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Different responses to shade of evergreen and deciduous oak seedlings and the effect of acorn size
Acta Oecologica 20 (6) (1999) 579−586 / © 1999 Éditions scientifiques et médicales Elsevier SAS. All rights reserved S1146609X99001034/FLA
Different responses to shade of evergreen and deciduous oak seedlings and the effect of acorn size Guo Ke a,b, Marinus J.A. Werger a* a
Department of Plant Ecology and Evolutionary Biology, Utrecht University, P.O. Box 800.84, 3508 TB Utrecht, the Netherlands. b Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China. * Corresponding author (fax: +31 30 2518366; e-mail: [email protected])
Received May 11, 1999; revised August 19, 1999; accepted September 13, 1999
Abstract — An evergreen oak species, Cyclobalanopsis multinervis, and a deciduous oak species, Quercus aliena var. acuteserrata were grown from acorns under two light levels (full sunlight and shade at about 18 % of full sunlight, simulating the light intensities in forest clearings and gaps, respectively) for one growing season. Three hypotheses were tested: (i) the deciduous species grows faster than the evergreen species in forest gaps and clearings; (ii) the deciduous species responds more strongly in terms of growth and morphology to variation in light climate than the evergreen species; and (iii) seedling size is positively correlated to acorn size. The results showed: (i) at both light levels, the deciduous seedlings gained significantly more growth in biomass and height than the evergreen seedlings; (ii) both species produced significantly more biomass in full sunlight than in shade, without showing any significant difference in height between treatments. Increase in light intensity improved the growth of the deciduous seedlings more strongly; (iii) at a similar age, the deciduous seedlings showed a greater response in leaf morphology and biomass allocation to variation in light levels, but when compared at a similar size, biomass allocation patterns did not differ significantly between species; (iv) bigger acorns tended to produce larger seedlings, larger leaf sizes and more leaf area, between and within species. These differences demonstrate that the deciduous species is gap-dependent and has the advantage over the evergreen species in forest gaps and clearings. © 1999 Éditions scientifiques et médicales Elsevier SAS Beech forest / deciduous species / evergreen species / light climate / morphological plasticity / seedling growth / seedling survival / Cyclobalanopsis multinervis / Quercus aliena var. acuteserrata
1. INTRODUCTION Most beech forests in the northern hemisphere are typically deciduous forests of the temperate zone [15]. Chinese beech forests, however, do not occur in the temperate zone but on the mountains of the subtropical zone [3, 15, 21, 22]. There, broad-leaved evergreen forests occur at lower altitudes, while needle-leaved forests occupy the higher parts. Beech forests occur in the transition zone between these forest belts, and contain many evergreen tree species [21]. In spite of the dominance of beech species in these forests, many other tree species can be found in the canopy. The species composition and structure of these mixed forests vary from place to place ([3]; pers. obs.). It is still largely unknown how these tree species regenerate. Cyclobalanopsis multinervis and Quercus aliena var. acuteserrata are two oak species occurring com-
monly in beech (Fagus engleriana and F. hayatae subsp. pashanica) forests around 1 400 m a.s.l. in the Dabashan Mountains, Sichuan, China. Below 1 400 m, C. multinervis, an evergreen oak, often occurs in the forest canopy. Above 1 400 m, it gradually decreases in tree size and frequency and occurs only under the canopy as the altitude increases and the temperature decreases. In contrast, adult trees of Q. aliena var. acuteserrata, a deciduous oak, are usually present in the canopy of the beech forests around 1 400 m, but its seedlings can hardly be found in the understorey of those forests [3]. The contrast in occurrence and population structure of the two oak species in the forests around 1 400 m indicates ecological differences between them. The persistence of the evergreen oak in the shade of the closed canopy of the beech forests suggests that it should be a shade-tolerant species, or a ‘stress-tolerant
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species’ (cf. [7, 8]). Absence of seedlings and juveniles of the deciduous oak under the closed canopy of the beech forests and frequent occurrence of its adults in the canopy suggest that its regeneration might take place in forest gaps or clearings, and it should be a less shade-tolerant species. According to Grime [8], the potential growth rate and the phenotypic plasticity of a stress-tolerant plant (associated with high stress and low disturbance) are low in contrast to those of a less stress-tolerant plant, i.e. a competitive plant (associated with low stress and low disturbance) or a ruderal plant (associated with low stress and high disturbance). From this perspective, growth and phenotypic plasticity of the two oak species can be expected to differ in response to variation in light climate. Thus, the following hypotheses are addressed: (i) the deciduous species grows faster than the evergreen species in forest gaps and clearings; (ii) the growth rate and morphology of the deciduous species are more plastic in response to variation in light climates. In addition, acorn size (fresh weight) varies substantially between and within both species. At the seedling stage, growth and survival are often affected by the amount of reserves stored in the seed [10, 16]. Larger acorns are regarded to produce greater seedlings [2]. Seedlings from larger acorns grow stronger and survive better [20]. Accordingly, we also hypothesize that larger acorns produce larger seedlings and this is valid for variation in acorn size between and within species. To test these hypotheses, we investigated the two oak species, as regards differences in seedling size, biomass allocation and a number of morphological traits related to light capture at two light levels simulating the light intensities in forest gaps and forest clearings. The purpose of this study is to examine the regeneration and growth strategies of the two oak species and improve the understanding of seedling performance and species regeneration in natural beech forests of subtropical China. 2. METHODS The experiment was performed at Daba Forest Farm, Sichuan (32°42’ N, 106°55’ E, 1 400 m a.s.l.), where the forests are mainly dominated by Fagus engleriana, F. hayatae subsp. pashanica, Quercus aliena var. acuteserrata, Carpinus cordata var. chinensis, C. fargesiana, etc. Acorns were collected on October 4th 1995 from the beech forest. The acorns of the deciduous species Q. aliena var. acuteserrata (‘Qa’ in brief) were from one tree and the acorns of the evergreen species C.
