Oecologia (2000) 123:168–174
© Springer-Verlag 2000
Andy Benowicz · Robert D. Guy Yousry A. El-Kassaby
Geographic pattern of genetic variation in photosynthetic capacity and growth in two hardwood species from British Columbia
Received: 12 July 1999 / Accepted: 24 November 1999
Abstract Geographic patterns of intraspecific variations in traits related to photosynthesis and biomass were examined in two separate common garden experiments using seed collected from 26 Sitka alder (Alnus sinuata Rydb.) and 18 paper birch (Betula papyrifera Marsh.) populations from climatically diverse locations in British Columbia, Canada. Exchange rates of carbon dioxide and water vapour were measured on 2-year-old seedlings to determine the maximum net instantaneous photosynthetic rate, mesophyll conductance, stomatal conductance, and photosynthetic water use efficiency. Height, stem diameter, root and shoot dry mass and fall frost hardiness data were also obtained. Mean population maximum photosynthetic rate ranged from 10.35 to 14.57 µmol CO2 m–2 s–1 in Sitka alder and from 14.76 to 17.55 µmol CO2 m–2 s–1 in paper birch. Based on canonical correlation analyses, populations from locations with colder winters and shorter (but not necessarily cooler) summers had higher maximum photosynthetic rates implying the existence of an inverse relationship between leaf longevity and photosynthetic capacity. Significant canonical variates based on climatic variables derived for the seed collection sites explained 58% and 41% of variation in the rate of photosynthesis in Sitka alder and paper birch, respectively. Since growing season length is reflected in date of frost hardiness development, an intrinsic relationship was found between photosynthetic capacity and the level of fall frost hardiness. The correlation was particularly strong for paper birch (r=–0.77) and less strong for Sitka alder (r=–0.60). Mean population biomass accumulation decreased with increased climate coldness. These patterns may be consequential for A. Benowicz · R.D. Guy (✉) · Y.A. El-Kassaby Department of Forest Sciences, Faculty of Forestry, The University of British Columbia, Vancouver, British Columbia, V6T 1Z4, Canada e-mail:
[email protected] Fax: +1-604-8229102 Y.A. El-Kassaby PRT Management Inc., 4-1028 Fort Street, Victoria, British Columbia, V8V 3K4, Canada
evaluation of the impact of climate change and extension of the growing season on plant communities. Key words Intraspecific genetic variation · Photosynthesis · Frost hardiness · Climate change · Growing season
Introduction One effect expected of global warming is an increase in growing season length, as recently documented using phenological data from European botanical gardens (Menzel and Fabian 1999). An increase in growing season length could impact fitness, depending on species or population differences in habit (deciduous vs evergreen), growth pattern (determinate vs indeterminate), and sensitivity to photoperiod or other external cues. Several studies have reported a negative relationship between photosynthetic rate and leaf longevity at the species level. Johnson and Tieszen (1976) found that photosynthetic capacity was inversely related to leaf longevity among species of various growth forms (evergreen shrubs, deciduous shrubs, perennial grasses, sedges and forbs) naturally occurring in one location in Alaska. A similar inverse relationship between leaf longevity and photosynthesis was found for a number of conifers as well as broad-leaved species in their native environments (Reich et al. 1992). Gower et al. (1993) compared two deciduous and three evergreen tree species in a common garden experiment and found a strong inverse correlation between leaf life-span and maximum net photosynthesis per unit leaf mass. No correlation was found when photosynthesis was expressed per unit leaf area. Reich et al. (1995) indicated that an inverse relationship based on photosynthetic rate calculated per unit area is more likely to hold true for angiosperms than for gymnosperms. The relationship between rate of photosynthesis and leaf longevity has not been characterized with respect to within-species genetic variation at the population level. There are reports of higher photosynthetic rates in popu-
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lations of evergreen conifers from colder regions (Wright 1971; Zhang et al. 1993; Oleksyn et al. 1998), and in situ studies have found an increased life-span of evergreen leaves in colder climates (e.g. Shoettle 1990; Kajimoto 1993). These observations suggest a positive relationship between photosynthetic rate and leaf longevity, but no genetic differences in the latter were found among Scots pine (Pinus sylvestris L.) and Norway spruce [Picea abies (L.) Karst.] populations in a common garden experiment (Reich et al. 1996). In contrast, population differences in leaf duration are common in deciduous species [e.g. eastern cottonwood (Populus deltoides Marsh.) (Ying and Bagley 1976) and red alder (Alnus rubra Bong.) (Ager et al. 1993; Hamann et al. 1998)], but no associated trends in photosynthetic rates have been reported. With respect to non-woody plants, correlation between gas exchange rates and life-span of the annual plant Polygonum arenastrum Boreau was reported by Geber and Dawson (1990). They found that small-leaved families tend to have higher gas exchange rates and shorter life-span compared to large-leaved families based on seeds collected from a single population. We examined intraspecific genetic variation in gas exchange and growth parameters in two northern deciduous hardwoods from the Betulaceae: Sitka alder (A. sinuata Rydb.) and paper birch (Betula papyrifera Marsh.). Both are fast-growing pioneer species found in a wide range of environments. Sitka alder is capable of nitrogen fixation in association with Frankia bacteria, whereas paper birch is not.
