Forest Ecology and Management 258 (2009) 1293–1300
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Establishment and early growth of introduced indigenous tree species in typical plantations and shrubland in South China Jun Wang a,b, Hai Ren a,*, Long Yang a,b, Wenjun Duan a,b a b
Heshan National Field Research Station of Forest Ecosystem, South China Botanical Garden, Chinese Academy of Sciences, Xingke Road 723, Tianhe District, Guangzhou, 510650, China Graduate University of the Chinese Academy of Sciences, Beijing, 100049, China
A R T I C L E I N F O
A B S T R A C T
Article history: Received 8 March 2009 Received in revised form 15 June 2009 Accepted 15 June 2009
Unsuccessful colonization by indigenous tree species into established plantations has retarded the succession of artiﬁcial plantations to more natural, secondary forests in South China. To understand how to improve colonization by seedlings of indigenous species, we determined how performance of indigenous seedlings is affected by seedling species (the shade-intolerant Castanopsis chinensis, the moderately shade-intolerant Michelia chapensis, and the shade-tolerant Psychotria rubra), the site into which the seedlings were transplanted (a mixed-legume plantation, a eucalyptus plantation, a mixednative plantation, a mixed-conifer plantation, and a shrubland), and site preparation (removal or retention of understory vegetation and litter). Seedling survival and growth were generally increased by removal of understory vegetation and litter. C. chinensis and M. chapensis grew better in the mixedlegume and mixed-conifer plantations, while P. rubra grew better in mixed-native and mixed-conifer plantations. Responses of the transplanted seedlings to environmental factors were species speciﬁc. The effects of light on seedling survival and growth were correlated with the shade tolerance of the species. Soil moisture was important; it was positively correlated with survival but negatively correlated with growth of C. chinensis seedlings. Growth of C. chinensis and M. chapensis was positively correlated with soil potassium, while growth of P. rubra was positively correlated with soil organic matter but negatively correlated with soil hydrolyzed nitrogen. These ﬁndings suggest that we should select suitable native species under the different plantations before improvement of plantations. Light and soil moisture are most important environmental factors for the selection of species speciﬁc. Site preparation and fertilizer are needed during the improvement of those plantations. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Colonization Indigenous tree species Transplanting Seedling performance Understory vegetation Litter
1. Introduction The climax vegetation in southern China is monsoon evergreen broad-leaved forest. Historically, this forest type was broadly distributed but because of intensive anthropogenic disturbances, particularly in the last half century, most of this forest was turned into pastures or grassland (Peng, 2003). To restore forest cover and ecosystem functions and services, the government established large plantations in this region in the past 20 years (SFA, 2005). However, most of these plantations were planted with nonindigenous, fast-growing pioneer tree species (Ren et al., 2007). After decades of development, habitat conditions in the plantations have somewhat improved and some native shrub species have colonized in the understory (Fang and Peng, 1997; Duan et al., 2008). Such plantations, however, are still dominated by trees and shrubs of the pioneer community, and indigenous tree species
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(H. Ren). 0378-1127/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2009.06.022
characteristic of the zonal climax community are scarce (Duan et al., 2008). Because of the low biodiversity and inadequate ecosystem services of the established plantations, silviculture management that can accelerate the succession of plantations to more natural stages is urgently required (Ren et al., 2002, 2007). Therefore, understanding how to promote establishment of native species in plantations is an essential objective of current restoration and forest management research. Many previous studies have demonstrated that lack of seed sources is the major bottleneck limiting the colonization of established plantations by indigenous species (McClanahan, 1986; Mclaren and Mcdonald, 2003; Denslow et al., 2006). Consequently, introduction of target species has been the focus of attempts to accelerate forest succession. The most common approach to accelerate forest succession has been to plant seedlings of target species in the established plantations into which the target species had failed to disperse naturally (McClanahan, 1986; Hardwick et al., 1997). The seedling, however, is a vulnerable stage in the life cycle of plants (Watson et al., 1997; Holl, 1998; Rey and Alcantara, 2000; Puerta-Pinero et al., 2007). Although introducing target
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species can eliminate the bottleneck of limited seed dispersal, many abiotic or biotic factors (such as inadequate soil water and nutrients, high temperature, herbivory, litter cover, and competition from understory vegetation) reduce seedling establishment and therefore limit recruitment (Howlett and Davidson, 2003; Lenz and Facelli, 2005; Dupuy and Chazdon, 2008). Understory vegetation and associated litter are thought to inﬂuence the establishment of tree seedlings. Removing understory vegetation and associated litter can beneﬁt the early phase of plant establishment by increasing light penetration, reducing fungal and bacterial pathogens, reducing physical barriers, and reducing competition (Brewer, 1999; Aranda et al., 2001, 2004; Stevenson and Smale, 2005; Charlotte et al., 2006; Knapp et al., 2006). In some other situations, however, understory vegetation and litter signiﬁcantly facilitate seedling emergence and recruitment by moderating temperature, humidity, and light penetration, and by improving soil nutrient status (Suding and Goldberg, 1999; Li and Ma, 2003). Moreover, many studies have found that the effects of understory vegetation and litter on seedling establishment were species speciﬁc and site speciﬁc (Suding and Goldberg, 1999; Yates et al., 2000; Janecek and Leps, 2005; Donath et al., 2006; Dupuy and Chazdon, 2008; Rodrı´guez-Calcerrada et al., 2008). Therefore, the effects of early successional communities (pioneer communities) on target seedlings may differ depending on the