplex and 35 Ceratoides plants in situ. Individual plants were selected using a completely randomized design. These studies included both a series of plant gas exchange measurements when the cuvenes were programmed to track ambient environmental conditions and a measurement series in which a single environmental factor was varied with other factors held constant. For example, to determine the temperature dependency of photosynthesis, irradiance was held constant using four 300-W Sylvania 'Cool Beam' lamps while the cuvette temperature was altered. Or, to assess the light dependency of net photosynthesis, the cuvettes were held at constant temperature while plants responded to the normal daily course of solar irradiance.

Carbon dioxide concentrations were determined by infrared gas analysis (Beckman Co.) and water vapor concentrations by lithium chloride hygrometry (Siemens Co.). Leaf temperatures were measured with fine wire thermocouples. Plant water potential was assessed with a Scholander pressure bomb (Waring and Cleary, 1967), and plant phenologic status was evaluated in a scheme similar to that of West and Wein (1971). Irradiance was measured with an Eppley pyranometer.

Leaf areas were determined with a photoelectric planimeter (Caldwell and Moore, 1971). As part of the calibration procedure the absolute accuracy of the gas exchange system was determined by periodically simulating photosynthesis and transpiration in an empty plant chamber using the integrated technique of Tranquillini and Caldwell (1972).

In addition to the nearly continuous series of gas exchange measurements during the 7-month period of 1970, photosynthetic rates were also determined in other years using a 14COg-labeling system (Tieszen et al., 1974). This was particularly helpful in determining photosynthetic capacity

Carbon Balance and Water Use of C3 and C 4 Shrubs 279

41.1 32.3

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Snowville (1581 m)

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Pig. 1. Climate diagram compiled from U.S. Weather Bureau data at Snowville, Utah, 36 km to the northeast of the study site, using the format of Walter and Lieth (1960). The abscissa represents the 12 mon ths of the year beginning in January. The blackened bar along the abscissa indicates mon ths of the year when the mean daily m in imum is below 0~ and the hatched bar indicates months with absolute minima below 0~ The number below the center of the abscissa indicates the mean durat ion of the frost-free period in days. One division on the ordinate represents either 10~ or 20 m m precipitation. Numbers to the left of the ordinate beginning at the top represent the highest temperature recorded at this site, the mean daily max imum temperature of the warmest month, mean daily temperature variation, mean daily min imum temperature of the coldest month, and the lowest temperature recorded at this site. At the top of the diagram the name of the station and elevation in meters, the mean annual temperature and precipitation are indicated from left to right with the number of years of observations at this site in brackets below the station name

Fig. 2. Soil moisture content determined gravimetrically for several depths in the soil profile beneath a mixed communi ty of Atriplex confertifolia and Ceratoides lanata for 1970. Vertical bars in the top frame represent individual precipitation events. F rom Moore and Caldwell (1972)

during the March and early April period since this was not included in the 1970 field gas exchange measurements .

To determine seasonal gas exchange of these shrubs, an interpolative model was designed. The model of net photosynthesis operates on a 1-h time step and assumes a basic hyperbolic function

2C P=Pmax['C/(I/~ma• 1] (1)

where I is solar irradiance, /max is max i mum irradiance for a particular time of the year, Pmax is the max imum photosynthet ic rate as measured in the field at a particular phenologic stage for prevailing water stress conditions, and C is a term expressing relative photosynthetic capacity at a particular temperature for a given phenologic stage. This relative capacity term, C, was derived from the measurement series involving the response of plant photosynthesis in which irradiance was held constant and temperature was varied independently of other environmental factors. Such measurements were taken for both species at several times during each major phenologic stage. From these data a series of quadratic polynomial equations was derived using least squares techniques to derive C.

The models for both species were then validated using the independent data set where net photosynthesis of these two species was measured under field conditions with the gas cuvette systems set to track ambient environmental conditions. Despite appreciable plant-to-plant variation


in the populat ion of these two species, these models predicted seasonal rates within 10% of actual measurements in the independent data set validation.

Dark respiration was evaluated with a similar model, but of the form

R = a . exp br (2)

where T is leaf temperature, R is dark respiration rate, and a and b are coefficients appropriate for each major phenologic stage for both species. These relationships were derived by least squares analysis f rom the measurement series in which dark respiration was determined at predetermined temperatures and subsequently validated against the other measurement series where dark respiration was measured with the system tracking ambient conditions. Transpirat ion rates were predicted by multiplying modelled photosynthetic rates by photosynthesis/ transpirat ion ratios appropriate to each phenologic stage and period during the year. These PIT ratios were measured in 1970.

The models were run on a 1-h time step basis, using air temperature and solar radiation data from a nearby Desert Biome site in Curlew Valley. Air temperatures were related to leaf temperatures by a series of polynomial equations for different periods of the year. Since it was only feasible to make detailed measurements of gas exchange in these species in the field over the entire season for a single year, the Pmax values for other years were based on water stress conditions, phenologic progression for these species during these years, and photosynthetic capacity data from the 14CO2 uptake technique. Leaf diffusive resistances for water vapor were determined using the basic formula of Gaastra (1959) in which the driving gradient for transpiration is taken as the difference in vapor concentration between saturated vapor pressure at leaf temperature and ambient vapor pressure. This gradient is then divided by the transpiration rate per unit leaf area. The leaf resistance technically includes both a boundary layer resistance and a stomatal diffusion resistance term. However, for these microphyllons shrubs the former term is a very minor component .

Community Biomass

To test hypotheses concerned with production and performance of complete stands of these species, nearly monospecific communit ies were selected for evaluation of biomass, communi ty structure, and turnover.

