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Selection of air pollution tolerant plants through the 20-years-long transplanting experiment in the Yeocheon industrial area, southern Korea Selection of air pollution tolerant plants through the 20-years-long transplanting experiment in...
Kim, Gyung Soon; Pee, Jeong Hoon; An, Ji Hong; Lim, Chi Hong; Lee, Chang Seok
2015-05-04 00:00:00
Animal Cells and Systems, 2015 Vol. 19, No. 3, 208–215, http://dx.doi.org/10.1080/19768354.2015.1033011 Selection of air pollution tolerant plants through the 20-years-long transplanting experiment in the Yeocheon industrial area, southern Korea a a a a b* Gyung Soon Kim , Jeong Hoon Pee , Ji Hong An , Chi Hong Lim and Chang Seok Lee a b Department of Biology, Graduate School, Seoul Women’s University, Seoul 139–774, Korea; Department of Bio and Environmental Technology, Seoul Women’s University, Seoul 139–774, Korea (Received 20 April 2014; received in revised form 20 January 2015; accepted 26 February 2015) To select a tolerant plant species for restoring a forest ecosystem that had been severely damaged by air pollutants discharged from the industrial complex, 26 sample plants were transplanted in the mountainous area around the Yeocheon Industrial Complex in southern Korea. This transplanting experiment has been in progress for 20 years from 1994 to 2013. Ten plant species died and 16 plant species survived during the transplanting experiment period. Among the surviving 16 plant species, we chose five species, Alnus firma, Eurya japonica, Styrax japonica, Ligustrum japonicum, and Sorbus alnifolia as the very tolerant species, and four species, Pinus densiflora, Elaeagnus umbellata, Quercus dentata, and Fraxinus rhynchophylla as the tolerant species. We prepared a vegetation map by interpreting aerial photographs for diagnostic assessment of the forest vegetation damaged by air pollution. We estimated grassland, shrubland, and forest on the vegetation map as vegetation types that were severely, moderately, and slightly damaged, respectively. To restore each vegetation type damaged at different levels, we prescribed very tolerant plant species that compose tree and shrub layers, tolerant species that compose a tree layer, and artificial aid at a minimum level for passive restoration of the grassland, shrubland, and forest zones, respectively. Additionally, we recommended E. umbellata, which can fix atmospheric nitrogen levels, as the fertilizer plant. We recommended S. japonica and S. alnifolia, which flourish in a disturbed and/or polluted environment, as species for protective planting in margin of a forest to be restored in grassland damaged severely. Keywords: damaged forest; ecological restoration; industrial complex; tolerant plants; transplanting experiment Introduction even under severe plant competition and imposition of air pollution stresses, some species increase their growth. Under the stress of air pollution and acid rain, vegetation This occurs if a competitive advantage is given to them by undergoes changes that may range from drastic to the relatively greater impact of the pollutant on other negligible. The ultimate effects on vegetation structure species in the vegetation, and the growth of other species are the result of different responses of competing plant in the same vegetation may be greatly reduced because of species (Kozlowski 1980; Luttermann & Freedman 2000; their lowered competitive potential (Kercher et al. 1980; Winterhalder 2000; Lee et al. 2004, 2007). Reduced Kozlowski 1980; Luttermann & Freedman 2000; Winter- photosynthesis and visible damage, such as chlorosis, halder 2000; Lee et al. 2004). lesions, and abscission, are preludes to growth inhibition Pollutants discharged beyond the limits of the buffer- and to mortality of the more sensitive plants, leading to ing capacity of an ecosystem prevent it from maintaining alteration of vegetation structure (Hällgren 1978;You its normal structure and function. Excessive land use and et al. 1998; Luttermann & Freedman 2000; Winterhalder ecological imbalance appear to be major factors that 2000; Lee et al. 2004, 2007). In addition, vegetation is threaten environmental stability on local as well as global also influenced by changes in reproductive capacity due to levels (Luttermann & Freedman 2000; Winterhalder 2000; air pollution and acid rain (Kramer & Kozlowski 1980; Lee et al. 2004, 2007). Symptoms of decline observed in Cox 1984) and by their interactions with plant diseases the vicinity of industrial complexes including Yeocheon and insects (Treshow 1975; Chakraborty et al. 2000; Percy where this study was carried out (Kim 1991; Lee 1992; et al. 2002). Lee et al. 2004, 2008), and in urban areas (Kim 1991; Imposed pollution stresses usually set in motion a Rhyu 1994; Rhyu & Kim 1994; Lee & Cho 2008), retrogression characterized by a reduction in structural correspond to such examples. In fact, global environ- complexity and function of vegetation (Luxmoore 1980; mental problems such as climate change are due to this Ravera 1987; Luttermann & Freedman 2000; Winter- functional imbalance between the pollution source and the halder 2000; Lee et al. 2004, 2007, 2008; Lee & Cho sink (UNEP 2009; Fenn et al. 2011). 