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Factors affecting establishment of Quercus liaotungensis Koidz. under mature mixed oak forest overstory and in shrubland
Forest Ecology and Management 176 (2003) 133±146
Factors affecting establishment of Quercus liaotungensis Koidz. under mature mixed oak forest overstory and in shrubland Qingkang Li, Keping Ma* Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, China Received 7 August 2001; received in revised form 13 February 2002; accepted 10 May 2002
Abstract From September 1999 to 2000, ®eld acorn burying experiments were conducted to examine the effects of gaps, litter cover and burying position, and simulated defoliation and cotyledon removal on oak (Quercus liaotungensis Koidz.) seedling establishment and biomass allocation in the understory of mixed oak forest in Dongling Mountain, Northern China. The effects of shrub and tree overstory were also studied in shrubland simultaneously. We found that acorn germination increased from 43.4 to 61.6%, that seedling recruitment increased from 33 to 47.6%, and that growth improved signi®cantly in gaps relative to that in understory habitats in mature oak forest. Both acorn germination and seedling recruitment showed strong positive correlation with openness of acorn burying sites (R2 0:659, P 0:001 and R2 0:477, P 0:034, respectively). Both acorn germination and seedling recruitment improved in order as follows for different burying treatments: placed on litter < on ground surface < buried at 5 cm depth in soil < buried at 3 cm depth in soil < covered with litter on ground surface. Furthermore, different burying treatments in¯uenced seedling growth and biomass allocation. Seedling grew tallest with thin stems from acorns covered by litter on the ground. Burying acorns too deeply in soil caused seedlings to allocate more dry mass to stem growth, and resulted in later emergence, shoot height decreases and leaf number reduction, which may lead to high mortality due to competition for light in shaded understorys. Simulated defoliation affected seedling dry mass accumulation signi®cantly (R2 0:899, P < 0:001) after considering defoliated loss during treatment, and complete defoliation caused mortality to rise to 16.7%. Similarly, cotyledon removal in¯uenced seedling dry mass accumulation (R2 0:746, P < 0:001), but had more serious effects on survival, causing 50% death where cotyledon were removed completely 1 month after emergence. The growth decline may increase mortality risks in future in shaded environments. In shrubland, we found that shrub or tree overstorys signi®cantly improved acorn germination (from 4.4 to 26.7%), seedling survival (from 11.1 to 100%) and recruitment (from 0.5 to 26.7%), but had no effects on growth in the ®rst growing season. At open sites in shrubland, seedling death resulted from direct or indirect effects of high light incidence. Overall, less acorn germination, seedling survival and recruitment occurred in shrubland than those beneath the mature forest canopy. In conclusion, in mature forest of Q. liaotungensis, we suggest that selected-cutting or canopy disturbance to permit light access to the understory will help to improve poor natural regeneration. With additional cage protection from browsers on acorns and herbivory free methods, burying acorns at 3 cm depth in soil or placed on ground with litter cover were the most effective methods to produce large number of seedlings. With facilitation of shrub or tree overstorys at early seedling stages in shrubland, direct burying acorns at 3 cm depth in soil was the most effective and economical technique for oak reforestation in such open early successional habitats. # 2002 Published by Elsevier Science B.V. Keywords: Quercus liaotungensis Koidz.; Establishment; Regeneration; Cotyledon removal; Defoliation * Corresponding author. Tel.: 86-10-82599518. E-mail address: [email protected] (K. Ma).
0378-1127/02/$ ± see front matter # 2002 Published by Elsevier Science B.V. PII: S 0 3 7 8 - 1 1 2 7 ( 0 2 ) 0 0 2 7 4 - 8
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1. Introduction Throughout the world, oaks (Quercus spp.) usually have poor natural regeneration in the forests where they occur (Watt, 1919; Crow, 1988; Thadami and Ashton, 1995; Gardiner and Hodges, 1998), and may begin to be replaced by long-lived and more shadetolerant species in the absence of periodic disturbance, e.g. ®re (Lorimer, 1984; Abrams, 1992). The regeneration of trees generally depends upon their ability to provide suf®cient seeds, the capacity of seeds to geminate and subsequent growth and survival of seedlings. In previous studies, biotic and abiotic factors cited as contributing factors to oaks' natural regeneration failure are insect parasitization of acorns, predation by small mammals, seedling herbivory, frost damage, competition from herbaceous weeds and low light levels (Watt, 1919; McGee, 1975; Crow, 1988; Lorimer et al., 1994; Le Duc and Havill, 1998), the precise limiting factors for seedling establishment and failure of natural regeneration are unclear. Deciduous broad-leaved forest is the zonal vegetation type in the temperate zone of northern-central China. Oak (Quercus liaotungensis Koidz.) forests or those where oaks were dominant species used to distribute in this region (Chen, 1995). Currently it is dif®cult to ®nd patches of oak forests in low hills and mountains because of anthropogenic activities or clear-cutting for cultivation, especially in the 1950± 1960s. However, contrary to its relative overstory importance and favorable mast production of acorns in fragmented secondary well-developed oak forests, Q. liaotungensis saplings were absent in the understorys, which indicated its poor natural regeneration (Zhu, 1982). In some regions, shrubland, grassland or farmland have replaced oak forests widely (Chen, 1995). It is urgent and important to restore the oak forest in such areas for environmental improvement, sustainable development and biodiversity conservation. To develop effective and economic techniques for restoration also requires the full understanding of natural regeneration processes and their limiting factors. The effects of following factors on acorn germination, subsequent seedling establishment and growth were in the focus of this study: (1) variation of light availability caused by gap creation in understorys of mixed oak forest; (2) litter cover on the ground and
acorn burying depth in soil; (3) simulated defoliation and cotyledon removal 1 month after emergence; (4) shrub and tree overstorys in shrubland. 2. Methods and site description 2.1. Study area This study was carried out in Beijing Forest Ecosystem Research Station (BFERS), 114 km southwest of Beijing (408000 N, 1158260 E, 1140 m in altitude). The area is in the Dongling Mountain Region in Northern China, with a temperate continental monsoon climate. Mean annual temperature averages 4.8 8C (January 10.1 8C; July 18.3 8C). Precipitation amounts to 612 mm per annual, 78% of annual rainfall occurs from June to August. The site for the ®rst three experiment is a welldeveloped mixed oak forest stand (NW-facing slope, 218, about 1225±1350 m in altitude), where Q. liaotungensis (45%) is dominant canopy tree species with 8±10 m in canopy heights and about 50-year-old. Canopy coverage is about 80%. The shrub layer is composed of Lespedeza bicolor, Spiraea pubescens, Abelia bi¯ora, Deutzia grandi¯ora, and Rhododendron mucronulatum. On the forest ¯oor, herbaceous species were abundant. The soil in this area is mountain brown earth, >50 cm in depth; litter layer, 2±5 cm; humus, 15±20 cm. The shrubland (S-facing slope, 108, 1100 m in altitude) where the fourth experiment was conducted is characterized as an open early successional environment after clear-cutting, where Spiraea trilobata, Spiraea pubescens, Ulmus macrocarpa, Prunus davidiana, Prunus armeniaca and Syringa pekinensis are dominant canopy shrubs, with heights of 1±3 m. Sparse large trees of Fraxinus rhynchophylla and Q. liaotungensis also occur and total canopy cover is 30±50%. Carex humilis var. nana, Calamagrositis arundinacea and Spodiopogon sibiricus comprise most of the herb layer. The soil is light mountain brown earth with stones or rocky, <50 cm in depth; litter layer, <1 cm. 2.2. Experimental design Acorns were collected from the ground in the ®eld during September 1999 and were planted in early
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October. Sound acorns from the same plot were used in each treatment to avoid potential germination differences. Same source acorns were used in second and fourth experiments. Four experiments were conducted as follows. 2.2.1. Gap effects experiment In the mature forest understory, large gaps (LG), small gaps (SG) and under canopy(UC) nearby were selected as light gradient to test acorn germination and seedling establishment response to gap. Three aluminum or iron hybrid metal net cages 30 cm 30 cm 35 cm were set up to protect the acorns from animals within nine burying microsites. Soil collected from nearby understory sites was added in the gaps to unify soil type. Fourty ®ve or 50 acorns were buried at 3 cm depth in soil at each site. Unfortunately, only 24 cages were left perfect, i.e. without damage by human or animal disturbances. 2.2.2. Litter cover and acorn burying position in soil experiment Eight large cages 50 cm 50 cm 50 cm were scattered randomly in the mixed oak forest understory to test burying depth and litter effects on acorn germination and seedling establishment. Inside each cage, 100 acorns were planted in 10 lines for ®ve treatments as follows: acorns buried at 5 cm (5 cm) and 3 cm (3 cm) depth in soil, placed on ground surface (GR), covered with 2.5 cm deep litter cover (LC, similar to natural state), acorns placed on the litter (2.5 cm, OL). Two lines formed one treatment, which was separated by small slices of 5 cm high metal net. Plastic net was also used to ®x the acorns in the treatments GR and OL. By the time of harvest in autumn, only three cages had not been damaged by wild boars due to good protection of the iron cages. The treatments 3 or 5 cm in four broken cages were also well protected. 2.2.3. Simulated defoliation and cotyledon removal experiment Six large cages 100 cm 100 cm 50 cm with 60 acorns each (buried in soil at 3 cm depth) were set up at 10 m interval in two randomly located lines in the understory. To simulate herbivory or predation effects on seedling survival, 60 seedlings of similar size were chosen for defoliation treatments (one con-
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trol, and four degrees: 25, 50, 75, and 100%). The defoliation was conducted carefully on every leaf by hand and defoliated part was taken to lab for dry mass. Thirty six seedlings were studied for the effects of cotyledon removal (one control, two degrees: half and complete cotyledon removal) 1 month after emergence. After the treatments were imposed, insecticide was sprayed every 2 weeks on all seedlings and watered in soil to avoid insect damage. 2.2.4. Facilitation of tree and shrub overstory in shrubland In shrubland, nine cages 100 cm 100 cm 50 cm with 60 acorns each (buried at 3 cm depth in soil) were scattered in three different microsites: open site (OS), where all vegetation was removed; under shrub overstory (USh) without herb disturbance; under tree overstory of oak (UTr) without ground disturbance. 2.3. Data collection and analysis Seedling emergence and survival were monitored monthly from May to October inclusive. Growth parameters (height, leaf area, leaf number, stem basal diameter) were also measured at the same time. At the time of harvesting, seedlings were excavated, rinsed with clean water until free of soil and separated into root, stem and leaf. After the measurement of growth and morphology, the plant components were oven dried for more than 24 h at 80 8C before obtaining dry mass. The light environment of each burying site was measured by ``®sheye'' techniques according to the procedures of Zipperlen and Press (1996), using a Minolta 2500 dxi camera and Winphot software (Version 5.0, ter Steege, 1997). Acorn germination, seedling survival and recruitment (from seeds to seedlings), growth and biomass allocation were analyzed by ANOVA to test for treatment effects. Chi-square analyses were carried out to test the treatments of defoliation and cotyledon removal on subsequent seedling survival. Simple correlation analyses were conducted between establishment and light availability of seedling growing sites (large gaps, small gaps and under canopy), as well as between biomass accumulation and degree of defoliation and cotyledon removal. All analyses were carried out using SAS (Release 6.12, SAS Institute, Inc.).
