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Long-term protection effects of national reserve to forest vegetation in 4 decades: biodiversity change analysis of major forest types in Changbai Mountain Nature Reserve, China BAI Fan1*, SANG WeiGuo1*†, LI GuangQi1, LIU RuiGang1, CHEN LingZhi1 & WANG Kun2 1

State Key Laboratory of Vegetation and Environment Change, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China; 2 Nature Reserve Bureau of Changbaishan, Jilin 210011, China

The Changbai Mountain Nature Reserve (CNR) was established in 1960 to protect the virgin Korean pine mixed hardwood forest, a typical temperate forest of northeast China. We conducted systematic studies of vascular diversity patterns on the north slope of the CNR mountainside forests (800－1700 m a.s.l.) in 1963 and 2006 respectively. The aim of this comparison is to assess the long-term effects of the protection on plant biodiversity of CNR during the interval 43 years. The research was carried out in three types of forests: mixed coniferous and broad-leaved forest (MCBF), mixed coniferous forest (MCF), and sub-alpine coniferous forest (SCF), characterized by different dominant species. The alpha diversity indicted by species richness and the Shannon-Wiener index were found different in the same elevations and forest types during the 43-year interval. The floral composition and the diversity of vascular species were generally similar along altitudinal gradients before and after the 43-year interval, but some substantial changes were evident with the altitude gradient. In the tree layers, the dominant species in 2006 were similar to those of 1963, though diversity declined with altitude. The indices in the three forest types did not differ significantly between 1963 and 2006, and these values even increased in the MCBF and MCF from 1963 to 2006. However, originally dominant species, P. koraiensis for example, tended to decline, while the proportion of broad-leaved trees increased, and the species turnover in the succession layers trended to shift to higher altitudes. The diversity pattern of the under canopy fluctuated along the altitudinal gradient due to micro-environmental variations. Comparison of the alpha diversity in the three forests shows that the diversity of the shrub and herb layer decreased with time. During the process of survey, we also found some rare and medicinal species disappeared. Analysis indicates that the changes of the diversity pattern in this region are caused by both nature and human factors. Meteorological records revealed that climate has changed significantly in the past 43 years. We also found the most severe human disturbance to the CNR forests in the process of another field survey that is the exploitation of herb medicines and Korean pine nuts. We hope this research would give some guidance to the future reserve management in Changbai Mountain area. plant species diversity, climate change, forest community, human activity, Changbai Mountain

Fossil fuel consumption is increasing, and the effect of human disturbances on the nature ecosystem is intensifying. These factors have caused great amount of dramatic climatic and ecological changes in extensive re-

Received March 6, 2007; accepted February 19, 2008 doi: 10.1007/s11427-008-0122-9 † Corresponding author (email: [email protected]) * Contributed equally to this work Supported by the National Natural Science Foundation of China (Grand No. 30590382)

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gions or even in global scales. These changes directly or indirectly are damaging the natural biological community composition, inducing the noticeable shift of forest distribution pattern and the loss of biodiversity in an unprecedented rate[1,2]. Human beings have been aware of such rapid changes of nature ecosystems and biological biodiversity, and made great efforts to rescue critical ecosystems and endangered species by launching active measures such as establishing nature reserve, enacting ecological conservation pacts between countries, implementing ecosystem restoration and management and so on[3−6]. The summer temperature in northeastern China has increased 0.15℃/10a during the past fifty years. This region is one of the fastest warming areas in China, and the warming rate is much higher than the average level of the global, north hemisphere and northeast Asia[6]. Thus the studies of plant distributions and diversity changes should been paid more attention in this area. Long-term records of field observation are necessary for analyzing the trends in ecosystems affected by environmental changes and human activities, especially the survey in the same community. This is the reliable research approach to assess biodiversity dynamics of plant communities and the results of conservation measures[7,8]. The Changbai Mountain Nature Reserve (CNR) was established in 1960 to protect the virgin mixed Korean pine and broad-leaved forest, which is the typical type of temperate forest in northeastern China. Due to the unique history and the large elevation range, the reserve is one of the most intact forests in China, and there are distinctive vertical plant community zones, which is an ideal place to learn the plant biodiversity and vertical distribution pattern of plants. Numbers of investigations have been carried out for this typical upland vegetation types to analyze the zonal community characteristics in the following zones, alpine tundra, dark conifer forest, and mixed Korea pine and broad-leaved forests[9−11]. A study systematically characterized the distribution pattern of vegetation in the CNR was conducted 43 years ago[12,13]. Fortunately, a set of original plot records from that survey are preserved. Although the tree cutting has been prohibited after the establishment of the natural reserve, there were still some human activates under the forest canopy. The representative studies about forest community dynamic in