Biomass of shoots was determined by harvest f rom a series of 16 randomly selected plots in the Atriplex communi ty (4.8 m 2) and 12 plots in the Ceratoides communi ty (1.2 m2). The greater number of plots and the larger plot size for the Atriplex-dominated stand was necessary because of a more unevenly distributed communi ty and the larger average size of Atriplex plants. Plot numbers were increased until the coefficient of variation was decreased to 15%. Standard errors ranged between 2 and 7% of the mean. Current year 's growth was separated from the remainder of the shoot material, and in some samplings all of the shoot material from these plots was completely separated into leaf and stem material for both current year 's and previous years' growth.

Tap roots, which constituted a small proportion of the belowground root system, were harvested individually f rom each of the plots from which shoot biomass was collected. The extensive lateral root system was harvested by a series of random soil cores using an 8.3 cm-diameter soil auger at depths of 5-30, 30-50, and 50-70 cm. Complete separation of roots f rom the soil was achieved by a flotation process using saturated NaC1 solution to maximize buoyancy of root materials. The material was then passed through a sieve with a 0.03-mm pore size (Fernandez, 1974).

Community Structure

To extend determinations of plant gas exchange rates measured on individual plants or plant branches to a communi ty area basis, the seasonal progression of foliage biomass in these communit ies is a necessary parameter. The amount of foliage varies during the season and differs for years of contrasting moisture and growth conditions. Therefore, biweekly foliage/total aboveground biomass ratios were determined for both species during a dry (1974) and a reasonably moist (1975) year. These foliage/biomass ratios were determined for three basic size classes of shrubs for each species.

Carbon Balance and Water Use of C a and C 4 Shrubs 281

To determine the proportional contribution of biomass in each communi ty for each of the three size classes of shrubs, line intercept transects were utilized. Fifteen 30-m transects in the Atriplex stand and ten 30-m transects in the Ceratoides communit ies were employed. Along these transects, individual plants were counted and plant canopy projections in the four cardinal directions were determined. These relative volume estimates for individual plants were related to biomass by an extensive series of individually harvested plants. Since foliage/biomass ratios vary with the size class of the shrubs, this method of weighting the proport ionate contribution of foliage for each size class group was utilized. The resulting values of foliage biomass per ground area could be referenced against the occasional total biomass inventories mentioned previously.

Carbon Content

The percentage carbon of all plant materials was determined by use of a carbon train that combusts materials at 800~ Oven-dried plant materials were finely ground and combusted in the furnace of the carbon train in a s t ream of oxygen. The exhaust of the furnace was passed through a saturated solution of Ag2SO4 to remove halogens, through silica gel to remove water vapor, and finally through N a O H in asbestos (Ascarite, 8-20 mesh, Ar thur Thomas Co,) to absorb CO2. The Ascarite was weighed before and after the combust ion to determine the mass of absorbed COz.

Soil Respiration

Field measurements of CO2 efflux from the soil surface were conducted in these communit ies using the classical ' inverted pail ' technique. Galvanized steel cans were placed on the soil surface with the walls of the can penetrating the soil to a depth of approximately 5 cm. These were insulated and covered by a waxed cardboard cover. These were located both directly under shrub canopies and in the shrub interspaces. Carbon dioxide was absorbed within these pails using 50 ml of 0.5 N N a O H ; the N a O H was titrated before and after each 10-day collection period. Dur ing each collection period, CO2 efflux from layers of sterilized soil was also determined in the field. This served as a control to determine the approximate amoun t of COz diffusion that might take place laterally within the soil profile and also any abiotic release of CO2 into these soils. The resulting correction applied to the CO2 efflux values was always less than 10%. Soil and air temperature were recorded within the collection vessels at the beginning and end of each period to compare with conditions outside the vessel. Heating of the soil surface underneath the collection vessel relative to adjacent soil surface areas was noticeable only during the warmest part of the summer in July and August , in which case soil surface temperatures were elevated only 1 to 2 ~ above those in the ambient environment. At depths of 1 cm, temperatures were the same in all cases. The location of the collection vessels was changed in the communi ty with each collection period.

Plant Litter Production

Data on shoot litter drop from individual plants of these species were derived from West and Fareed (1973) and West and Gunn (1974). This included the monthly drop of litter from 10 individual plants of each species over a 2-year period. This litter was collected in net traps located beneath each shrub and separated into categories of principal plant organs. Litter deposition was related to biomass of these shrubs, which was, in turn, related to a ground area basis using the biomass data for these communit ies described above.

Shoot Production

Shoot production was determined by biomass harvests in late July or early August when new shoot growth for the season was completed. Foliage drop of current year 's leaves during the


summer period preceding the biomass harvest was used to correct these production figures. This correction, however, was usually relatively small, ranging between 2 and 9% for annual shoot production.

Belowground Productivity

Belowground production was determined using the 14C/~2C dilution technique of Caldwell and Camp (1974). To assess the annual fractional turnover of the belowground biomass, this technique involves labeling a plot of vegetation with t4CO2 early in the season, followed by extraction of root system samples within 7 days using a soil auger and a determination of the relative ~*C/~zc ratio in cellulose tissues of the root system. The same assay is conducted in the same plot at the end of the growing season. A turnover coefficient is calculated based on the dilution of this 14C/~2C ratio over the season. This turnover coefficient is the fractional portion of the total root biomass that is produced during this growing season. Root system production is the product of the turnover coefficient and the belowground biomass measured early in the season. This technique has the advantage of eliminating the necessity of determining the proportion of dead and living roots, which is extremely difficult in these shrub communities where most of the root material is in the form of fine lateral root elements. It is also independent of death and decay of old root elements during the growing season.

Soil Water Extraction

Soil moisture content was determined by neutron probe at several depths in the soil profile using 10 access tubes installed in both communities since 1967 (Gast6, 1969). Soil moisture extraction during the growing season was determined at each depth interval by subtraction over each sampling period, which was usually 10 to 14 days. Since the neutron probe technique is not effective above 15 cm, it was necessary to make assumptions concerning the availability of moisture in the upper 15 cm of the profile for extraction by the root system. Half of the soil water in the upper 15 cm was considered available for extraction. This comprised the largest unknown factor in this soil moisture extraction estimation.