habitat provided by the community and the species of seedling. Few studies, however, have determined which factors most affect establishment of indigenous tree seedlings when such seedlings are planted in subtropical plantations and shrublands. Effective management of the plantations and shrublands to facilitate succession to more natural forests requires that researchers identify the determinants of seedling establishment and recruitment of indigenous species. In this study, we transplanted seedlings of three indigenous tree species (shade-intolerant Castanopsis chinensis, moderately shadetolerant Michelia chapensis, and shade-tolerant Psychotria rubra) into four typical plantations and one shrubland. The plantations and shrubland (which was 23 years old and undergoing natural succession) were located in South China. Our objectives were to determine how performance (survival and growth) of the transplanted indigenous seedling is affected by (1) the species of seedling; (2) the community into which the seedling is transplanted; and (3) retention or removal of litter and understory vegetation. We also wanted to determine the key environmental factors determining the survival and growth of indigenous seedlings. 2. Materials and methods 2.1. Study area The study area was located at the Heshan National Field Research Station of Forest Ecosystem, Chinese Academy of Science (1128540 E, 228410 N), Heshan City, Guangdong, South China. This area is characterized by a typical subtropical monsoon climate with a mean annual temperature of 21.7 8C. The mean annual rainfall is 1700 mm, and most rainfall occurs between May and September. The annual evapo-transpiration potential is approximately 1600 mm (Duan et al., 2008). The elevation ranges from 0 to 90 m, and the soil is laterite. The zonal climax vegetation is subtropical monsoon evergreen broad-leaved forest, the closest example of which is located at Dinghushan Mountain Natural Reserve, about 70 km north of the research station. In 1984, experimental plantations were established at the study area on homogenous degraded hilly land to restore the degraded ecosystems. At the same time, part of the degraded land was left unplanted and without further disturbance and had naturally
succeeded to the shrubland stage. The dominant species in the degraded land before plantation establishment were Ischaemum indicum, Eriachne pallescens, and Baeckea frutescens. Five experimental sites were selected in different plantations and shrubland. The CP site (3.17 ha) was a mixed-conifer plantation, and the main established species were Pinus massoniana and Cunninghamia lanceolata, with mean basal area of 227 cm2. The LP site (3.99 ha) was a mixed-legume plantation, and the main established species were Acacia mangium, Acacia auriculaeformis, Acacia confuse, and Acacia holosericea, with mean basal area of 255 cm2. The EP site (1.79 ha) was a eucalyptus plantation, and the main established species was Eucalyptus exserta, with mean basal area of 154 cm2. The NP site (2.68 ha) was a mixed-native species plantation, and the main established species were Schima superba and Cinnamomum burmanii, with mean basal area of 201 cm2. The SL site (3.5 ha) was a shrubland that had undergone natural succession from the former degraded land and which was dominated by Ilex asprella, Evodia lepta, and Trema tomentosa, with mean basal area of 28 cm2. All the trees in above plantations were planted at 2.5 m 2.5 m spacing. All four plantations and the shrubland had been left to develop naturally without anthropogenic disturbance. 2.2. Study species The three species selected in this study were C. chinensis, M. chapensis, and P. rubra. All three are native and common in the zonal climax monsoon broad-leaved forest in South China. C. chinensis is a relatively shade-intolerant tree that can reach 30 m in height and can grow in a wide variety of forest types and light conditions ranging from forest understory to large gaps (Du and Huang, 2008). M. chapensis is a tall moderately shade-tolerant tree and is always a canopy tree species, reaching 30 m in height (Liu, 1996). P. rubra is a shade-tolerant small tree that grows in shady and humid microhabits (Ren et al., 1997) of late successional plantations and secondary forests. 2.3. Experimental design We designed a 3 5 2 factorial experiment to examine how the survival and growth of target seedlings were affected by species (three species of seedlings), site (ﬁve sites), and treatment (two treatments: removal or retention of understory vegetation and litter; understory vegetation and litter were treated as one combined factor). The experiment was established according to a split-plot design with whole plots in a randomized complete block design. At each site, three blocks were established. Each block was then subdivided into six subplots, and the levels of understory vegetation and litter (presence or absence) were established as follows. In three randomly selected plots, aboveground understory vegetation and litter were left in place. In the other three plots, aboveground understory vegetation and litter were cleared by hand before seedlings were transplanted and every 2 weeks thereafter during the experiment. Each plot was surrounded by a 1-m-high nylon mesh fence to prevent herbivory by rodents. Seedlings of C. chinensis and P. rubra for transplanting in the ﬁeld were grown from the seeds collected from the monsoon broad-leaved forest in the Dinghushan Biosphere Reserve. Seedlings of M. chapensis were obtained from the Forestry Institute of Guangdong Province, China. All seedlings for transplanting were about 6 months old, and no signiﬁcant differences for the initial size of the seedlings were found among the three species. Thirty seedlings of one species were transplanted into each plot just after an occurrence of rain in late April 2007 (the rainy season). Each species was represented by two plots (presence or absence of understory vegetation and litter) in each block. Transplanted