K. Guo, M.J.A. Werger
multinervis (Cm) were picked from a patch of forest floor (1995 was a lapse year for these species, and not many individuals were fruiting). These acorns were then put into a pot and buried in the soil at a depth of 20 cm in order to store them in a forest-like environment. On April 30th 1996, the acorns were dug up and 100 acorns of the deciduous oak and fifty acorns of the evergreen oak were weighed individually and planted in pots filled with about 1.5 L soil from the forest floor. The soil was well mixed before. One acorn was used for each pot. The pots were randomly divided into two groups. One group was exposed to full sunlight (‘light’ in brief), while the other group was put beneath a bamboo screen that created a light climate of about 18 % of full sunlight (‘shade’ in brief). The experimental set-up thus consisted of two species and two light levels arranged in a factorial design (abbreviation used to indicate treatments: Cm-light, Cm-shade, Qa-light and Qa-shade). The average acorn fresh weight of the deciduous species (Qa) was 1 911 ± 49 mg (mean ± SE), which was significantly higher than the mean acorn weight (1 281 ± 58 mg) of the evergreen species (one-way ANOVA, F = 64.70, P < 0.001). There was no difference in acorn weight within species between the two light levels (planned comparison showed F = 0.984, P = 0.325 for the deciduous species and F = 0.956, P = 0.332 for the evergreen species). Dates of emergence of each seedling and start of leaf flush were recorded. Of the deciduous species, 47 in shade and 50 in light emerged around May 30th. Of the evergreen species, 24 in each light treatment emerged around June 12th. The apical buds of some seedlings recurrently burst and some new leaves flushed in summer or autumn after a period of earlier growth. Such newly developed shoots have been called ‘lammas shoots’ [23]. Seedlings having an additional flush were noted. Biomass allocation patterns have been shown to change throughout ontogeny [4]. To compare the two species at similar size, fourteen or sixteen seedlings (seven or eight in each light treatment) of the deciduous species were harvested at 3-week intervals after emergence because the deciduous species was assumed to grow faster than the evergreen species. In this way, harvests were performed four times and 58 seedlings (29 in each light treatment) were harvested before the final harvest around September 25th. At the final harvest, 34 deciduous seedlings (sixteen in shade and eighteen in light) were harvested. Five seedlings got damaged and were excluded. For the evergreen species, two seedlings in the shade were Acta Oecologica
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damaged before September and the 46 remaining seedlings (22 in shade and 24 in light) were harvested around September 25th. At harvest time, shoot height, length of lammas shoot and leaf dimensions (i.e. leaf length Ll, and leaf width Lw) were measured. The dry mass of roots, stems, leaves and of the remains of cotyledons and acorn shells were weighed after drying to constant mass at about 90 °C. Total seedling biomass refers to the sum of root, stem and leaf mass without the remains of cotyledons and shells. Leaf area (LA) was calculated by using the following linear regressions that were based on exact measurements. For Cm: LA = 15 + 0.605 × Ll × Lw ~ n = 11, R 2 = 99.1 %, P < 0.001 !
For Qa: LA = –16 + 0.649 × Ll × Lw ~ n = 432, R 2 = 98.6 %, P < 0.001 !
Leaf size was calculated for each individual, i.e. mean area per leaf of a seedling. Specific leaf area (SLA), leaf area ratio (LAR), leaf mass ratio (LMR) and root mass ratio (RMR) were calculated according to the formulas given by Hunt [11]. Minitab (release 9.2) and Statistica (release 4.5) were used to perform the calculations and statistical tests. Planned comparisons for acorn size and experimental results were done by using Statistica. For the final harvest, a general linear model (two-way ANCOVA) was used to test for effects of acorn fresh weight, species identity, light treatment and the interaction between species and light. Values of biomass, root mass, stem mass, leaf mass, leaf area and shoot:root ratio were transformed by square root, and the values of leaf number, leaf size (area per leaf), specific leaf area and leaf area ratio were logarithmically transformed in order to meet the assumptions of ANCOVA [18]. Bartlett Chi-square test was used to examine the homogeneity of variance and F-test was used to examine the parallelism of regression equations in the analysis. In terms of biomass, the evergreen seedlings at the final harvest were most similar to the deciduous seedlings on their sixth week after emergence. For this reason, the deciduous seedlings harvested at the sixth week after emergence and the evergreen seedlings at final harvest were used to compare the two species at similar size in the same general linear model of ANCOVA without transformation of the original data. Vol. 20 (6) 1999
3. RESULTS 3.1. Height and biomass In terms of shoot height and biomass, big acorns tended to produce large seedlings. This was true for both species (table II , figure 1). Seedlings of the evergreen species C. multinervis remained significantly smaller than the seedlings of the deciduous species Q. aliena at the final harvest (tables I, II, figure 1). Seedling biomass of the evergreen species at the final harvest was not more (df = 1 and 55, F = 2.051, P = 0.158) than that of the deciduous species at the sixth week after emergence (table I, figure 2). Light did not significantly affect final seedling height (tables I, II). However, it differently affected recurrent flushes of shoot and leaves in the deciduous species. Among the 46 evergreen seedlings, 21 out of the 22 in shade and 22 out of the 24 in light had an additional flush as from July, but among the deciduous seedlings, none of the sixteen seedlings in shade and only seven out of the eighteen in light had an additional flush. This resulted in a marked increase in the final height of seedlings by, on average, 11.4 ± 0.9, 18.4 ± 1.6 and 8.6 ± 2.9 mm (mean ± SE) for Cmshade, Cm-light and Qa-light plants, respectively. In both species, light significantly affected seedling biomass at the final harvest (table II). Seedlings in light gained more biomass than seedlings in shade (table I). This response was strikingly stronger in the deciduous seedlings than in the evergreen seedlings, as was indicated by the highly significant effect of the interaction between species and light on biomass (table II). In the deciduous species, mean biomass of seedlings grown in light was about 228 % that of seedlings in shade, whereas for the evergreen it was about 147 % (table I). The mass of cotyledon remains at the final harvest tended to be less in shade than in light (table I), but not significant (table II). 3.2. Leaf traits At final harvest, the evergreen seedlings had relatively more leaves than the deciduous seedlings at the same light levels, but their leaves were significantly smaller (tables I, II). The mean leaf size of the evergreen seedlings was only about one-third to onequarter that of the deciduous seedlings. This resulted in a smaller leaf area per seedling in the evergreen as compared to the deciduous species (tables I, II, figure 1). The seedlings of both species developed significantly more but smaller leaves in light than in shade (tables I, II, figure 1). As a result light did not significantly affect total leaf area per seedling in both species (table II, figure 1).