Results

Gas Exchange Activity

Photosynthesis

T h e da i ly p r o g r e s s i o n o f ne t p h o t o s y n t h e s i s in cuve t t e s p r o g r a m m e d to t r ack

a m b i e n t e n v i r o n m e n t a l c o n d i t i o n s is s h o w n for severa l days d u r i n g the 1970

season fo r b o t h species (Fig. 3). C o m p a r a b l e , essen t ia l ly c loud less days were se lec ted fo r each m o n t h d e p i c t e d in this F igu re . In a d d i t i o n to the ac tua l m e a s -

u r e d ra tes o f p h o t o s y n t h e s i s , va lues p r e d i c t e d by the p h o t o s y n t h e t i c m o d e l s

a re a lso s h o w n in this F igure . T h e h igh ra tes o f ne t p h o t o s y n t h e s i s a n t i c i p a t e d

fo r the C4 species, Atriplex confertifolia, were n e v e r f o u n d in this s tudy. T h e m a x i m u m p h o t o s y n t h e t i c ac t iv i ty for b o t h species was in the spr ing p e r i o d

o f A p r i l a n d M a y w h e n soil m o i s t u r e was m o s t p len t i fu l a n d w h e n m o s t o f the leaves on the p lan t s were y o u n g . U n d e r the m o s t f a v o r a b l e c o n d i t i o n s

fo r b o t h species in t he field, Ceratoides lanata of t en e x h i b i t e d h i g h e r p h o t o s y n - the t i c ra tes t h a n d id Atriplex. T h e h ighes t p h o t o s y n t h e t i c ra tes o b s e r v e d in

Carbon Balance and Water Use of Ca and C4 Shrubs 283

APRI L MAY JULY AUGUST 15 Atriplex

�9 _ - - -

.~ ~= "~l ~1'5 : [ ~ , 1 / . . , ] ~ ' , / ,-'.,(30/4,, ' " ,, ,, / ' ~ / ~ t ' (29/5> , Cereloides (0'/7) I (07/8 >

0 / . . . . . 8 12 16 8 12 16 B 12 16 8 (2 16 TIME OF DAY

OCTOBER ...~.... (03/lO)l

8 12 16 Fig. 3. Daily progression of net photosynthesis measured in the gas exchange cuvettes tracking ambient environmental conditions during several dates during 1970 (solid lines). Comparabfe, nearly cloudless days were selected to represent photosynthetic activity for these 5 months. Exact dates are given in parenthesis in each frame. Predicted net photosynthetic rates based on the gas exchange model are also shown (dashed lines)

the field were 22 and 29 mg dm- 2 h - i (for leaf area of one side of leaf) for Atriplex and Ceratoides, respectively.

Later in the season during the summer months, photosynthetic activity of both species was reduced as soil moisture was depleted, prevailing temperatures increased, and average age of the foliage advanced. Finally, in August, photosynthetic activity of Ceratoides was absent in many individuals sampled, while Atriplex maintained some net photosynthetic capacity, particularly during the morning hours. A low level of photosynthetic activity was observed in both species in late September and early October.

Leaf Diffusion Resistance

The average leaf diffusion resistance during the middle 7 h of the day when plants were most active in photosynthesis is plotted for several days throughout the season for both species in Figure 4. Leaf diffusion resistance predictably increased during the growing season. However, there was no distinction in the average magnitude of this parameter between the two species at any given time of the y e a r - e v e n during the spring when both species were most active in photosynthesis. Thus, the hypothesis that the C4 species should display generally higher leaf diffusion resistances under comparable environmental conditions is certainly not supported in these measurements. In the populations of both species, individuals varied considerably in diffusion resistance later in the season.

Photosynthesis~Transpiration Ratios

The photosynthesis/transpiration ratios, P/T, exhibited by foliage of these two species under field conditions, differed little during the spring when photosyn-


2C

15

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Apr Moy dun dut Aug

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Fig. 4. Seasonal progression of average daily leaf diffusive resistances in 1970. Each point represents the average resistance for the middle 7-h portion of the day when the plants were most active in photosynthesis

Fig. 5. Photosynthesis/transpiration ratios for several days during 1970. Each point represents the average daily value for this ratio

thetic activity was greatest. In Figure 5 each data point represents the average PIT ratio for a day, or a major portion thereof, when the plants were in cuvettes programmed to track ambient environmental conditions. In the spring PIT ratios of both species were high and essentially equivalent. Later in the season, PIT ratios of both species declined. However, the decline was much more abrupt for Ceratoides. Thus, during the later part of the growing season the C4 plant did exhibit higher P/T ratios.

Carbon Balance and Water Use of the Communities

To evaluate hypotheses concerned with the performance of these species on a community basis it was necessary to determine the principal components of the carbon balance and water use for these communities. This analysis is based on the 2-year period of 1973 to 1974, which included a wet and a dry year. The annual precipitation effective in recharging the soil profile during the winter months and in providing moisture for the subsequent growing season is most meaningfully tabulated on the basis of a water year beginning October 1. For the period October, 1972, to September, 1974, corresponding to the 1973 and 1974 seasons, a year of above-average precipitation was experienced during the first 12-month period (132% of normal) followed by a year of below-normal precipitation (80% of normal), and the 24-month period was within 6% of a 28-year average for this area (see Fig. 1).

