Distribution, abundance, and effect on plant species diversity of Sasa borealis in Korean forests

Distribution, abundance, and effect on plant species diversity of Sasa borealis in Korean forests Background: Sasa borealis (Hack.) Makino, a clonal dwarf bamboo, is widespread in Korean forests. Although S. borealis is native to that country, its growth habit can cause considerable harm when occupying particular areas where it dominates and influences those forested communities. However, few reports have described the extent of its inhibitory effects on the vigor of co-existing plant species. Therefore, we investigated the distribution, abundance, and diversity of other plant species in the communities where this plant occurs in the east-central forests on the Korean Peninsula. Results: S. borealis was most commonly found at an elevational range of 800 to 1,200 m, on gentle, usually lower, and near valley northern slopes. Out of the 13 forest communities based on 447 forest stands that we surveyed, S. borealis was detected in eight communities, mostly where Quercus mongolica dominates. In particular, it was more common in late-successional mixed stands of Q. mongolica, other deciduous species, and the coniferous Abies holophylla. Because of their ability to expand rapidly in the forest, this plant covered more than 50% of the surface in most of our research plots. Species diversity declined significantly (F =78.7, p = 0.000) as the abundance of S. borealis increased in the herb stratum. The same trend was noted for the total number of species (F =18.1, p = 0.000) and species evenness (F =91.5, p =0.000). Conclusions: These findings clearly demonstrate that S. borealis is a weed pest and severely hinders species diversity. Authorities should be implementing various measures for ecological control to take advantage of declining chance after the recent synchronized massive flowering of S. borealis. Keywords: Dwarf bamboo, Quercus mongolica forest, Native weedy pest, Synchronized massive flowering Background Ulleung Island, Jeju Island, and in North Korea, respect- Sasa borealis (Hack.) Makino is a native plant species that ively (Lee 2003). belongs to Bambusoideae. It can be found on almost any This evergreen dwarf bamboo shows a clonal habit. mountain in Korea, including national parks (Lee and Lim Once established, the plants annually produce new 2002), and has been reported from the southern to the ramets (culms) on their long, thin rhizomes (Makita northern regions, e.g., Mts. Baegun, Wolchul, Jiri, Naejang, 1998) and grow approximately 1 to 2 m tall. Because of Deogyu, Sobaek, Chiak, Odae, and Seorak (Ahn et al. 2004; the physiological integration between connected Oh et al. 2005; Choung et al. 2009;Kim 2012;Parketal. rhizomes, they can overcome resource deficiencies 2012; Cerny et al. 2013). Although three other species of (Saitoh et al. 2002). In addition, their very shade-tolerant Sasa—S. kurilensis, S. quelpaertensis,and S. coreana—grow nature means that they can occupy the forest floor and in Korea, their populations are isolated and found only on become dominant as their populations increase infinitely (Yuruki et al. 1987; Park et al. 2012). Consequently, the density of aboveground evergreen shoots is high * Correspondence: yschoung@kangwon.ac.kr throughout the year while their thick, round rhizomes Department of Biological Sciences, Kangwon National University, completely also occupy the underground space. These Chuncheon 24341, South Korea attributes make the plants very competitive within the Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Cho et al. Journal of Ecology and Environment (2018) 42:9 Page 2 of 7 lower strata of a forest, and pure patches can be main- on Natural Resources in Korean National Parks (Choung tained for long periods (Oshima 1961; Nakashizuka et al. 2004). Those studies of 447 forested plots in the 1988; Hiura et al. 1996; Narukawa and Yamamoto 2002). east-central portion of the Korean Peninsula focused on In Japan, plants within the Sasa genus are regarded as the period of 1992 to 2014 and covered most of Gangwon serious weed pests (Li et al. 1992). In the 1950s, the Province and part of Chungcheong Province, including Japanese Forestry Research Institute reported that Danyang and Jecheon. Four variables were examined as approximately 50% of the area in Japanese national parks potential factors in determining the establishment and was covered with these plants, and that they accounted spread of S. borealis: elevation, slope, topography, and as- for 90% of the coverage in Hokkaido (Oshima 1961). On pect. The abundance of all plant species in each plot was Jeju Island in Korea, S. quelpaertensis covers approxi- analyzed by the Braun-Blanquet dominance scale for each mately 76% of the northern slopes at Mt. Halla National of four strata, based on plant height: (1) tree (T1), > 8 m Park, from 400 m up to the top. These circumstances tall; subtree (T2), 5∼8 m; shrub (S), 1∼5 m; and herb (H), are especially threatening to the survival of rare plant < 1 m. The number of plots where S. borealis presented species such as Empetrum nigrum var. japonicum, Genti- was 76 with either 15 m × 15 m (46) or 20 m × 20 m (30). ana chosenica, Primula modesta var. hannasanensis, and We first conducted a cluster analysis to classify vegeta- Ranunculus borealis in subalpine zones (Northeastern tion types, using cover data transformed by the Asia Biodiversity Institute 2017). square-root arcsign (Peck 2016) and then determined The current massive flowering cycle for S. borealis began the frequency and abundance of S. borealis within com- nationwide in 2013 (Cho et al. 2017). As a typical mono- munities. Those communities were named according to carpic plant, culms in the flowering patches tend to die off the one or two dominant tree species (cover > 50%) and within 1 year. Therefore, this type of reproductive event other species that were deemed to be significant indica- has an enormous effect on the vegetation dynamics of a tors, as revealed by an analysis by Peck (2016). From our forest dominated and suppressed by Sasa. Although it may 447 plots, 642 taxa were identified (Lee 2015). be too early to determine whether this event enables other Speciesdiversity wasevaluated by stratum, and S. species to regenerate naturally or allows S. borealis to borealis abundance (% cover) was assessed within the re-populate a site, this phenomenon gives us the opportun- herbaceous stratum. For species diversity using the ity to investigate whether a species that normally inhibits same size 46 plots (15 m × 15 m each), we applied diversity in South Korean forests might also experience its the Shannon-Weiner index (H′ = −∑ p log p ), where i e i own natural decline on such a large spatial scale. p represented relative cover. Species evenness (E)was In Korea, the Act on the Conservation and Use of Bio- calculated as E =H′/log S (S number of species), logical Diversity has been enacted to preserve and protect while species richness was defined as the number of biodiversity by designating some plants, including invasive individual species on a plot. The growth form was re- aliens, as ecosystem-disturbing species (Ministry of Envir- corded for each species, as we have previously de- onment 2017). Although S. borealis is native to that coun- scribed (Choung et al. 2012). For this, the categories try, we believe that its growth habit can cause considerable of tree, shrub, and herb respectively included trees harm when occupying particular areas where it dominates and subtrees; shrubs, vines, prostrate woody plants, and influences those forested communities. Under such and subshrubs; and herbs and climbing herbs. conditions, the diversity of other plant species appears to Differences among plots and strata were examined by be very low. However, these scenarios have not yet been of- one-way ANOVA, followed by a Bonferroni post hoc ficially documented or quantified in Korea. Our research analysis. Regression analysis was used to investigate the goals were to explore the physical habitats and forest com- responses of diversity indices based on S. borealis coverage. munities in which S. borealis occurs and to determine how All data were examined with