diurnal and seasonal variations in gas exchange and water relations of lowland and upland black...

Diurnal and seasonal variations in gas exchange and water relations of lowland and upland black spruce ecotypes

Abdenbi Zine El Abidine, James D. Stewart, Pierre Y. Bernier, and Andre P. Plamondon

Abstract: Gas exchange and water relations were measured on seedlings from two pairs of upland and lowland black spruce (Picea mariana (Mill.) BSP) populations. The seedlings were planted under natural atmospheric conditions in exterior sand beds. Measurements were carried out on eight separate days during the summer of 1992. Diurnal and seasonal responses of gas exchange and water relations parameters to natural changes in environmental factors were analyzed for possible ecotypic differences. Differences were found among the four populations and within one of the two upland-lowland pairs. However, no differences could be linked significantly to an upland-lowland ecotypic differentiation. The physiological responses are discussed with respect to diurnal and seasonal changes in environmental factors and to similarities with results from an earlier experiment involving mature trees from the same four populations.

Key words: Picea mnariuna, water stress, net photosynthesis, stomata1 conductance.

R&sum& : Nous avons mesurt les tchanges gazeux et les relations hydriques de semis d'Cpinette noire (Picea mariana (Mill.) BSP) de deux paires de populations issues de milieux contrastants (sec et humide). Les semis Ctaient plantts sous des conditions atmosphtriques naturelles dans des lits de sable. Nous avons effectuC les mesures pendant huit jours repartis au cours de I'ttC 1992. Les responses diurnes et saisonnikres des Cchanges gazeux et des relations hydriques aux variations des facteurs environnementaux ont CtC analysCes pour dCceler la prCsence de differences Ccotypiques. Nous avons trouvC certaines diffkrences entre les quatre populations, et entre les populations des milieux contrastant dans une des deux paires. Cependant, nous n'avons observC aucune difference significative attribuable une diffkrentiation Ccotypique. Le texte prCsente une analyse des rCponses physiologiques en fonction des variations journalikres et saisonnikres des facteurs environnementaux, ainsi qu'une comparaison avec des rCsultats similaires obtenus sur des arbres matures des quatre m&mes populations.

Mots clis : Picea mariana, stress hydrique, photosynthkse nette, conductance stomatique.

Introduction

Advances in our understanding of plantation establishment in the boreal forest have confirmed the important role of water stress in the reduction of early seedling growth (Grossnickle and Blake 1986; Bernier 1993). Mitigation of water stress impact rests on strategies requiring improved physiological

Received June 25, 1994.

A. Zine El Abidine,' J.D. Stewart,* and A.P. Plamondon. Centre de recherche en biologie forestibre, Facultt de foresterie et de gtomatique, UniversitC Laval, Sainte-Foy, QC G1K 7P4, Canada. P.Y. Berr~ier.~ Canadian Forest Service, Quebec Region, Natural Resources Canada, P.O. Box 3800, Sainte-Foy, QC G1V 4C7, Canada.

' Present address: ~ c o l e Nationale Forestibre d71ngCnieurs, B.P. 5 1 1, Tabriquet, SalC, Morocco. Present address: Department of Renewable Resources, University of Alberta, Edmonton, AB T6G 2H1, Canada. Author to whom all correspondence should be addressed.

knowledge of species used in reforestation (Burdett 1990; Margolis and Brand 1990).

This study is the last in a series of three carried out on various aspects of black spruce (Picea mariana (Mill.) BSP) ecophysiology. The common theme of all three studies was the search for differences in drought tolerance between populations originating from contrasting environments. Several studies by previous investigators have failed to find ecotypic differences in black spruce (see Zine El Abidine et al. 1994a for a brief review). However, important characteristics for seedling establishment, such as the response of gas exchange and water relations to low soil moisture and to changes in climatic factors, were mostly ignored in these comparisons.