Changbai Mountain areas were carried out by Hao et al.[14], Wu and Dai[15] and Li et al.[16]. These investigations revealed the plant diversity features and recover statuses of the disturbed secondary mixed Korean pine / broad-leaved forests in the time span of 10~15 years. Jin’s research on the plant community diversity dynamics of secondary forest in Changbai Mountain covers about 28 years[17]. However, the report of the long-term (longer than 3 decades) changes of forest plant diversity and assessing the conservation efficiencies of nature reserves is rare. The aim of the present study is to examine whether significant differences occurred in the forest biodiversity patterns of vascular plant species on the North Slope of the CNR by comparing the field observations in 1963 and 2006. Analysis and discussion of the possible reasons for the changes, involving global warming and human activities, is relevant to assessing the long-term protective effects of the CNR and to planning future management strategies.

1 Methods 1.1 Study area CNR is located in Jilin Province, northeastern China. This region, situated on the border between China and North Korea, covers an area of 196 456 hm2. The weather is predominantly affected by monsoon. The year-round conditions are characterized by a mountain climate with dry and windy springs, short and rainy summers, cool and foggy autumns, and cold and long winters. Along with increasing elevation, the temperature decreases, while the abundant precipitation increases. The prevailing direction of strong winds is the west-south-west (WSW)[18] (Table 1). The forest zones distribute below 2000 m a.s.l. and vertically changed with altitude[19,20]. The mixed Korea pine and broad-leaved forest is the typical zonal vegetation of this region[1]. The research was carried out on the north slope of Changbai Mountain (800~1700 m a.s.l.). The geographic coordinates of the investigation area are within 127°55′~ 128°08′ E 42°04′~42°23′ N. The annual mean temperature in this area decreased from 2.32℃ to –2.29℃, annual precipitation increased from 703.62 mm to 967.28 mm along the altitude[18]. The soil types also appeared vertical zonal spectrum[21]. According to the climatic records from 1958 to 2006

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in Songjang meteorological station (721.4 m a.s.l; 42°25 N / 128°07′ E) located on the north edge of CNR, the annual mean temperature of the beginning 5 years (1958~1962) is 2.58℃, and the annual mean precipitation is 697.92 mm, while in the recent five years (2002~2006), the annual mean temperature is 3.67℃ with more than 1℃ increase, and the annual mean precipitation declines to 630.1mm with no significant different to 5 decades ago. The annual mean temperature at each year of 1990s is usually higher than that in 1980s, and it is fluctuated and gradually increased about 0.37℃/decade. The mean value after 1985 is 2.7℃ higher than the total 45-year average level. Another ground climatic record (from 1982~2003) in climatic observation field of Changbai Mountain Forest Ecosystem Research Station, Chinese Academy of Sciences analyzed by Zhang et al.[22] shows that there is a significant descending trend in annual total sunshine hours and day sunshine percent with the elevation decrease in Changbai Mountain broad-leaved forests. Chen (1964) divided the forest communities (within elevation 800~1700 m) into 3 types according to different dominant tree species compositions. We still chose the 3 type in the 2006 survey. They are: (1) mixed coniferous and broad-leaved forest zone (MCBF) (below 1100 m a.s.l), dominated by Pinus koraiensis, Acer mono, Tilia amurensis, Ulmus davidiana var. japonica, Quercus Mongolica, etc.; (2) mixed coniferous forest zone (MCF) (1100~1400 m a.s.l), dominated by P. koraiensis, Picea jezoensis var. komarovii, Abies Table 1