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Fig. 1. Seedling emergence dynamics (a), acorn germination (b), seedling survival (c) and recruitment (c) (S.E.) across the large gap (LG), small gaps (SG) and under canopy (UC). Means sharing the same letter are not signi®cantly different from one another at P < 0:05 using Duncan multiple range test.
3. Results 3.1. Gaps effects on seedling establishment and seedling growth Seedling emergence was earlier in gaps than under canopies. Whereas in gaps, 20±40% were emergent in May, most seedling emergence occurred later under canopies (Fig. 1a). ANOVA analyses showed that acorn germination differed between sites (P < 0:05, Fig. 1b), and the most occurred in the large gaps. Seedling recruitment showed a similar trend as germination (P < 0:05, Fig. 1d). There were no differences
in seedling survival among three light conditions in the ®rst growing season (P > 0:05, Fig. 1c). Acorn germination and seedling recruitment were positively correlated with openness at each acorn burial site (R2 0:659, P < 0:001 and R2 0:447, P 0:034, respectively, Fig. 2 a and b), but seedling survival was not signi®cantly correlated with openness (R2 0:133, P 0:588). Seedlings in the large gaps grew tallest, faster and gained more dry mass than other seedlings, and they also had longer roots, greater leaf area, lower SLA (speci®c leaf area) than those from the other two sites (Table 1). Some seedlings had second ¯ushes in the
Fig. 2. Acorn germination (a), seedling survival (b) in relation to openness of growing sites (LG, SG and UC) in the understory of mixed mature oak forest (simple linear regression analysis).
Site
H (cm)
BD (mm)
RL (cm)
LMR
StMR
RMR
WhM (g)
SLA (m2 kg 1)
RGR (g g 1 W 1)
LAR (m2 kg 1)
RSR
RD (mm)
LA (cm2)
UC SG LG Pr > F
12.5 0.4 a 12.2 0.6 a 16.2 0.5 b ***
1.5 0.1 a 1.9 0.1 b 2.60 0.1 c ***
11.9 0.7 a 15.7 1.1 b 28.4 1.1 c ***
0.34 0.03 a 0.30 0.01 b 0.27 0.01 c ***
0.35 0.07 a 0.33 0.03 a 0.31 0.06 a ns
0.3 0.3 a 0.4 0.2 b 0.4 0.1 c ***
0.3 0.02 a 0.5 0.1 b 1.3 0.1 c ***
34.6 0.9 a 27.3 0.8 b 21.7 0.6 c ***
0.01 0.003 a 0.02 0.003 b 0.07 0.007 c ***
11.3 0.5 a 8.2 0.3 b 5.8 0.2 c ***
0.5 0.3 a 0.6 0.4 b 0.8 0.3 c ***
2.4 0.1 a 3.3 0.1 b 4.3 0.1 c ***
29.2 2.8 a 41.2 4.4 b 71.4 4.8 c ***
a Three microsites are large gaps (LG), small gaps (SG) and under the canopy (H, height; BD, stem basal diameter; RL, root length; LMR, leaf mass ratio; StMR, stem mass ratio; RMR; root mass ratio; WhM, whole seedling dry mass; SLA, speci®c leaf area; RGR, relative growth rate; LAR, leaf area/seedling dry mass; RSR, root:shoot ratio; RD, root collar diameter; LA, total leaf area). b Values with different letters in each column are signi®cantly different (Duncan multiple range test, * P < 0:05; ** P < 0:01; *** P < 0:001; ns, not signi®cant).
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Table 1 ANOVA analyses on growth and biomass allocation (S.E.) of Q. liaotungensis seedlings growing at different microsites in mature oak foresta,b
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Fig. 3. Seedling dynamics (a), acorn germination (b), seedling survival (c) and recruitment (d) (S.E.) from acorns placed on litter (OL), covered with litter (LC), exposed on ground surface (GR), buried at 3 cm (3 cm) depth in soil and 5 cm (5 cm). Means sharing the same letter are not signi®cantly different from one another at P < 0:05 using Duncan multiple range test. (* P < 0:05;** P < 0:01; ns, not signi®cant).
HL and ML treatments, and a few plants had third ¯ushes in large gaps. But no multiple ¯ushes were observed for seedlings growing beneath the canopy. 3.2. Effects of acorn burying position on seedling establishment and seedling growth Excepting acorns that had been placed on the ground surface, most of the seedlings were emergent by July, which coincided with the rains from late June to August (Fig. 3a). Acorn germination and seedling recruitment were in the order: placed on litter < exposed on ground surface < buried at 5 cm depth in soil < at 3 cm depth in soil < covered by litter on ground (Fig. 3 a and d). Seedlings survived very well when acorns were buried in the soil or covered by litter (Fig. 3c). Different planting depths in soil had no signi®cant effects on seedling survival in the ®rst year. It is surprising to ®nd high survival of seedlings produced from acorns lying on the ground surface, but those late emergent seedlings cannot fully develop before the onset of winter and may be easily damaged by cold. Different acorn planting positions not only in¯uenced seedling establishment, but also seedling growth
and biomass allocation. Covering acorns with litter increased height growth but decreased stem basal diameter and leaf number more or less compared to those buried at 3 cm in soil (Table 2). Seedlings produced by acorns buried in soil at 3 cm depth had the largest stem basal diameters and greatest leaf number but they were intermediate in height. Nevertheless, seedlings emerging from acorns planted at 3 cm depth in soil, generally outperformed those produced from acorns that had been planted at 5 cm depth, exposed on ground surface or placed on litter (Table 2). Owing to early leaf shedding, seedlings grown from acorns that were placed on litter were excluded from the analysis on biomass allocation. Seedling that grew from acorns covered by litter had greater root length, whole dry mass and faster relative growth rates than those in treatments GR and 5 cm. Seedlings from acorns that were placed on the ground surface had signi®cantly smaller stem lengths, RL, dry mass and RGR than those from other treatments (Table 2). Burying acorn too deep in soil decreased the root length (RL), leaf area ratio (LAR), leaf mass ratio (LMR), whole dry mass and RGR, but increased stem length and stem mass ratio (Table 2).