Carbon Balance and Water Use of C3 and C~ Shrubs 285

Table 1. Biomass and standing carbon pools for the Atriplex confertifolia- and Ceratoides lanata- dominated communities. These values are averages for 1973 and 1974. Standard errors within years ranged between 2 and 7% of the mean values

Plant component Atriplex Ceratoides

Biomass Carbon p o o l B iomass Carbon pool (g m- 2) (gm 2) (g m- 2) (g m- 2)

Current year's shoot growth: Foliage 99 32 70 30 Stems 23 9 8 3

Previous year's shoot growth 339 161 203 100

Total shoot system 461 202 281 133

Tap roots 68 29 78 37

Lateral root system 5-30 cm depth 923 339 640 271

30-50 cm depth 510 191 602 272 50-70 cm depth 385 131 581 241

Total root system 1886 690 1901 821

Total 2347 892 2182 954

Community Biomass

Assessment of biomass is an integral component of an analysis of community productivity and carbon balance. The 2-year average standing crop for 1973 and 1974 is represented both in terms of biomass and standing carbon pools on a ground area basis in Table 1. These are based on late July harvests during both years after the current year's shoot growth was completed. A large proportion of the total biomass is below ground in both communities and is composed primarily of the profuse lateral root system. The differences in aboveground biomass between the two communities reflect the somewhat different growth forms of these two species. Ceratoides is a smaller plant maintaining less perennial shoot biomass above the crown, while Atriplex is a somewhat larger shrub with much more persistent woody shoot tissue.

Because of the technical difficulties in accurately assessing living and dead tissues in the biomass on a large scale-part icular ly for the belowground sys- t e m - t h e s e biomass and standing carbon pool values include both living and dead materials. Thus, it is unwise to attribute particular significance to the apparent differences between the two communities in terms of total betowground biomass or standing root/shoot ratios in these systems. For example, the previous years' woody shoot growth of Atriplex confertifolia contains a substantial amount of secondary xylem tissue that is not living. This, combined with the unknown proportion of dead root elements in the belowground system, would warrant caution in drawing meaningful conclusions concerning the apparently smaller root/shoot ratio of the Atriplex community. The foliage displayed per


ground area in the Atriplex community is, however, clearly greater than in the Ceratoides-dominated community, and this parameter is relatively free of errors since dead foliage is rarely retained on these shrubs for significant periods of time.

Community Gas Exchange

The annual course of carbon fixation by photosynthesis, carbon loss in shoot respiration during nighttime periods, and water loss through transpiration on a ground area basis in these two communities are depicted for 1973 and 1974 in Figure 6. These are derived from the gas exchange models and the determinations of foliage per unit ground area, which were based on the biweekly foliage/ biomass ratios, community biomass measurements, and the community structure analysis described earlier.

The total average values of annual carbon fixation by community photosynthesis and carbon loss in dark respiration from Figure 6 are included in the community carbon balance representations of Figure 7. In this carbon balance all flux values are represented as g carbon m-2 yr-1 and none of the standing carbon pool values are contained in Figure 7 since they are presented in Table 1. The average annual carbon fixation was 240 and 223 g C m -2 yr 1 for the Atriplex and Ceratoides communities, respectively. Mean annual water loss in transpiration for this 2-year period (Fig. 6) was 11.7 and 12.3 cm for the Atriplex and Ceratoides communities. Based on these values of community photosynthesis and transpiration over this 2-year period, there is little indication that the Atriplex community either fixes significantly more carbon or transpires much less water in the course of this carbon fixation than the Ceratoides community.

Productivity

Productivity in the carbon balance of Figure 7 is represented as carbon actually incorporated into new plant parts. In established perennial communities, productivity of both the above- and belowground systems is a function of the fractional turnover, i.e., the proportion of the standing biomass pools that is renewed each year. The fractional turnover values are represented for these communities for 1973 and 1974 in Table 2. The aboveground turnover is based on harvests of the current year's shoot growth with corrections applied for foliage of the current year deposited as litter during the growing season of that year. The belowground turnover is based on the 14C/12C dilution technique described earlier. These estimates of fractional turnover of the belowground system are independent of the proportion of living and dead root tissues, and new shoot harvests were composed entirely of living materials. The average annual fractional turnover of the shoot system for these 2 years was about the same in the two communities, although it differed much less between the wet and dry years in the Ceratoides community than in the Atriplex community. Turnover

Carbon Balance and Water Use of C3 and C4 Shrubs 287

1973 ATRIPLEX 1974

5

g 4

L~ 5

~ 0

g ~ 0 . . . . . . . . . . . . . . . I~ Mor Apt Moy Jun Oul Aug Sep Oct Mot Apt Moy Jun dul Aug Sep Oct

5

-8 4

iE ~ 5

~g '$' 2"

g l

~ 0

1975 CERATOIDES 1974

L

%1 :lz

# ~ o , , , ,-<'-"~ . . . . . . . , - - ' r - -

Mar Apt Moy'dun'dul Aug Sep Oct Mar Apt May dun dul Aug Sep Oct

Fig. 6. Seasonal progression of photosynthetic carbon fixation, dark respiration, and transpiration perm 2 ground area for 1973 and 1974 for the Atriplex and Ceratoides communities. Gas exchange rates per foliage mass were derived from the model operating on the meteorologic data for these 2 years. The seasonal progression of foliage mass per ground area in the two communities was derived from biweekly foliage/biomass ratio determinations, community biomass assessments, and other information on community structure

Table2. Fractional turnover of shoot and root systems of Atriplex conJertifolia- and Ceratoides lanata-dominated communities

Community Shoot system Root system

1973 1974 1973 1973 1974 Tap roots Lateral roots Lateral roots

Atriplex 0 .32+a 2 0.001 0.21 • 0.001 0. I2_+G 2 0.02 0.24_+~ 2 0.09 0.23__a 2 0.02 Ceratoides 0.27_+cr 2 0.001 0.28+cr 2 0.001 0.02_+cr 2 0.02 0.12_+a / 0.09 0.15+~r 2 0.02