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seedlings were watered shortly after planting but were not watered again and were not fertilized during the experiment, which ended in December 2008. The number of dead transplanted seedlings and also the height and basal diameter of seedlings were recorded monthly during the ﬁrst 6 months and bimonthly in the rest of the experiment. Each dead seedling was marked with a plastic tag. After the experiment ended (20 months after transplanting), up to 10 plants (roots and shoots) per plot were randomly chosen and collected if more than 10 seedlings survived, while all surviving seedlings were collected if fewer than 10 seedlings survived in the plot. The different fractions of the plants (leaves, stem and roots) were split (Wang et al., unpublished data). The collected seedlings were oven dried at 65 8C for 72 h and then weighed. 2.4. Environmental conditions Soil chemical properties were determined just before the seedlings were transplanted. Approximately 10 soil cores (4-cm diameter, 0–20-cm depth) were taken from each block of each site. Soil samples from each block were pooled together, air-dried, and then sieved for analysis for chemical characteristics. Soil chemical properties (including soil organic matter, hydrolyzed nitrogen, available phosphorus, and exchangeable potassium) were analyzed by standard methods (Standford and English, 1949; Olsen et al., 1954; Institute of Soil Science, 1978). For measurement of soil bulk density, three intact soil cores within depth of 5 cm from the soil surface were collected randomly from each plot of each site, using stainless steel ring (depth and diameter of 5 cm, respectively) after removing the litter and humus layer. The physical and chemical characteristics of soil collected from the ﬁve sites were shown in Table 1. Bulk density tended to be highest at the NP site and was lowest at the CP site. Soil organic matter content did not differ among the sites. Soil hydrolyzed nitrogen was higher at the LP site than at the SL site and was intermediate at the other sites. Exchangeable potassium tended to be highest at the LP site and lowest at the EP site. Available phosphorus was relatively high at the SL site but did not signiﬁcantly differ among the sites. Microclimatic conditions, including soil moisture content and light penetration (% above-canopy sunlight reaching understory) were measured in each block. Soil water content (%, g of water per 100 g of dry soil) in the top 10 cm of the mineral soil was determined during the dry season (in July, September, and December of 2007, and in March, July, and September of 2008). Ten soil cores (4-cm diameter) were extracted randomly from each experimental block for both treatments of understory vegetation and litter (presence or absence), and then pooled. Light penetration in the understory was expressed as a percentage (total light radiation in the understory/total light radiation in an open area outside of the experimental sites 100). The total light radiation was measured between 1200 and 1400 h on 1 day with clear weather condition in July 2007 and 2008 using a LICOR-LI-250 light meter (LI-COR, Lincoln, Nebraska, USA). Composition of understory
vegetation was determined, and the percentage of canopy cover in plots where vegetation was not removed was visually assessed throughout the study. Litter on the soil surface (above the mineral soil) was collected from eight randomly selected areas (1 m 1 m) in each site. The mass of the litter was determined after the litter had been dried at 65 8C for 72 h. 2.5. Data analysis The effects of site, species, and understory vegetation and litter on ﬁnal transplanted seedling survival and growth were assessed using three-way ANOVAs for a randomized block design. Site was treated as a blocking factor. The effects of site and understory vegetation and litter on soil water content were assessed using two-way ANOVAs. Differences in environmental conditions among different forests were analyzed using one-way ANOVA. Variables were log10 or arcsine square-root transformed when they did not satisfy normality assumptions. Multiple comparison analyses (LSD) were used when ANOVAs were signiﬁcant at a = 0.05. Because all transplanted seedlings of M. chapensis in one plot at the shrubland site (SL) had died by the end of experiment, M. chapensis at the SL site was not included for multiple comparison analyses. Multiple stepwise regression analysis was used to determine relationships between survival and growth of seedling and environmental factors. In addition, canonical redundancy analyses (RDA) (Lepsˇ and Sˇmilauer, 2003) were used to analyze the relative effects of environmental variables on seedling survival and growth. Because all transplanted seedlings of M. chapensis in one plot at the shrubland site had died by the end of experiment, the three species were analyzed together for seedling survival, while seedling growth of each species was analyzed individually. All analyses were performed with SPSS 11.5 and CANOCO 4.5 for Windows. 3. Results 3.1. Environmental conditions In plots where vegetation and litter had not been removed, the main understory herbaceous species in the four plantation and shrubland sites was Ottochloa nodosa. The percentage of coverage by the understory plants during the experiment tended to be high in the LP site, but no signiﬁcant differences were found among the ﬁve sites (Table 2). At the start of the experiment, standing litter biomass on the soil surface was higher at the NP and LP sites than at the EP and SL sites and was intermediate at the CP site (Table 2). Light penetration in the understory, which was determined in July 2007 and 2008, was higher at the LP and CP sites than at the NP sites and was intermediate at the other sites (Table 2). ANOVA showed that soil water content was signiﬁcantly affected by site (F = 7.535, P < 0.000) and site preparation (removal or retention of understory vegetation and litter) (F = 24.306, P < 0.000), but the interaction between site and litter removal was not signiﬁcant (F = 0.766, P < 0.552). Soil water content was signiﬁcantly lower in plots with removal of understory vegetation
Table 1 Physical and chemical characteristics of soil collected from the ﬁve sites. Values (means SE) are based on data collected just before the experiment began and from plots where vegetation and litter had not been removed. Site
Soil bulk density (g/cm3)
Soil organic matter (g/kg)
Hydrolyzed nitrogen (mg/kg)
Exchangeable potassium (mg/kg)
Available phosphorus (mg/kg)
EP NP LP CP SL
1.40 0.07b 1.54 0.07a 1.39 0.10b 1.25 0.07c 1.46 0.09ab
1.38 0.01a 1.55 0.10a 1.57 0.36a 1.57 0.11a 1.46 0.09a
105.82 8.13ab 101.27 5.89ab 120.25 1.85a 100.21 4.32ab 96.13 2.16b
67.47 1.92c 111.60 17.18ab 122.20 10.48a 99.57 5.32ab 86.03 6.78bc
1.97 1.04a 1.82 0.40a 1.97 0.58a 2.32 0.93a 2.89 1.47a
Means in a column followed by different letters are signiﬁcantly different (P < 0.05) according to a one-way ANOVA and an LSD test. EP, eucalyptus plantation; NP, mixednative species plantation; LP, mixed-legume plantation; CP, mixed-conifer plantation; SL, shrubland.