SPSS software (SPSS 2013; plant species diversity is affected by the dominance of this ver. 22). species. These findings could then be used to develop strat- egies for ecological control and manipulation. Results Methods Distribution and abundance for Sasa borealis We used a database incorporating information that we The most common habitats for Sasa borealis were had gathered previously in our National Ecosystem Survey determined by examining site conditions (Fig. 1). Our for the Ministry of Environment (Choung et al. 1997, plot surveys revealed plants of that species on 76 of 1998; Choung and Oh 1999; Choung and Hong 2001; 447 plots. This species was less likely to occur in the Choung et al. 2002, 2003; Choung and Lee 2012;Choung elevational classes of lowlands (100 to 240 m) and and Kim 2013), plus data collected for Korea Long-term highlands (1,360 to 1,555 m) and was more common Ecological Research (Choung et al. 2013) and the Survey (61.9% of all plots) at elevations of 800 to 1,200 m. Cho et al. Journal of Ecology and Environment (2018) 42:9 Page 3 of 7 Fig. 1 Frequency of Sasa borealis in Korean forests. In each panel, gray bars indicate relative distribution (%) of 447 investigated plots; green bars, relative distribution (%) of 76 plots in which S. borealis occurs. LS, lower slope; MS, middle slope; US, upper slope Plants of S. borealis preferred more gentle slopes, i.e., S. borealis occurring forest communities 0° to 47°, and were not found in steeper areas. In par- The 447 plots were classified into 13 communities (domin- ticular, this species was most frequently counted ant—dominant_other significant indicator species): Quercus (40.8%) on slopes ranging from 20° to 30°, followed by variabilis—Pinusdensiflora_Ulmusmacrocarpa, Q. variabi- 30° to 40° (33% of all plots where it occurred). Overall, lis—Q. dentata_Spodiopogon sibiricus, P. densiflora—Q. these plants tended to be more common, topologically, variabilis_Q. serrata, P. densiflora_Rhododendron mucro- on near valleys and lower slopes (61.6%) and were less nulatum, P. densiflora_Rubus crataegifolius, P. densiflora— frequent on ridges and mountain tops. With regard to Juglans mandshurica_Persicaria filiformis, Q. mongolica— the aspect variable, S. borealis was more common on Carpinus laxiflora_Lindera obtusiloba, Q. mongolica_Sy- northern slopes (315°~45°) and relatively less frequent neilesis palmata, Q. mongolica_R. schlippenbachii, Q. mon- on southern and western slopes. golica—Abies holophylla_S. borealis, Q. mongolica_Lychnis Of the 76 plots containing S. borealis,those plants cognata, Q. mongolica—Fraxinus mandshurica_Philadel- covered more than half of the surface on 58% of those phus schrenckii,and Q. mongolica—Betula ermanii_Cacalia plots. This high spread value was rare for species found praetermissa. in the herbaceous layer in general. Because of its clonal Of these 13, S. borealis appeared within eight of them habit, the average coverage and standard deviation for (Fig. 2). Except for the P. densiflora—Q. variabilis_Q. ser- plots with S. borealis were 53.3 and 31.7, and abun- rata community (no. 3 in Fig. 2), Quercus mongolica was dance did not differ significantly among classes for any the dominant species, occurring on 96% of all plots. The of the four variables (Table 1). highest coverage by S. borealis, 61%, was measured in the Cho et al. Journal of Ecology and Environment (2018) 42:9 Page 4 of 7 Table 1 Percent coverage of Sasa borealis plants according to site variables of elevation, slope, topography, and aspect Elevation Slope Topography Aspect Class (m) Cover (%) Class (°) Cover (%) Class Cover (%) Class (°) Cover (%) 200~400 53.5 ± 12.3 (8) ≤ 10 59.8 ± 9.9 (8) Valley 62.7 ± 6.9 (13) 315~45 57.1 ± 5.6 (30) 400~600 34.0 ± 19.4 (4) 10~20 58.4 ± 11.1 (8) Lower slope 55.7 ± 6.5 (23) 45~135 59.6 ± 7.2 (18) 600~800 62.2 ± 9.0 (13) 20~30 48.9 ± 6.1 (31) Middle slope 55.8 ± 9.7 (13) 135~225 57.1 ± 9.2 (15) 800~1000 53.1 ± 5.1 (29) 30~40 57.2 ± 7.1 (21) Upper slope 41.3 ± 6.6 (23) 225~315 28.9 ± 7.9 (10) 1000~1200 53.1 ± 8.6 (18) 40~50 46.6 ± 10.7 (8) Ridge and top 65.8 ± 21.8 (4) 1200~1400 