Fig. 7. Carbon balance of the Atriplex and Ceratoides communities for the 2-year period of 1973 and 1974. All values designate annual carbon flux rates (g C m -2 yr-1). Carbon fixation by photosynthesis and loss in shoot respiration are taken from the total annual fluxes in Figure 6 and carbon efflux from the soil surface is derived from Figure 8. Carbon incorporated into new shoot growth, tap roots, and annual turnover of the lateral root system is derived from the fractional turnover rates for these 2 years (Table 2) and the standing carbon pools in these components for each year. Carbon flux in shoot litter drop is taken from West and Fareed (1973) and West and Gunn (1974)

of the lateral root system was reasonably consistent between years and markedly greater in the Atriplex community. Thus, Atriplex appeared to be making a larger carbon investment than Ceratoides in renewing root elements each year. These differences in turnover rates are reflected in the components of the carbon balance (Fig. 7) where carbon incorporated into new shoots, tap roots, and annual turnover of the lateral root system is derived as the product of the fractional turnover and the standing carbon pools for these 2 years. Atriplex apparently incorporated a greater proportion of the annual photosynthetic carbon fixation into plant tissues both above and below ground than did Ceratoides. Thus, productivity and water use efficiency for actual plant growth were appar-


Fig. 7

ently somewhat greater in the Atriplex community. However, as will be discussed later, this greater productivity is probably not a function of C4 photosynthesis, but may reflect other properties of these two species.

Other Components of the Carbon Balance

Carbon flux in the form of litter from shoots has been taken from data of 1972 and 1973 (West and Fareed, 1973; West and Gunn, 1974), which also represents a 2-year period composed of a wet and dry year.

Because of the apparently large annual investment of carbon in root system turnover in both communities, another index of carbon deployment to the belowground system was sought. For a plant-soil system in complete equilibrium, soil respiration measured as CO2 efflux from the soil surface should provide an estimate of the total carbon committed to the belowground system by primary producers in the form of root respiration, production of new root material, as well as the annual increment of shoot litter that eventually becomes incorporated into the soil in the absence of herbivory. Although it is unlikely that


3.C

2.G

1.0

x

3o!

8 2.0

1.0

Atriplex /i

t~

S 77;7 Cerotoides "~ A

d F M A M O d A S O N MONTH

Fig. 8. Seasonal progression of CO 2 efflux from the soil surface in the Atriplex and Ceratoides communities during 1974. The values for the collections beneath shrub canopies and in the canopy interspace are represented separately

these communities are in complete carbon equilibrium, as will be discussed later, CO 2 efflux from the soil surface was assessed as a conservative approxima- tion of carbon commitment to the belowground system. The seasonal course of CO2 efflux from the soil surface is shown in Figure 8 for the two communities. Though efflux from both sites exhibited variations during the season largely due to periods of differing soil surface temperature and moisture conditions, there were essentially no differences in CO 2 efflux measured directly beneath shrub canopies or in the interspace between shrubs, and there was a very low coefficient of variation among replicate samples (usually less than 5% of the mean values). There was no significant difference in the annual soil respiration between communities nor between years when measured over a 4-year period from 1973 through 1976. The total annual carbon flux from the soil surface is included in the carbon balance schemes of Figure 7. These quantities corrobo- rate the large belowground productivity determinations.

Independent techniques and data sets have been used to determine the parameters of the carbon balance representations of Figure 7, and none of the quantities has been determined by subtraction. Therefore, the representations have not been forced to a perfect balance.

Water Extraction

Annual transpiration of these communities based on plant gas exchange determinations (Fig. 6) suggests that only about half of the annual precipitation was available for transpiration by the vegetation in these sites. To provide an independent estimate of water transpired in these communities, annual water extraction


Fig. 9. Annual water extraction I.O from the soil profile in the Atriplex .~_ (1) and Ceratoides (e ) communities calculated from water content data '~ |

of 4 years and represented as a fraction of the annual precipitation "~ ,0 .5 for the water year (October through ~ ._~ September). Annual transpirational o water loss for the 2 years depicted ~ in Figure 6 and represented as a ~

o fraction of the annual precipitation during the water year for the Atriplex (A) and Ceratoides (�9 communities

Ai i

0

i zx' O

]50 l l 200 250 3~3 Precipitation (rnm)

from the profile was calculated from soil moisture content data over 4 years. These values are represented as the ratio of water extraction/annual precipitation for the 4 years in Figure 9. In the same Figure, the ratio of annual transpiration/precipitation based on the values of Figure 6 are presented. Although calculations of water extraction based on moisture content data necessarily involve assumptions about the fate of moisture in the uppermost layer of the profile (see "Methods"), it appears that the proportion of the annual precipitation ultimately transpired by the vegetation is about the same when determined by these independent methods. Only approximately half of the annual precipitation (54%+a0.9%) during the 6years represented is ultimately channeled through the transpiration stream of the vegetation, and the two communities appear to transpire equivalent amounts of water on an annual basis.

Discussion

The physiologic advantages conferred by the C4 photosynthetic pathway in suppressing photorespiratory carbon loss and also effecting higher photosynthesis/transpiration ratios should be of benefit in any environment where solar radiation is plentiful and water is a constraint on production (Bj6rkman, 1975). The occurrence of the C4 pathway in many unrelated families of plants and the prevalence of species with this pathway in tropical environments would attest to the success of this evolutionary elaboration of normal C3 photosynthesis in these environments. In temperate environments, C4 species are also widely represented, and in an evolutionary context, the incursion of the C4 pathway into cooler environments may yet be in process.

Although Atriplex confertifolia has evolved to survive in a cool temperate environment, both in terms of survival at very cold temperatures and photosynthesis at low temperatures, it still possesses the physiologic characteristics of C~ photosynthesis even when photosynthesizing at low temperature (Caldwell et al., 1977). Yet the assumed benefits to be realized from C4 photosynthesis were not evident in this study since most of the hypotheses posed were not supported.