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Table 2 The main understory herbaceous species, canopy coverage by the main understory species, standing litter biomass, and light penetration in the ﬁve sites. Values (means SE) are from plots where vegetation and litter had not been removed. Site
Main understory herbaceous species
Standing litter biomass (g/m2)
Light penetration (%)
EP NP LP CP SL
Ottochloa Ottochloa Ottochloa Ottochloa Ottochloa
29.3 5.2a 40.0 15.2a 60.6 2.3a 45.0 13.0a 31.7 8.8a
361 38b 877 107a 1124 134a 741 134ab 288 13b
12.42 2.07ab 9.35 2.18b 22.71 3.94a 23.27 4.24a 18.38 5.40ab
nodosa + Melastoma dodecandrum nodosa nodosa nodosa nodosa + Melastoma dodecandrum
Means in a column followed by different letters are signiﬁcantly different (P < 0.05) according to a one-way ANOVA and an LSD test. Light penetration means percent of above-canopy sunlight reaching the understory.
and litter than in control at the LP site and at SL site in both December 2007 and March 2008. Soil water content varied considerably in the course of experiment, the soil water content in December 2007 tended to be lowest among the six samplings between July 2007 and September 2008. 3.2. Seedling survival Seedlings suffered 8–95% mortality during the 20-month experiment, and mainly occurred during the ﬁrst summer at all the ﬁve study sites (Fig. 1). The accumulated seedling survival was signiﬁcantly affected by site, treatment, and species. In addition, there was a signiﬁcant interaction between the site and species. In general, seedling survival was greater when understory vegetation
and litter were removed rather than left in place (Fig. 1). Survival of M. chapensis and P. rubra seedlings at the LP site, however, tended to be higher if understory vegetation and litter were retained (Fig. 1). Survival of M. chapensis seedlings at the SL site was lowest among the ﬁve sites in both treatments and signiﬁcantly lower than that at NP and CP sites (P < 0.05). When understory vegetation and litter were removed, survival of P. rubra seedling at LP site was signiﬁcantly lower than other sites (P < 0.05). 3.3. Seedling height, basal diameter, and biomass ANOVA results showed that seedling height, basal diameter, and biomass were signiﬁcantly affected by site, treatment, and also the interaction between site and species. Removal of understory
Fig. 1. Survival of Castanopsis chinensis, Michelia chapensis, and Psychotria rubra seedlings as affected by removal (VR) or retention (CK) of understory vegetation and litter at ﬁve sites. EP, eucalyptus plantation; NP, mixed-native species plantation; LP, mixed-legume plantation; CP, mixed-conifer plantation; SL, shrubland.
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Fig. 2. Height, basal diameter, and biomass of Castanopsis chinensis, Michelia chapensis, and Psychotria rubra seedlings as affected by removal (VR) or retention (CK) of understory vegetation and litter at ﬁve sites. Different lowercase letters above bars indicate signiﬁcant differences between CK and VR at the same site. Mean separation was based on a one-way ANOVA followed by an LSD test. Because all transplanted seedlings of M. chapensis in one plot at the shrubland site (SL) had died by the end of experiment, M. chapensis at the SL site was not included for multiple comparison analyses.