Table 2 ANOVA analyses on growth and dry mass allocation (S.E.) of Q. liaotungensis seedlings from the acorns with different planting positionsa,b Planting position
H (cm)
LC GR 3 cm 5 cm OL Pr > F
10.3 8.8 8.9 6.1 6.8 ***
BD (mm)
3.0 2.3 2.2 2.1 3.5
a ab bc d cd
1.6 1.5 1.7 1.4 1.2 **
0.2 0.3 0.3 0.2 0.7
LN (n) ab ab b bc c
3.0 3.2 3.9 3.8 2.3 ***
0.7 1.5 1.0 1.0 1.2
StL (cm) ac ab b b c
13.5 9.9 13.7 15.8 ±c *
1.0 1.3 0.8 0.7
RL (cm) a b a a
14.7 12.3 15.3 12.1 ± *
1.0 4.8 1.1 0.9
LMR a b a ab
0.33 0.41 0.38 0.25 ± *
StMR 0.03 0.03 0.01 0.02
a b ab c
0.26 0.21 0.31 0.44 ± *
RMR 0.02 0.02 0.01 0.02
a ab b c
0.40 0.38 0.31 0.31 ± *
WhM (g) 0.03 0.04 0.01 0.01
a ab b b
0.7 0.5 0.7 0.6 ± *
0.2 0.2 0.2 0.1
RGR (mg g
SLA (m2 kg 1) a b ab ab
31.9 33.9 33.8 36.5 ± *
0.9 2.2 0.9 1.2
a ab ab b
1.3 0.9 1.2 1.1 ± *
1
LAR W 1) (cm2 g 1)
0.3 0.3 0.2 0.1
a a ab b
105.0 134.6 127.9 89.9 ± *
10 a 3 bc 6 ac 6a
RSR 0.59 0.64 0.46 0.45 ± *
LA (cm2)
RD (mm)
0.06 0.09 0.03 0.02
a bc c c
3.4 2.6 2.8 2.5 ± *
0.2 0.3 0.2 0.2
a b ab b
46.8 53.1 47.8 25.1 ± *
5.8 a 15 a 4.6 a 2.7 b
a Acorns burying positions are covered by litter (LC), exposed on the ground surface (GR) and on litter (OL), and buried at 3 cm or 5 cm depth in soil. (H, height; BD, stem basal diameter; LN, leaf number; StL, stem length; RL, root length; LMR, leaf mass ratio; StMR, stem mass ratio; RMR; root mass ratio; WhM, whole seedling dry mass; SLA, speci®c leaf area; PGR, relative growth rate; LAR, leaf area/seedling dry mass; RSR, root: shoot ratio; RD, root collar diameter, LA, total leaf area). b Values with different letters in each column are signi®cantly different (Duncan multiple range test). c Data was absent because too few seedling survived until the time of harvesting,* P < 0:05; ** P < 0:01; *** P < 0:001.
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Fig. 4. The effects defoliation (a) and cotyledon removal (b) on subsequent seedling survival (Chi-square test) and dry mass accumulation (c and d) (simple linear regression analysis). (* P < 0:05; ** P < 0:01; ns, not signi®cant).
In general, the seedlings that grown from acorns buried in soil or covered by litter grew better than those in other treatments. Seedlings that grew from acorns buried too deeply in soil or growing without protection may suffer increased mortality as resulting from slow growth or non-optimal resource allocation. 3.3. Effects of simulated defoliation and cotyledon removal on seedling survival and biomass accumulation Even after 75% defoliation, seedlings survived well until the end of the growing season. However, complete defoliation caused seedling mortality to reach 16.7% which was signi®cantly worser than for undefoliated seedlings (X 2 8:276, P 0:044) (Fig. 4a). Complete cotyledon removal seriously decreased seedling survival to 50%, which was signi®cantly lower than seedlings without cotyledon removal (X 2 12:727, P < 0:001) (Fig. 4b). The defoliation not only in¯uenced the subsequent survival, but also decreased the dry biomass accumulation signi®cantly in ®rst growing season (R2 0:899, P < 0:001) (Fig. 4 c and d). So did cotyledon removal (R2 0:746, P < 0:001). The decrease of biomass will inevitably increase the possibility of mortality,
especially in the highly competitive or resource limited conditions, such as in shaded understorys and where repeated defoliation occurs. 3.4. Seedling establishment in shrubland Similar to seedling emergence dynamics in large gaps under mature mixed oak forest, seedlings at open sites in shrubland where high light availability occurred, emerged earlier than those in other treatments in the shrubland (Fig. 5a). Even although seedlings produced from acorns placed under shrub or tree overstorys emerged about 1 month later than seedlings from acorns planted at open sites, acorn germination, seeding survival and recruitment in the shade were signi®cantly better than those in the open sites (Fig. 5). However, there were no difference among treatments in height, leaf area, leaf number or stem basal diameter among the three treatments. During summer, some leaves of seedlings growing in open sites appeared to have been bleached by strong direct light, and which subsequently died. These observations concur with Kitzberger et al. (2000) who found that strong direct light caused yellowish coloration and death of seedling in open ®elds even after adding water.
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Fig. 5. Seedling dynamics (a), acorn germination (b), seedling survival (c) and recruitment (d) (S.E.) from acorns buried in open site without vegetation cover (OS), under shrub canopy(USh) and under tree canopy (UTr). Means sharing the same letter are not different from one another signi®cantly P < 0:05 using Duncan multiple range test.
Due to mortality, few seedlings were available for growth study for open sites. Consequently, biomass allocation studies were not conducted which may have resulted in loss of important information. 4. Discussion 4.1. Gap effects on seedling establishment and biomass accumulation Light as well as other resources would increase to understory plants and tree seedlings after gaps in canopies are created (Chazdon and Fetcher, 1984; Canham, 1988). The importance of gaps for establishment and growth of different tree species has been documented widely throughout the world (Brokaw, 1985; Uhl et al., 1988). In this study, not only acorn germination and seedling recruitment of Q. liaotungensis were signi®cantly better in gaps than in shaded understory, but also they tend to survive better. These results coincide with previous ®ndings that light played an important role in the establishment of oak seedling. For example, Suh and Lee (1998) found that although more acorns remained in subplots within forests than in clear-cut
areas, more acorns germinated in clear-cuts, and heights of seedling in large clear-cuts were greater than those under canopies or in small gaps. Germination of Quercus (section Erythrobalanus) was greater in gap centers and north edges of gaps than in understory sites (Ashton and Larson, 1996), but low light increased the time necessary for germination to take place. Lorimer et al. (1994) found that removal of understory vegetation resulting in light increment enhanced Quercus spp. seedling survival to 90% in contrast to less than 30% for seedlings beneath the mature stands. The replacement of Quercus petraea by Carpinus betulus was due to its light compensation point being higher than the maximum available light under the main tree canopies in the wood (Le Duc and Havill, 1998). By contrast, some studies found that shade facilitated acorn germination, especially in arid areas. For example, cleared or cut sites had low acorn emergence and seedling survival in contrast with higher values obtained under the canopy (Bran et al., 1990; Callaway, 1992a; Weltzin and McPherson, 1999). Truax et al. (2000) also found that Q. robur achieved better growth and survival of seedling in a relatively shaded stand. Previous research suggested that Quercus seedling establishment response to light
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availability varies among species. For example, Figueroa-Rangel and Olvera-Vargas (2000) found that the presence of oak seedlings for a range of species was strongly associated with percentage of openness, e.g. Q. candicass, Q. laruina, Q. rugosa, Q. castanea, Q. crassipes required about 6.4, 2.9, 6.8, 13 and 8.1%, respectively, for successful establishment. Nevertheless, most researchers have found positive effects of increased light increase in gaps on oak seedling establishment because of enhancement on oak seedling growth (Kolb and Steiner, 1990). Even though oak seedlings may grow at irradiance as low as 1% of full light, the dry mass of oak seedlings usually increases with light intensity (Finzi and Canham, 2000; Jarvis, 1964; Ovington and MacRae, 1960). In this study, we found that oak seedlings grew faster, taller and accumulated more dry mass when they occupied large gaps in the canopy. They also produced multiple ¯ushes in large gaps than those growing under the canopy. Jarvis (1964) found that whole dry mass, maximum photosynthetic rate, RGR, root mass ratio, survival of Q. petraea seedling increased with light availability increasing. He also found that shading resulted in increased SLA, LAR and decreased root weight, RSR and assimilation rate. Expecting Q. rubra which grew well with intermediate light availability, seedlings survived better in gap centers than elsewhere (Ashton and Larson, 1996). LoÈf (2000) also found that for Q. robur L., greatest seedling growth and survival occurred in the clear-cuts. Espelta et al. (1995) found that young seedlings survived better under closed canopies but he concluded that the sapling stage would only be attained in stands where suf®cient radiation penetrates the leaf canopy to enhance growth of older seedlings. This conclusion was also reached by Tanouchi et al. (1994) who found that in spite of the presence of large seedling and sapling banks of Q. acuta, Q. gilva, Q. salicina and Q. sessilifolia and survival of 60±80%, the young trees are unlikely to attain canopy positions from within closed stand due to their very small annual height increment (less than 5 cm in 3 years). Combined the results from this and previous studies, we conclude that gap creation should bene®t natural regeneration of Q. liaotungensis forest through enhancement of seedling establishment and growth in mature mixed oak forests.