In two previous studies, we looked at the seasonal patterns of water relations parameters in mature trees (Zine El Abidine et al. 1994a) and at the response of seedlings to drought (Zine El Abidine et al. 1994b) using populations from lowland and upland origins. These studies did not reveal any consistent significant differences between black spruce populations from the two contrasting environments. A study on the response of gas exchange to natural fluctuations of environmental factors in seedlings was needed to complete the

Can. J. Bot. 73: 716-722 (1995). Printed in Canada / ImprimC au Canada

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comparison. The objective of this study was therefore to determine if differences existed in diurnal patterns and seasonal trends of gas exchange and water relations among seedlings from black spruce populations originating from lowland and upland sites.

Materials and methods

Plant material The study was conducted at the Laurentian Forestry Centre in Sainte-Foy, Quebec, Canada. Seeds from four black spruce populations originating from two upland (UL) and two lowland (LL) sites were obtained from the Canadian Forest Service's seed collection. The contrasting sites were paired geographically, with one pair from the province of Quebec (LLQ, ULQ) and the other from the province of Ontario (LLO, ULO). The upland populations originated from well-drained sites where black spruce grew in associa- tion with jack pine (Pinus banksiana Lamb.). The lowland populations originated from poorly drained sites character- ized by the presence of Sphagnum spp. mosses. Details on the geographical origins of the populations are given in Zine El Abidine et al. (1994~).

In mid-June 1991, the seeds were sown in containers (Rigipot 67-50, IPL, Saint-Damien, Que.) filled with a mixture of peat and vermiculite (4: 1, v/v). The seedlings were grown under standard conditions in a commercial green- house for 4 months (18-h photoperiod, 25:18"C 1ight:dark temperature, daily irrigation and twice-weekly fertilization), followed by 2 months outdoors and 5 months in a cold room at 2°C. In mid-May 1992, the seedlings were transplanted outdoors into four rectangular boxes (100 x 250 x 60 cm) containing a 4: 1 mixture of fine sand and peat. Each of these sand beds was divided into four units, to which one of the four populations was randomly assigned. In each unit, 100 seedlings were planted with a 10-cm spacing. At the time of planting, height and root collar diameter of the seedlings were 14.0 cm and 1.7 mm, respectively, with no significant differences among the four populations. From mid-May to mid-June, the seedlings were irrigated and fertilized twice a week with 20:20:20 N-P-K (Plant Products Co. Ltd., Brampton, Ont.). From mid-June on, the seedlings were left under natural atmospheric conditions.

Sampling Measurements were made across a range of environmental conditions on eight separate days during the growing season: July 16 and 23, August 6 and 12, September 2, 16, and 24, and October 6. On each day of measurement, 16 seedlings, one per population per sand bed, were chosen at random for measurements of predawn water potential. Similar samplings were carried out on the same day for measurements of gas exchange rates and xylem water potential, and for pressure- volume (P - V) curve determination.

Gas exchange measurements Gas exchange was measured on selected seedlings from the four populations, starting in the morning as soon as the foliage was dry (between 07:OO and 09:00), and then every 2 h until sunset (seven measurements per day in July but only

five per day in October). Net photosynthesis (P,), stomata1 conductance to water vapour (gSw), transpiration (E), and internal C02 concentration (ci) were measured under ambient climatic conditions with a portable photosynthesis system (LI-6200, LI-COR Inc., Lincoln, Nebr.) using a well- ventilated 0.25-L cuvette. Water use efficiency (WUE) was calculated from instantaneous measurements of net photosynthesis divided by transpiration. Measurements were made on the current-year needles from the upper half of the seedlings. The shoots used for gas exchange measurements were clipped and dried at 75°C for 36 h for dry mass determination. Each measurement used a different set of seedlings.