vegetation and litter signiﬁcantly increased the height of C. chinensis seedlings at the LP and CP sites and of P. rubra seedlings at the CP and SL sites but signiﬁcantly decreased the height of M. chapensis seedlings at the LP site (Fig. 2a–c). Removal of understory vegetation and litter signiﬁcantly increased the basal diameter of C. chinensis seedlings at the EP, LP, and CP sites and of P. rubra seedlings at the EP, CP, and SL sites (Fig. 2d and f). The height and basal diameter of C. chinensis seedlings were highest at the LP site when understory vegetation and litter had been removed (Fig. 2a and d, P < 0.05). When understory vegetation and litter were removed, the height and basal diameter for M. chapensis seedlings were greater at the CP site than at the EP site (P < 0.05), while the seedling height was less at the EP site than at the LP site when understory vegetation and litter were retained (P < 0.05). The height and basal diameter of P. rubra seedlings were greater at the SL and CP sites than at the EP and LP sites when understory vegetation and litter were removed (P < 0.05), while the values were greater at the SL than at the CP site in the control treatment (P < 0.05). Removal of understory vegetation and litter signiﬁcantly increased the biomass of C. chinensis seedling at the EP, LP, and CP sites (Fig. 2g) and of P. rubra seedlings at the NP, CP, and SL sites (Fig. 2i). Biomass of C. chinensis seedlings was greater at the LP site than at the other sites when understory vegetation and litter were removed (P < 0.05). The biomass of M. chapensis seedlings was not signiﬁcantly affected by site or by removal of understory vegetation and litter (Fig. 2h, P > 0.05). With removal of understory vegetation and litter, the biomass of P. rubra seedlings was signiﬁcantly higher at the NP, CP, and SL sites than at the EP and LP sites (P < 0.05). When understory vegetation and litter were retained, the biomass of P. rubra seedlings was higher at the SL site than at the CP site (P < 0.05).
3.4. Relationship between environmental factors and seedling survival and growth The RDA model indicated that seedling survival for all three species was strongly and positively correlated with soil moisture (SWC), and that the survival of P. rubra seedlings was negatively correlated with light intensity in the understory (light) and soil hydrolyzed nitrogen (HN) (Fig. 3). Light intensity in the understory and soil exchangeable potassium (K) were strongly and positively correlated with growth of C. chinensis and M. chapensis seedlings, and especially with their basal diameter and biomass. In addition, soil moisture was strongly and negatively correlated with the growth of C. chinensis seedlings (Fig. 3). Stepwise regression indicated that the growth of C. chinensis seedlings was best explained by soil exchangeable potassium and soil moisture and that the growth of M. chapensis seedlings was best explained by soil exchangeable potassium (Table 3). The growth of P. rubra seedlings was strongly and positively correlated with soil organic matter (SOM) but negatively correlated with soil hydrolyzed nitrogen (Fig. 3), which was consistent with the results of the stepwise regression (Table 3). 4. Discussion 4.1. Effects of understory vegetation and litter on seedling performance Our results showed that removal of understory vegetation and litter generally increased both seedling survival and seedling growth. The poorer performance of seedlings when transplanted in plots with intact understory vegetation and litter could be attributed to competition for resources (light, soil water, and nutrients) or allelopathic effects of litter (Holl, 1998; Brewer, 1999;
J. Wang et al. / Forest Ecology and Management 258 (2009) 1293–1300
Fig. 3. Canonical redundancy (RDA) biplots illustrating the effects of environmental factors on survival and growth of Castanopsis chinensis, Michelia chapensis, and Psychotria rubra seedlings. Arrows indicate explanatory variables (environmental factors), while lines (without arrows) indicate response variables for seedling survival and growth. H, height; BD, basal diameter; B, total biomass; Light, light penetration in the understory; SBD, soil bulk density; SWC, soil water content; SOM, soil organic matter; HN, hydrolyzed nitrogen; K, exchanged potassium; AP, available phosphorus.
Stevenson and Smale, 2005; Devine et al., 2007). Nevertheless, litter can also enhance seedling establishment by reducing soil erosion and surface crusting, increasing water inﬁltration, and moderating soil temperatures (Keeley, 1992; Prach et al., 1996; Ibanez and Schupp, 2002). In this study, the effect of litter could not be separated from the effect of living understory plants. In some cases, removal of understory vegetation and litter did not improve seedling performance. For example, the survival and Table 3 Stepwise regression analysis and associated regression coefﬁcients explaining relationships between survival and growth of seedlings and environmental factors. Regression equation
C. chinensis Height Basal diameter Biomass
Y = 78.873 4.175X1 + 0.264X2 Y = 8.899 0.435X1 + 0.26X2 Y = 18.859 1.323X1 + 0.0.95X2
0.498 0.506 0.415
0.000 0.000 0.001
M. chapensis Survival Height Basal diameter Biomass
Y = 1.483 + 0.093X1 + 0.018X3 Y = 2.902 + 0.289X2 Y = 2.328 + 0.034X2 Y = 2.316 + 0.078X2
0.359 0.247 0.212 0.177
0.002 0.007 0.014 0.026
P. rubra Height
Y = 49.999 0.482X4 + 17.713X5
Species and dependent variable (Y)
X1, soil water content; X2, soil exchanged potassium; X3, light penetration in the understory; X4, soil hydrolyzed nitrogen; X5, soil organic matter.