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Table I. Seedling height (mm), biomass (mg) and its components, cotyledon mass (mass of cotyledon remains), leaf number (leaves per plant), leaf size (area per leaf, mm2), leaf area (leaf area per plant, mm2), specific leaf area (SLA, mm2⋅mg–1), leaf area ratio (LAR, mm2⋅mg–1), leaf mass ratio (LMR), root mass ratio (RMR) and shoot to root ratio (S/R) of two species (Cm, Cyclobalanopsis multinervis; Qa, Quercus aliena var. acuteserrata) at the two light treatments at the final harvest. Values are mean ± SE. Values in italics in brackets are the results at the sixth week after emergence for the deciduous species. Species light levels Height Biomass Root mass Stem mass Leaf mass Cotyledon mass Leaf number Leaf size Leaf area SLA LAR LMR RMR S/R
Cm shade
Cm light
56 ± 4 498 ± 59 206 ± 27 74 ± 11 218 ± 24 193 ± 17 4.1 ± 0.2 630 ± 62 2 554 ± 224 12.6 ± 0.5 5.69 ± 0.30 0.45 ± 0.01 0.41 ± 0.01 1.47 ± 0.05
68 ± 4 731 ± 67 307 ± 31 116 ± 12 308 ± 29 212 ± 12 5.3 ± 0.3 608 ± 56 3 045 ± 237 10.2 ± 0.3 4.36 ± 0.17 0.43 ± 0.01 0.41 ± 0.01 1.44 ± 0.05
Leaf number was not significantly affected by acorn size (table II), but seedlings from large acorns tended to develop relatively large leaves (table II, figure 1). Thus, total leaf area per seedling tended to increase with the increase in acorn size (table II, figure 1). Specific leaf area of the deciduous species was significantly larger than that of the evergreen species. The specific leaf area was markedly larger in shade than in light for both species and that of the deciduous species responded more strongly to changes in light levels than that of the evergreen species (tables I, II). At final harvest, leaf area ratio of the deciduous seedlings was significantly smaller than that of the evergreen seedlings in both light levels (tables I, II). Leaf area ratio of the deciduous seedlings, however, was significantly greater than that of the evergreen seedlings when comparing the two species at similar size, for example, comparing the deciduous seedlings harvested at the sixth week after emergence with the evergreen seedlings at final harvest (table I; df = 1 and 55, F = 151.365, P < 0.001). Shade-grown seedlings of both species had a higher leaf area ratio than seedlings grown in full sunlight (tables I, II). 3.3. Biomass allocation At final harvest, the evergreen species had partitioned proportionally more biomass to leaves than the deciduous species. The leaf mass ratio of the evergreen species was about twice that of the deciduous species,
Qa shade 94 ± 3 1 256 ± 109 745 ± 74 149 ± 13 360 ± 29 184 ± 12 2.9 ± 0.2 2 471 ± 247 6 877 ± 556 19.1 ± 0.6 5.52 ± 0.18 0.29 ± 0.01 0.59 ± 0.01 0.72 ± 0.05
(103 ± 5) (875 ± 61) (384 ± 35) (112 ± 5) (379 ± 29) (291 ± 13) (2.7 ± 0.2) (3 554 ± 226) (9 603 ± 790) (25.3 ± 0.8) (10.93 ± 0.40) (0.43 ± 0.01) (0.44 ± 0.01) (1.30 ± 0.07)
Qa light 99 ± 3 2 868 ± 155 2 082 ± 118 256 ± 15 531 ± 37 216 ± 12 4.2 ± 0.4 1 776 ± 154 6 904 ± 417 13.1 ± 0.3 2.41 ± 0.10 0.18 ± 0.01 0.73 ± 0.01 0.38 ± 0.02
(87 ± 8) (811 ± 124) (378 ± 61) (107 ± 17) (326 ± 48) (286 ± 36) (3.1 ± 0.3) (1 628 ± 231) (4 956 ± 725) (15.2 ± 0.5) (6.15 ± 0.33) (0.40 ± 0.01) (0.46 ± 0.02) (1.17 ± 0.08)
while the root mass ratio of the evergreen species was only about two-thirds that of the deciduous species. The allocation patterns resulted in a significantly higher shoot:root ratio in the evergreen seedlings as compared to the deciduous seedlings (tables I, II). Light treatments had a strong effect on biomass allocation pattern at the final harvest (tables I, II). The high significance of the interactive effect between species and light on LMR, RMR and S/R indicated that the two species had different responses in these ratios to changes in light (table II). The deciduous species showed a stronger response in all these ratios than the evergreen species (table I). The biomass allocation patterns of the deciduous seedlings exhibited pronounced changes throughout the growing season. The leaf mass ratio and shoot:root ratio of the deciduous seedlings decreased and the root mass ratio increased with time, or with seedling size (table I). At similar size, biomass allocation patterns of the two species were very similar. Comparing the evergreen seedlings at the final harvest with the deciduous seedlings harvested at the sixth week after emergence, for example, there was no significant difference in each of these ratios (table I; df = 1, 55, F = 0.257, 0.873 and 1.149, P = 0.614, 0.354 and 0.288 for leaf mass ratio, root mass ratio and shoot:root ratio, respectively). Acta Oecologica
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Figure 1. Seedling size in relation to acorn fresh weight of Cyclobalanopsis multinervis and Quercus aliena var. acuteserrata under full sunlight and shade treatments. The significance levels of the regressions are given as: ns P > 0.05; * P < 0.05; ** P < 0.01; *** P < 0.001.
4. DISCUSSION
4.1. Length of growing season and growth rates
The results of this experiment demonstrate that seedlings of the deciduous species grew faster at both light levels simulating the light climates at forest clearings and gaps, and responded more strongly in growth rate and morphology to variation in light climate than the evergreen species. Greater plasticity of the deciduous seedlings in morphology and physiology allows the deciduous species to profit more from high light conditions than the evergreen species. For this reason, the deciduous species has the advantage over the evergreen species in forest gaps and clearings.
Considering the striking difference in seedling size (biomass) at final harvest between the two species in this experiment, annual growth of the deciduous seedlings is expected to be higher than that of the evergreen seedlings. The growing period of the evergreen species has no clear initial and end dates but it is most likely to last longer than that of deciduous species (cf. [9]). In Daba Forest Farm, the deciduous oak species has an annual growing period, from bud break to leaf shed, of about 160 d, while the evergreen oak species sustains leaves during the whole year.
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Table II. Two-way ANCOVA results of height (mm), biomass and its components, mass of cotyledon remains, leaf number (leaves per plant), leaf size (area per leaf), leaf area (leaf area per plant), specific leaf area (SLA), leaf area ratio (LAR), leaf mass ratio (LMR), root mass ratio (RMR) and shoot to root ratio (S/R) at the final harvest. A general-linear-model (Minitab release 9.2) was used to carry out the analysis, with species identity and light level as the two factors and the acorn fresh weight as covariate. To satisfy the assumptions of ANCOVA (including the homogeneity of variance and the parallelism of regression equations), some original values were transformed before performing the ANCOVA. The degree of freedom is 1 for each factor and the interaction and is 75 for the error. Items
Transformation
Height
–
Biomass
Square-root
Root mass
Square-root
Stem mass
Square-root
Leaf mass
Square-root
Cotyl. mass
–
Leaf number
Logarithm
Leaf size
Logarithm
Leaf area
Square-root
SLA
Logarithm
LAR
Logarithm
LMR
–
RMR
–
S/R
Square-root
F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P
It is, however, not to be expected that the evergreen species realizes much more growth during the prolonged growing season (or beyond the growing season of the deciduous species), considering the abundant snow cover and low temperatures during winter at Daba at 1 400 m altitude. In Beibei, Chongqing (about 215 m a.s.l. and three degrees south of Daba), Cornelissen [5] found that winter growth in height and leaf area were virtually nil in all three broad-leaved evergreen species in his experiment, Castanopsis fargesii, Sloanea leptocarpa and Elaeocarpus japonicus from an evergreen broad-leaved forest of subtropical China. Also Schulze et al. [17], in a comparative study between Fagus sylvatica (deciduous) and Picea abies (evergreen), found that the effect of a prolonged
Seedsize
Species (Sp)
Light (L)
Sp × L
23.877 0.000 91.465 0.000 77.613 0.000 72.653 0.000 61.210 0.000 246.066 0.000 1.634 0.205 28.249 0.000 43.200 0.000 14.479 0.000 20.208 0.000 4.672 0.034 2.598 0.111 3.053 0.085
22.130 0.000 79.862 0.000 185.485 0.000 6.968 0.010 0.372 0.544 119.286 0.000 19.686 0.000 58.289 0.000 35.365 0.000 120.126 0.000 6.767 0.011 118.167 0.000 267.410 0.000 213.075 0.000
3.777 0.056 107.095 0.000 153.754 0.000 36.759 0.000 17.176 0.000 1.922 0.170 18.695 0.000 8.943 0.004 0.028 0.867 79.479 0.000 170.614 0.000 25.564 0.000 44.194 0.000 26.358 0.000
1.967 0.277 48.290 0.000 96.148 0.000 3.298 0.073 0.863 0.356 0.553 0.460 0.872 0.353 3.006 0.087 0.941 0.335 8.032 0.006 55.407 0.000 13.138 0.001 41.762 0.000 23.875 0.000
growing season in spruce was very small, and its annual carbon gain would be reduced by only 9 % if the growing season would be the same length as for the beech. In this experiment, after 15 weeks of growth the evergreen seedlings were about the same size or even slightly smaller than the deciduous seedlings that had been growing for only 6 weeks. At final harvest, the biomass of the evergreen seedlings was on average less than half that of the deciduous seedlings. These striking differences indicate that seedlings of the deciduous species, which were characterized by a greater leaf area ratio (LAR) at a similar size and a larger specific leaf area (SLA) than the evergreen species, had a considerably higher annual growth, Acta Oecologica
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sunlight they were considerably different (0.415 and 0.240 mg⋅mm–2, respectively). This result corresponds to the findings of Bazzaz and Carlson [1] and Osunkoya et al. [14] that plasticity of physiological parameters is generally higher in gap-dependent species (early successional species) than in shade-tolerant species (late successional species). Thus, the deciduous species appears to be more plastic both in terms of morphological and physiological responses to variation in light climate. 4.3. Biomass allocation
Figure 2. Seedling biomass of the deciduous species at the two light levels in the growing season. Standard errors are shown only upwards.