Rates of Carbon Fixation

Photosynthetic rates per unit of foliage material of Atriplex were not superior and, in fact, were lower than the highest rates reported for the C3 species (Fig. 3). In view of the moderately low leaf diffusive resistances exhibited by Atriplex during the period of peak photosynthetic activity (Fig. 4), maximum photosynthetic rates were not particularly high. The maximum observed rate for Atriplex confertifolia (22 mg dm-2 h-1) was only approximately 1/z to 1/4 of leaf photosynthetic rates commonly reported for many agronomic C4 species (Black, 1973). This maximum rate was about half of that reported for Atriplex lentiformis under field conditions at high temperatures in the desert of southern California (Pearcy and Harrison, 1974). These maximum rates of A. confertifolia were comparable with those reported by Pearcy et al. (1974) for A. hymenelytra in Death Valley, California. However, they reported only 2 days of measurements, and leaf diffusive resistances were at least twice as great as minimum values we report for A. confertifolia.

The absence of particularly high photosynthetic rates in A. confertifolia was not due to insufficiently high temperatures at this time of year. During the late spring when A. confertifolia exhibited its highest rates of photosynthesis, the temperature optimum for photosynthesis ranged from 14 to 18~ (White, 1976) and mean daily maximum temperatures at this time of year range between 14 and 21~ Under optimized laboratory conditions using a focused xenon arc lamp to achieve light saturation of photosynthesis, this species has never been found to exhibit higher photosynthetic rates than those measured in the field (Caldwell and Camp, unpublished data). The evolutionary adaptation of A. confertifolia to optimize photosynthetic rates at lower temperatures than is the case for most C4 species may have resulted in a compromise with the maximum rates of photosynthesis that could be achieved. However, another C4 species, Atriplex sabulosa, native to cool oceanic habitats in northern Europe, exhibited rates as high as 49 mg dm -2 h-1 at 20~ leaf temperature under laboratory conditions (Bj6rkman, 1975). The performance of this coastal species under field conditions is, however, not known.

Although there was more foliage displayed per ground area in the Atriplex community (Table 1), carbon fixation per land area was not significantly greater than in the Ceratoides community (Fig. 7).

Seasonal Timing of Photosynthetic Activity

The hypothesis that the C4 species should delay the onset of photosynthetic activity and growth until midsummer when solar irradiation would be most intense and the warmest temperatures normally associated with optimal C4 photosynthesis would be prevalent, is clearly refuted in this particular situation. Although Ceratoides is somewhat more photosynthetically active in the very early spring, the periods of highest photosynthetic rates of these two species were basically coincident. The timing of leaf and shoot development as well as root growth was also very similar in the two species (Fernandez and Caldwell,


1975; West and Fareed, 1973; West and Gunn, 1974). The primary moisture recharge of the soil profile is the result of winter precipitation (see Fig. 2). Therefore, this C4 species may have been forced to evolve the capacity for photosynthesis at low temperatures prevalent during the spring when C3 species are normally active in this environment in order to avail its elf of the period of most abundant and reliable soil moisture supply rather than to attempt to exploit a warmer period of the year to which C4 photosynthesis is normally considered to be better suited.

This early season initiation of growth and photosynthetic activity of Atriplex is in distinct contrast to generalizations of phenologic patterns of C4 grasses in temperate environments. For example, in both the semiarid short-grass prairie and the more mesic tall-grass prairie of the Great Plains of North America, C~ grasses are generally considered to delay growth and development until much later in the growing season when compared to their C3 counterparts, which initiate growth in the early spring (Williams, 1974; Harrison, 1975; Ties- zen, 1970). Furthermore, C4 grasses often tend to be distributed in warmer microhabitats of the prairie (Tieszen, 1970). Although the short-grass prairies may receive about the same annual precipitation as the Great Basin sites of our study, a much greater proportion is received in the summer season. Thus, moisture is likely to be more available for Ca grasses, which delay development and photosynthetic activity until the warmest period of the year.

Although Atriplex initiates leaf growth and photosynthetic activity almost as early in the spring as Ceratoides and also exhibits its highest rates of photosynthesis in the spring, it does prolong photosynthetic activity at a low level much longer in the dry late summer months than Ceratoides (Figs. 3 and 6). This prolonged period of photosynthesis compensates for the somewhat lower photosynthetic rates of A triplex. However, as emphasized earlier, the annual photosynthetic carbon fixation in the two communities is about the same (Fig. 7). The curtailment of photosynthesis and transpiration by Ceratoides in the driest period of late summer is not necessarily a reflection of the inability of this species to extract water. In controlled laboratory experiments, Ceratoides and Atriplex displayed an equivalent capacity to extract water from soils of water potentials down to -80 bars, which is more negative than in the driest conditions yet measured in these field sites (Moore et al., 1972). Although the factors controlling this late summer curtailment of photosynthesis and metabolic activity by Cera- toides are not known, this may be a conservative behavior of considerable survival value. Long-term observations at a similar experimental site in western Utah 350 km south of our site have indicated that Atriplex confertifoIia suffered rather high population mortality during years of severe drought while Cera- toides did not (Hutchings and Stewart, 1953). In an inactive state Ceratoides might be much more resistant to extreme desiccation.

Water Use Efficiency

The photosynthesis/transpiration ratios exhibited by both Atriplex eonfertiJolia and Ceratoides lanata are high when compared with nonagricultural plants


from other arid habitats. Although not often reported in the literature, the most ecologically meaningful parameter is PIT ratios expressed on a daily basis rather than instantaneous values. The ratios exhibited by Atriplex and Ceratoides (Fig. 5) are higher than daily P/T ratios reported for several arid-land species in western Australia (Hellmuth, 1971) and in the Negev Desert of Israel, with the exception of Artemisia herba-alba, which displayed daily ratios equal to those for these two cool desert species (Lange et al., 1969). These high PIT ratios of Atriplex and Ceratoides are undoubtedly attributable in large part to the cool leaf and environmental temperatures prevailing during the spring period when these species are most photosynthetically active.