Materials and methods Plant material Sitka alder and paper birch open-pollinated seeds were collected from 26 and 18 sites in British Columbia, respectively (Tables 1, 2). Each collection was made from at least ten well distributed trees. Seeds from individual trees within each site were mixed. The seeds were sown in styroblocks (PSB313B, cavity volume 65 ml) in a commercial nursery located on south Vancouver Island (latitude 48°35’ N, longitude 123°24’ W, elevation 50 m). After one growing season, the seedlings were potted into plastic containers (volume 2.65 l) and left outside for a second year. The plants were fertilized and watered to ensure optimum growing conditions. The Sitka alder experiment was started in spring 1996 and was followed by the paper birch experiment 1 year later.
Table 1 Locations of sampled Sitka alder populations Population
Latitude
Longitude
Elevation (m)
Adam’s Plateau Bella Coola Bute Inlet Chine Nose Summit Cold Creek Cranbrook Cypress Park Dease Lake Glena Bay Green Mountain Hemlock Valley Hope Slide Kimsquit River Kitlope River Knight Inlet McKay Lake McKendrick Pass Owikeno Lake Phoenix Powell River Roberts Lake Roger’s Pass Sproat Lake Stikine River Valemount Vanderhoof
51°06’ N 52°19’ N 50°56’ N 54°27’ N 50°49’ N 49°35’ N 49°22’ N 58°45’ N 50°35’ N 49°03’ N 49°23’ N 49°16’ N 52°53’ N 53°03’ N 51°06’ N 49°45’ N 54°50’ N 51°34’ N 49°05’ N 49°59’ N 50°13’ N 51°19’ N 49°18’ N 58°00’ N 52°50’ N 53°56’ N
119°33’ W 126°46’ W 125°05’ W 126°08’ W 120°07’ W 117°05’ W 123°12’ W 130°03’ W 117°52’ W 124°21’ W 121°56’ W 121°15’ W 127°10’ W 127°36’ W 125°48’ W 125°17’ W 126°45’ W 126°31’ W 118°35’ W 124°39’ W 125°30’ W 117°34’ W 125°04’ W 130°02’ W 119°15’ W 123°49’ W
1280 800 960 1430 1310 640 980 869 607 1100 1013 762 800 820 790 914 1190 1080 1219 660 366 1219 640 915 850 1287
Table 2 Locations of sampled paper birch populations Population
Latitude
Longitude
Elevation (m)
Sardine Creek Bush Creek Lee Creek Skeena River Little Oliver Creek Burdick Creek Juniper Creek St. Mary River Wilson Creek Porcupine Creek Frost Lake Mars Creek Cuisson Lake Raft Creek Eaglet Lake Tabor Lake Amanita Lake Barnes Creek
52°47’ N 50°49’ N 50°46’ N 54°30’ N 54°42’ N 55°11’ N 55°08’ N 49°38’ N 50°04’ N 49°15’ N 53°47’ N 51°22’ N 52°31’ N 52°31’ N 54°06’ N 53°55’ N 54°08’ N 50°34’ N
122°14’ W 119°45’ W 119°32’ W 128°34’ W 128°16’ W 127°47’ W 127°43’ W 116°03’ W 117°23’ W 117°10’ W 122°38’ W 118°18’ W 122°24’ W 121°31’ W 122°21’ W 122°22’ W 121°47’ W 118°50’ W
760 1250 600 70 270 480 350 990 915 840 975 990 762 830 685 915 760 850
Growth Growth variables for Sitka alder were measured on 25 plants per population: height after the first growing season (H1), and height (H2), shoot dry mass (SDW), root dry mass (RDW) and main stem diameter at the root-shoot transition zone (DIAM) after the second growing season. For paper birch, height (H1), stem diameter at the root-shoot transition zone (DIAM1), shoot dry mass (SDW) and root dry mass (RDW) were measured after the first growing season on 30 seedlings per population. Height (H2) and stem diameter (DIAM2) were determined after the second growing season for 25 plants per population.
