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Dioecious species are an important component of terrestrial ecosystems, representing more than 14 000 angiosperm species (Renner & Ricklefs, 1995). Many dominant woody species in forest ecosystems, including members of Salicaceae and Aceraceae, are dioecious. Male and female individuals of dioecious species have been shown to differ physiologically and ecologically from one another at current concentrations of atmospheric carbon dioxide (CO2). For example, female Acer negundo had a higher photosynthetic rate than males (Dawson & Ehleringer, 1993), while the opposite was true for Salix arctica (Jones et al., 1999). Female A. negundo, S. arctica and Thalictrum fendleri significantly outnumbered males in mesic or high-nutrient sites, while males were more numerous in xeric or low-nutrient sites (Freeman et al., 1976; Dawson & Bliss, 1989; Dawson & Ehleringer, 1993). Grant & Mitton (1979) found that the ratio of female to male Populus tremuloides clones on the Front Range in Colorado was 1.27 below 2450 m of elevation, but was only 0.56 above 2900 m.
The physiological and ecological differences between genders were hypothesized to have arisen as a result of different reproductive costs incurred by male and female plants, with females typically investing more in reproduction than do males (Lloyd & Webb, 1977; Allen & Antos, 1988; Dawson & Ehleringer, 1993; Dawson & Geber, 1999). Growth and physiological differences between genders have also been observed before reproduction (Bourdeau, 1958). If carbon assimilation of male and female individuals of dioecious species is differentially affected by CO2 enrichment, their productivity, distribution and population structure might be altered as atmospheric CO2 concentration rises. However, little is known about the gender-specific physiological responses to elevated CO2 by P. tremuloides or any other species. Because of their prominence in terrestrial ecosystems, not accounting for gender-specific variation in carbon assimilation in dioecious species could lead to incorrect estimates of the potential responses of plants to global environmental changes (Jones et al., 1999).
While it has been well documented that atmospheric CO2 enrichment can substantially increase photosynthesis and plant growth (Strain & Cure, 1986, 1994; Curtis & Wang, 1998), our understanding of the effects of rising CO2 on plant dark respiration (Rd) is much less certain. The mechanisms controlling photosynthetic and respiratory responses to CO2 are different (Bunce & Ziska, 1996) and what we have learned about photosynthetic responses to elevated CO2 cannot be readily extrapolated to respiratory responses. Indeed, Rd at elevated CO2 has been found to increase significantly in some studies, but to decrease significantly in others (Amthor, 1991; Poorter et al., 1992; Drake et al., 1999; Amthor, 2000). The importance of Rd as a component of the plant and ecosystem carbon budget, however, must not be overlooked, since up to 50% of carbon assimilated by photosynthesis can be lost through respiration (Kira, 1975; Amthor, 1989; Bunce, 1994). Despite their different responses to elevated CO2, photosynthesis and respiration are two interdependent processes, and both provide reductants and ATP to meet energy demands for growth and maintenance (Kromer, 1995; Foyer & Noctor, 2000). It is therefore reasonable to expect a possible differential effect of CO2 enrichment on the respiration of male and female P. tremuloides plants, if their photosynthesis differs in responding to elevated CO2. To our knowledge, no studies have been conducted to investigate the effects of elevated CO2 on Rd of male and female individuals of any dioecious species.
The primary objective of our study was to examine the carbon assimilation physiology and growth of male and female P. tremuloides trees grown at ambient or elevated CO2. We chose P. tremuloides, a dioecious woody species, because it is the most widespread tree species in North America (Fowells, 1965) and is important both ecologically and economically (Farmer, 1996). Although the trees in our study did not reach reproductive size, gender-related differences in physiology and growth in dioecious species often occur before the onset of flowering (Bourdeau, 1958). We hypothesized that female trees would have higher photosynthetic and respiratory rates than male trees, and that soil nitrogen (N) availability would interact with CO2 levels in affecting physiological and growth responses to CO2 enrichment. Our secondary objective was to gain insight into the mechanisms of CO2 effects on leaf Rd by investigating the relationship between leaf Rd and leaf chemistry. We hypothesized that leaf Rd would be positively related to the supply of respiratory substrates, or leaf carbohydrates, as well as to the demand for energy from respiration, indicated by leaf N level.
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We found significant differences in photosynthetic rates between male and female P. tremuloides at both ambient and elevated CO2; males were more responsive to elevated CO2 than were females. Our results lead us to reject our initial hypothesis that females would have higher A than males. Since gender difference in P. tremuloides occurs before the onset of flowering, the different reproductive costs of males and females (Lloyd & Webb, 1977; Allen & Antos, 1988) may not be the only reason for the physiological and ecological differences between genders. The male P. tremuloides trees were able to sustain a higher rate of carbon assimilation in part because they had higher stomatal conductance throughout the season. The males also had some biochemical characteristics that enabled them to fix CO2 at a higher rate than females. For instance, Rubisco in the leaves of male trees had a higher maximum rate for CO2 fixation as shown by a higher Vcmax. At higher Ci, male trees also were less limited by rates of ribulose-1.5-biphosphate (RuBP) regeneration and triose phosphate utilization because they had higher Jmax and PiRC. In addition, since soil N availability did not affect these responses, it is likely that gender-specific differences in carbon assimilation at high CO2 will persist, even when soil nutrient levels are low. This is important because low soil N availability is a major factor limiting carbon assimilation at elevated CO2 (Gunderson & Wullschleger, 1994; Curtis et al., 2000). However, other environmental factors such as temperature might also affect the responses of dioecious species to elevated CO2. Jones et al. (1999) found that elevated-CO2-grown female S. arctica had lower A than males at 12°C, while the opposite was true at 5°C.