nephrolepis, Larix olgensis var. changpaiensis etc.; and (3) sub-alpine coniferous forest zone (SCF) (1500~1700 m a.s.l), dominated by P. jezoensis var. komarovii, L. olgensis var. changpaiensis, A. nephrolepis, and Betula ermanii. (2) and (3) were both named with cool temperate conifer zones. There is B. ermanii dwarf forests within 1800-2000 m above the conifer zone. Because of the incomplete data in this forest type, we omitted it in our field survey. 1.2 Study methods 1.2.1 Field survey. By the information of plot records in 1963 from Chen et al.[13], we remeasured the same plots in 2006. The plots were chosen according to the records, which contained information about elevations, landforms, slope gradients, aspects, and dominant species in each forest type. The field observations in 1963 survey were carried out from June to August, and the 2006 was from July to August. In order to achieve comparable results, we utilized the same sampling method in 2006 as the 1963 inventory. From the 63 plots sampled in 1963, we chose 52 plots (20 m×20 m) with clear location records and distinct geographic characteristics. A minimum of two plots were sampled in each 100 m altitudinal interval, and at least 10 plots were included in each forest type (Table 1). Each plot contains four sub-plots (10 m×10 m) for surveying trees, four shrub sub-plots (10 m×10 m), and

Altitude, temperature, precipitation, and plot characteristics of the survey area along the northern slope of Changbai Mountain

Altitude (m) 800

Annual mean temperature a) (℃) 2.32

Annual precipitation a) (mm) 703.62

Forest type

Human activity

MCBF

A, B

Number of plots 13

900

1.81

728.95

1000

1.29

755.19

3

1100

0.78

782.37

5

1200

0.27

810.53

1300

-0.24

839.70

1400

-0.75

869.92

2

1500

-1.26

901.23

2

1600 1700

-1.78

933.67

-2.29

967.28

10

6 MCF

SCF

A, B, C

B,C

3

4 4

a) Data from Chi et al.[18]. MCBF: Mixed coniferous and broad-leaved forests; MCF: Mixed coniferous-leaved forests; SCF: Sub-alpine coniferous forest. A, Collecting Korean pine nuts. B, Collecting herbs and medicinal plant materials. C, Tourism.

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four herb sub-plots (1 m×1 m). The plot positions were determined by GPS, which also recorded the elevation, topography, and other environmental information. All living trees with height ≥1.3 m in the tree sub-plots were tallied by species and DBH. The canopy was divided into the main story (≥8 cm DBH) and the succession layer (<8 cm DBH), representing the main composition and the future trend of the forest ecosystem, respectively. In the shrub and herb sub-plots, records of every stem were organized by species or species group, abundance, coverage and average height. If there are human activities, the type of human activities were recorded. 1.2.2 Biodiversity Index. Species richness (S) was measured as the total number of species at each altitudinal interval, and the Shannon-Wiener index (H) based on the Altered Important Value (AIV; Ma et al., 1995) were used to measure species richness weighted by species evenness, and to show the distribution pattern of plant diversity within plots at the same altitude. These two indices were calculated for the canopy (DBH ≥ 8 cm), succession (DBH < 8 cm), shrub, and herb layers respectively. Species richness was determined as the total number of species in each altitudinal interval. The values of the Shannon-Wiener index are generally defined as follows[23−25]: s

H = − ∑ pi ln pi , i =1

where s is the total number of species in a plot, and pi is the AIV corresponding to the species. The AIV was used to measure the relative importance of the plant species in the community. The AIV values were determined as follows: AIV(tree layer) = ( Relative dominance+Relative abundance+Relative height ) /3 × 100% AIV(shrub/herb layer) = ( Relative coverage+Relative abundance+Relative height ) /3 × 100%

1.2.3 Statistics methods. We calculated the varied biodiversity indexes of each forest type respectively, after classified plots into forest types in each elevation. We used the average value and standard error of each index to describe the biodiversity statuses of three forests in 1963 and 2006. The T-test was used to assess the differences among the Shannon-Wiener index (H) mean values for plots of each forest types.