2008). Sudden imposition of severe air pollution stress Considering the fact that population size and land sometimes occurs so rapidly that feedback mechanisms cannot operate to select for resistant species. Nevertheless, use intensity have been expanding continuously, such *Corresponding author. Email: leecs@swu.ac.kr © 2015 Korean Society for Integrative Biology ECOLOGY, POPULATION BIOLOGY, & ANIMAL BEHAVIOR Animal Cells and Systems 209 ecological imbalance is likely to increase even more in the other was to prepare a restoration plan for damaged forest future (Lee et al. 2004, 2008; Lee & Cho 2008). In fact, vegetation around the Yeocheon industrial complex by industrialized and urbanized areas have been expanding arranging various plant species with different tolerance steadily and the real size of degraded vegetation, such as levels in each zone divided based on pollution levels grassland and shrubland, has increased proportionally to derived from vegetation degradation. such land transformation in the Yeocheon industrial complex (Lee 1993; Ministry of Environment, 1996; Lee Methods et al. 2004, 2007). Moreover, vegetation decline induces Study area structural simplification and functional weakening of plant communities, consequently leading to negative effects on The Yeocheon industrial complex, which is located on the other biotic communities (Lee & Cho 2008; Lee et al. southern coast of the Korean Peninsula, is the represent- 2008). In this respect, restoration of degraded ecosystems ative industrial complex of Korea (Figure 1). This is urgently required to prevent the spread of such additive industrial complex was constructed in the early 1970s pollution damage (Gunn 1995; Lee et al. 2004, 2008). and is still expanding. Industrial activities in this complex Restoration of an ecosystem damaged by environ- focus on the heavy chemical industry including petro- mental pollution can be achieved either through improve- chemical production. The major pollutant is primarily ment of the environment by preventing pollutants from SO .SO emission in the Yeocheon industrial complex is 2 2 pollution sources or by establishing plants tolerant to the about 25,000 tons per annum, and the ambient SO is 0.02 pollutants (Bradshaw 1992; Gunn 1995, 1996; Dobson ppm, with an annual mean of the highest daily value of et al. 1997; Lee et al. 2004, 2007, 2008). Species tolerant 0.06 ppm. Such severe air pollution not only has caused to environmental pollution can persist through growth and vegetation degradation to the extent that the former forest reproduction or even expand their distribution range in the is degraded to grassland, but has also led to soil polluted environment (Kercher et al. 1980; Kozlowski acidification, with a mean pH of 4.4 and a range from 1980; Luttermann & Freedman 2000; Winterhalder 2000; 3.5 to 6.7 (Ministry of Environment 1996; Lee et al. Lee et al. 2004, 2007). 2004, 2007). Species that have a high ecological value or are Due to such acidification, the soil contains one-third to 2+ 2+ common in the polluted environment usually have a one-half lower Ca and Mg contents and two or three 3+ tolerance to corresponding pollutants (Lee et al. 2004, times higher Al content compared to that of the healthy 2007, 2008). It is, therefore, reasonable to select tolerant reference area (Ministry of Environment 1996; Lee et al. species in the polluted area (Bell et al. 1993; Lee et al. 2004, 2007). 