Contrary to expectations, PIT ratios of Atriplex foliage were not greater than those of Ceratoides during the spring period. Atriplex also did not display greater leaf diffusive resistances, as was anticipated (Fig. 4). The lack of particularly high photosynthetic rates of Atriplex and the failure of this species to restrict stomatal aperture at this time of year are likely reasons for the similarity of the PIT ratios of these two species. Photosynthesis/transpiration ratios of AtripIex were clearly superior to those of Ceratoides in the hot summer season. Yet, since Ceratoides completed a greater proportion of its annual carbon fixation in the spring and early summer than Atriplex, on an annual basis the amount of carbon fixed per ground area relative to the amount of water transpired was about the same in the two communities (Figs. 7 and 9).

Productivity

Although the photosynthetic carbon fixation and water use in the two communities were nearly equivalent, productivity, gauged as carbon incorporated into new plant growth, and thus water use efficiency for plant growth were greater in the Atriplex community. This species was able to incorporate 37% more carbon into above- and belowground productivity over this 2-year period. This difference, however, probably reflects other attributes of these species rather than characteristics specifically linked with the different photosynthetic pathways. There is, for example, some indication that Ceratoides may bear somewhat higher maintenance respiration costs or suffer greater carbon loss in the belowground system.

Respiration associated with biosynthesis of plant tissue is commonly considered to be primarily a function of the amount of carbon incorporated into new plant tissues as theoretical calculations of Penning de Vries et al. (1974) suggest. Using their coefficients, growth respiration associated with shoot production would be 6.1 and 5.0 g C m -2 yr-1 for Atriplex and Ceratoides, respectively. If the remainder of shoot respiration is considered as maintenance respiration, these values would be 15 and 12 g C m -2 yr -a for the Atriplex and Ceratoides communities. Since the current year's shoot material constitutes all the foliage and the most metabolically active stem tissues on the plant, maintenance respiration would be primarily associated with current year's shoot growth. The ratio of maintenance respiration to carbon incorporated into current year's shoot growth is essentially the same for the two communities, suggesting they


have similar basic rates of maintenance respiration for the shoots. However, in the belowground system either maintenance respiration or other forms of carbon loss appear substantially greater in the Ceratoides community. This is based on the difference between CO2 efflux from the soil surface and carbon incorporated into belowground production.

If these plant-soil systems were in complete carbon equilibrium, the annual CO2 efflux from the soil surface should represent the summation of root maintenance respiration, growth respiration associated with new root production, CO2 released from the decomposition of a cohort of dead root elements equal to the quantity of new root production, and CO2 released from the decomposition of the equivalent of an annual deposition of shoot litter. It is unlikely that these communities are in complete carbon equilibrium. This area has a long grazing history. Though grazing by domestic animals had been excluded for 6 years prior to these studies, there may yet be a very slow accumulation of biomass in both above- and belowground components of these communities. Furthermore, these soils are reasonably young, having only been exposed from the receding Great Salt Lake for a period of approximately 7000 years (Eardley et al., 1957) and are probably accreting soil humus carbon. Nevertheless, these systems may not be far from equilibrium since the sum of carbon efflux from the soil surface and shoot respiration equal about 90% of the photosynthetic carbon fixation in both communities.

The carbon efflux from the soil was about the same for the two communities (Fig. 7) and remained constant over a 4-year period. The differences between this soil carbon efflux and carbon incorporated into root production is much greater for the Ceratoides community (Fig. 7). Some of the soil carbon efflux would be due to growth respiration, but this should be greater in the Atriplex community because of the larger root production term. [Based on coefficients of Penning de Vries et al. (1974), belowground growth respiration would be 21 and 15 g C m -2 yr-1 for Atriplex and Ceratoides, respectively.] Therefore, assuming basic decomposition rates to be equivalent in the two communities, the greater differential between soil CO2 efflux and belowground productivity in the Ceratoides community may reflect greater maintenance respiration rates of the root system or other forms of carbon loss such as that due to decomposition of carbon exudates. Sizable differences in maintenance respiration rates among species are common (Penning de Vries, 1975; McCree, 1974). If Cera- toides does have larger belowground maintenance respiration rates, this could be associated with factors such as the behavior of this species with regard to salt. In these saline soils Ceratoides apparently restricts the uptake of salt at the roots, while Atriplex allows salts to flow through the plant, and subsequently the salts are secreted through bladder hairs on the leaves (Breckle, 1974). Ceratoides may incur greater metabolic costs in salt exclusion by root membranes.

Other Components of the Carbon Balance

By encompassing a 2-year period, including years of both comparatively wet and dry conditions, it is anticipated that the major components of the carbon


balance included in Figure 7 are reasonably representative. Nevertheless, it is not surprising that shoot litter production is not exactly equivalent to annual new growth of shoots during this 2-year period. The litter data were taken from the 2-year period of 1972 to 1973, while the remainder of the information in this balance scheme is derived for 1973 and 1974. Furthermore, it is likely that the deposition of stem litter may be episodic in nature and would likely not be in equilibrium with shoot production over a 2-year period, particularly for Atriplex whose large woody stems may stand for years. For example, a heavy fall of stem material has been occasionally witnessed following intense wind or thunderstorms.

Though all of the major components of the carbon balance in these communities have been separately determined, and are represented in Figure 7, there are facets that have not been measured. For example, the carbon invested in radial stem increments of previous year's growth, which would be more important for Atriplex, has not been measured; nor have the winter respiratory costs in either community been determined. Another unknown factor is herbivory of aboveground material by insects and hares. The herbivory of belowground material would necessarily be included in the belowground fractional turnover term as it is measured by the techniques employed in this study. Although none of these components has been measured, all are likely to be of rather minor importance in view of the magnitude of the major components represented in Figure 7.