thereby confirming our first hypothesis. This corresponds with the results of Cornelissen et al. [6] who have shown that deciduous species grow consistently faster than evergreen species and that mean relative growth rates were closely correlated with leaf area ratio and specific leaf area in eighty woody species from the British Isles and northern Spain. 4.2. Morphology and plasticity Leaf size and specific leaf area are two important leaf traits that vary with environmental conditions. In this experiment, the deciduous seedlings showed a greater change in leaf size and specific leaf area than the evergreen seedlings. Although both species had smaller leaf sizes and specific leaf areas in full sunlight than in shade, the differences in leaf sizes between light treatments were not significant for the evergreen species. This shows that the deciduous oak, the faster growing species, has a greater plasticity in these leaf traits in response to light climate than the evergreen seedlings. Such a positive correlation between the degree of plasticity and relative growth rates has previously been reported for herbaceous species [12]. The leaf area (per seedling) did not significantly differ at final harvest between light levels in either species (tables I, II). The difference in biomass production between light treatments, however, was more pronounced in the deciduous than in the evergreen species. This suggests that the net assimilation rate (NAR) shows a greater response to light in the deciduous species. This interpretation gains further support from data on the ratio of biomass to leaf area at the final harvest. In shade, the ratios of the deciduous seedlings and the evergreen seedlings were similar (0.183 and 0.195 mg⋅mm–2, respectively), but in full Vol. 20 (6) 1999
Biomass allocation patterns change throughout ontogeny [4]. This shift resulted in the considerable differences in biomass allocation patterns at final harvest between two species and between two light treatments for the deciduous species. This point of view was supported by the small differences in the ratios between two species at a similar seedling size and the changes in leaf mass ratio, root mass ratio and shoot:root ratio throughout the growing season. The changes in these ratios were stronger in light than in shade. This is consistent with the faster growth and larger seedling size (biomass) at final harvest in light than in shade. 4.4. Effect of acorn size Bigger acorns tended to produce larger seedlings. This tendency was found for both species, although in full sunlight, the regression of seedling height on acorn fresh weight was not statistically significant for either species (figure 1). This is consistent with the results of other studies on seedling survival and growth of oaks. Bonfil [2] found a positive correlation between seed mass and seedling survival and growth in Quercus rugosa and Q. laurina and the same was found for seedlings of Q. dealbata and Q. griffıthii by Tripathi and Khan [20]. Lone and Jones [13] found that the species with larger mean acorn size produced larger seedlings in a study of fourteen oak species in North America. Sonesson [19], however, concluded that growth and survival of Q. robur seedlings were independent of their cotyledons from the time of first leafing onwards (about 1 week after emergence). We plotted cotyledon dry mass of the deciduous species against harvest time and found that before the third week after emergence, the cotyledon mass was reduced by about three-quarters of the total mass reduction of the entire growing season. This suggests that the translocation of the acorn reserves to the growing seedling mainly happened at the early stage of seedling development before the first leaf set is displayed. However, we also found that some seedlings of the deciduous species, whose cotyledons were removed 1 week after emergence without destroying
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the seedlings, developed very slowly and survived only about 2 months under the shade of the closed forest canopy, while most of the seedlings with cotyledons survived the entire growing season. This demonstrates that cotyledon reserves are still very important for a seedling for longer than 1 week after emergence when the seedling grows under unfavourable conditions. In conclusion, the results of this experiment showed that the deciduous species Q. aliena var. acuteserrata had many characteristics in common with less shadetolerant (or competitive) plants and the evergreen species C. multinervis had many characteristics of shade-tolerant plants [7, 8]. This is consistent with the occurrence of the two species in the beech forests in Daba. The adult trees of the deciduous oak in the forests probably grow from forest gaps or disturbed clearings, and the evergreen oak under the canopy may regenerate and can persist in the understorey. Acknowledgments We thank Dr H. Huber, Dr J.F. Stuefer, two anonymous referees and the associate editor, Dr H. Koelewijn, for their help in statistical analysis and constructive comments on an early version of the manuscript. Guo Ke thanks Prof. Li Bosheng in Beijing and Mr Yue Weiyuan, Zhou Jun, Tian Liangmao, Li Rensheng, Xu Yuanjun in Daba Forest Farm, Sichuan, China, for their practical help in this study. Financial support by the National Science Foundation of China, the Chinese Academy of Sciences and the Royal Netherlands Academy of Arts and Sciences are acknowledged.
REFERENCES [1] Bazzaz F.A., Carlson R.W., Photosynthetic acclimation to variability in the light environment of early and late successional plants, Oecologia 54 (1982) 313–316. [2] Bonfil C., The effects of seed size, cotyledon reserves, and herbivory on seedling survival and growth in Quercus rugosa and Q. laurina (Fagaceae), Am. J. Bot. 85 (1998) 79–87. [3] Cao K.F., Fagus dominance in Chinese montane forests: Natural regeneration of Fagus lucida and Fagus hayatae var. pashanica, Ph.D. thesis, Wageningen Agricultural University, the Netherlands, 1995. [4] Coleman J.S., McConnaughay K.D.M., Ackerly D.D., Interpreting phenotypic variation in plants, Trends Ecol. Evol. 9 (1994) 187–191. [5] Cornelissen J.H.C., Interactive effects of season and light environment on growth of evergreen tree seedlings in the humid subtropics, Can. J. Bot. 74 (1996) 589–598.