growth of M. chapensis and P. rubra seedlings decreased at the LP site when understory vegetation and litter were removed. At the LP site, soil water content tended to be lower than at the other sites, and retaining understory vegetation and litter signiﬁcantly increased soil moisture. Based on canonical redundancy analysis (Fig. 3), a soil moisture deﬁcit was detrimental to the survival of M. chapensis and P. rubra seedlings. In contrast to M. chapensis and P. rubra seedlings, C. chinensis seedlings survived better and grew better when understory vegetation and litter were removed. C. chinensis is a fast-growing species with a long tap root (Wang et al., unpublished data) and might not strongly respond to the water condition of the top 10 cm soil, as has been documented for oak seedlings (Devine et al., 2007). The three species sometimes responded differently to the treatments. It agrees with other reports that the effects of these kinds of treatments are often species speciﬁc (Isselstein et al., 2002; Donath et al., 2006). 4.2. Effects of plant community on seedling performance One of the main objectives of this study was to determine which kind of plant community was suitable for colonization by introduced indigenous tree seedlings. The results showed that seedling survival and growth varied considerably among species and sites. Light is an especially important factor determining plant survival and growth (Beckage and Clark, 2003; Ostertag et al., 2008). In this study, the growth of shade-intolerant C. chinensis and moderately shade-tolerant M. chapensis was positively correlated
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with light intensity in the understory, while the survival of P. rubra was strongly and negatively correlated with light intensity in the understory. These results are consistent with previous observations, i.e., the effect of irradiance on seedling survival and growth was correlated with the shade tolerance of the species (Sack and Grubb, 2002; Mclaren and Mcdonald, 2003). Additionally, the effect of light intensity in the understory on seedling survival was not consistent with its effects on seedling growth, which support the idea that seedling survival and growth could respond to light conditions with different patterns. This is the same as Sa´nchezGo´mez et al.’s (2006) ﬁndings. Besides light conditions, soil physical and chemical properties were correlated with seedling survival and growth. Soil moisture can greatly affect seedling establishment (Kajimoto, 2002; Mclaren and Mcdonald, 2003; Castro et al., 2005; Climent et al., 2006), and in the current study, the survival of transplanted seedlings was highly correlated with soil water content. In the South China, where this study was conducted, rain falls in only a few months each year but often with great intensity, resulting in substantial seasonal variation and long periods of drought (Shen et al., 2000). Therefore, survival and growth of most seedlings were better in habitats with higher soil moisture. The growth of C. chinensis seedlings, however, was negatively correlated with soil water content, perhaps because this species responds strongly to light, and greater light penetration decreases soil water content (Duan et al., 2008). Soil bulk density is an indicator of soil structure, and increases in bulk density usually reduce seedling survival and growth (de Villalobos et al., 2005). In our study, however, the correlation between soil bulk density and seedling survival and growth was weak. Response of seedling to soil nutrition in the current study was species speciﬁc. Among the soil nutrition variables measured, soil exchangeable potassium was the most important factor affecting basal diameter and biomass of C. chinensis and M. chapensis seedlings, and soil organic matter was the most important factor affecting the height of P. rubra seedlings. That these factors are limiting is reasonable because the plantations and shrubland in our study were bare land 23 years earlier. Given that this period of revegetation has been relatively short (too short to sufﬁciently improve soil nutrition), soil organic matter content, exchangeable potassium, and other soil nutrients may limit the establishment of introduced indigenous tree species at these sites (Duan et al., 2008). The effect of soil hydrolyzed nitrogen on seedling performance also depended on the plant species. In our study, soil hydrolyzed nitrogen was negatively correlated with the survival and growth of P. rubra but weakly and positively correlated with the survival and growth of C. chinensis and M. chapensis seedlings, suggesting that P. rubra seedlings are not adapted for colonizing nitrogen-rich habitats. Furthermore, in nitrogen-enriched sites, increased growth of understory herbaceous vegetation can increase the competition for water and other resources (Davis et al., 1999), thereby reducing the growth of the transplanted indigenous seedlings. 4.3. Implications for management Effective restoration requires knowledge about how seedlings of the indigenous species respond to the environment (Elmarsdottir et al., 2003). The current study indicated that seedling survival and growth were greatly affected by light and soil moisture. Therefore, attempts to re-establish indigenous plant species must consider these two environmental factors. It is also likely that additions of potassium fertilizer and organic matter will improve seedling performance in some sites. Restoration strategies should be based on knowledge of the abiotic and biotic factors affecting plant establishment. The results
of this study indicate that planting of suitable tree seedlings in conjunction with suitable site preparation may be an effective method of establishing indigenous tree species in established plantations and shrublands where seed sources are absent. Selection of suitable indigenous tree species for regenerating the current shrublands and established plantations, which have been undergoing natural succession since their establishment, should accelerate succession to a more natural and more desirable plant community. For example, shade-intolerant C. chinensis was suitable for transplanting in habitats with high light such as the CP and LP sites, while shade-tolerant P. rubra was suitable for shady habitats such as the NP site. In addition, removal of understory vegetation and litter will often improve seedling growth and establishment. Results from our study should contribute to the design of effective restoration strategies and should help forest managers to regenerate current plantations and shrublands in South China. Because plant community was not replicated in this study, inferences about differences between communities should be cautious. Our study, however, measured seedling survival and growth for only 20 months. A better understanding of the