4.2. Effects of acorn burying position on seedling establishment and growth Viability of Quercus acorns declines or lose rapidly if acorns lose water without protection on the ground surface after falling from tree (Borchert et al., 1989; Harmer, 1995). We found that about 3 cm deep litter cover improved acorn germination of Q. liaotungensis to a peak of 70%, in contrast to 58.1, 45, 28.3 and 8.3% for acorns buried in soil at 3, 5 cm, placed on ground surface or directly on the litter layer respectively. Jarvis (1964) found that the loss of moisture by acorns covered with litter was much less than for those exposed on the ground surface, and that water content was positively related to viability. The germination of Q. laurina was improved by 15% when acorns were covered by 3 cm deep litter on ground surface (Camacho-Cruz et al., 2000). Despite the positive effects of litter, such as increased germination, decrease of moisture and temperature extremes (Barton and Geeson, 1996), negative effects of litter also existed. From this study, the acorns on the litter germinated less and suffered high mortality contrasting to other treatment, because litter may present a physical barrier to germination and emergence (Facelli and Pickett, 1991), increase etiolation of seedlings resulting in increased risk of physical damage (Barrett, 1931), cause greater fungal infection or even herbivory (Facelli, 1994). So, covering acorns with too much or too little litter may have negative effects, 1.9±2.5 cm (0.75±1 in.) seemed optimal for the establishment of chestnut oak seedlings (Barrett, 1931). In our study, about 3 cm deep litter cover seemed optimal for acorn germination of Q. liaotungensis. Burying is helpful to seedling establishment of oaks. In this study, we found that burying acorns at 3 cm depth in soil signi®cantly enhance their germination and seedling recruitment in addition to litter cover, relative to those exposed on bare ground surfaces and litter. Although, there is no signi®cant difference in seedling survival between acorns buried at 3 and 5 cm depth in soil in the ®rst growing season, they showed some differences in germination, emergence time, recruitment, and growth, especially allocation of more resources to stems and fewer to leaves for the latter. Timing of emergence also plays a critical role in seedling establishment in plant species,
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particularly under competitive conditions (Miller et al., 1994). For example, seedling recruitment for buried acorns was twice that of surface-sown acorns due to improved germination. Ovington and MacRae (1960) found that more than 80% of acorns germinated in soil at 2.5 cm depth and that less than 1% germinated on bare ground because of root desiccation. Kollmann and Schill (1996) also found that Q. petraea germinated 62±86% more at 5±6 cm depth in the soil than on the surface across different microsites. About 59% of oak seedling death was attributed to desiccation in some habitats without protection (Fuchs et al., 2000). Burying acorns too deeply in soil may also increase seedling mortality due to delayed emergence and nonoptimal allocation of resources. Watt (1919) found that planting too deeply in soil decreases germination of oaks. Iida (1996) found that emergence of Q. mongolica germinants was poorer when planted at 10 cm depth than when planted super®cially, and germinants failed to emerge when planted if at 25 cm depth. Burying protects acorns from rodent predation by limiting odor diffusion. Borchert et al. (1989) found that vertebrates removed >53% of acorns placed on the ground surface in contrast to about 7± 48% of acorns buried in the ground cover or in the soil. In this study, boar predation through the broken cages was stronger for acorns exposed on ground surface and on litter than for those were buried in soil at 3 and 5 cm depth. 4.3. Simulated defoliation effects on seedling survival and growth Herbivores in seral communities are reported to consume only a small proportion of the productivity (Odum, 1960). However, exclusion of herbivores in old-®eld communities produces important changes in community structure and population dynamics (Brown, 1985). Height growth and survival of Q. robur seedling increased by 20 and 5±45%, respectively, with insecticide treatment in the ®eld (LoÈf, 2000). Oak seedling usually undergo repeated defoliation by the larvae of various Lepedopteran species, and their establishment and growth were restricted in consequence, which could explain the failure of regeneration under a canopy of mature oaks (Shaw, 1974), or reduction of competitive ability of the grazed plants (Edwards et al., 1992). In current study,
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although, defoliation had less severe effects on seedling survival than those caused by cotyledon removal, more than 16.7% of seedlings died after the complete defoliation 1 month after emergence. Similarly, Negi et al. (1996) found that herbivory at shaded microsite accounted for 63.2% mortality of Q. ¯oribunda seedling. In this study, some seedlings re¯ushed after complete defoliation and produced young shoot, which may cause repeated insect defoliation, because oakfeeding species such as Lepidoptera prefer young leaves for seasonal decline of leaf proteins and increment of tannins concentrations (Feeny, 1970). As a result, repeated defoliation occur and cause more serious damages to seedling. 4.4. Cotyledon removal effects on seedling survival and growth The cotyledon is very important for acorn germination and subsequent seedling establishment, growth and survival because it serves as the main nutrient resources for young seedlings (Ovington and MacRae, 1960). Whereas complete removal of cotyledons 1 month after seedling emergence in this study, caused up to 50% seedling mortality, half removal of the cotyledons had no direct effects on seedling survival in the ®rst growing season. This result contrasts with Andersson and Frost (1996) who found no negative effects of cotyledon removal on survival of Q. robur during the ®rst growing season, and with Sonesson (1994) who found no effects of cotyledon removal on Q. robur seedling growth and survival at the time of the ®rst lea®ng, even when seedlings had established on poor soil. Nevertheless, our results are consistent with Bon®l (1998), who found that survival of Q. rugosa seedlings from medium sized acorns was lowered by 17% due to cotyledons removal 1 month after emergence in glasshouse studies, he also reported 60% mortality of Q. laurina occurred when cotyledons were removed. Similarly, after one growing season, Frost and Rydin (1997) found large negative effects of cotyledon removal not only on competitive ability, but biomass and survival. It is widely reported that 30±90% viability loss of acorn is due to insect parasites. Weevils cause acorn death completely in some individuals in non-mast
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years (Crawley and Long, 1995). Barrett (1931) found that about 40% of acorns attached to well-developed seedlings had been damaged by weevils or gall forming insects in chestnut oak. We found that most of the attached acorns on 27 dead seedlings in July showed signs of insects damage. At harvest, we found 116 out of 237 (48.9%) acorns had been damaged to some extent by insects parasite. Therefore, cotyledon reserves play an important role in seedling growth and survival even after the emergence in the ®rst growing season and future performance for Q. liaotungensis, especially for those in unfavorable conditions.
by as much as 19-fold and also increased seedling recruitment 30- or 60-fold for Q. emoryi in savanna in North American (Weltzin and McPherson, 1999). Overstory shade bene®ts are complicated by indirect effects of shade on seedling microenvironments that may also affect seedling performance. Shade can also improve survival of oak seedlings by reducing heat or water stress or providing protection from herbivores (Crow, 1988; Callaway, 1992b). Shrub cover also improves the retention of seeds and reduces animal browsing signi®cantly (Dubois et al., 2000).
4.5. Shrub facilitation
For mixed mature oak forest, predation on cotyledons and defoliation of seedlings, heavy insect parasitism of acorns, low light availability in the understory, litter depth and soil properties are among the limiting factors for natural regeneration. Results from this study and previous studies suggest that selective-cutting or intermediate canopy disturbance would be a good management policy to encourage natural regeneration in oak woods. For reafforesation, sowing acorns in soil at 3 cm depth was the most effective technique to maintain and favor regeneration. While too deep and thick litter may cause negative effects on seedling recruitment. Where shrub or sparse tree canopies exist, direct seeding in soil appeared to be the most effective and economic method for oak restoration.
In the early successional shrubland, we found that acorns germinated better and seedling survived better when acorns were buried under the ovestorys of shrubs or trees, indicating positive effects of shade in sunny open habitats. Our results are in consistent with Zhang (2001) who found recruitment of Q. liaotungensis seedlings correlated positively with vegetation cover when acorns were buried in soil on south facing slopes. Similarly, Callaway and D'Antonio (1991) reported that shrubs could have strong facilitative effects on the survival of Q. agrifolia seedlings and Callaway (1992a) found that the presence of shrubs raised the survival of 1-year Q. douglasii seedlings from zero to 30±50% because of shade bene®ts and acorn protection from predation and herbivory. In the cleared or cut sites, acorn emergence and seedling survival were lower than under the canopy (e.g. Q. ilex and Q. pubescens) (Bran et al., 1990). Not only shrubs have bene®ts to germination and survival, but other vegetation cover also have. Kollmann and Schill (1996) found that Q. petraea germinated more in unmown sites than mown areas where grass had been cut (20% vs. 5%). Negi et al. (1996) found that ground herbage clearance at sunny microsites accounted for 53.4% mortality Q. ¯oribunda seedlings. Truax et al. (2000) found that red oak and bur oak (Q. macrocarpa) could be successfully grown herbicide-free using shelterwood systems in mesic forested environments in southern Quebec. Provisions of arti®cial or natural shade increased seedling emergence and subsequent survival
4.6. Management implication
Acknowledgements This research was supported by National Natural Science Foundation of China (Nos. 39893360, 39770131 and 39970136). We sincerely thank Mr. Xiaodong Yu, Jingsheng Zhang, Zhongfei Li, Wei Chen and Miss Wenjie Yan for ®eld data collection. We are deeply indebted to all staffs of BFERS for their great support in ®eld. The authors gratefully thank two anonymous reviewers for their helpful comments.