2004). Differential tolerance among plant species to the Vegetation in this area before the construction of this polluted environment can be evaluated comparing survival industrial complex was covered with pine forest domi- rate, growth, vitality, etc. of plant species inhabiting and nated by Pinus densiflora and Pinus thunbergii. However, transplanted to the polluted environment (Taylor 1978; pollution, which occurred after the industrial complex Bell et al. 1993; Lee et al. 2004). began operating, degraded vegetation into shrubland, Transplanting experiments play a mediating role grassland, and young pine stand (Lee 1993; Ministry of between field surveys and stress tests and can thereby Environment 1996; Lee et al. 2004, 2007). provide significant applicable information. In particular, such experiments can aid in selecting tolerant species that Plant transplantation have a high restoration potential even though they are not preexistent in the polluted area (Lee et al. 2004). The We transplanted sample plants to the polluted site located at Yeocheon industrial complex, where the experiment was a distance of 500 m from the pollution source (Figure 1). executed, is the representative industrial complex of Two-year-old healthy seedlings of 26 species were prepared Korea, and its vegetation distribution pattern reflects as sample plants in 1994. Sample plants were planted in the bare ground prepared by removing the existing vegetation vegetation damage that is dependent on the distance dominated by Miscanthus sinensis. Seedlings were planted from the pollution source and topographic condition (Lee regularly at intervals of 0.5 m. To reduce bias deriving from et al. 2004). Therefore, this area provides a suitable site planting location we rotated the order of sample plants in for selecting tolerant plants to air pollution through a each line. transplanting experiment. This study had two objectives. The first was to select The responses of sample plants were assessed in tolerant plants by comparing external damage, growth August of 2013, the 20th year after the transplantation; state, apical dominance, growth of the annual ring, and survival rate was checked in 1996, the third year after survival rate of plant species grown in the polluted transplanting. The responses were inspected by comparing mountainous area around the Yeocheon industrial complex leaf damage, growth state, apical dominance, growth of in southern Korea for 20 years after transplantation. The the annual ring, and survival rate based on Table 1. 210 G.S. Kim et al. Figure 1. A map showing vegetation state of the study area, Yeocheon industrial complex. E indicates the experimental site. Degree of leaf surface injury was classified into five the growth by dividing them into two kinds of sample groups: very severe (more than 75% of total leaf area plants. A regression equation was obtained by accumulating damaged), severe (50–74% of total leaf area damaged), growth values obtained from each sample plant. A regres- moderate (25–49% damaged), slight (less than 25% sion coefficient of the equation was used as the growth damaged), and none (not damaged). Degree of growth index of each sample plant. Each growth index was state was also classified into five groups: very good, good, recalculated by giving values 5 and 1 to the highest and moderate, poor, and very poor. Apical dominance was the lowest indices, respectively. We obtained a tolerance index of sample plants by summing the tolerance index classified into two groups depending on the presence or absence of the phenomenon. Survival rate was obtained values of five factors and defined this as a synthetic from the percentage of surviving plants to that of all tolerance index. The order of tolerance of each plant species placed plants. For quantitative evaluation, a value was was determined based on the synthetic tolerance index attributed to each index degree, ranging from 5 (the most (Table 2). In this transplanting experiment, we regarded tolerant) to 1 (the most sensitive; Table 1). Core of the plants for which the tolerance order was ranked within the annual ring was sampled above ground at a 30-cm height. upper one-third among 26 plants transplanted for experi- mental study as a tolerant species (Lee et al. 2004). Growth of the annual ring was measured with an increment core measurement instrument (GRUBE, Germany) with a In order to prove the appropriateness of tolerant plants precision at the 0.01-mm level. Growth of the annual ring selected by the transplanting experiment throughout the differs between trees and shrubs. Therefore, we evaluated long period for 20 years, the result of this study was Animal Cells and Systems 211 Table 1. Criteria for evaluation of tolerance level in the field transplanting experiment. Degree element 1 2 3 4 5 Leaf surface injury Very severe Severe Moderate Slight None Vitality Very bad Bad Moderate Good Very good Apical dominance No apical dominance ––– Apical dominance Growth of annual ring Growth index recalculated by providing values 5 and 1 to the highest and the lowest indices Survival