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[6] Cornelissen J.H.C., Diez P.C., Hunt R., Seedling growth, allocation and leaf attributes in a wide range of woody plant species and types, J. Ecol. 84 (1996) 755–765. [7] Cornelissen J.H.C., Castro-Diez P., Carnelli A.L., Variation in relative growth rate among woody species, in: Lambers H., Poorter H., Van Vuuren M.M.I. (Eds.), Inherent Variation in Plant Growth. Physiological Mechanisms and Ecological Consequences, Backhuys Publishers, Leiden, the Netherlands, 1998, pp. 363–392. [8] Grime J.P., Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory, Am. Nat. 111 (1977) 1169–1194. [9] Hashimoto R., Shirahata M., Comparative study of leaf carbon gain in saplings of Thujopsis dolabrata var. hondai and Quercus mongolica var. grosseserrata in a cool-temperate deciduous forest, Ecol. Res. 10 (1995) 53–64. [10] Hewitt N., Seed size and shade-tolerance: a comparative analysis of North American temperate trees, Oecologia 114 (1998) 432–440. [11] Hunt R., Plant Growth Analysis, Edward Arnold, London, 1978. [12] Lambers H., Poorter H., Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences, Adv. Ecol. Res. 23 (1992) 187–261. [13] Lone T.J., Jones R.H., Seedling growth strategies and seed size effects in fourteen oak species native to different soil moisture habitats, Tree 11 (1996) 1–8. [14] Osunkoya O.O., Ash J.E., Hopkins M.S., Graham A.W., Influence of seed size and seedling ecological attributes on shade-tolerance of rain-forest tree species in northern Queensland, J. Ecol. 82 (1994) 149–163. [15] Peters R., Beech Forests, Kluwer Academic Publishers, Dordrecht, 1997. [16] Saverimuttu T., Westoby M., Seedling longevity under deep shade in relation to seed size, J. Ecol. 84 (1996) 681–689. [17] Schulze E.D., Fuchs M., Fuchs M.I., Spatial distribution of photosynthetic capacity and performance in a mountain spruce forest of Northern Germany. III. The significance of the evergreen habit, Oecologia 30 (1977) 239–248. [18] Sokal R.R., Rohlf F.J., Biometry, W.H. Freeman and Company, New York, 1981. [19] Sonesson L.K., Growth and survival after cotyledon removal in Quercus robur seedlings, grown in different natural soil types, Oikos 69 (1994) 65–70. [20] Tripathi R.S., Khan M.L., Effects of seed weight and microsite characteristics on germination and seedling fitness in two species of Quercus in a subtropical wet hill forest, Oikos 57 (1990) 289–296. [21] Wu Z.Y. (Ed.-in-Chief), The Vegetation of China, Scientific Press, Beijing, 1980, in Chinese. [22] Zhou G.L., Li X.D., Species composition and structure of Chinese beech forests, Nat. Hist. Res. 3 (1994) 21–26. [23] Zimmermann M.H., Brown C.L., Trees: Structure and Function, Springer-Verlag, New York, 1971.
Acta Oecologica
Different responses to shade of evergreen and deciduous oak seedlings and the effect of acorn size Guo Ke a,b, Marinus J.A. Werger a* a
Department of Plant Ecology and Evolutionary Biology, Utrecht University, P.O. Box 800.84, 3508 TB Utrecht, the Netherlands. b Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China. * Corresponding author (fax: +31 30 2518366; e-mail: [email protected])
Received May 11, 1999; revised August 19, 1999; accepted September 13, 1999
Abstract — An evergreen oak species, Cyclobalanopsis multinervis, and a deciduous oak species, Quercus aliena var. acuteserrata were grown from acorns under two light levels (full sunlight and shade at about 18 % of full sunlight, simulating the light intensities in forest clearings and gaps, respectively) for one growing season. Three hypotheses were tested: (i) the deciduous species grows faster than the evergreen species in forest gaps and clearings; (ii) the deciduous species responds more strongly in terms of growth and morphology to variation in light climate than the evergreen species; and (iii) seedling size is positively correlated to acorn size. The results showed: (i) at both light levels, the deciduous seedlings gained significantly more growth in biomass and height than the evergreen seedlings; (ii) both species produced significantly more biomass in full sunlight than in shade, without showing any significant difference in height between treatments. Increase in light intensity improved the growth of the deciduous seedlings more strongly; (iii) at a similar age, the deciduous seedlings showed a greater response in leaf morphology and biomass allocation to variation in light levels, but when compared at a similar size, biomass allocation patterns did not differ significantly between species; (iv) bigger acorns tended to produce larger seedlings, larger leaf sizes and more leaf area, between and within species. These differences demonstrate that the deciduous species is gap-dependent and has the advantage over the evergreen species in forest gaps and clearings. © 1999 Éditions scientifiques et médicales Elsevier SAS Beech forest / deciduous species / evergreen species / light climate / morphological plasticity / seedling growth / seedling survival / Cyclobalanopsis multinervis / Quercus aliena var. acuteserrata
1. INTRODUCTION Most beech forests in the northern hemisphere are typically deciduous forests of the temperate zone [15]. Chinese beech forests, however, do not occur in the temperate zone but on the mountains of the subtropical zone [3, 15, 21, 22]. There, broad-leaved evergreen forests occur at lower altitudes, while needle-leaved forests occupy the higher parts. Beech forests occur in the transition zone between these forest belts, and contain many evergreen tree species [21]. In spite of the dominance of beech species in these forests, many other tree species can be found in the canopy. The species composition and structure of these mixed forests vary from place to place ([3]; pers. obs.). It is still largely unknown how these tree species regenerate. Cyclobalanopsis multinervis and Quercus aliena var. acuteserrata are two oak species occurring com-
monly in beech (Fagus engleriana and F. hayatae subsp. pashanica) forests around 1 400 m a.s.l. in the Dabashan Mountains, Sichuan, China. Below 1 400 m, C. multinervis, an evergreen oak, often occurs in the forest canopy. Above 1 400 m, it gradually decreases in tree size and frequency and occurs only under the canopy as the altitude increases and the temperature decreases. In contrast, adult trees of Q. aliena var. acuteserrata, a deciduous oak, are usually present in the canopy of the beech forests around 1 400 m, but its seedlings can hardly be found in the understorey of those forests [3]. The contrast in occurrence and population structure of the two oak species in the forests around 1 400 m indicates ecological differences between them. The persistence of the evergreen oak in the shade of the closed canopy of the beech forests suggests that it should be a shade-tolerant species, or a ‘stress-tolerant
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species’ (cf. [7, 8]). Absence of seedlings and juveniles of the deciduous oak under the closed canopy of the beech forests and frequent occurrence of its adults in the canopy suggest that its regeneration might take place in forest gaps or clearings, and it should be a less shade-tolerant species. According to Grime [8], the potential growth rate and the phenotypic plasticity of a stress-tolerant plant (associated with high stress and low disturbance) are low in contrast to those of a less stress-tolerant plant, i.e. a competitive plant (associated with low stress and low disturbance) or a ruderal plant (associated with low stress and high disturbance). From this perspective, growth and phenotypic plasticity of the two oak species can be expected to differ in response to variation in light climate. Thus, the following hypotheses are addressed: (i) the deciduous species grows faster than the evergreen species in forest gaps and clearings; (ii) the growth rate and morphology of the deciduous species are more plastic in response to variation in light climates. In addition, acorn size (fresh weight) varies substantially between and within both species. At the seedling stage, growth and survival are often affected by the amount of reserves stored in the seed [10, 16]. Larger acorns are regarded to produce greater seedlings [2]. Seedlings from larger acorns grow stronger and survive better [20]. Accordingly, we also hypothesize that larger acorns produce larger seedlings and this is valid for variation in acorn size between and within species. To test these hypotheses, we investigated the two oak species, as regards differences in seedling size, biomass allocation and a number of morphological traits related to light capture at two light levels simulating the light intensities in forest gaps and forest clearings. The purpose of this study is to examine the regeneration and growth strategies of the two oak species and improve the understanding of seedling performance and species regeneration in natural beech forests of subtropical China. 2. METHODS The experiment was performed at Daba Forest Farm, Sichuan (32°42’ N, 106°55’ E, 1 400 m a.s.l.), where the forests are mainly dominated by Fagus engleriana, F. hayatae subsp. pashanica, Quercus aliena var. acuteserrata, Carpinus cordata var. chinensis, C. fargesiana, etc. Acorns were collected on October 4th 1995 from the beech forest. The acorns of the deciduous species Q. aliena var. acuteserrata (‘Qa’ in brief) were from one tree and the acorns of the evergreen species C.