Water relations Xylem water potential was measured with a pressure chamber (PMS Instruments, Corvallis, Oreg.) before dawn, between 04:OO and 05:OO (q,,), and following each gas exchange measurement (9,). Measurements performed during the day used twigs sampled on the seedlings used for gas exchange measurements. A final set of 16 seedlings was harvested for P - V analysis following the last measurement of the day before sunset. Shoots were excised at the root collar; stems were recut under distilled water and stood in beakers sealed in plastic bags. The shoots were allowed to resaturate over- night in the dark at room temperature (approx. 23°C). The following morning, P-V curves were obtained using the Richards method of sap expression with a 0.5-MPa over- pressure maintained for 10 min, as described in Zine El Abidine et al. (1993). Values of osmotic potential at full turgor (\kTFT) and at turgor-loss point (\kTTLP) were obtained from the P- V curves using the PVC program developed by Schulte and Hinckley (1985).

Environmental conditions On each measurement date, volumetric water content of the soil in each sand bed was measured gravimetrically on soil samples taken at a depth of 10 cm, at four locations equally spaced along each bed. Air temperature and humidity were measured inside the cuvette during the gas exchange measurements. Evaporative demand expressed as absolute humidity deficit (AHD) was calculated from air temperature and vapour pressure inside the cuvette. Photosynthetic photon flux density (PPFD) was measured with a quantum sensor (LI-190SB, LI-COR Inc.) mounted above the cuvette. Air temperature inside the cuvette was used as an estimate of leaf temperature (Dang et al. 1991).

Additional measurements of environmental conditions were recorded hourly on a datalogger. Air temperature and relative humidity (207 probe, Campbell Science, Logan, Utah) as well as PPFD (LI-190SB probe) were measured at seedling height. Soil temperatures at a depth of 10 cm were measured at four points in each sand bed using copper-constantan thermocouples. Rainfall was recorded using a tipping-bucket rain gauge.

During the study period, maximum and minimum daily air temperatures ranged from 27.8 to 1 1.5"C and from 13.7 to - 1.3"C, respectively. Daily maximum and minimum relative humidity ranged from 100 to 76.5% and from 74.5 to 15.72%, respectively. Total rainfall during the 3-month study period was 602.4 mm.

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Fig. 1. (a) Diurnal courses of photosynthetic photon flux density (PPFD), (b) absolute humidity deficit (AHD), (c) air temperature, (d) net photosynthesis, (e) stomatal conductance for water vapour, (f) xylem water potential; (g) intracellular CO, concentration, (h) water-use efficiency (WUE), and (i) transpiration of black spruce seedlings growing in raised sand beds under field conditions. Points in (a), (b), and (c) are four-measurement means. Points in all other graphs are 16-seedling means (f 1 SE). 0, July 23; m, Sept. 2; 0, Oct. 6.

Time (Solar Hour) Time (Solar Hour) Time (Solor Hour)

Experimental design and statistical analyses The experimental design contained four blocks or sand beds. Each block was divided into four units and each unit planted with 100 seedlings from one of the four experimental populations. Depending on the length of the day, between 8 and 10 of these were used for the different physiological measurements on each measurement date. Results were analyzed as a split-plot design. Main plots were the populations. Subplots were the dates and hours of measurements. Statistical analyses were performed on hourly measurements of the different variables for each day, and on the daily maximum value of each parameter over the study period. Analyses of variance were performed using the GLM procedure of the SAS software (SAS Institute Inc., Cary, N.C.). Bartlett's test and the plot of ANOVA residuals were used to test the homogeneity of the variance and normality of the residuals. Com- parisons between contrasting sites (lowland versus upland) were made using a priori contrasts (Steel and Torrie 1980). Statistical tests were considered significant when P < 0.05.

Results and discussion Diurnal patterns of physiological responses Figure 1 shows hourly measurements of environmental and physiological variables for three representative days of measurements. The highest rates of gas exchange occurred in mid-morning before peak AHD and air temperature (Figs. 1 b and lc). The low rate of Pn (Fig. Id) observed in the earli- est morning readings was associated with low light intensity (Fig. la), low air temperature (Fig. lc), and low stomatal conductance (Fig. le). The afternoon drop in Pn was related to stomatal closure as a result of the high evaporative demand, even if soil water content was not limiting. Statistical analysis of hourly values of gas exchange (results not shown) revealed no significant differences between the populations from upland and lowland origins.