Gas exchange Exchange rates of carbon dioxide and water vapour were determined during the second growing season using open gas exchange systems (LCA3 and LCA4, Analytical Development Company, UK) with a Parkinson broadleaf chamber (PLC3). The Sitka alder measurements took place between 19–25 July 1997 on 25 seedlings per population. Paper birch gas exchange rates were measured on 21 plants per population between 20–25 July 1998. Equal numbers of plants per population per day were measured. Plants measured on the same day constituted one block for statistical analysis. An artificial light source (35-W Eye Dichro-Cool halogen lamp, Iwasaki Electric Company, Japan) was used to illumi-
170 nate the leaf chamber with 1200 µmol m–2 s–1 photosynthetic photon flux density (PPFD). The measurements were taken on sunny days with sunlight PPFD exceeding 1000 µmol m–2 s–1 to ensure that the measured leaves were induced to high light. Gas exchange rates were recorded twice for one, fully expanded sun leaf per plant and the average was used in the data analyses. The concentration of carbon dioxide in air entering the leaf chamber and its relative humidity were controlled at 330 µl l–1 and 45%, respectively. Temperature was recorded and used as a covariate. It ranged from 20.2 to 30.9°C for Sitka alder and from 26.5 to 36.9°C for paper birch. Based on carbon dioxide and water vapour exchange rates, the following quantities were obtained as described in von Caemmerer and Farquhar (1981): transpiration rate (E, mmol H2O m–2 s–1), stomatal conductance (gs, mmol H2O m–2 s–1), intracellular CO2 concentration (Ci) and net photosynthesis (A, µmol CO2 m–2 s–1). In both experiments, A approximates the maximum photosynthetic rate, since the measurements were taken on plants grown in optimum or near optimum conditions with respect to moisture and nutrient supply and PPFD exceeded the light saturation point. Photosynthetic instantaneous water use efficiency was calculated as the ratio of A to E. Mesophyll conductance (gm, mol CO2 m–2 s–1) was calculated by dividing A by Ci (Ludlow and Jarvis 1971).
perature (MAT). Variables approximating precipitation levels were also derived and tried but did not yield any significant relationships. The models were developed for British Columbia and adjacent portions of Yukon, Alberta and the United States between 48°30’ and 62°00’ N using normalized weather records from 513 stations and were verified with independent data from 45 stations (Rehfeldt et al. 1999). Separate canonical correlations were performed on Sitka alder and paper birch data between the set of variables related to gas exchange and growth (response variables) and the set of climatic variables (predictor variables). The response variables were: A, gm, gs, A/E, H1, H2, DIAM, SDW, and RDW for Sitka alder and A, gm, gs, A/E, H1, H2, DIAM1, DIAM2, SDW, and RDW for paper birch. The same predictor variables were used in both analyses: MTCM, MTWM, COLD, FFP, NFFD and MAT. Population means of growth variables and least-squares means of gas exchange variables adjusted for significant covariate effect (P0.77) on CLIM1, the first climatic canonical variable (Table 4). Thus, CLIM1 approximated climate coldness with respect to winter temperatures and days without frost. Among gas exchange variables, A and gs were correlated significantly with CLIM1 (Table 4). As for Sitka alder, A was higher in pa-
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A strong correlation (r=–0.77) was found between I–6 measured in October and A measured in July (Fig. 4). Higher maximum rates of photosynthesis in summer were found in populations that developed earlier frost hardiness in fall.