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Factors affecting establishment of Quercus liaotungensis Koidz. under mature mixed oak forest overstory and in shrubland Qingkang Li, Keping Ma* Institute of Botany, The Chinese Academy of Sciences, Beijing 100093, China Received 7 August 2001; received in revised form 13 February 2002; accepted 10 May 2002
Abstract From September 1999 to 2000, ®eld acorn burying experiments were conducted to examine the effects of gaps, litter cover and burying position, and simulated defoliation and cotyledon removal on oak (Quercus liaotungensis Koidz.) seedling establishment and biomass allocation in the understory of mixed oak forest in Dongling Mountain, Northern China. The effects of shrub and tree overstory were also studied in shrubland simultaneously. We found that acorn germination increased from 43.4 to 61.6%, that seedling recruitment increased from 33 to 47.6%, and that growth improved signi®cantly in gaps relative to that in understory habitats in mature oak forest. Both acorn germination and seedling recruitment showed strong positive correlation with openness of acorn burying sites (R2 0:659, P 0:001 and R2 0:477, P 0:034, respectively). Both acorn germination and seedling recruitment improved in order as follows for different burying treatments: placed on litter < on ground surface < buried at 5 cm depth in soil < buried at 3 cm depth in soil < covered with litter on ground surface. Furthermore, different burying treatments in¯uenced seedling growth and biomass allocation. Seedling grew tallest with thin stems from acorns covered by litter on the ground. Burying acorns too deeply in soil caused seedlings to allocate more dry mass to stem growth, and resulted in later emergence, shoot height decreases and leaf number reduction, which may lead to high mortality due to competition for light in shaded understorys. Simulated defoliation affected seedling dry mass accumulation signi®cantly (R2 0:899, P < 0:001) after considering defoliated loss during treatment, and complete defoliation caused mortality to rise to 16.7%. Similarly, cotyledon removal in¯uenced seedling dry mass accumulation (R2 0:746, P < 0:001), but had more serious effects on survival, causing 50% death where cotyledon were removed completely 1 month after emergence. The growth decline may increase mortality risks in future in shaded environments. In shrubland, we found that shrub or tree overstorys signi®cantly improved acorn germination (from 4.4 to 26.7%), seedling survival (from 11.1 to 100%) and recruitment (from 0.5 to 26.7%), but had no effects on growth in the ®rst growing season. At open sites in shrubland, seedling death resulted from direct or indirect effects of high light incidence. Overall, less acorn germination, seedling survival and recruitment occurred in shrubland than those beneath the mature forest canopy. In conclusion, in mature forest of Q. liaotungensis, we suggest that selected-cutting or canopy disturbance to permit light access to the understory will help to improve poor natural regeneration. With additional cage protection from browsers on acorns and herbivory free methods, burying acorns at 3 cm depth in soil or placed on ground with litter cover were the most effective methods to produce large number of seedlings. With facilitation of shrub or tree overstorys at early seedling stages in shrubland, direct burying acorns at 3 cm depth in soil was the most effective and economical technique for oak reforestation in such open early successional habitats. # 2002 Published by Elsevier Science B.V. Keywords: Quercus liaotungensis Koidz.; Establishment; Regeneration; Cotyledon removal; Defoliation * Corresponding author. Tel.: 86-10-82599518. E-mail address: [email protected] (K. Ma).
0378-1127/02/$ ± see front matter # 2002 Published by Elsevier Science B.V. PII: S 0 3 7 8 - 1 1 2 7 ( 0 2 ) 0 0 2 7 4 - 8
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1. Introduction Throughout the world, oaks (Quercus spp.) usually have poor natural regeneration in the forests where they occur (Watt, 1919; Crow, 1988; Thadami and Ashton, 1995; Gardiner and Hodges, 1998), and may begin to be replaced by long-lived and more shadetolerant species in the absence of periodic disturbance, e.g. ®re (Lorimer, 1984; Abrams, 1992). The regeneration of trees generally depends upon their ability to provide suf®cient seeds, the capacity of seeds to geminate and subsequent growth and survival of seedlings. In previous studies, biotic and abiotic factors cited as contributing factors to oaks' natural regeneration failure are insect parasitization of acorns, predation by small mammals, seedling herbivory, frost damage, competition from herbaceous weeds and low light levels (Watt, 1919; McGee, 1975; Crow, 1988; Lorimer et al., 1994; Le Duc and Havill, 1998), the precise limiting factors for seedling establishment and failure of natural regeneration are unclear. Deciduous broad-leaved forest is the zonal vegetation type in the temperate zone of northern-central China. Oak (Quercus liaotungensis Koidz.) forests or those where oaks were dominant species used to distribute in this region (Chen, 1995). Currently it is dif®cult to ®nd patches of oak forests in low hills and mountains because of anthropogenic activities or clear-cutting for cultivation, especially in the 1950± 1960s. However, contrary to its relative overstory importance and favorable mast production of acorns in fragmented secondary well-developed oak forests, Q. liaotungensis saplings were absent in the understorys, which indicated its poor natural regeneration (Zhu, 1982). In some regions, shrubland, grassland or farmland have replaced oak forests widely (Chen, 1995). It is urgent and important to restore the oak forest in such areas for environmental improvement, sustainable development and biodiversity conservation. To develop effective and economic techniques for restoration also requires the full understanding of natural regeneration processes and their limiting factors. The effects of following factors on acorn germination, subsequent seedling establishment and growth were in the focus of this study: (1) variation of light availability caused by gap creation in understorys of mixed oak forest; (2) litter cover on the ground and
acorn burying depth in soil; (3) simulated defoliation and cotyledon removal 1 month after emergence; (4) shrub and tree overstorys in shrubland. 2. Methods and site description 2.1. Study area This study was carried out in Beijing Forest Ecosystem Research Station (BFERS), 114 km southwest of Beijing (408000 N, 1158260 E, 1140 m in altitude). The area is in the Dongling Mountain Region in Northern China, with a temperate continental monsoon climate. Mean annual temperature averages 4.8 8C (January 10.1 8C; July 18.3 8C). Precipitation amounts to 612 mm per annual, 78% of annual rainfall occurs from June to August. The site for the ®rst three experiment is a welldeveloped mixed oak forest stand (NW-facing slope, 218, about 1225±1350 m in altitude), where Q. liaotungensis (45%) is dominant canopy tree species with 8±10 m in canopy heights and about 50-year-old. Canopy coverage is about 80%. The shrub layer is composed of Lespedeza bicolor, Spiraea pubescens, Abelia bi¯ora, Deutzia grandi¯ora, and Rhododendron mucronulatum. On the forest ¯oor, herbaceous species were abundant. The soil in this area is mountain brown earth, >50 cm in depth; litter layer, 2±5 cm; humus, 15±20 cm. The shrubland (S-facing slope, 108, 1100 m in altitude) where the fourth experiment was conducted is characterized as an open early successional environment after clear-cutting, where Spiraea trilobata, Spiraea pubescens, Ulmus macrocarpa, Prunus davidiana, Prunus armeniaca and Syringa pekinensis are dominant canopy shrubs, with heights of 1±3 m. Sparse large trees of Fraxinus rhynchophylla and Q. liaotungensis also occur and total canopy cover is 30±50%. Carex humilis var. nana, Calamagrositis arundinacea and Spodiopogon sibiricus comprise most of the herb layer. The soil is light mountain brown earth with stones or rocky, <50 cm in depth; litter layer, <1 cm. 2.2. Experimental design Acorns were collected from the ground in the ®eld during September 1999 and were planted in early
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October. Sound acorns from the same plot were used in each treatment to avoid potential germination differences. Same source acorns were used in second and fourth experiments. Four experiments were conducted as follows. 2.2.1. Gap effects experiment In the mature forest understory, large gaps (LG), small gaps (SG) and under canopy(UC) nearby were selected as light gradient to test acorn germination and seedling establishment response to gap. Three aluminum or iron hybrid metal net cages 30 cm 30 cm 35 cm were set up to protect the acorns from animals within nine burying microsites. Soil collected from nearby understory sites was added in the gaps to unify soil type. Fourty ®ve or 50 acorns were buried at 3 cm depth in soil at each site. Unfortunately, only 24 cages were left perfect, i.e. without damage by human or animal disturbances. 2.2.2. Litter cover and acorn burying position in soil experiment Eight large cages 50 cm 50 cm 50 cm were scattered randomly in the mixed oak forest understory to test burying depth and litter effects on acorn germination and seedling establishment. Inside each cage, 100 acorns were planted in 10 lines for ®ve treatments as follows: acorns buried at 5 cm (5 cm) and 3 cm (3 cm) depth in soil, placed on ground surface (GR), covered with 2.5 cm deep litter cover (LC, similar to natural state), acorns placed on the litter (2.5 cm, OL). Two lines formed one treatment, which was separated by small slices of 5 cm high metal net. Plastic net was also used to ®x the acorns in the treatments GR and OL. By the time of harvest in autumn, only three cages had not been damaged by wild boars due to good protection of the iron cages. The treatments 3 or 5 cm in four broken cages were also well protected. 2.2.3. Simulated defoliation and cotyledon removal experiment Six large cages 100 cm 100 cm 50 cm with 60 acorns each (buried in soil at 3 cm depth) were set up at 10 m interval in two randomly located lines in the understory. To simulate herbivory or predation effects on seedling survival, 60 seedlings of similar size were chosen for defoliation treatments (one con-
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trol, and four degrees: 25, 50, 75, and 100%). The defoliation was conducted carefully on every leaf by hand and defoliated part was taken to lab for dry mass. Thirty six seedlings were studied for the effects of cotyledon removal (one control, two degrees: half and complete cotyledon removal) 1 month after emergence. After the treatments were imposed, insecticide was sprayed every 2 weeks on all seedlings and watered in soil to avoid insect damage. 2.2.4. Facilitation of tree and shrub overstory in shrubland In shrubland, nine cages 100 cm 100 cm 50 cm with 60 acorns each (buried at 3 cm depth in soil) were scattered in three different microsites: open site (OS), where all vegetation was removed; under shrub overstory (USh) without herb disturbance; under tree overstory of oak (UTr) without ground disturbance. 2.3. Data collection and analysis Seedling emergence and survival were monitored monthly from May to October inclusive. Growth parameters (height, leaf area, leaf number, stem basal diameter) were also measured at the same time. At the time of harvesting, seedlings were excavated, rinsed with clean water until free of soil and separated into root, stem and leaf. After the measurement of growth and morphology, the plant components were oven dried for more than 24 h at 80 8C before obtaining dry mass. The light environment of each burying site was measured by ``®sheye'' techniques according to the procedures of Zipperlen and Press (1996), using a Minolta 2500 dxi camera and Winphot software (Version 5.0, ter Steege, 1997). Acorn germination, seedling survival and recruitment (from seeds to seedlings), growth and biomass allocation were analyzed by ANOVA to test for treatment effects. Chi-square analyses were carried out to test the treatments of defoliation and cotyledon removal on subsequent seedling survival. Simple correlation analyses were conducted between establishment and light availability of seedling growing sites (large gaps, small gaps and under canopy), as well as between biomass accumulation and degree of defoliation and cotyledon removal. All analyses were carried out using SAS (Release 6.12, SAS Institute, Inc.).