regeneration of plantations and shrublands will require multiple long-term ﬁeld experiments. Acknowledgements This study was supported by the National Natural Science Foundation of China (30670370), the National Basic Research Program of China (2009CB421101) and Guangdong & Guangzhou Program (07118249, 2007J1-C0471, 2008A030203007). The authors are indebted to Prof. Zhian Li, Dr. Nan Liu, Miss. Danyan Li for helpful comments, anonymous reviewers for their valuable comments on the early version of the manuscript, Prof. Bruce Jaffee for English editing, Mr. Yongbiao Lin and Mr. Xingquan Rao for ﬁeld assistance. Reference Aranda, I., Gil, L., Pardos, J.A., 2004. Improvement of growth conditions and gas exchange of Fagus sylvatica L. seedlings planted below a Pinus sylvestris L. stand after thinning the pinewood. Trees, Structure and Function 162, 153–164. Aranda, I., Gil, L., Pardos, J.A., 2001. Effects of thinning in a Pinus sylvestris L. stand on foliar water relations of Fagus sylvatica L. seedlings planted within the pinewood. Trees, Structure and Function 15, 358–364. Beckage, B., Clark, J.S., 2003. Seedling survival and growth of three forest tree species: the role of spatial heterogeneity. Ecology 84, 1849–1861. Brewer, J.S., 1999. Effects of competition, litter, and disturbance on an annual carnivorous plant (Utricularia juncea). Plant Ecology 140, 159–165. Castro, J., Zamora, R., Hodar, J.A., Gomez, J.M., 2005. Alleviation of summer drought boosts establishment success of Pinus sylvestris in a Mediterranean mountain: an experimental approach. Plant Ecology 181, 191–202. Charlotte, V., Francois, F., Fawziah, G., Alexandre, B., 2006. Competitive effects of herbaceous vegetation on tree seedling emergence, growth and survival: does gap size matter? Journal of Vegetation Science 17, 481–488. Climent, J.M., Aranda, I., Alonso, J., Pardos, J.A., Gil, L., 2006. Developmental constraints limit the response of Canary Island pine seedlings to combined shade and drought. Forest Ecology and Management 231, 164–168. Davis, M.A., Wrage, K.J., Reich, P.B., Tjoelker, M.G., Schaeffer, T., Muermann, C., 1999. Survival, growth, and photosynthesis of tree seedlings competing with herbaceous vegetation along a water-light-nitrogen gradient. Plant Ecology 145, 341–350. Denslow, J.S., Uowolo, A.L., Hughes, R.F., 2006. Limitations to seedling establishment in a mesic Hawaiian forest. Oecologia 148, 118–128. de Villalobos, A.E., Pelaez, D.V., Elia, O.R., 2005. Factors related to establishment of Prosopis caldenia Burk. seedlings in central rangelands of Argentina. Acta Oecologica 27, 99–106. Devine, W.D., Harrington, C.A., Leonard, L.P., 2007. Post-planting treatments increases growth of Oregon white oak (Quercus garryana Dougl. ex Hook.) seedlings. Restoration Ecology 15, 212–222. Donath, T.W., Holzel, N., Otte, A., 2006. Inﬂuence of competition by sown grass, disturbance and litter on recruitment of rare ﬂood-meadow species. Biological Conservation 130, 315–323. Du, Y., Huang, Z., 2008. Effects of seed mass and emergence time on seedling performance in Castanopsis chinensis. Forest Ecology and Management 255, 2495–2501.
J. Wang et al. / Forest Ecology and Management 258 (2009) 1293–1300
Duan, W., Ren, H., Fu, S., Wang, J., Zhang, J., Yang, L., Huang, C., 2008. Community comparison and determinant analysis of understory vegetation in six plantations in south China. Restoration Ecology, doi:10.1111/j.1526-100X.2008.00444.x. Dupuy, J.M., Chazdon, R.L., 2008. Interacting effects of canopy gap, understory vegetation and leaf litter on tree seedling recruitment and composition in tropical secondary forests. Forest Ecology and Management 255, 3716–3725. Elmarsdottir, A., Aradottir, A.L., Trlica, M.J., 2003. Microsite availability and establishment of native species on degraded and reclaimed sites. Journal of Applied Ecology 40, 815–823. Fang, W., Peng, S.L., 1997. Development of species diversity in the restoration process of establishing a tropical man-made forest ecosystem in China. Forest Ecology and Management 99, 185–196. Hardwick, K., Healey, J., Elliott, S., Garwood, N., Anusarnsunthorn, V., 1997. Understanding and assisting natural regeneration processes in degraded seasonal evergreen forests in northern Thailand. Forest Ecology and Management 99, 203–214. Holl, K.D., 1998. Effects of above- and below-ground competition of shrubs and grass on Calophyllum brasiliense (Camb.) seedling growth in abandoned tropical pasture. Forest Ecology and Management 109, 187–195. Howlett, B.E., Davidson, D.W., 2003. Effects of seed availability, site conditions, and herbivory on pioneer recruitment after logging in Sabah, Malaysia. Forest Ecology and Management 184, 369–383. Ibanez, I., Schupp, E.W., 2002. Effects of litter, soil surface conditions, and microhabitat on Cercocarpus ledifolius Nutt. seedling emergence and establishment. Journal of Arid Environments 52, 209–221. Institute of Soil Science, Chinese Academy of Science (CAS), 1978. Soil physical and chemical analysis. Shanghai Technology Press of China, Shanghai (in Chinese). Isselstein, J., Tallowin, J.R.B., Smith, R.E.N., 2002. Factors affecting seed germination and seedling establishment of fen-meadow species. Restoration Ecology 10, 173–184. Janecek, S., Leps, J., 2005. Effect of litter, leaf cover and cover of basal internodes of the dominant species Molinia caerulea on seedling recruitment and established vegetation. Acta Oecologica 28, 141–147. Kajimoto, T., 2002. Factors affecting seedling recruitment and survivorship of the Japanese subalpine stone pine, Pinus pumila, after seed dispersal by nutcrackers. Ecological Research 17, 481–491. Keeley, J.E., 1992. Recruitment of seedlings and vegetative sprouts in unburned chaparral. Ecology 73, 1194–1208. Knapp, B.O., Wang, G.G., Walker, J.L., Cohen, S., 2006. Effects of site preparation treatments on early growth and survival of planted longleaf pine (Pinus palustris Mill.) seedlings in North Carolina. Forest Ecology and Management 226, 122–128. Lepsˇ, J., Sˇmilauer, P., 2003. Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge. Lenz, T.I., Facelli, J.M., 2005. The role of seed limitation and resource availability in the recruitment of native perennial grasses and exotics in a South Australian grassland. Austral Ecology 30, 684–694. Li, Q., Ma, K., 2003. Factors affecting establishment of Quercus liaotungensis Koidz. under mature mixed oak forest overstory and in shrubland. Forest Ecology and Management 176, 133–146. Liu, Y.H., 1996. Flora of China. Science Press, Beijing (in Chinese). McClanahan, T.R., 1986. The effects of a seed source on primary succession in a forest ecosystem. Vegetatio 65 178-178. Mclaren, K.P., Mcdonald, M.A., 2003. The effects of moisture and shade on seed germination and seedling survival in a tropical dry forest in Jamaica. Forest Ecology and Management 183, 61–75.