2 Results 2.1 Floral composition and structure change The 1963 survey found 202 species, 144 genera, and 61 families of vascular plants, including 38 tree species, 32 shrub species, 127 herb species and 5 lianas species within the altitudinal range of 800~1700 m a.s.l. The numbers of species slightly declined in 2006, we found 197 species, belonging to 141 genera and 58 families, including 37 tree species, 32 shrub species, 123 herb species, and 5 lianas species in 2006. The forest types were defined by the tree species composition. The AIV composition of dominant tree species in the canopy (DBH≥8 cm) is shown in Table 2, which indicates the different structure characteristics at the same elevation in 1963 and 2006. In 800~1100 m a.s.l., P. koraiensis is still the predominant species, but the AIV declines from 0.27 to 0.19. The proportion of the broad-leaved tree species increased, and Q. mongolica became the newly dominant tree. In 1100~1400 m a.s.l., the AIV of A. nephrolepis increased, though that of other conifer trees (e.g. L. olgensis var. changpaiensis and P. koraiensis) lost their dominant status. The same with the lower zones, the proportion of the broad-leaved tree species for example, A. mono and Betula platyphylla, increased . In 1500~1700 m a.s.l., the sub-alpine conifer tree species dominated in this forest community. The AIV showed the similar trend with 1100~1400 m a.s.l. P. jezoensis var. komarovii and A. nephrolepis exchanged their places. The AIV of A. nephrolepis increased to 44%. However, values of larch and fir deceased significantly. In addition, the proportion of broad-leaved tree species Acer ukurunduense increased. Those results show that the dominant species in 2006 are generally similar to 1963. Nevertheless, some important changes in species status and proportion occurred in the three types of forest. The dominant tree species in 2006 survey are similar to Chen’s results[13] and complied with the 1963 forest types. Other similar results concerning these three forests have been reported[20]. Therefore, it is reasonable and comparable to base the 43 years change analysis on mixed coniferous and broad-leaved forest (MCBF), mixed coniferous forest (MCF), and sub-alpine coniferous forest (SCF). The specific composite changes of pine, spruce, fir, larch, and some deciduous broad-leaved species were described in following section.

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Table 2 Composition of dominant species in the canopy of the three forest types Forest type MCBF MCF SCF

Year

Component of tree species (DBH≥8 cm) and AIV (×10)

1963

PK2.7+AM1.5+AN1.3 +TA1.0+AP0.8+Others2.7

2006

PK1.9+AM1.3+AN1.2+QM1.0+TA0.8+ Others 3.8

1963

LO2.9+PK2.6+AN2.5+ PJ1.1+ Others 0.9

2006

AN2.7+LO2.2+PK2.2+PJ0.6+ Others 2.3

1963

LO3.9+PJ3.4+AN1.9+ Others 0.8

2006

AN4.4+PJ2.6+LO1.3+ Others 1.7

AN, Abies nephrolepis; LO, Larix olgensis var. changpaiensis; PJ, Picea jezoensis var. komarovii; PK, Pinus koraiensis; QM, Quercus mongolica; AM, Acer mono; AP, A. pseudo-sieboldianum; TA, Tilia amurensis.

Richness and evenness of shrub layer dropped a lot. In herb layer, the richness reduced to a half of the past, but evenness rose a little. Shannon-Wiener and Pielou indexes of shrub and herb layers in MCF reduced. In herb layer of MCF, the Shannon-Wiener index significantly fell by 25%, and the richness fell even by 40%. In SCF herb layer, there is a 20% descended in Shannon-Wiener index, 23% down in richness, and a statistically insignificant decrease in shrub layer.

2.2 The plant diversity changes in 3 forest types We analyzed the general trends of plant abundance, richness, and evenness in 3 forests in 1963 and 2006 in the context of climatic changes. Results suggest that the trend of plant diversity of tree layer and under story layer are inverse, that is tree diversity slightly increased, but under story layer significantly decreased (Table 3). The abundance, richness and evenness of canopy and success layer in MCBF increased slightly. The richness and diversity indexes increased, of which Shannon-Wiener index of success layer increased to 25%, but not significant. The Pielou evenness index of canopy layer decreased, while success layer increased. Plant diversity index declined very little (0.3%), whereas Pielou evenness index dropped more than10%. For plant richness, increment appeared in canopy layer, but the opposite in success layer. The diversity of the shrub and herb layer significantly decreased in the three forests. In MCBF, the plant biodiversity of shrub and herb layers greatly decreased. Shannon-Wiener index of both layers fell by 20%.