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multinervis (Cm) were picked from a patch of forest floor (1995 was a lapse year for these species, and not many individuals were fruiting). These acorns were then put into a pot and buried in the soil at a depth of 20 cm in order to store them in a forest-like environment. On April 30th 1996, the acorns were dug up and 100 acorns of the deciduous oak and fifty acorns of the evergreen oak were weighed individually and planted in pots filled with about 1.5 L soil from the forest floor. The soil was well mixed before. One acorn was used for each pot. The pots were randomly divided into two groups. One group was exposed to full sunlight (‘light’ in brief), while the other group was put beneath a bamboo screen that created a light climate of about 18 % of full sunlight (‘shade’ in brief). The experimental set-up thus consisted of two species and two light levels arranged in a factorial design (abbreviation used to indicate treatments: Cm-light, Cm-shade, Qa-light and Qa-shade). The average acorn fresh weight of the deciduous species (Qa) was 1 911 ± 49 mg (mean ± SE), which was significantly higher than the mean acorn weight (1 281 ± 58 mg) of the evergreen species (one-way ANOVA, F = 64.70, P < 0.001). There was no difference in acorn weight within species between the two light levels (planned comparison showed F = 0.984, P = 0.325 for the deciduous species and F = 0.956, P = 0.332 for the evergreen species). Dates of emergence of each seedling and start of leaf flush were recorded. Of the deciduous species, 47 in shade and 50 in light emerged around May 30th. Of the evergreen species, 24 in each light treatment emerged around June 12th. The apical buds of some seedlings recurrently burst and some new leaves flushed in summer or autumn after a period of earlier growth. Such newly developed shoots have been called ‘lammas shoots’ [23]. Seedlings having an additional flush were noted. Biomass allocation patterns have been shown to change throughout ontogeny [4]. To compare the two species at similar size, fourteen or sixteen seedlings (seven or eight in each light treatment) of the deciduous species were harvested at 3-week intervals after emergence because the deciduous species was assumed to grow faster than the evergreen species. In this way, harvests were performed four times and 58 seedlings (29 in each light treatment) were harvested before the final harvest around September 25th. At the final harvest, 34 deciduous seedlings (sixteen in shade and eighteen in light) were harvested. Five seedlings got damaged and were excluded. For the evergreen species, two seedlings in the shade were Acta Oecologica
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damaged before September and the 46 remaining seedlings (22 in shade and 24 in light) were harvested around September 25th. At harvest time, shoot height, length of lammas shoot and leaf dimensions (i.e. leaf length Ll, and leaf width Lw) were measured. The dry mass of roots, stems, leaves and of the remains of cotyledons and acorn shells were weighed after drying to constant mass at about 90 °C. Total seedling biomass refers to the sum of root, stem and leaf mass without the remains of cotyledons and shells. Leaf area (LA) was calculated by using the following linear regressions that were based on exact measurements. For Cm: LA = 15 + 0.605 × Ll × Lw ~ n = 11, R 2 = 99.1 %, P < 0.001 !
For Qa: LA = –16 + 0.649 × Ll × Lw ~ n = 432, R 2 = 98.6 %, P < 0.001 !
Leaf size was calculated for each individual, i.e. mean area per leaf of a seedling. Specific leaf area (SLA), leaf area ratio (LAR), leaf mass ratio (LMR) and root mass ratio (RMR) were calculated according to the formulas given by Hunt [11]. Minitab (release 9.2) and Statistica (release 4.5) were used to perform the calculations and statistical tests. Planned comparisons for acorn size and experimental results were done by using Statistica. For the final harvest, a general linear model (two-way ANCOVA) was used to test for effects of acorn fresh weight, species identity, light treatment and the interaction between species and light. Values of biomass, root mass, stem mass, leaf mass, leaf area and shoot:root ratio were transformed by square root, and the values of leaf number, leaf size (area per leaf), specific leaf area and leaf area ratio were logarithmically transformed in order to meet the assumptions of ANCOVA [18]. Bartlett Chi-square test was used to examine the homogeneity of variance and F-test was used to examine the parallelism of regression equations in the analysis. In terms of biomass, the evergreen seedlings at the final harvest were most similar to the deciduous seedlings on their sixth week after emergence. For this reason, the deciduous seedlings harvested at the sixth week after emergence and the evergreen seedlings at final harvest were used to compare the two species at similar size in the same general linear model of ANCOVA without transformation of the original data. Vol. 20 (6) 1999
3. RESULTS 3.1. Height and biomass In terms of shoot height and biomass, big acorns tended to produce large seedlings. This was true for both species (table II , figure 1). Seedlings of the evergreen species C. multinervis remained significantly smaller than the seedlings of the deciduous species Q. aliena at the final harvest (tables I, II, figure 1). Seedling biomass of the evergreen species at the final harvest was not more (df = 1 and 55, F = 2.051, P = 0.158) than that of the deciduous species at the sixth week after emergence (table I, figure 2). Light did not significantly affect final seedling height (tables I, II). However, it differently affected recurrent flushes of shoot and leaves in the deciduous species. Among the 46 evergreen seedlings, 21 out of the 22 in shade and 22 out of the 24 in light had an additional flush as from July, but among the deciduous seedlings, none of the sixteen seedlings in shade and only seven out of the eighteen in light had an additional flush. This resulted in a marked increase in the final height of seedlings by, on average, 11.4 ± 0.9, 18.4 ± 1.6 and 8.6 ± 2.9 mm (mean ± SE) for Cmshade, Cm-light and Qa-light plants, respectively. In both species, light significantly affected seedling biomass at the final harvest (table II). Seedlings in light gained more biomass than seedlings in shade (table I). This response was strikingly stronger in the deciduous seedlings than in the evergreen seedlings, as was indicated by the highly significant effect of the interaction between species and light on biomass (table II). In the deciduous species, mean biomass of seedlings grown in light was about 228 % that of seedlings in shade, whereas for the evergreen it was about 147 % (table I). The mass of cotyledon remains at the final harvest tended to be less in shade than in light (table I), but not significant (table II). 3.2. Leaf traits At final harvest, the evergreen seedlings had relatively more leaves than the deciduous seedlings at the same light levels, but their leaves were significantly smaller (tables I, II). The mean leaf size of the evergreen seedlings was only about one-third to onequarter that of the deciduous seedlings. This resulted in a smaller leaf area per seedling in the evergreen as compared to the deciduous species (tables I, II, figure 1). The seedlings of both species developed significantly more but smaller leaves in light than in shade (tables I, II, figure 1). As a result light did not significantly affect total leaf area per seedling in both species (table II, figure 1).