The daily pattern of WUE remained quite constant throughout the growing season (Fig. lh). WUE was at its highest level early in the morning when cool and humid air reduced transpiration to a minimum. It decreased rapidly to reach a

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Table 1. Summary of analysis of variance for gas exchange parameters of four black spruce populations growing outdoors in sand beds.

Source of variation df p" ~ S W E WUE Ci

Population 3 0.4360 0.0019 0.0211 0.0445 0.4643 Date 7 O.OOU1 0.0001 0.0001 0.0001 0.0001 Population x date 21 0.4375 0.2193 0.7083 0.8395 0.9971 LLQ versus ULQ 1 0.8899 0.7054 0.6083 0.7575 0.8943 LLO versus ULO 1 0.1357 0.1958 0.2939 0.9787 0.9039 M S error 93* 0.0002 0.0827 0.4132 0.4290 469.01

NOTE: Results are presented as probability values and mean square errors from analysis of variance with contrasts for net photosynthesis (P,), stomatal conductance (g,,), transpiration (E), water use efficiency (WUE), and internal CO, concentration (ci). LLQ, lowland Quebec; ULQ, upland Quebec; LLO, lowland Ontario; ULO, upland Ontario.

*92 for g,,, 91 for WUE, and 83 for ci.

lower stable value later in the morning when the transpiration rate was maximum (between 09:OO and 11:OO) (Fig. li). Internal C 0 2 concentration (q) was high early in the morning and in the evening when P, was at the lowest point (Fig. lg). High values of ci in black spruce are typical of well-watered conditions for black spruce when stomatal conductance is high and changes in q are driven by net photosynthesis. Low values of q indicate that stomatal closure limits C 0 2 diffusion to the chloroplasts (Stewart et al. 1995). Similar patterns of WUE and q have been observed by Dickmann et al. (1992) in two hybrids of Populus.

Xylem water potential was high at sunrise, decreased rapidly to reach a midday minimum between 10:OO and 15:00, and increased again in late afternoon (Fig. If). This typical pattern has been reported for seedlings (Pothier et al. 1989) and mature black spruce trees (Vowinckel et al. 1975), as well as for other tree species (HincMey et al. 1978). The decrease in xylem water potential was not related to changes in bulk soil water status but rather to an increased air temperature and AHD, leading to an increase in transpiration.

Seasonal pattern of gas exchange Analysis of the daily maximum values of gas exchange parameters showed no significant differences between seedlings from upland and lowland origins (Table 1). The date of measurement had a significant effect on all variables, but there was no significant population x date interaction. Sig- nificant differences among populations in several of the gas exchange parameters resulted from differences between the Quebec and Ontario populations. These differences were not analyzed in detail, since we were interested in ecotypic rather than geographic effects.

In all four populations, maximum values of net photosynthesis (PnMAX), stomatal conductance (gsMAx), and transpiration (EMAX) decreased by 77, 67, and 79%, respectively, from the first date of measurement on July 16 to the last one on October 6 (Fig. 2). The decreases of PnMAX and EMAX were more regular than that of gsMAx. The seasonal pattern of PnMAx was similar to that described by Delucia and Smith (1987) for Engelmann spruce (Picea engelmannii Parry) in the subalpine forest of the Rocky Mountains but contrasted with the findings of Vowinckel et al. (1975), who observed no seasonal trend in PnMAX of mature black spruce trees growing under Quebec subarctic conditions. Rates of PnMAX

measured by Vowinckel et al. (1975) were about 0.02 pmol . g-' . s-I, much lower than the 0.05-0.15 pmol . g-I . s-I measured in this study, suggesting a strong climatic limita- tion of Pn throughout the subarctic growing season.