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Fig. 1. Seedling emergence dynamics (a), acorn germination (b), seedling survival (c) and recruitment (c) (S.E.) across the large gap (LG), small gaps (SG) and under canopy (UC). Means sharing the same letter are not signi®cantly different from one another at P < 0:05 using Duncan multiple range test.
3. Results 3.1. Gaps effects on seedling establishment and seedling growth Seedling emergence was earlier in gaps than under canopies. Whereas in gaps, 20±40% were emergent in May, most seedling emergence occurred later under canopies (Fig. 1a). ANOVA analyses showed that acorn germination differed between sites (P < 0:05, Fig. 1b), and the most occurred in the large gaps. Seedling recruitment showed a similar trend as germination (P < 0:05, Fig. 1d). There were no differences
in seedling survival among three light conditions in the ®rst growing season (P > 0:05, Fig. 1c). Acorn germination and seedling recruitment were positively correlated with openness at each acorn burial site (R2 0:659, P < 0:001 and R2 0:447, P 0:034, respectively, Fig. 2 a and b), but seedling survival was not signi®cantly correlated with openness (R2 0:133, P 0:588). Seedlings in the large gaps grew tallest, faster and gained more dry mass than other seedlings, and they also had longer roots, greater leaf area, lower SLA (speci®c leaf area) than those from the other two sites (Table 1). Some seedlings had second ¯ushes in the
Fig. 2. Acorn germination (a), seedling survival (b) in relation to openness of growing sites (LG, SG and UC) in the understory of mixed mature oak forest (simple linear regression analysis).
Site
H (cm)
BD (mm)
RL (cm)
LMR
StMR
RMR
WhM (g)
SLA (m2 kg 1)
RGR (g g 1 W 1)
LAR (m2 kg 1)
RSR
RD (mm)
LA (cm2)
UC SG LG Pr > F
12.5 0.4 a 12.2 0.6 a 16.2 0.5 b ***
1.5 0.1 a 1.9 0.1 b 2.60 0.1 c ***
11.9 0.7 a 15.7 1.1 b 28.4 1.1 c ***
0.34 0.03 a 0.30 0.01 b 0.27 0.01 c ***
0.35 0.07 a 0.33 0.03 a 0.31 0.06 a ns
0.3 0.3 a 0.4 0.2 b 0.4 0.1 c ***
0.3 0.02 a 0.5 0.1 b 1.3 0.1 c ***
34.6 0.9 a 27.3 0.8 b 21.7 0.6 c ***
0.01 0.003 a 0.02 0.003 b 0.07 0.007 c ***
11.3 0.5 a 8.2 0.3 b 5.8 0.2 c ***
0.5 0.3 a 0.6 0.4 b 0.8 0.3 c ***
2.4 0.1 a 3.3 0.1 b 4.3 0.1 c ***
29.2 2.8 a 41.2 4.4 b 71.4 4.8 c ***
a Three microsites are large gaps (LG), small gaps (SG) and under the canopy (H, height; BD, stem basal diameter; RL, root length; LMR, leaf mass ratio; StMR, stem mass ratio; RMR; root mass ratio; WhM, whole seedling dry mass; SLA, speci®c leaf area; RGR, relative growth rate; LAR, leaf area/seedling dry mass; RSR, root:shoot ratio; RD, root collar diameter; LA, total leaf area). b Values with different letters in each column are signi®cantly different (Duncan multiple range test, * P < 0:05; ** P < 0:01; *** P < 0:001; ns, not signi®cant).
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Table 1 ANOVA analyses on growth and biomass allocation (S.E.) of Q. liaotungensis seedlings growing at different microsites in mature oak foresta,b
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Fig. 3. Seedling dynamics (a), acorn germination (b), seedling survival (c) and recruitment (d) (S.E.) from acorns placed on litter (OL), covered with litter (LC), exposed on ground surface (GR), buried at 3 cm (3 cm) depth in soil and 5 cm (5 cm). Means sharing the same letter are not signi®cantly different from one another at P < 0:05 using Duncan multiple range test. (* P < 0:05;** P < 0:01; ns, not signi®cant).
HL and ML treatments, and a few plants had third ¯ushes in large gaps. But no multiple ¯ushes were observed for seedlings growing beneath the canopy. 3.2. Effects of acorn burying position on seedling establishment and seedling growth Excepting acorns that had been placed on the ground surface, most of the seedlings were emergent by July, which coincided with the rains from late June to August (Fig. 3a). Acorn germination and seedling recruitment were in the order: placed on litter < exposed on ground surface < buried at 5 cm depth in soil < at 3 cm depth in soil < covered by litter on ground (Fig. 3 a and d). Seedlings survived very well when acorns were buried in the soil or covered by litter (Fig. 3c). Different planting depths in soil had no signi®cant effects on seedling survival in the ®rst year. It is surprising to ®nd high survival of seedlings produced from acorns lying on the ground surface, but those late emergent seedlings cannot fully develop before the onset of winter and may be easily damaged by cold. Different acorn planting positions not only in¯uenced seedling establishment, but also seedling growth
and biomass allocation. Covering acorns with litter increased height growth but decreased stem basal diameter and leaf number more or less compared to those buried at 3 cm in soil (Table 2). Seedlings produced by acorns buried in soil at 3 cm depth had the largest stem basal diameters and greatest leaf number but they were intermediate in height. Nevertheless, seedlings emerging from acorns planted at 3 cm depth in soil, generally outperformed those produced from acorns that had been planted at 5 cm depth, exposed on ground surface or placed on litter (Table 2). Owing to early leaf shedding, seedlings grown from acorns that were placed on litter were excluded from the analysis on biomass allocation. Seedling that grew from acorns covered by litter had greater root length, whole dry mass and faster relative growth rates than those in treatments GR and 5 cm. Seedlings from acorns that were placed on the ground surface had signi®cantly smaller stem lengths, RL, dry mass and RGR than those from other treatments (Table 2). Burying acorn too deep in soil decreased the root length (RL), leaf area ratio (LAR), leaf mass ratio (LMR), whole dry mass and RGR, but increased stem length and stem mass ratio (Table 2).