Belowground Carbon Costs

Both species displayed a heavy commitment of energy to the belowground system. Over this 2-year period the ratio of belowground to aboveground production was in excess of 3 for both communities. Although it was not possible to measure root respiration independently, the carbon costs of root system maintenance are likely large when compared to the shoot system. The hypothesis that the C4 species might be able to devote less of its carbon resource to the belowground system because of greater water use efficiency in gas exchange was not supported in this study. In fact, the fractional turnover of the belowground system was consistently higher over this 2-year period than for the Ceratoides community (Table 2). The reasons for the apparent continual reexplo- ration of the same soil profile by established perennial root systems is not clear. On theoretical grounds it may be argued that this is necessary for water uptake, particularly in dry soils (Caldwell, 1976), or it may be essential for nutrient uptake. Nevertheless, the costs appear to be very high. It is appropriate to mention, however, that a significant commitment of carbon to the belowground system is not unique to these communities. Comparatively large values of fractional turnover and productivity have also been recently reported for the belowground system in an arctic tundra (Shaver and Billings, 1975), a short-grass prairie (Coleman, 1976), and a deciduous forest (Harris and Cole- man, personal communication).


Utilization of the Moisture Resource

Although precipitation during the 7-month period from October through April constitutes on the average only 60% of the annual precipitation, this moisture is most effective in recharging the soil profile. As indicated in Figure 2 for 1970, a year when summer precipitation was about 20% above long-term average, rainfall during these warm months did not have a noticeable effect in supplying moisture to the soil profile except for the immediate surface zone. Based on the independent assessments of soil moisture extraction and transpiration of the vegetation in these two communities (Fig. 9), it would appear that approximately only half of the annual precipitation is effectively utilized by the vegetation of these communities. There is essentially no overland flow in this nearly level basin nor loss of moisture to ground water or subsurface flow. If the system is in hydrologic balance, moisture not transpired would necessarily be lost either directly from the snowpack during the winter months or from soil surface evaporation. The evaporation component is not often parti- tioned from evapotranspiration in hydrologic studies. However, in areas of rather low vegetal cover of the soil surface, an appreciable evaporation term might be expected. For example, Tanner and Jury (1976) recently reported soil surface evaporation of a potato field to be roughly half of the total evapotranspiration in the early growing season during two years in which the soil was intermittently wetted due to rainfall or irrigation. Certainly, the potential for an appreciable evaporation component exists in these shrub communities.

Sublimation losses from the snowpack are also a potential loss. During the cold months of the year most of the precipitation is in the form of snow, and the soil surface is frozen for a period of several months. Before both the snowpack and the soil surface thaw allowing moisture to infiltrate into the profile, the potential for direct evaporation from the snow would exist. During a 3-month winter period in the Sierra Nevada of California, snowpack evaporation losses on the order of 30 mm have been reported (West, 1959). Though likely not as important as soil surface evaporation, this is still a loss of potential consequence in this cold-winter desert shrubland.

In the absence of disturbance in these communities, the interspaces between shrubs in either of these communities are bare of other higher plant vegetation. Although rooting densities are not as great in the interspaces, particularly near the soil surface, most of the profile in these communities is thoroughly permeated by roots of these shrubs (Fig. 10). The soil surface moisture is apparently not effectively exploited by these shrubs, particularly during the warm summer months when root growth in the upper part of the profile ceases (Fernandez and Caldwell, 1975). Even the somewhat prolonged period of photosynthesis and transpiration of the C4 species, Atriplex, during the warmest and driest part of the summer (Figs. 3 and 6) is associated with prolonged root growth activity deep in the profile rather than root growth near the soil surface (Fernan- dez and Caldwell, 1975). Though an average of 40% of the annual precipitation is received between May and September, this moisture is not only less effective in recharging the soil profile, but is much less reliable. Over a 28-year period the coefficient of variation for precipitation at this time of year is 40%, while


Depth (cm)-

0 - 1 5

15-50

50 -45

Relative Biomass 25 5 0 7 5 IO0

i t i

I

I

I !~IH| Fig. 10. Relative distribution of lateral root biomass beneath the shrub canopies (open bars) and in the shrub interspaces (shaded bars) for the upper portion of the soil profile in the Atriplex communi ty

the coefficient of variation is only 23% for precipitation of the remainder of the year. Although these shrubs appear to utilize only about half of the annual precipitation, there does not appear to be an available niche for even ephemeral higher plant vegetation in these communities if undisturbed. Yet, when disturbed, e.g., by heavy grazing, annual vegetation quickly invades the shrub interspaces. In any case, both of the shrub communities seem to be exploiting the annual moisture resource to about the same extent.

Conclusions

Though employing different photosynthetic pathways, both species appear equally competent when success is gauged by parameters such as photosynthetic carbon gain by the community, water use efficiency for photosynthesis, and utilization of the annual moisture resource. Both species have a sizable energy commitment to the belowground system. The maintenance of somewhat greater foliage per ground area and greater productivity in the Atriplex community probably involves aspects of the physiology of these two species unrelated to photosynthetic pathways, such as maintenance respiration. Ceratoides lanata, however, does not appear to be competitively inferior because of this lesser amount of biomass production. In fact, long-term observations in western Utah suggest that in the absence of grazing, the percentage cover of Ceratoides lanata slowly increased over a 40-year period while that of Atriplex confertifolia decreased in communities similar to those we have studied (Holmgren and Hutch- ings, 1972).

Acknowledgements. This research was supported by the U.S. IBP Desert Biome (National Science Found. Grant No. G.B.32139) and the Utah Agricultural Experiment Station. We gratefully ac- knowledge these individuals for their contributions to this work: R.S. Hol thausen for soil moisture extraction calculations and thoughtfull discussions of the manuscript , O.A. Fernandez for contributions to techniques and data collection, H.L. Neuber for drafting and laboratory assistance, and K.A. Marshall for computer programming services. This is Journal paper no. 2193 of the Utah Agricultural Experiment Station.

Carbon Balance and Water Use of C3 and C~ Shrubs 299

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Received April 1, 1977

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Carbon balance, productivity, and water use of cold-winter ... et al 1977.pdf · Leaf areas were determined with a photoelectric planimeter (Caldwell and Moore, 1971). As part of