PnMAX and g,,,, for the four populations were positively correlated with minimum (night) soil (R2 = 0.60, 0.84) and air temperatures (R2 = 0.44, 0.69) (Fig. 2). PnMAX showed a gradual decline over the season (Fig. 2a) and did not respond to the differences in environmental conditions among the last three days of measurement (Figs. 2d-2f), suggesting a weak link with day to day variations in climatic factors. Variations of gsMAx (Fig. 2b), on the other hand, followed a pattern similar to those of the various temperature measurements (Fig. 2f), suggesting a strong causal link (Figs. 2b and 2f). Seasonal decline in PnMAX has been attributed to a decrease in photosynthetic capacity resulting from a combi- nation of aging of foliage and of declining minimum (night) temperature and day length (Delucia and Smith 1987; Kozlowski et al. 1991). Decreases of Pn with increasing needle age have been observed under controlled conditions in black spruce (D'Aoust 1978) and in the field in Pacific sil- ver fir (Abies amabilis (Dougl.) Forbes) (Teskey et al. 1984) and red spruce (Picea rubens Sarg.) (McLaughlin et al. 1990). According to Kozlowski et al. (1991), changes in net photosynthesis result from alterations in leaf structure, stomatal behaviour, enzyme activity, shift in photorespira- tion and dark respiration, and changes in the relative size of sources and sinks of photosynthates. The observed decrease in gas exchange parameters with increased age has also been associated with the accumulation of waxes that block stomatal pores in older foliage (Teskey et al. 1984).

Seasonal patterns of water relations An analysis of the daily values of water relations parameters showed weak differences among populations in \kTFT and

(Table 2). The effect of measurement date was highly significant on all variables, but there was no significant interaction between population and date, indicating a consistency of response over time in all four populations (Fig. 3). Orthogonal contrasts revealed no significant differences between seedlings from upland and lowland origins (Table 2). However, closer examination within each upland-lowland pair showed a significant (P < 0.04) difference in osmotic potential at full turgor between the two Ontario populations

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Fig. 2. (a) Seasonal courses of maximum net photosynthesis, (b) stomata1 conductance for water vapour, and (c) transpiration of seedlings from four black spruce populations growing in raised sand beds under field conditions. Points are four-seedling means (+ 1 SE). Levels of (d) absolute humidity deficit (AHD) and (e) photosynthetic photon flux density (PPFD) were recorded at the maximum rate of net photosynthesis. (f) Soil and air minimum and maximum temperatures were recorded at night and midday, respectively.

a -$- L o w l a n d Quebec

U ~ l a n d Quebec

--& owla and O n t a r i o

Up land O n t a r i o

f

--c-- Min. s o i l ternp. - Max. a i r temp.

0 - Min. a i r t e m p . -15

I I I I

J U I ~ ~ u g ~ e p t 0c t . l J U I ~ ~ u g . I I

Sept . Oct.

Table 2. Summary of analysis of variance for water relations parameters of four black spruce populations growing outdoors in sand beds.

Source of variation d f *XB * x ~ ~ ~ *TFT **TLP

Population 3 0.5666 0.6666 0.0796 0.0367 Date 7 0.0001 0.0001 0.0001 0.0001 Population x date 21 0.3436 0.1925 0.9500 0.5875 LLQ versus ULQ 1 0.5393 0.7956 0.1121 0.1232 LLO versus ULO 1 0.2247 0.3613 0.0429 0.0632 MS error 93 * 0.0528 0.0076 0.0041 0.0088

NOTE: Results are presented as probability values and mean square errors from analysis of variance with contrasts for predawn xylem water potential ('Px,) (MPa), midday xylem water potential ('P,,,,) (MPa), osmotic potential at full turgor ('P*,) (MPa), and osmotic potential at turgor-loss point ('P,,,,) (MPa). Other abbreviations as in Table 1.

*91 for 'P,,,,.