Table 2 ANOVA analyses on growth and dry mass allocation (S.E.) of Q. liaotungensis seedlings from the acorns with different planting positionsa,b Planting position
H (cm)
LC GR 3 cm 5 cm OL Pr > F
10.3 8.8 8.9 6.1 6.8 ***
BD (mm)
3.0 2.3 2.2 2.1 3.5
a ab bc d cd
1.6 1.5 1.7 1.4 1.2 **
0.2 0.3 0.3 0.2 0.7
LN (n) ab ab b bc c
3.0 3.2 3.9 3.8 2.3 ***
0.7 1.5 1.0 1.0 1.2
StL (cm) ac ab b b c
13.5 9.9 13.7 15.8 ±c *
1.0 1.3 0.8 0.7
RL (cm) a b a a
14.7 12.3 15.3 12.1 ± *
1.0 4.8 1.1 0.9
LMR a b a ab
0.33 0.41 0.38 0.25 ± *
StMR 0.03 0.03 0.01 0.02
a b ab c
0.26 0.21 0.31 0.44 ± *
RMR 0.02 0.02 0.01 0.02
a ab b c
0.40 0.38 0.31 0.31 ± *
WhM (g) 0.03 0.04 0.01 0.01
a ab b b
0.7 0.5 0.7 0.6 ± *
0.2 0.2 0.2 0.1
RGR (mg g
SLA (m2 kg 1) a b ab ab
31.9 33.9 33.8 36.5 ± *
0.9 2.2 0.9 1.2
a ab ab b
1.3 0.9 1.2 1.1 ± *
1
LAR W 1) (cm2 g 1)
0.3 0.3 0.2 0.1
a a ab b
105.0 134.6 127.9 89.9 ± *
10 a 3 bc 6 ac 6a
RSR 0.59 0.64 0.46 0.45 ± *
LA (cm2)
RD (mm)
0.06 0.09 0.03 0.02
a bc c c
3.4 2.6 2.8 2.5 ± *
0.2 0.3 0.2 0.2
a b ab b
46.8 53.1 47.8 25.1 ± *
5.8 a 15 a 4.6 a 2.7 b
a Acorns burying positions are covered by litter (LC), exposed on the ground surface (GR) and on litter (OL), and buried at 3 cm or 5 cm depth in soil. (H, height; BD, stem basal diameter; LN, leaf number; StL, stem length; RL, root length; LMR, leaf mass ratio; StMR, stem mass ratio; RMR; root mass ratio; WhM, whole seedling dry mass; SLA, speci®c leaf area; PGR, relative growth rate; LAR, leaf area/seedling dry mass; RSR, root: shoot ratio; RD, root collar diameter, LA, total leaf area). b Values with different letters in each column are signi®cantly different (Duncan multiple range test). c Data was absent because too few seedling survived until the time of harvesting,* P < 0:05; ** P < 0:01; *** P < 0:001.
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Fig. 4. The effects defoliation (a) and cotyledon removal (b) on subsequent seedling survival (Chi-square test) and dry mass accumulation (c and d) (simple linear regression analysis). (* P < 0:05; ** P < 0:01; ns, not signi®cant).
In general, the seedlings that grown from acorns buried in soil or covered by litter grew better than those in other treatments. Seedlings that grew from acorns buried too deeply in soil or growing without protection may suffer increased mortality as resulting from slow growth or non-optimal resource allocation. 3.3. Effects of simulated defoliation and cotyledon removal on seedling survival and biomass accumulation Even after 75% defoliation, seedlings survived well until the end of the growing season. However, complete defoliation caused seedling mortality to reach 16.7% which was signi®cantly worser than for undefoliated seedlings (X 2 8:276, P 0:044) (Fig. 4a). Complete cotyledon removal seriously decreased seedling survival to 50%, which was signi®cantly lower than seedlings without cotyledon removal (X 2 12:727, P < 0:001) (Fig. 4b). The defoliation not only in¯uenced the subsequent survival, but also decreased the dry biomass accumulation signi®cantly in ®rst growing season (R2 0:899, P < 0:001) (Fig. 4 c and d). So did cotyledon removal (R2 0:746, P < 0:001). The decrease of biomass will inevitably increase the possibility of mortality,
especially in the highly competitive or resource limited conditions, such as in shaded understorys and where repeated defoliation occurs. 3.4. Seedling establishment in shrubland Similar to seedling emergence dynamics in large gaps under mature mixed oak forest, seedlings at open sites in shrubland where high light availability occurred, emerged earlier than those in other treatments in the shrubland (Fig. 5a). Even although seedlings produced from acorns placed under shrub or tree overstorys emerged about 1 month later than seedlings from acorns planted at open sites, acorn germination, seeding survival and recruitment in the shade were signi®cantly better than those in the open sites (Fig. 5). However, there were no difference among treatments in height, leaf area, leaf number or stem basal diameter among the three treatments. During summer, some leaves of seedlings growing in open sites appeared to have been bleached by strong direct light, and which subsequently died. These observations concur with Kitzberger et al. (2000) who found that strong direct light caused yellowish coloration and death of seedling in open ®elds even after adding water.
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Fig. 5. Seedling dynamics (a), acorn germination (b), seedling survival (c) and recruitment (d) (S.E.) from acorns buried in open site without vegetation cover (OS), under shrub canopy(USh) and under tree canopy (UTr). Means sharing the same letter are not different from one another signi®cantly P < 0:05 using Duncan multiple range test.
Due to mortality, few seedlings were available for growth study for open sites. Consequently, biomass allocation studies were not conducted which may have resulted in loss of important information. 4. Discussion 4.1. Gap effects on seedling establishment and biomass accumulation Light as well as other resources would increase to understory plants and tree seedlings after gaps in canopies are created (Chazdon and Fetcher, 1984; Canham, 1988). The importance of gaps for establishment and growth of different tree species has been documented widely throughout the world (Brokaw, 1985; Uhl et al., 1988). In this study, not only acorn germination and seedling recruitment of Q. liaotungensis were signi®cantly better in gaps than in shaded understory, but also they tend to survive better. These results coincide with previous ®ndings that light played an important role in the establishment of oak seedling. For example, Suh and Lee (1998) found that although more acorns remained in subplots within forests than in clear-cut
areas, more acorns germinated in clear-cuts, and heights of seedling in large clear-cuts were greater than those under canopies or in small gaps. Germination of Quercus (section Erythrobalanus) was greater in gap centers and north edges of gaps than in understory sites (Ashton and Larson, 1996), but low light increased the time necessary for germination to take place. Lorimer et al. (1994) found that removal of understory vegetation resulting in light increment enhanced Quercus spp. seedling survival to 90% in contrast to less than 30% for seedlings beneath the mature stands. The replacement of Quercus petraea by Carpinus betulus was due to its light compensation point being higher than the maximum available light under the main tree canopies in the wood (Le Duc and Havill, 1998). By contrast, some studies found that shade facilitated acorn germination, especially in arid areas. For example, cleared or cut sites had low acorn emergence and seedling survival in contrast with higher values obtained under the canopy (Bran et al., 1990; Callaway, 1992a; Weltzin and McPherson, 1999). Truax et al. (2000) also found that Q. robur achieved better growth and survival of seedling in a relatively shaded stand. Previous research suggested that Quercus seedling establishment response to light
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availability varies among species. For example, Figueroa-Rangel and Olvera-Vargas (2000) found that the presence of oak seedlings for a range of species was strongly associated with percentage of openness, e.g. Q. candicass, Q. laruina, Q. rugosa, Q. castanea, Q. crassipes required about 6.4, 2.9, 6.8, 13 and 8.1%, respectively, for successful establishment. Nevertheless, most researchers have found positive effects of increased light increase in gaps on oak seedling establishment because of enhancement on oak seedling growth (Kolb and Steiner, 1990). Even though oak seedlings may grow at irradiance as low as 1% of full light, the dry mass of oak seedlings usually increases with light intensity (Finzi and Canham, 2000; Jarvis, 1964; Ovington and MacRae, 1960). In this study, we found that oak seedlings grew faster, taller and accumulated more dry mass when they occupied large gaps in the canopy. They also produced multiple ¯ushes in large gaps than those growing under the canopy. Jarvis (1964) found that whole dry mass, maximum photosynthetic rate, RGR, root mass ratio, survival of Q. petraea seedling increased with light availability increasing. He also found that shading resulted in increased SLA, LAR and decreased root weight, RSR and assimilation rate. Expecting Q. rubra which grew well with intermediate light availability, seedlings survived better in gap centers than elsewhere (Ashton and Larson, 1996). LoÈf (2000) also found that for Q. robur L., greatest seedling growth and survival occurred in the clear-cuts. Espelta et al. (1995) found that young seedlings survived better under closed canopies but he concluded that the sapling stage would only be attained in stands where suf®cient radiation penetrates the leaf canopy to enhance growth of older seedlings. This conclusion was also reached by Tanouchi et al. (1994) who found that in spite of the presence of large seedling and sapling banks of Q. acuta, Q. gilva, Q. salicina and Q. sessilifolia and survival of 60±80%, the young trees are unlikely to attain canopy positions from within closed stand due to their very small annual height increment (less than 5 cm in 3 years). Combined the results from this and previous studies, we conclude that gap creation should bene®t natural regeneration of Q. liaotungensis forest through enhancement of seedling establishment and growth in mature mixed oak forests.