Olsen, S.R., Cole, C.V., Watanable, F.S., Dean, L.A., 1954. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular 939, Washington D.C.. Ostertag, R., Giardina, C.P., Cordell, S., 2008. Understory colonization of eucalyptus plantation in Hawaii in relation to light and nutrient levels. Restoration Ecology 16, 475–485. Peng, S.L., 2003. Study and application of restoration ecology in tropical and subtropical China. Science Press, Beijing (in Chinese). Prach, K., Leps, J., Michalek, J., 1996. Establishment of Picea abies seedlings in a central European mountain grassland: an experimental study. Journal of Vegetation Science 7, 681–684. Puerta-Pinero, C., Gomez, J.M., Valladares, F., 2007. Irradiance and oak seedling survival and growth in a heterogeneous environment. Forest Ecology and Management 242, 462–469. Ren, H., Huang, P., Zhang, Q.M., Hou, C.M., 2002. Forest resources and its ecosystem service in Guangdong, China. Chinese Environmental Science Press, Beijing (in Chinese). Ren, H., Peng, S.L., Sun, G.C., Yu, Z.Y., 1997. The ecological comparison of Psychotria rubra and Rhodomyrtus tomentosa in south China. Acta Phytoecologica Sinica 21 (4), 386–392 (in Chinese, with English abstract). Ren, H., Shen, W., Lu, H., Wen, X., Jian, S., 2007. Degraded ecosystems in China: status, causes, and restoration efforts. Landscape and Ecological Engineering 3, 1–13. Rey, P.J., Alcantara, J.M., 2000. Recruitment dynamics of ﬂeshy-fruited plant (Olea europaea): connecting patterns of seed dispersal to seedling establishment. Journal of Ecology 88, 622–633. Rodrı´guez-Calcerrada, J.A., Pardos, J.A., Gil, L., Aranda, I., 2008. Ability to avoid water stress in seedlings of two oak species is lower in a dense forest understory than in a medium canopy gap. Forest Ecology and Management 255, 421–430. Sa´nchez-Go´mez, D., Valladares, F., Zavala, M.A., 2006. Performance of seedlings of Mediterranean woody species under experimental gradients of irradiance and water availability: trade-offs and evidence for niche differentiation. New Phytologist 170, 795–806. Sack, L., Grubb, P.J., 2002. The combined impacts of deep shade and drought on the growth and biomass allocation of shade-tolerant woody seedlings. Oecologia 131, 175–185. SFA (State Forestry Administration), 2005. The sixth national forest resources inventory and the status of forest resources. Green China 2, 11–12. Shen, W.J., Peng, S.L., Zhou, G.Y., Lin, Y.B., Ren, H., 2000. Hydrological properties and water balance of grassland ecosystem in Hesan hill region. Acta Phytoecologica Sinica 24 (2), 162–168 (in Chinese, with English abstract). Standford, S., English, L., 1949. Use of ﬂame photometer for analysis of Na, K and Ca. Agronomy Journal 41, 446–447. Stevenson, B.A., Smale, M.C., 2005. Seed bed treatment effects on vegetation and seedling establishment in a New Zealand pasture one year after seeding with native woody species. Ecological Management & Restoration 6, 124–131. Suding, K.N., Goldberg, D., 1999. Variation in the effects of vegetation and litter on recruitment across productivity gradients. Journal of Ecology 87, 436–449. Watson, I.W., Westoby, M., Holm, A.M., 1997. Continuous and episodic components of demographic change in arid zone shrubs: models of two Eremophila species from Western Australia compared to published data on other species. Journal of Ecology 85, 833–846. Yates, C.J., Hobbs, R.J., Atkins, L., 2000. Establishment of perennial shrub and tree species in degraded Eucalyptus salmonophloia (Salmon Gum) remnant woodlands: effects of restoration treatments. Restoration Ecology 8, 135–143.