rate (%) Below 20.0 20.1–40.0 40.1–60.0 60.1–80.0 80.1–100.0 compared with the results selected by applying different scale. Mapping was carried out using ArcView GIS (ESRI 2008). methods such as field survey, exposure experiment to SO , toxic Al , and another transplanting experiment 2 3+ conducted for a short period for one year (Lee et al. 2004). Results A comparison of the results was carried out based on similarity between the tolerance orders of sample plants Among the sample plants of 26 species, 10 species from different methods. A similarity index was obtained including Ailanthus altissima, Carpinus laxiflora, Fir- by using the following equation (Kent & Cocker 1992) miara simplex, P. thunbergii, Populus tomentiglandulosa, Quercus variabilis, Rhododendron mucronulatum, Rhodo- 2C SIðsimilarity indexÞ¼ dendron yedoense var. poukhanense, Robinia pseudoaca- AþB cia, and Zelkova serrata died; therefore, the tolerance where A = number of tolerant species selected in the level was assessed for the surviving 16 species (Table 2). transplant; B = number of tolerant species selected in each Fraxinus rhynchophylla showed severe leaf damage, selection method; C = number of species common to both and Sorbus alnifolia, Quercus serrata, Quercus acutis- methods. sima, Ligustrum obtusifolium, Pinus rigida, and Celtis Monochrome aerial photographs (1:15,000 scale) sinensis showed medium damage. On the other hand, taken in May of 2010 were used to identify vegetation Alnus firma, Eurya japonica, and Ligustrum japonicum types and landscape boundaries. Vegetation types and did not show any leaf damage, and Styrax japonica, landscape elements identified on these photographs were Elaeagnus umbellata, P. densiflora, Quercus aliena, confirmed in the field. The identified landscape attributes Quercus dentata, and Quercus mongolica showed a little were overlapped onto topographical maps at 1:25,000 damage (Table 2). Table 2. Tolerance index of sample plants evaluated through transplanting experiment for 20 years in the Yeocheon industrial complex. Leaf Apical Annual Survival Synthetic tolerance Order of damage Vitality dominance ring rate index tolerance A. firma 5 5 5 5.00 5 25.00 1 E. japonica 5 5 5 5.00 5 25.00 1 S. japonica 4 5 5 4.21 5 23.22 3 L. japonicum 5 4 5 2.40 5 21.40 4 S. alnifolia 3 5 5 2.53 5 20.53 5 P. densiflora 4 5 5 2.21 3 19.21 6 E. umbellata 4 3 5 2.00 2 16.00 7 Q. dentata 4 3 1 3.74 4 15.74 8 F. rhynchophylla 2 4 1 2.44 4 13.44 9 Q. aliena 4 3 1 2.24 3 13.24 10 Q. serrata 3 4 1 1.76 4 12.76 11 Q. acutissimas 3 2 1 2.57 4 12.57 12 L. obtusifolium 3 3 1 1.38 4 12.38 13 C. sinensis 3 2 1 1.99 4 11.99 14 Q. mongolica 4 1 1 1.99 3 10.99 15 P. rigida 3 2 1 2.07 2 10.07 16 Notes: Tolerant species indicate those that the order of tolerance is within the ninth. Five species ranked within the upper fifth order in tolerance level were subdivided into very tolerant species. 212 G.S. Kim et al. The vitality of Q. mongolica was very bad, and that of Similarity was the highest when comparing the experi- Q. acutissima, P. rigida, and C. sinensis was bad. A. ment result with the one-year transplanting experiment firma, E. japonica, P. densiflora, S. alnifolia, and S. (50.0%), and the index was lower in the following order: 3+ japonica showed very good vitality, and F. rhynchophylla, with Al solution culture (42.1%), field survey (40.0%), L. japonicum, and Q. serrata showed relatively good and SO fumigation (37.5%). vitality. On the other hand, vitality of E. umbellata, L. The result of this study, carried out by the field obtusifolium, Q. aliena, and Q. dentata was of medium transplanting experiment, reflects the actual response of level (Table 2). the sample plants exposed directly for long periods to the Species ranked in higher tolerance levels within the polluted environment. Moreover, the very tolerant plants seventh order, such as A. firma, E. japonica, S. japonica, also grow well in the unpolluted environment of this area, L. japonicum, S. alnifolia, P. densiflora, and E. umbellata which corresponds to a warm temperate zone. Therefore, showed apical dominance, whereas species ranked in the tolerant plants selected from this study could play lower level below the eighth order did not show apical diverse roles in the structure and function of vegetation dominance. Among plants selected as tolerant species, two that may be used for restoration in the future (Bell et al. species, Q. dentata and F. rhynchophylla, did not show 1993; Lee et al. 2004, 2007). Evidence from another apical dominance (Table 2). restoration program also showed that