Although male P. tremuloides had higher A compared with females throughout the growing season, females had significantly greater biomass components than males in low-N soil and at ambient CO2. This discrepancy in the A and biomass responses to elevated CO2 was most likely due to the greater leaf area and therefore greater carbon assimilation in females in low-N soil. Another possible explanation for this discrepancy was the lower stem Rda in females than in males. Stem Rda can comprise a sizeable portion of the whole plant carbon budget because of the large stem surface area. In young Betula pendula trees, for example, stem respiration accounted for as much as 23% of total plant respiration (Wang et al., 1998). Higher stem Rda in male trees could therefore have offset the higher A and resulted in lower biomass accumulation in male trees. Our results are consistent with those of Laporte & Delph (1996), who found that male Silene latifolia had consistently higher A, but failed to grow larger than females. Sakai & Burris (1985) found that female P. tremuloides clones growing in nutrient-poor soils near our research site had larger numbers of ramets and greater basal area than did male clones, indicating more vegetative growth by females in this habitat. In contrast, Dawson & Ehleringer (1993) observed greater vegetative growth in male than female A. negundo in xeric habitats, even when males showed lower A than females.
We observed significant negative adjustment of photosynthesis at high CO2 in both males and females, but there was little difference in adjustment between genders, notwithstanding that males had a smaller reduction in Vcmax, Jmax and PiRC than females at elevated CO2. The magnitude of photosynthetic adjustment found in our study (14–16%) was smaller than the overall 21% negative adjustment across 39 species in 20 studies reported by Gunderson & Wullschleger (1994). In a study with hybrid poplar (Populus × euramericana) on the same research site, Curtis et al. (1995) found that the level of adjustment ranged from 9% stimulation to 52% reduction, with the average being an 18% reduction in photosynthetic capacity. Negative adjustment of A was also more profound in P. × euramericana grown in low- than in high-N soil. In a meta-analysis of 24 studies, we found significant negative adjustment in plants grown in small pots (< 0.5 l), but no consistent evidence for overall negative adjustment in plants grown in large pots (Curtis & Wang, 1998). It seems that photosynthetic adjustment is a common but not universal response by plants to growth under high concentrations of atmospheric CO2.
We found no CO2 effect on gs in either male or female trees, although males had significantly higher gs than females, with the difference being greater at elevated than at ambient CO2. This is different from what we observed in well-watered male P. tremuloides genotypes, where elevated CO2 significantly reduced the gs of plants in both low- and high-N soil (Wang et al., 2000). In both studies, however, we found that plants with less sensitive stomatal responses to CO2 enrichment were more responsive photosynthetically to elevated CO2; in other words, the less the reduction of gs at high CO2, the greater the photosynthetic responses. The variation in gs response to CO2 enrichment in P. tremuloides is typical of the substantial variation in gs responses to CO2 observed among woody plants. We also found that females had greater fine root mass than males at elevated CO2. Since some areas are likely to become drier with rising atmospheric CO2 and increased evaporation (Rind et al., 1990), forest ecosystems in these regions will probably be subject to more frequent and/or severe drought stress. Greater fine root mass and lower stomatal conductance could allow female trees to develop a competitive edge over male trees in chronically dry regions or during drought.
Elevated CO2 can have direct and indirect effects on Rd (Amthor, 1991; Thomas & Griffin, 1994). What was observed in our study was primarily the indirect effect of elevated CO2 because leaf Rd was measured at growth CO2 concentrations. The increased daytime leaf Rda at elevated CO2 that we observed can be explained in part by lower SLA, hence greater leaf biomass per unit leaf area, and greater total nonstructural carbohydrate (TNC) in higher-CO2-grown plants. Since enzymes catalysing respiratory reactions are generally present in amounts that exceed that required to explain the observed rates of respiration in mature leaves (Amthor, 1991), higher leaf carbohydrate content at high CO2 commonly leads to higher leaf Rda (Azcon-Bieto & Osmond, 1983; Farrar, 1985; Hrubec et al., 1985; Amthor, 1989; Lambers et al., 1989; Thomas et al., 1993). Higher carbohydrate content might also enhance leaf Rd through increased phloem loading and translocation (Amthor, 2000), which require a higher rate of respiration. The lower leaf Rda observed in elevated-CO2-grown plants in some studies (Lambers et al., 1989; Baker et al., 1992; Wullschleger & Norby, 1992) has been attributed to lower leaf N or protein content compared with ambient-CO2-grown plants. We found no correlation between daytime leaf Rda and N content, which was significantly lower in elevated-CO2-grown plants, but we did observe a positive correlation between leaf Rda and starch content, which was significantly higher in elevated-CO2-grown plants. We initially hypothesized that leaf Rda would be positively correlated to both starch and N contents, but our results suggest that the respiratory substrate level is more important than the total leaf N content in determining leaf Rda in fast-growing P. tremuloides. This suggestion is supported by the results of Azcon-Bieto & Osmond (1983), who found a positive correlation between Rda and carbohydrate level and between Rda and A, which has shown a consistent stimulation by elevated CO2 in a variety of C3 species.
In summary, we found differential effects of elevated CO2 on carbon assimilation in the male and female P. tremuloides trees that we studied. As a result, the productivity, distribution and population structure of P. tremuloides may be altered as atmospheric CO2 concentration rises if the gender difference is widespread. Because of the prominence of dioecious species in terrestrial ecosystems, gender-specific physiological responses provide a new mechanism by which community structure and functioning might be affected by atmospheric CO2 enrichment.