Discussion
Fig. 4 Maximum net photosynthetic rate (A) of paper birch populations measured in July versus fall frost hardiness. Frost hardiness was measured in October at –6°C and is expressed as index of injury (I–6)
Table 4 Canonical structure based on paper birch data: correlations between climatic variables and their first canonical variable (CLIM1) and between the response variables and CLIM1. Critical values of the correlation coefficient are 0.456 at P=0.05 and 0.575 at P=0.01 (n=18) [abbreviations as in Table 3 except stem diameter (DIAM1), shoot dry mass (SDW) and root dry mass (RDW) after the first growing season, and stem diameter (DIAM2) after the second growing season] Climatic variables
CLIM1
Response variables
CLIM1
MTCM MTWM COLD FFP NFFD MAT
0.78 –0.01 0.89 0.77 0.79 0.56
A gm gs A/E H1 H2 DIAM1 DIAM2 SDW RDW
–0.64 –0.30 –0.51 –0.33 0.81 0.33 0.28 –0.01 0.70 –0.22
per birch populations from locations with lower winter temperatures and fewer frost-free days. Height and SDW after the first growing season loaded highly and positively on CLIM1 (Table 4). Height after the second growing season was not related to CLIM1. Based on canonical redundancy analysis, 23% of the variance of all response variables was explained by CLIM1. A considerable portion of variation in A, H1 and SDW was explained since squared correlations between these variables and CLIM1 were between 0.41 and 0.68. Canonical correlations based on latitude, longitude, elevation and distance from the coast were less successful in explaining variation in growth and gas exchange variables (13% explained) than canonical correlation based on climatic variables. Over 38% of the variation in A was explained by the first and the only significant canonical correlation. The geographic pattern of variation in A of paper birch populations is presented in Fig. 3.
Intraspecific variations in Sitka alder and paper birch gas exchange variables indicate that there is an inverse relationship between photosynthetic capacity per unit leaf area and leaf longevity in northern hardwoods. Leaf longevity was not directly measured since the relationship was determined in retrospect, but relative differences among the populations in terms of the length of the active growing period can be inferred from the level of fall frost hardiness. Growth cessation is a prerequisite for the development of frost hardiness (Weiser 1970) and plants that stop growing earlier typically develop earlier frost resistance (e.g. Pauley and Perry 1954; Cannell et al. 1987; Hurme et al. 1997). These differences reflect population adaptation to differences in growing season based on climate. An intrinsic relationship between fall frost hardiness and A was found, presumably because both traits can be related to length of the inherent growing season and, therefore, leaf duration. The relationship between A and leaf duration appears to be quite strong. In Sitka alder, 56% of the variation in population mean A was explained by CLIM1 (as a proxy for the length of the available growing season at the site of origin), while 36% was explained by the level of fall frost resistance (a proxy measure of the genetically programmed growth period). Corresponding numbers for paper birch were 41% and 59%, respectively. Locations characterized by lower winter temperatures and a shorter frost-free period have a shorter growing season. On the other hand, summer temperatures in seed collection sites can be either positively (along latitudinal or elevational gradients) or negatively (along the coastinterior transect) related to the length of the growing season. Therefore MTWM is not a good indicator of growing season length. In both Sitka alder and paper birch, A was higher in populations from climates with lower MTCM, COLD, MAT, FFP and NFFD, but was unrelated to MTWM. Corresponding to the results of analysis based on derived climatic variables, canonical correlation analysis based on location variables (latitude, longitude, elevation and distance from the coast) also detected higher A in populations from colder regions. In Sitka alder, A increased with elevation, latitude and distance from the coast, while in paper birch, A increased mainly with elevation and distance from the coast. Leaf nitrogen content typically increases with elevation, particularly when expressed on a per unit leaf area basis (Körner 1989). Weih and Karlsson (1999) report that this pattern is genetically determined in two populations of mountain birch [B. pubescens Ehrh. ssp. cze-
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repanovii (Orlova) Hämet-Ahti] from different elevations in Sweden. These authors suggest that high leaf N (and, by extension, high photosynthetic capacity) is part of a syndrome that permits cold-region plants to maintain growth under low-temperature conditions at the expense of an ability to optimally utilize periods of higher temperatures. Our results do not fully support this view. The lack of a relationship between A and MTWM suggests that growing season temperature is less important than duration. Our ability to detect a distinct geographic trend in A in Sitka alder and paper birch may be related to the large number of plants sampled per population and to the range of tested populations that may have included climatically more diverse locations than those sampled for other species. For example, Dang et al. (1994) found only a very weak southeast-to-northwest trend in photosynthesis for red alder populations in coastal British Columbia. Given the more moderate climate, it is likely