species that were The annual ring of A. firma, E. japonica, and S. dominant prior to disturbance can be successfully reintro- japonica showed very good growth, and that of Q. dentata duced to the disturbed site where restoration is required showed good growth. The annual ring growth of Q. (Cooper & MacDonald 2000; Lee et al. 2004, 2007). acutissima, S. alnifolia, F. rhynchophylla, L. japonicum, Q. aliena, P. densiflora, and P. rigida showed medium Consideration for ecological restoration of damaged growth. On the other hand, the annual ring of E. umbellata, vegetation C. sinensis and that of Q. mongolica, Q. serrata, and L. A vegetation map of the vicinity of the Yeocheon obtusifolium showed poor and very poor growths, respect- industrial complex in southern Korea, where this study ively (Table 2). was carried out, is shown in Figure 1. The vegetation map A. firma, E. japonica, S. japonica, L. japonicum, and shows that the pine stand is a dominant vegetation type, S. alnifolia showed a very high survival rate and Q. which forms a matrix in the landscape of this area. P. dentata, F. rhynchophylla, Q. serrata, Q. acutissima, L. densiflora and P. thunbergii dominated this pine stand as obtusifolium, and C. sinensis showed a relatively high this is typical of coastal forests in Korea (Lee 1993; survival rate. On the other hand, P. densiflora, Q. aliena, Ministry of Environment 1996). Distribution of vegetation and Q. mongolica showed a moderate survival rate and E. along the distance from the pollution source shows the umbellata and P. rigida showed a bad survival rate (Table 2). order of grassland, shrubland (dominated by S. japonica The tolerance level was determined by synthesizing community), and forest (dominated by P. densiflora – P. the above-mentioned results. Nine species that had a thunbergii). Such a distributional trend might be related to tolerance order ranked within the upper one-third among the air pollutants being transported with the land and sea the 26 plant species transplanted for experimental study breeze (Lee et al. 2004, 2007). The grassland was were regarded as tolerant species: A. firma, E. japonica, S. composed of M. sinensis, Phytolacca americana, Puer- japonica, L. japonicum, S. alnifolia, P. densiflora, E. aria thunbergiana, and Melica onoei communities (Lee umbellata, Q. dentata, and F. rhynchophylla. Among the et al. 2004, 2007). These communities composing the tolerant species, species ranked within the upper fifth grassland were the vegetation types markedly damaged order of the tolerance level were subdivided into very due to severe air pollution. Mixed grasslands tended to tolerant plants. Ten plant species died during the 20-year distribute in the ridge parts somewhat distant from the transplanting experiment and were regarded as sensitive pollution source compared with the other grasslands. Shrubland occurred in the areas closer to the pollution plants. source, but the effects of air pollution were mitigated by topographic conditions, such as a valley, in the faced slope Discussion and in the mid-slope opposite to the pollution source. A comparison of the results among different tolerance Forest was established in areas distant from the pollution test methods source or in cases of light air pollution, such as at the base of a mountain, on the slope opposite to the pollution The result of this study was then compared with the source (Lee et al. 2004, 2007). results evaluated by a field survey and a short-term one- year transplanting experiment performed in the vicinity of Grassland and shrubland were concentrated around the the Yeocheon industrial complex, in SO fumigation, and pollution source of the Namhae Chemical Company. 3+ These grasslands or shrublands resulted from forest in solution culture including toxic Al (Lee et al. 2004). Animal Cells and Systems 213 decline caused by pollution damage (Lee 1992, 1993; plants that make up the final biodiversity of the ecosystem Ministry of Environment 1996). and should be able to recolonize by their own efforts In the studies of point sources of air pollution, there is (Dobson et al. 1997). Our reclamation goal was to a general observation of ecological damage becoming reestablish a forest with diverse strata and functions in progressively less severe as the distance from the source this barren mountain; therefore, we applied the concept of increased. This pattern closely tracked the gradients of the novel ecosystem (Hobbs et al. 2009; Zedler et al. pollution, which were characterized by a roughly expo- 2012; Hobbs et al. 2013). Novel ecosystems are known as