2.3 Spatial pattern changes of forest community along altitude Comparing the field surveying of 1963 with that of 2006, we found that there is no obvious change in vegetation structure and plant diversity along an altitudinal gradient (Figure 1). 2.3.1 Change trend of tree layer. As the principle component of forest community, the characteristic of tree layer (tree height≥1.3m) did not significantly change. The changing trend of stem density, basal area at breast height, and richness along altitude in 2006 is similar to that in 1963. In the whole surveying elevation range, the

Table 3 Plant diversity dynamics of three forest type between 1963 and 2006 MCBF Forest type Success layer

Shrub layer

Herb layer

Main story

Success layer

Shrub layer

Herb layer

Main story

Success layer

Shrub layer

Herb layer

1963

6

5

10

26

5

5

6

19

4

5

5

26

2006

8

6

8

13

7

6

6

11

5

4

5

20

1963

1.64 (0.05)

1.12 (0.09)

2.01 (0.03)

2.61 (0.07)

1.21 (0.07)

0.94 (0.11)

1.48 (0.08)

2.46 (0.06)

1.11 (0.06)

0.99 (0.14)

1.14 (0.17)

2.73 (0.10)

1.73 (0.05) *

1.36 (0.07) *

1.68 (0.06) ***

2.07 (0.05) ***

1.37 (0.06) *

1.17 (0.14) *

1.26 (0.10) **

1.77 (0.06) ***

1.11 (0.09) *

1.04 (0.10) *

0.89 (0.14) *

2.40 (0.08) **

1963

0.85

0.72

0.85

0.80

0.76

0.62

0.86

0.82

0.85

0.77

0.74

0.87

2006

0.86

0.76

0.78

0.81

0.75

0.65

0.83

0.80

0.74

0.69

0.72

0.81

H 2006 t-test Jsw

SCF

Main story

Canopy layers S

MCF

MCBF: Mixed coniferous and broad-leaved forests; MCF: Mixed coniferous-leaved forests SCF: Sub-alpine coniferous forests. α=0.05; ***, P<0.01, very significant difference; **, 0.010.05, not significant difference.

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Figure 1 The change pattern comparisons of forest community along an altitudinal gradient between 1963 and 2006 in Changbai Mountaint Natural Reserve. (a) Stem density in tree layer; (b) stem basal area at breast height in tree layer; (c) species richness in tree layer; (d) species richness in under-wood layer; (e)－(h) Shannon-Wiener index for main story, succession layer, shrub layer, and herb layer.

stem density increased from the bottom, and then sharply declined at 1400 m a.s.l, increased until 1500 m a.s.l as peak, and finally decreased gradually with the altitude (Figure 1(a)). Basal area at breast height fluctuated in 1400~1500 m a.s.l, unrelated with altitude (Figure 1(b)). Tree species diversity of canopy layer, richness and Shannon-Wiener index for example, has a negative relationship with altitude (Figure 1(c) and (e)). The same results, mentioned above, have been proved in other altitudinal gradient pattern studies on the north slope of Changbai Mountain[20,26]. In MCBF, distributing below 1000 m a.s.l., there is a suitable hydro-thermal condition for plant growth, and broad-leaved tree accounts for a high proportion. Rich plant species and complex community structure are the main characters in

this type of forest. Such community features have caused inter-specific surviving competition and self thinning, which lowered stem density of tree layer, and raised proportion of big tree and crown density. Therefore, the total basal area at breast height is not affected by stem density, and has kept in a certain level steadily in 43 years. With the increased elevation, the proportion of conifer species which are more adaptive to the alpine environments continuously increased, and the broad-leaved trees gradually disappeared at the same time. The higher the elevation is, the less is the tree richness. The area between broad-leaved tree dominant forest and conifer tree dominant forest is the forest ecotone, in which the tree layers dynamically succeeded (Anna, 2004). Shan-