that there is less selective pressure for differentiation in A along the coast (within the range of sampled red alder populations) compared to the selective pressures caused by changes in environmental conditions towards the continental interior. Although a high photosynthetic capacity should be advantageous, there may be associated costs that increase with the length of the growing season. A trade-off between leaf retention and photosynthetic rate has been previously shown to occur between species but, to our knowledge, this is the first report of such a pattern existing within species at the population level. The physiological basis of the trade-off is not known, but leaves with higher A may age more rapidly due to, for example, higher rates of photooxidation. Photosynthetic capacity may therefore be one of the internal plant factors interacting with external factors (e.g. night length, temperature) that have an impact on onset and rate of leaf senescence. Within individual plants for example, sun leaves typically have higher A but also age more rapidly than shade leaves (e.g. Ackerly and Bazzaz 1995). The negative correlation between A and leaf life-span may also be an indirect consequence of adaptation to factors other than growing season. For example, populations with thicker leaves or lower shoot:root ratio may have higher nitrogen content and higher A per unit leaf area. Greater growth allocation to roots is often observed in plants from colder regions (e.g. Cannell and Willet 1976). Indeed, we observed lower shoot:root ratios in northern Sitka alder populations and in inland paper birch populations (data not presented). A lower shoot:root ratio should also help to minimize effects of higher water loss due to higher gs found in populations from colder regions. Alternatively, populations from higher altitudes or latitudes could extract soil nitrogen more efficiently as an adaptation to lower rates of organic matter mineralization at low temperatures. Such population differentiation would not be expected in Sitka alder which, through its ability to fix nitrogen symbiotically, is less likely to depend on soil nitrogen levels. Anoth-
er possibility is that coastal populations may be subject to more competition for light and may have been selected for greater shade tolerance. Lower photosynthetic capacity in shade-tolerant plants has been shown for a number of species (e.g. Kubiske et al. 1996). Kikuzawa’s (1995) theoretical cost-benefit model of leaf longevity predicts that optimum leaf longevity decreases with increasing maximum photosynthetic rate under the assumption that the optimum leaf life-span should be of a duration to maximize carbon gain per plant. According to the model, the optimum time for a leaf replacement is the time taken to maximize leaf marginal carbon gain (i.e. assimilation less maintenance and construction costs). For species growing in seasonal climates, if the optimum time is longer than the length of the favourable growing season, then the leaf habit is evergreen; if shorter, then the leaf habit is deciduous. Even though the model is in apparent agreement with our results, it cannot explain differences in leaf longevities among and within deciduous tree species. To maximize carbon gain per plant, the leaves of deciduous trees should, theoretically, last as long as assimilation exceeds maintenance respiration. Leaf shedding is one of the various changes taking place at the end of the growing season that enables plants to tolerate or avoid stress imposed by unfavourable environmental conditions. Leaf longevity is therefore optimized not only to maximize carbon gain but also to increase chances of plant survival. The trade-off between carbon gain and survival is commonly reflected in lower biomass accumulation in populations from colder regions (see Morgenstern 1996). We find a similar relationship between climate coldness and plant size for Sitka alder and paper birch populations. Negative correlations between most growth variables and photosynthetic capacity suggest that differences in the length of the inherent growth period had a larger impact on biomass accumulation than differences in A. Negative or non-significant correlations between rate of photosynthesis and plant size parameters are often reported in the literature (e.g. Sorensen and Ferrell 1973; Mebrahtu and Hanover 1991; Zhang et al. 1993). On the other hand, photosynthetic capacity and leaf longevity are only two of several factors that can affect biomass accumulation. Covariation in these other factors (e.g. carbon allocation to root growth) may be paramount. Plant factors that impact on biomass accumulation will be affected by climate change to various degrees that may increase or decrease plant productivity. In some regions, an increase in tree growth may be attributed, at least partially, to the lengthening of the growing season due to increased temperature (Menzel and Fabian 1999). However, populations from climatically diverse locations are likely to be affected by climate change to different extents. Leaf abscission is typically under photoperiodic control whereas bud break is not. Locally adapted populations may therefore make good use of an earlier spring, but not an extended autumn. Nevertheless, our
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data suggest that an extended growing season resulting from climate change may cause higher carbon gain than expected in populations from colder regions relative to those from warmer regions.
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