nential decrease in intensity as the distance from the the systems of abiotic, biotic, and social components (and source increased (Freedman 1995; Gheorghe & Ion 2011). their interactions) that, by virtue of human influence, If a forested ecosystem is being affected by air differ from those that prevailed historically and have a pollution, then the tree stratum is generally impacted first tendency to self-organize and manifest novel qualities and is stripped away. As trees decline, shrubs and then the without intensive human management (Hobbs et al. 2013; ground vegetation are affected. This syndrome of sequen- Temperton et al. 2014). This area was changed vastly tial death of horizontal strata of the terrestrial vegetation because of industrial activities (Lee et al. 2004, 2007) and has been described as a peeling or layered vegetation the trends are expected to continue into the future. In this effect (Gordon & Gorham 1963; Woodwell 1970). There- respect, we adopted the concept of a novel ecosystem, fore, the degree of pollution is reflected in the actual which allows for more flexibility in biodiversity conser- vegetation, and thereby, the restoration sector could be vation under conditions of rapid change and significant zoned based on the vegetation state. Based on this alteration, rather than restoration based on singular vegetation damage pattern, we divided grassland, shrub- trajectories rooted in historical composition and function land, and forest into very severely, severely, and slightly (Temperton et al. 2014). damaged vegetation types, respectively. Then, we pre- For restoring the grassland, plant species composing scribed the restorative treatments for each vegetation type both tree and shrub layers should be introduced and the as: very tolerant species that compose tree and shrub most tolerant plants should be introduced in terms of layers for grassland that was damaged severely, tolerant tolerance level. In consideration of these two viewpoints, species that compose the tree layer for shrubland damaged we prescribed A. firma and S. alnifolia as trees and E. moderately, and passive restoration for forest damaged japonica, S. japonica, and L. japonicum as shrubs. To slightly. restore the shrubland, P. densiflora and Q. dentata were Grasslands caused by pollution damage also appeared recommended. Conversely, for the forest, we prescribed in sites distant from the pollution source. However, artificial aid at a minimum level, which can help the grasslands were restricted to the ridges in these sites, passive restoration that is already in progress. In addition, which were located beyond the first ridge from the we recommended E. umbellata, which can fix atmospheric pollution source. Based on our interpretation of this nitrogen (Song et al. 1993), as the fertilizer plants, and S. vegetation map, we decided that the spatial range within japonica and S. alnifolia, which flourish in the disturbed the first ridge was the sector in which restoration efforts and/or polluted environment (Lee et al. 2008), as species should be concentrated. for protective planting in margin of forest to be restored in grassland damaged severely (Table 3). Restoration plan for each vegetation type Restoration planning pursued in this study followed the principle of ecological restoration, because the plan is Studies of restoration have chosen species for restoration based on the diagnostic assessment of the state of the on the basis of the following criteria: (1) species important actual vegetation (SERI & PWG 2004). On the other for restoring ecosystem function, (2) species that are to be the main components of the final ecosystem, and (3) hand, restoration planning carried out in this study Table 3. Damage degree of forest vegetation evaluated on the bases of the vegetation type and restoration level and method determined based on the results. Vegetation type Damage degree Restoration level Restoration practice Grassland Severely damaged Active restoration Introduction of plant species composing tree (A. firma and S. alnifolia) and shrub (E. japonica, S. japonica, and L. japonicum) layers Shrubland Moderately Partially active Introduction of plant species composing tree layer (P. densiflora and damaged restoration Q. dentata) Forest Slightly damaged Passive restoration Artificial aid to facilitate passive restoration 214 G.S. Kim et al. Hobbs RJ, Higgs ES, Harris JA. 2009. Novel ecosystems: displayed flexibility by adopting the concept of the novel implications for conservation and restoration. 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