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non-Wiener index shows a supporting fluctuation in our research. The peak occurred in the middle section (1100 －1200 m a.s.l.), and a significant fluctuation of stem density and basal area at breast height appeared in the elevation 1400 m a.s.l. 2.3.2 Trend of plant diversity under canopy. It is distinct from tree layer, plant diversity of shrub and herb layers in both 1963 and 2006 changed with altitude well. The under-canopy plants are more sensitive to the environmental changes than the top trees[27]. The composition and structure of the shrub and herb are easily affected by micro environments. According to the biodiversity value, tree layer biodiversity (canopy and succession layers) in 2006 is higher than that in 1963, whereas of the value in shrub and herb is contrary, obvious drop in the herb layer. We find some similar trend in the shrub and herb biodiversity between 1963 and 2006. In these two layers, the high richness and Shannon-Wiener values appear in high and low altitude, and bottom ones in middle altitude. For these two indices, the lowest point distributes in elevations 1300 m a.s.l. and 1200 m a.s.l. respectively (Figure 1(d) and (h)). Two peak values of the herb plant diversity exist in 1000 m a.s.l. and 1500 m a.s.l. in 1963. However, there is no obvious peak in 2006, and the substitute phenomenon is the moderate decreasing rate around the past peak elevation. In the shrub layer, Shannon-Wiener index generally declines with the rise of altitude. For this index, 1000~1100 m a.s.l. and 1400 m a.s.l. are the two peak point, and the obvious valley appears in 1200 m a.s.l. (Figure 1(g)). Both the two peaks coincide with the ecotones of different types of forest. This phenomenon supports the edge effect hypothesis. That is the plant diversity increases at the community boundaries[25,28]. Because of surveying time and sample area differences, the relationship between under canopy plant diversity and altitude is still a controversy[20,29]. 2.3.3 Similitude and difference in community change trend. Although climatic change is obvious in global scale, there is no great change for the altitudinal pattern of climatic and soil environmental factors in North Slope of Changbai Mountain[18,22]. The plant community composition and spatial diversity pattern are still determined by these factors. Further more, the conservation management, such as prohibiting cutting trees in CNR, soundly protected canopy trees and the forest structure. 954

The entire forest spatial pattern in North Slope of Changbai Mountain has not been disturbed by human activities. Nevertheless, we should not neglect the 2 differences in plant spatial pattern between 1963 and 2006. The first is that the herb-layer biodiversity peak disappears in the ecotones. This suggests that the herb layer is being disturbed by other factors, except for under canopy environment. The second is the great spatial-pattern difference between 2 surveying in succession layer (Figure 1(f)). A certain relationship between plant diversity of succession layer and altitude is obvious in 1963. The diversity value increases with altitude at the lower altitude. After reaching the peak at 900 m a.s.l., the value appears a negative correlation with elevation until to the middle elevation. Then, another peak appears at 1500 m a.s.l. However, there is no such a relation in 2006, 2 peaks at 1000 and 1400 m a.s.l.. As the progress of tree layer’s succession goes up, the determinants of plant structure in succession layer has changed from climate and soil factors to the micro environments under canopy. Therefore, further specific analysis of biodiversity changes and its reasons in each forest types is necessary.

3 Discussion The initial effect of external factors in one community usually is on keystone species, such as dominant tree species and highly sensitive herb species. Then the deep effect extends to the entire community through the interactions between plants[30,31]. Biodiversity of tree layer in MCBF and MCF increases from 1963 to 2006, but the value of shrub layer decreases; while biodiversities of all layers in SCF decreases in the same period. We conducted systematically comprehensive analysis in the factors that cause these changes. These factors contain the following aspects: climatic change and human disturbance, statistics comparisons of AIV composition and keystone species in each forest types, and plant physiological characters in canopy, succession and under canopy layers (Figure 2). 3.1 Biodiversity change in MCBF MCBF is the zonal forest ecosystem of this region. With its high stability and resistance to disturbances, different generations of Korean Pine distribute in this community[1,32]. The human disturbances in this forest are the collection of potherb, wild mushroom, Chinese herbal

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Figure 2 Important value changes of different shade-toleration species in three forest type of Changbai Mountain between 1963 and 2006. M, Main canopy story; S, succession layer; U, under-canopy layer; SI, shade-intolerant species; I, intermediate-tolerant species; ST, shade-tolerant species.

medicine and pine nut. Among these factors, pine nut collection is slight, so the main disturbances focus on the under layers. Consistent with our analysis, the co-dominant tree species and orders haven’t changed significantly. Referred to our survey, the top three AIV species from big to small are Korean pine, Acer and fir (Table 2). But the human effects on shrub and herb layers are obvious. The reduction of the richness and biodiversity in these layers reaches up to more than 20%. What’s more, the warming climate will aggravate the worsening situation in this area[31]. The research on the Korean pine in succession layers shows that the decline of this species cannot be simply determined by its bad regeneration ability under the closed canopy. As we know, the lack of light limits the growth of the pine seedling. So, in our sampling fields, there are just seedlings, no saplings[32]. Korean pine is still the dominant tree species in our study, but its AIV decreases from 0.27 in 1963 to 0.19 in 2006. The second co-dominant species accounts for more percent, and the proportion of other broad-leaved species increases. That caused the Korean pine declined for a certainty in forest. The generation succession of MCBF has been simulated by Markov chain model[33]. The results showed that the Korean pine decreased due to the lack of seedlings, thereby broad-leaved species increase. As a result of the increasing crown density in tree layer, the proportion of shade-tolerant species in succession and under