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Table I. Seedling height (mm), biomass (mg) and its components, cotyledon mass (mass of cotyledon remains), leaf number (leaves per plant), leaf size (area per leaf, mm2), leaf area (leaf area per plant, mm2), specific leaf area (SLA, mm2⋅mg–1), leaf area ratio (LAR, mm2⋅mg–1), leaf mass ratio (LMR), root mass ratio (RMR) and shoot to root ratio (S/R) of two species (Cm, Cyclobalanopsis multinervis; Qa, Quercus aliena var. acuteserrata) at the two light treatments at the final harvest. Values are mean ± SE. Values in italics in brackets are the results at the sixth week after emergence for the deciduous species. Species light levels Height Biomass Root mass Stem mass Leaf mass Cotyledon mass Leaf number Leaf size Leaf area SLA LAR LMR RMR S/R
Cm shade
Cm light
56 ± 4 498 ± 59 206 ± 27 74 ± 11 218 ± 24 193 ± 17 4.1 ± 0.2 630 ± 62 2 554 ± 224 12.6 ± 0.5 5.69 ± 0.30 0.45 ± 0.01 0.41 ± 0.01 1.47 ± 0.05
68 ± 4 731 ± 67 307 ± 31 116 ± 12 308 ± 29 212 ± 12 5.3 ± 0.3 608 ± 56 3 045 ± 237 10.2 ± 0.3 4.36 ± 0.17 0.43 ± 0.01 0.41 ± 0.01 1.44 ± 0.05
Leaf number was not significantly affected by acorn size (table II), but seedlings from large acorns tended to develop relatively large leaves (table II, figure 1). Thus, total leaf area per seedling tended to increase with the increase in acorn size (table II, figure 1). Specific leaf area of the deciduous species was significantly larger than that of the evergreen species. The specific leaf area was markedly larger in shade than in light for both species and that of the deciduous species responded more strongly to changes in light levels than that of the evergreen species (tables I, II). At final harvest, leaf area ratio of the deciduous seedlings was significantly smaller than that of the evergreen seedlings in both light levels (tables I, II). Leaf area ratio of the deciduous seedlings, however, was significantly greater than that of the evergreen seedlings when comparing the two species at similar size, for example, comparing the deciduous seedlings harvested at the sixth week after emergence with the evergreen seedlings at final harvest (table I; df = 1 and 55, F = 151.365, P < 0.001). Shade-grown seedlings of both species had a higher leaf area ratio than seedlings grown in full sunlight (tables I, II). 3.3. Biomass allocation At final harvest, the evergreen species had partitioned proportionally more biomass to leaves than the deciduous species. The leaf mass ratio of the evergreen species was about twice that of the deciduous species,
Qa shade 94 ± 3 1 256 ± 109 745 ± 74 149 ± 13 360 ± 29 184 ± 12 2.9 ± 0.2 2 471 ± 247 6 877 ± 556 19.1 ± 0.6 5.52 ± 0.18 0.29 ± 0.01 0.59 ± 0.01 0.72 ± 0.05
(103 ± 5) (875 ± 61) (384 ± 35) (112 ± 5) (379 ± 29) (291 ± 13) (2.7 ± 0.2) (3 554 ± 226) (9 603 ± 790) (25.3 ± 0.8) (10.93 ± 0.40) (0.43 ± 0.01) (0.44 ± 0.01) (1.30 ± 0.07)
Qa light 99 ± 3 2 868 ± 155 2 082 ± 118 256 ± 15 531 ± 37 216 ± 12 4.2 ± 0.4 1 776 ± 154 6 904 ± 417 13.1 ± 0.3 2.41 ± 0.10 0.18 ± 0.01 0.73 ± 0.01 0.38 ± 0.02
(87 ± 8) (811 ± 124) (378 ± 61) (107 ± 17) (326 ± 48) (286 ± 36) (3.1 ± 0.3) (1 628 ± 231) (4 956 ± 725) (15.2 ± 0.5) (6.15 ± 0.33) (0.40 ± 0.01) (0.46 ± 0.02) (1.17 ± 0.08)
while the root mass ratio of the evergreen species was only about two-thirds that of the deciduous species. The allocation patterns resulted in a significantly higher shoot:root ratio in the evergreen seedlings as compared to the deciduous seedlings (tables I, II). Light treatments had a strong effect on biomass allocation pattern at the final harvest (tables I, II). The high significance of the interactive effect between species and light on LMR, RMR and S/R indicated that the two species had different responses in these ratios to changes in light (table II). The deciduous species showed a stronger response in all these ratios than the evergreen species (table I). The biomass allocation patterns of the deciduous seedlings exhibited pronounced changes throughout the growing season. The leaf mass ratio and shoot:root ratio of the deciduous seedlings decreased and the root mass ratio increased with time, or with seedling size (table I). At similar size, biomass allocation patterns of the two species were very similar. Comparing the evergreen seedlings at the final harvest with the deciduous seedlings harvested at the sixth week after emergence, for example, there was no significant difference in each of these ratios (table I; df = 1, 55, F = 0.257, 0.873 and 1.149, P = 0.614, 0.354 and 0.288 for leaf mass ratio, root mass ratio and shoot:root ratio, respectively). Acta Oecologica
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Figure 1. Seedling size in relation to acorn fresh weight of Cyclobalanopsis multinervis and Quercus aliena var. acuteserrata under full sunlight and shade treatments. The significance levels of the regressions are given as: ns P > 0.05; * P < 0.05; ** P < 0.01; *** P < 0.001.
4. DISCUSSION
4.1. Length of growing season and growth rates
The results of this experiment demonstrate that seedlings of the deciduous species grew faster at both light levels simulating the light climates at forest clearings and gaps, and responded more strongly in growth rate and morphology to variation in light climate than the evergreen species. Greater plasticity of the deciduous seedlings in morphology and physiology allows the deciduous species to profit more from high light conditions than the evergreen species. For this reason, the deciduous species has the advantage over the evergreen species in forest gaps and clearings.
Considering the striking difference in seedling size (biomass) at final harvest between the two species in this experiment, annual growth of the deciduous seedlings is expected to be higher than that of the evergreen seedlings. The growing period of the evergreen species has no clear initial and end dates but it is most likely to last longer than that of deciduous species (cf. [9]). In Daba Forest Farm, the deciduous oak species has an annual growing period, from bud break to leaf shed, of about 160 d, while the evergreen oak species sustains leaves during the whole year.