(LLO and ULO), but no such significant difference between suggests a strong juvenile to mature correlation in water rela- the seedlings from the two Quebec populations (LLQ and tions parameters. ULQ). A similar difference had been obtained in the analysis Predawn water (\k,) and midday (\kxMID) xylem water of the water relations parameters of mature trees from the potential of the four populations did not show any consistent same (LLO and LTLO) populations (Zine El Abidine et al. seasonal pattern (Fig. 3). \k, remained above -0.5 MPa, 1994a). This consistency between seedlings and mature trees reflecting the high soil water availability in the sand beds.

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Fig. 3. Seasonal courses of predawn xylem water potential (q,,), midday xylem water potential (q,,,,), and osmotic potential at turgor-loss point (q,,,,) of seedlings from four black spruce populations growing in raised sand beds under natural atmospheric conditions, as well as of volumetric soil water contents in the sand beds. All points are four-measurement means (f 1 SE).

July I

A u g u s t I S e p t e m b e r O c t o b e r

-

-

-

-

-

Under such well-watered conditions, decreases in qxMID were associated with increases in transpiration following an increase in air temperature and absolute humidity deficit. High levels of qxMID were the result of stomata1 closure.

Osmotic potential at turgor-loss point (qTTLP) showed a consistent seasonal decline from early average values of -1.44 MPa to -2.36 MPa at the end of the study period (Fig. 3c). The decrease in qTTLP after shoot elongation is associated with ontogenetic changes at the cellular level, which are themselves driven by the decrease in temperature and photoperiod (Tyree et al. 1978; Colombo 1987; Gross- nickle 1989). The decline in qTTLP at the end of the growing season can be caused by increases in foliar concentrations of sugars, amino acids, and inorganic ions (Abrams 1988; Kozlowski 1992).

In early summer, during rapid growth, the difference between qnTLP and qxMID was small in all four populations (Fig. 3). During that period, seedlings often came close to turgor loss despite abundant soil water. The difference between qxMID and qnTLP increased throughout the summer along with the resultant resistance to turgor loss. Turgor loss, a consequence of water stress, results in cessation of growth and perturbation of most physiological processes within plants and can threaten the survival of newly planted seedlings (Turner 1986; Burdett 1990; Kozlowski et al. 1991).

* x B

* x M l D

* n T L P -;- Upland O n t a r i o

Conclusions

In this study, water relations parameters and gas exchange of seedlings from two upland and two lowland black spruce populations did not differ consistently in response to diurnal or seasonal variations in environmental conditions. This lack of clear difference between upland and lowland populations of black spruce supports previous results from studies in which mature trees and seedlings from the same populations were compared using different attributes (Zine El Abidine et al. 1994a, 19946). Given the mostly negative results from other studies in which populations were tested for ecotypic differences using morphological or physiological traits (reviewed in Zine El Abidine et al. 1994a), it is now clear that ecotypic differences in black spruce are neither wide- spread nor well defined. Pollen contamination, dispersal of seeds among the populations, and variability among families within populations are all possible causes of the relative homogeneity among regional populations of black spruce (Parker et al. 1983; Boyle 1990; Di-Giovani and Kevan 1991).

Although we could not find any difference that could be linked to ecotypic differentiation, differences were found between the two geographical origins and between the two populations within one of the two upland-lowland pairs.

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Similar differences were also found in an earlier study on mature trees from the same four populations (Zine El Abidine et al. 1994a). This consistency of response from seedlings and mature trees supports the validity of early testing of seedlings for desirable physiological traits at a later age.

Acknowledgements

We are grateful to Michkle Bernier-Cardou and Carole HCbert for their help in statistical analyses, and to Pierre Davignon for his technical assistance. Financial support for Dr. Zine El Abidine was provided by the Canadian Interna- tional Development Agency and by the Doctoral Studies Sup- port Program of UniversitC Laval.

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diurnal and seasonal variations in gas exchange and water relations of lowland and upland black...

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