canopy layers have risen by 27% and 4% respectively from 1963 to 2006 (Figure 2). This is another evidence for the decline of Korean pine and the increase of broad-leaved species. It also caused the increase of the biodiversity in tree layer. Meanwhile, as the crown density of tree layer increases, the micro environment under canopy becomes more shading and homogenous, which lead to the rise of evenness and the increasing proportion of shade species, and the reduction of biodiversity. The obvious change in AIV appears in Q. mongolica. The AIV of Q. mongolica is just 0.03 in 1963, and fast rises to 0.10 in 2006. In the latest survey, this species has become new co-dominant species. Some research pointed out that the more proportion Korean pine occupies in the community, the more timber volume and water holding ability the forest obtains. Site condition varies from moist to dry in soil with the decline of the Korean pine, so such water-liking and shade-intolerant broad-leaved species can not healthily grow. This creates a good environment for Q. mongolica which is more adapted to dry soil condition. The Q. mongolica forest is thought as the possible succession direction of disturbed Korean pine forest[34,35]. Zhang et al.[22] summarized the climatic data from 1980 to 2000, and concluded the fluctuated increase of temperature, and the insignificant changed precipitation. Global warming will exacerbate the dry trend of forest site in this region, and promote the succession to Q. mongolica with the co-effect of

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human being disturbance. 3.2 Biodiversity changes in MCF MCF is in the middle section of 2 other forest communities, and its structure stability and resistance to disturbance are weak. However, it is the most severely disturbed by human. The heavy undermining to under canopy and tree layer of this forest is mainly imposed by widely pine nut collection and tourism industry. Especially, the large range collection of pine nuts greatly reduced the seed source for Korean pine regeneration. That follows by the worsened regeneration condition which is a crushing lower to one species[1]. Replacement of dominant species in tree layer (Table 2), sharply decline of plant diversity, and the decrease of evenness in under canopy layers are the concrete phenomena of frequent and severe human disturbance to forest ecosystem[36]. A. nephrolepis was the third dominant tree species in 1963. But it has exceeded the 1963’s first dominant species L. olgensis var. changpaiensis to be the major dominant one in 2006. Korean pine declines from the second place in 1963 to the third in 2006. For A. nephrolepis is a shade-tolerant species, proportion of shade-tolerant species has increased (Figure 2). The AIV of P. jezoensis var. komarovii greatly decreases from 1.1 in 1963 to 0.6 in 2006. This change induces a big difference in dominant species between 2 surveys, and has caused an obvious fall of evenness index in tree layer. In the other side, other broad-leaved species increases from 0.9 to 2.3, this is the main reason for the increases of biodiversity and richness in tree layer, similar with MCBF. The reason of obvious decline in tree species AIV is speculated to be tree mortality, nature disasters and human activities under tree layer. Many fallen trees were found in the sample plots. Heart rot and strong wind are the main cause of this large number of fallen trees according to the experiences of native people. The temporal shelters constructed by pine nut collectors and forest protectors were all made of nearby trees. But for the poor wood quality of A. nephrolepis, rare wood products were got from this species, which lead to the maintenance of A. nephrolepis in the forest, and the others tree species declined. Forest gaps formed by dead trees and fallen ones reduced the crown density of tree layer. That has caused variance of micro environment under tree layers, which can be evidenced by 9% rise of 956