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Table II. Two-way ANCOVA results of height (mm), biomass and its components, mass of cotyledon remains, leaf number (leaves per plant), leaf size (area per leaf), leaf area (leaf area per plant), specific leaf area (SLA), leaf area ratio (LAR), leaf mass ratio (LMR), root mass ratio (RMR) and shoot to root ratio (S/R) at the final harvest. A general-linear-model (Minitab release 9.2) was used to carry out the analysis, with species identity and light level as the two factors and the acorn fresh weight as covariate. To satisfy the assumptions of ANCOVA (including the homogeneity of variance and the parallelism of regression equations), some original values were transformed before performing the ANCOVA. The degree of freedom is 1 for each factor and the interaction and is 75 for the error. Items
Transformation
Height
–
Biomass
Square-root
Root mass
Square-root
Stem mass
Square-root
Leaf mass
Square-root
Cotyl. mass
–
Leaf number
Logarithm
Leaf size
Logarithm
Leaf area
Square-root
SLA
Logarithm
LAR
Logarithm
LMR
–
RMR
–
S/R
Square-root
F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P F-ratio P
It is, however, not to be expected that the evergreen species realizes much more growth during the prolonged growing season (or beyond the growing season of the deciduous species), considering the abundant snow cover and low temperatures during winter at Daba at 1 400 m altitude. In Beibei, Chongqing (about 215 m a.s.l. and three degrees south of Daba), Cornelissen [5] found that winter growth in height and leaf area were virtually nil in all three broad-leaved evergreen species in his experiment, Castanopsis fargesii, Sloanea leptocarpa and Elaeocarpus japonicus from an evergreen broad-leaved forest of subtropical China. Also Schulze et al. [17], in a comparative study between Fagus sylvatica (deciduous) and Picea abies (evergreen), found that the effect of a prolonged
Seedsize
Species (Sp)
Light (L)
Sp × L
23.877 0.000 91.465 0.000 77.613 0.000 72.653 0.000 61.210 0.000 246.066 0.000 1.634 0.205 28.249 0.000 43.200 0.000 14.479 0.000 20.208 0.000 4.672 0.034 2.598 0.111 3.053 0.085
22.130 0.000 79.862 0.000 185.485 0.000 6.968 0.010 0.372 0.544 119.286 0.000 19.686 0.000 58.289 0.000 35.365 0.000 120.126 0.000 6.767 0.011 118.167 0.000 267.410 0.000 213.075 0.000
3.777 0.056 107.095 0.000 153.754 0.000 36.759 0.000 17.176 0.000 1.922 0.170 18.695 0.000 8.943 0.004 0.028 0.867 79.479 0.000 170.614 0.000 25.564 0.000 44.194 0.000 26.358 0.000
1.967 0.277 48.290 0.000 96.148 0.000 3.298 0.073 0.863 0.356 0.553 0.460 0.872 0.353 3.006 0.087 0.941 0.335 8.032 0.006 55.407 0.000 13.138 0.001 41.762 0.000 23.875 0.000
growing season in spruce was very small, and its annual carbon gain would be reduced by only 9 % if the growing season would be the same length as for the beech. In this experiment, after 15 weeks of growth the evergreen seedlings were about the same size or even slightly smaller than the deciduous seedlings that had been growing for only 6 weeks. At final harvest, the biomass of the evergreen seedlings was on average less than half that of the deciduous seedlings. These striking differences indicate that seedlings of the deciduous species, which were characterized by a greater leaf area ratio (LAR) at a similar size and a larger specific leaf area (SLA) than the evergreen species, had a considerably higher annual growth, Acta Oecologica
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sunlight they were considerably different (0.415 and 0.240 mg⋅mm–2, respectively). This result corresponds to the findings of Bazzaz and Carlson [1] and Osunkoya et al. [14] that plasticity of physiological parameters is generally higher in gap-dependent species (early successional species) than in shade-tolerant species (late successional species). Thus, the deciduous species appears to be more plastic both in terms of morphological and physiological responses to variation in light climate. 4.3. Biomass allocation
Figure 2. Seedling biomass of the deciduous species at the two light levels in the growing season. Standard errors are shown only upwards.
thereby confirming our first hypothesis. This corresponds with the results of Cornelissen et al. [6] who have shown that deciduous species grow consistently faster than evergreen species and that mean relative growth rates were closely correlated with leaf area ratio and specific leaf area in eighty woody species from the British Isles and northern Spain. 4.2. Morphology and plasticity Leaf size and specific leaf area are two important leaf traits that vary with environmental conditions. In this experiment, the deciduous seedlings showed a greater change in leaf size and specific leaf area than the evergreen seedlings. Although both species had smaller leaf sizes and specific leaf areas in full sunlight than in shade, the differences in leaf sizes between light treatments were not significant for the evergreen species. This shows that the deciduous oak, the faster growing species, has a greater plasticity in these leaf traits in response to light climate than the evergreen seedlings. Such a positive correlation between the degree of plasticity and relative growth rates has previously been reported for herbaceous species [12]. The leaf area (per seedling) did not significantly differ at final harvest between light levels in either species (tables I, II). The difference in biomass production between light treatments, however, was more pronounced in the deciduous than in the evergreen species. This suggests that the net assimilation rate (NAR) shows a greater response to light in the deciduous species. This interpretation gains further support from data on the ratio of biomass to leaf area at the final harvest. In shade, the ratios of the deciduous seedlings and the evergreen seedlings were similar (0.183 and 0.195 mg⋅mm–2, respectively), but in full Vol. 20 (6) 1999
Biomass allocation patterns change throughout ontogeny [4]. This shift resulted in the considerable differences in biomass allocation patterns at final harvest between two species and between two light treatments for the deciduous species. This point of view was supported by the small differences in the ratios between two species at a similar seedling size and the changes in leaf mass ratio, root mass ratio and shoot:root ratio throughout the growing season. The changes in these ratios were stronger in light than in shade. This is consistent with the faster growth and larger seedling size (biomass) at final harvest in light than in shade. 4.4. Effect of acorn size Bigger acorns tended to produce larger seedlings. This tendency was found for both species, although in full sunlight, the regression of seedling height on acorn fresh weight was not statistically significant for either species (figure 1). This is consistent with the results of other studies on seedling survival and growth of oaks. Bonfil [2] found a positive correlation between seed mass and seedling survival and growth in Quercus rugosa and Q. laurina and the same was found for seedlings of Q. dealbata and Q. griffıthii by Tripathi and Khan [20]. Lone and Jones [13] found that the species with larger mean acorn size produced larger seedlings in a study of fourteen oak species in North America. Sonesson [19], however, concluded that growth and survival of Q. robur seedlings were independent of their cotyledons from the time of first leafing onwards (about 1 week after emergence). We plotted cotyledon dry mass of the deciduous species against harvest time and found that before the third week after emergence, the cotyledon mass was reduced by about three-quarters of the total mass reduction of the entire growing season. This suggests that the translocation of the acorn reserves to the growing seedling mainly happened at the early stage of seedling development before the first leaf set is displayed. However, we also found that some seedlings of the deciduous species, whose cotyledons were removed 1 week after emergence without destroying
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the seedlings, developed very slowly and survived only about 2 months under the shade of the closed forest canopy, while most of the seedlings with cotyledons survived the entire growing season. This demonstrates that cotyledon reserves are still very important for a seedling for longer than 1 week after emergence when the seedling grows under unfavourable conditions. In conclusion, the results of this experiment showed that the deciduous species Q. aliena var. acuteserrata had many characteristics in common with less shadetolerant (or competitive) plants and the evergreen species C. multinervis had many characteristics of shade-tolerant plants [7, 8]. This is consistent with the occurrence of the two species in the beech forests in Daba. The adult trees of the deciduous oak in the forests probably grow from forest gaps or disturbed clearings, and the evergreen oak under the canopy may regenerate and can persist in the understorey. Acknowledgments We thank Dr H. Huber, Dr J.F. Stuefer, two anonymous referees and the associate editor, Dr H. Koelewijn, for their help in statistical analysis and constructive comments on an early version of the manuscript. Guo Ke thanks Prof. Li Bosheng in Beijing and Mr Yue Weiyuan, Zhou Jun, Tian Liangmao, Li Rensheng, Xu Yuanjun in Daba Forest Farm, Sichuan, China, for their practical help in this study. Financial support by the National Science Foundation of China, the Chinese Academy of Sciences and the Royal Netherlands Academy of Arts and Sciences are acknowledged.
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