4.2. Effects of acorn burying position on seedling establishment and growth Viability of Quercus acorns declines or lose rapidly if acorns lose water without protection on the ground surface after falling from tree (Borchert et al., 1989; Harmer, 1995). We found that about 3 cm deep litter cover improved acorn germination of Q. liaotungensis to a peak of 70%, in contrast to 58.1, 45, 28.3 and 8.3% for acorns buried in soil at 3, 5 cm, placed on ground surface or directly on the litter layer respectively. Jarvis (1964) found that the loss of moisture by acorns covered with litter was much less than for those exposed on the ground surface, and that water content was positively related to viability. The germination of Q. laurina was improved by 15% when acorns were covered by 3 cm deep litter on ground surface (Camacho-Cruz et al., 2000). Despite the positive effects of litter, such as increased germination, decrease of moisture and temperature extremes (Barton and Geeson, 1996), negative effects of litter also existed. From this study, the acorns on the litter germinated less and suffered high mortality contrasting to other treatment, because litter may present a physical barrier to germination and emergence (Facelli and Pickett, 1991), increase etiolation of seedlings resulting in increased risk of physical damage (Barrett, 1931), cause greater fungal infection or even herbivory (Facelli, 1994). So, covering acorns with too much or too little litter may have negative effects, 1.9±2.5 cm (0.75±1 in.) seemed optimal for the establishment of chestnut oak seedlings (Barrett, 1931). In our study, about 3 cm deep litter cover seemed optimal for acorn germination of Q. liaotungensis. Burying is helpful to seedling establishment of oaks. In this study, we found that burying acorns at 3 cm depth in soil signi®cantly enhance their germination and seedling recruitment in addition to litter cover, relative to those exposed on bare ground surfaces and litter. Although, there is no signi®cant difference in seedling survival between acorns buried at 3 and 5 cm depth in soil in the ®rst growing season, they showed some differences in germination, emergence time, recruitment, and growth, especially allocation of more resources to stems and fewer to leaves for the latter. Timing of emergence also plays a critical role in seedling establishment in plant species,
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particularly under competitive conditions (Miller et al., 1994). For example, seedling recruitment for buried acorns was twice that of surface-sown acorns due to improved germination. Ovington and MacRae (1960) found that more than 80% of acorns germinated in soil at 2.5 cm depth and that less than 1% germinated on bare ground because of root desiccation. Kollmann and Schill (1996) also found that Q. petraea germinated 62±86% more at 5±6 cm depth in the soil than on the surface across different microsites. About 59% of oak seedling death was attributed to desiccation in some habitats without protection (Fuchs et al., 2000). Burying acorns too deeply in soil may also increase seedling mortality due to delayed emergence and nonoptimal allocation of resources. Watt (1919) found that planting too deeply in soil decreases germination of oaks. Iida (1996) found that emergence of Q. mongolica germinants was poorer when planted at 10 cm depth than when planted super®cially, and germinants failed to emerge when planted if at 25 cm depth. Burying protects acorns from rodent predation by limiting odor diffusion. Borchert et al. (1989) found that vertebrates removed >53% of acorns placed on the ground surface in contrast to about 7± 48% of acorns buried in the ground cover or in the soil. In this study, boar predation through the broken cages was stronger for acorns exposed on ground surface and on litter than for those were buried in soil at 3 and 5 cm depth. 4.3. Simulated defoliation effects on seedling survival and growth Herbivores in seral communities are reported to consume only a small proportion of the productivity (Odum, 1960). However, exclusion of herbivores in old-®eld communities produces important changes in community structure and population dynamics (Brown, 1985). Height growth and survival of Q. robur seedling increased by 20 and 5±45%, respectively, with insecticide treatment in the ®eld (LoÈf, 2000). Oak seedling usually undergo repeated defoliation by the larvae of various Lepedopteran species, and their establishment and growth were restricted in consequence, which could explain the failure of regeneration under a canopy of mature oaks (Shaw, 1974), or reduction of competitive ability of the grazed plants (Edwards et al., 1992). In current study,
143
although, defoliation had less severe effects on seedling survival than those caused by cotyledon removal, more than 16.7% of seedlings died after the complete defoliation 1 month after emergence. Similarly, Negi et al. (1996) found that herbivory at shaded microsite accounted for 63.2% mortality of Q. ¯oribunda seedling. In this study, some seedlings re¯ushed after complete defoliation and produced young shoot, which may cause repeated insect defoliation, because oakfeeding species such as Lepidoptera prefer young leaves for seasonal decline of leaf proteins and increment of tannins concentrations (Feeny, 1970). As a result, repeated defoliation occur and cause more serious damages to seedling. 4.4. Cotyledon removal effects on seedling survival and growth The cotyledon is very important for acorn germination and subsequent seedling establishment, growth and survival because it serves as the main nutrient resources for young seedlings (Ovington and MacRae, 1960). Whereas complete removal of cotyledons 1 month after seedling emergence in this study, caused up to 50% seedling mortality, half removal of the cotyledons had no direct effects on seedling survival in the ®rst growing season. This result contrasts with Andersson and Frost (1996) who found no negative effects of cotyledon removal on survival of Q. robur during the ®rst growing season, and with Sonesson (1994) who found no effects of cotyledon removal on Q. robur seedling growth and survival at the time of the ®rst lea®ng, even when seedlings had established on poor soil. Nevertheless, our results are consistent with Bon®l (1998), who found that survival of Q. rugosa seedlings from medium sized acorns was lowered by 17% due to cotyledons removal 1 month after emergence in glasshouse studies, he also reported 60% mortality of Q. laurina occurred when cotyledons were removed. Similarly, after one growing season, Frost and Rydin (1997) found large negative effects of cotyledon removal not only on competitive ability, but biomass and survival. It is widely reported that 30±90% viability loss of acorn is due to insect parasites. Weevils cause acorn death completely in some individuals in non-mast
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years (Crawley and Long, 1995). Barrett (1931) found that about 40% of acorns attached to well-developed seedlings had been damaged by weevils or gall forming insects in chestnut oak. We found that most of the attached acorns on 27 dead seedlings in July showed signs of insects damage. At harvest, we found 116 out of 237 (48.9%) acorns had been damaged to some extent by insects parasite. Therefore, cotyledon reserves play an important role in seedling growth and survival even after the emergence in the ®rst growing season and future performance for Q. liaotungensis, especially for those in unfavorable conditions.
by as much as 19-fold and also increased seedling recruitment 30- or 60-fold for Q. emoryi in savanna in North American (Weltzin and McPherson, 1999). Overstory shade bene®ts are complicated by indirect effects of shade on seedling microenvironments that may also affect seedling performance. Shade can also improve survival of oak seedlings by reducing heat or water stress or providing protection from herbivores (Crow, 1988; Callaway, 1992b). Shrub cover also improves the retention of seeds and reduces animal browsing signi®cantly (Dubois et al., 2000).
4.5. Shrub facilitation
For mixed mature oak forest, predation on cotyledons and defoliation of seedlings, heavy insect parasitism of acorns, low light availability in the understory, litter depth and soil properties are among the limiting factors for natural regeneration. Results from this study and previous studies suggest that selective-cutting or intermediate canopy disturbance would be a good management policy to encourage natural regeneration in oak woods. For reafforesation, sowing acorns in soil at 3 cm depth was the most effective technique to maintain and favor regeneration. While too deep and thick litter may cause negative effects on seedling recruitment. Where shrub or sparse tree canopies exist, direct seeding in soil appeared to be the most effective and economic method for oak restoration.
In the early successional shrubland, we found that acorns germinated better and seedling survived better when acorns were buried under the ovestorys of shrubs or trees, indicating positive effects of shade in sunny open habitats. Our results are in consistent with Zhang (2001) who found recruitment of Q. liaotungensis seedlings correlated positively with vegetation cover when acorns were buried in soil on south facing slopes. Similarly, Callaway and D'Antonio (1991) reported that shrubs could have strong facilitative effects on the survival of Q. agrifolia seedlings and Callaway (1992a) found that the presence of shrubs raised the survival of 1-year Q. douglasii seedlings from zero to 30±50% because of shade bene®ts and acorn protection from predation and herbivory. In the cleared or cut sites, acorn emergence and seedling survival were lower than under the canopy (e.g. Q. ilex and Q. pubescens) (Bran et al., 1990). Not only shrubs have bene®ts to germination and survival, but other vegetation cover also have. Kollmann and Schill (1996) found that Q. petraea germinated more in unmown sites than mown areas where grass had been cut (20% vs. 5%). Negi et al. (1996) found that ground herbage clearance at sunny microsites accounted for 53.4% mortality Q. ¯oribunda seedlings. Truax et al. (2000) found that red oak and bur oak (Q. macrocarpa) could be successfully grown herbicide-free using shelterwood systems in mesic forested environments in southern Quebec. Provisions of arti®cial or natural shade increased seedling emergence and subsequent survival
4.6. Management implication
Acknowledgements This research was supported by National Natural Science Foundation of China (Nos. 39893360, 39770131 and 39970136). We sincerely thank Mr. Xiaodong Yu, Jingsheng Zhang, Zhongfei Li, Wei Chen and Miss Wenjie Yan for ®eld data collection. We are deeply indebted to all staffs of BFERS for their great support in ®eld. The authors gratefully thank two anonymous reviewers for their helpful comments.
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