shade-intolerant species in succession layer and another 5% rise in under tree layer from 1963 to 2006. 3.3 Biodiversity changes in SCF Area above 1500 m a.s.l. in North Slope of Changbai Mountain is assigned to develop tourism industry. Several measures of limiting tourism shuttles and fixed visiting tours have reduced the effects of tourism activities on nature ecosystem. But the reality of deduction in plant diversity is unquestionable attributed to human disturbances. The decrease rate of biodiversity in shrub and herb layers in this forest is the least among the 3 forests. This result complies with the common rule that biodiversity loss positively relates with disturbance extent of human being to natural communities[36,37]. Because of historical and traffic problems, tourism industry development of Changbai Mountain hasn’t reached its highest capacity, but the new airport construction will change this situation. The rapidly rising visitor number will add more pressure to natural ecosystem. The natural virgin state of SCF will be further threatened by such economic development. The change pattern of plant species composition in SCF resembled with that in MCF during this 43 years period, A. nephrolepis which replaced dominant places of L. olgensis var. changpaiensis in 1963 has become the major dominant species in 2006. As the 13% rise of the A. nephrolepis AIV, the proportion of shade-tolerant species greatly increases by 20%. The proportions of shade-intolerant species in succession and under wood layers have risen by 10% and 3% during 43 years respectively. Alternations of tree layer induce the decrease in crown density, and then evenness of all layers decreased[9]. Because of the high elevation, there are just a few tree species suitable to this environment. No big change happens in tree species richness, and the tree biodiversity index has decreased a little during 43 years. From our survey, the integrality of spatial pattern of forest plant community in Chanbai Mountain Nature Reserve has been completely conserved, and the general effects of protection are efficient. The prohibition of tree cutting has helped to preserve the tree layer. However, global warming has caused an obviously proportion increase in broad-leaved tree species, meanwhile human activity in the forest, such as tourism and pine nuts collection, has disturbed the under canopy plants and the succession layer. Generally, it is thought that human activities under canopy can not greatly alter the landscape,

BAI Fan et al. Sci China Ser C-Life Sci | Oct. 2008 | vol. 51 | no. 10 | 948-958

so human activities are permitted and neglected. The effects of frequent human disturbances[27] would gradually influence plant growth and tree regeneration. The keystone species and herb layers, sensitive to environmental changes, could be affected at first. Then crown density and under canopy environment change, which would disorder the essential symbiosis. Finally, permanent changes of ecosystem features and functions will be formed[5].

4 Conclusions The 2 community field observations of interval time were used to analyze the forty three years change of plant species diversity of Changbai Mountains on the north slope in altitude interval of 800~1700 m. From this research, we assessed the protection effect in this reserve. By contrasting the two surveys, we found that the conserve measures, such as forbidding tree cutting, soundly protecting tree layers, and the integrality of spatial pattern of forest plant community was been conserved completely. The co-dominant species in each type of forest was similar between 2006 and 1963. There was an obvious negatively correlation between species diversity in tree layers and the altitude. However, plant diversity was mainly controlled by micro environment for the under canopy layer. The temperature in Changbai Mountain area fluctuated increasing during 1963~2006. Human activities, such as illegal collection and tourism industry, disturbed all the three forests at certain extents, and caused some biodiversity and co-dominant species change. Biodiversity of shrub and herb layers in three forests significantly declined. Both diversity and evenness indices in MCBF increased. The reduction of the AIV of original domi1

dilemma. Ecol Appl, 1999, 9: 1459－1476

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nant species Korean pine and the rising of that value for Mongolic oak shows a possible succession for this forest. The increasing proportion of broad-leaved species brings about the larger proportion of shade-tolerant species under canopy. The evenness of tree layers in MCF and SCF both dropped. For biodiversity, it is increase in MCF and decrease in SCF. A. nephrolepis replaced dominant species L. olgensis var. changpaiensis (in 1963), and become the major dominant species. Shade-intolerant species was invading the forest gapes during this period. Land utilization can be divided into 3 phases: agriculture phase, industrial phase and information phase respectively[38]. The establishment of CRN has avoided the disastrous damage to nature ecosystem which appears in the industrial phase with the timber demanding as its main character. Nature reserve does have obvious positive effects on the protection of ecosystem integrity. The disturbances under trees would not cause significant landscape changes in short time. But the long term interference would have negative influences on plant diversity. As the science and technology advancing, there are less and less limits in human activities. The range, that human could arrive at, is larger and larger. However, some valuable nature ecosystems, which are fortunately remained for historical or geographic reasons, are suffering some uncertain nature and human damage. Tourism and estate industries are in the beginning period in Changbai Mountain. Therefore, it is necessary to soundly plan the tourism industry development in CRN. Hopefully, the reinforced management and plan can change the decreasing trend of Korean pine forest and recover the lost shrub and herb diversity in the future.

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