42.0 ± 20.0 (4) Data are means ± standard error, with number of plots shown in parentheses. Aspect for three plots were not determined Q. mongolica—Abies holophylla_S. borealis community trend was noted for the total number of species (F = (no. 10 in Fig. 2, right side). That particular community is 18.1, p = 0.000) and species evenness (F = 91.5, p = considered relatively late-successional (Lee 2015), where 0.000). This was especially true when S. borealis covered Q. mongolica co-dominates with Tilia amurensis, Abies more than 75% of the surface in a plot. In that case, the holophylla,and Acer pseudosieboldianum.In addition to diversity index for the herb stratum was as low as 0.536, several other tree species, its tree stratum or the shrub which then limited the availability of water and nutrients stratum in this community is occupied by Rhododendron to plants in the canopy. However, diversity within the shillipenbachi and Lindera obtusiloba. tree, subtree, and shrub strata did not tend to be corre- Among the eight communities in which S. borealis lated with the dominance of S. borealis. Although the di- grows, that species covered more than 50% of the forest versity of shrub species tended to decrease as the floor in five of them (Fig. 2). For the remaining three frequency of S. borealis rose, this trend was not statisti- communities, lower overall coverage by those plants was cally significant and possibly resulted, instead, because due to less amenable site conditions, including a lower of the limited sample size. elevation, an upper slope facing south (no. 8), an upper In the herb stratum, H′ values for herbaceous species slope or ridge at high elevation (nos. 11 and 13), or the were significantly reduced as the abundance of S. borea- purity of the Q. mongolica stands that precluded compe- lis increased (F = 45.8, p = 0.000; Table 2). When cover- tition from other species. age by that species was > 75%, the diversity index in such plots was as low as 0.314. In particular, the number Effect of S. borealis on plant species diversity, based on of herbaceous species averaged 31 when S. borealis stratum and growth form abundance was < 5% but totaled only six when Sasa At the plot level, values for species diversity declined sig- coverage was > 75% (F = 45.8, p = 0.000). Similar trends nificantly (F = 78.7, p = 0.000) as the abundance of S. were noted for species evenness and total number of borealis increased in the herb stratum (Fig. 3). The same species (F = 65.8, p = 0.000). The species diversity of tree Fig. 2 Left, frequency of Sasa borealis in 13 communities identified from surveys of 447 total plots. Right, abundance (% cover) of S. borealis plants in communities shown on left. On right, error bars indicate significant differences at p < 0.05. Communities: 1, Quercus variabilis—Pinus densiflora_Ulmus macrocarpa;2, Q. variabilis—Q. dentata_Spodiopogon sibiricus;3, P. densiflora—Q. variabilis_Q. serrata;4, P. densiflora_Rhododendron mucronulatum;5, P. densiflora_Rubus crataegifolius;6, P. densiflora—Juglans mandshurica_Persicaria filiformis;7, Q. mongolica—Carpinus laxiflora_Lindera obtusiloba;8, Q. mongolica_Syneilesis palmata;9, Q. mongolica_R. schlippenbachii; 10, Q. mongolica—Abies holophylla_S. borealis; 11, Q. mongolica_Lychnis cognata; 12, Q. mongolica—Fraxinus mandshurica_Philadelphus schrenckii; and 13, Q. mongolica—Betula ermanii_Cacalia praetermissa Cho et al. Journal of Ecology and Environment (2018) 42:9 Page 5 of 7 Fig. 3 Plant species diversity (H′), richness, and evenness as a function of Sasa borealis abundance (% cover) in 4 strata. Data points are mean values. Strata: T1, tree; T2, subtree; S, shrub; H, herb and shrub species in the herb stratum also tended to be areas of slopes, ranging from lower valleys to mountain lower, but those differences were not significant due to tops. The same observations have been reported by Ji and the small sample size. Park (2008)and Park (2013). Jang et al. (2012)have sug- gested that the distribution of S. borealis is similar to that Discussion of Q. mongolica because the former can appear in various Populations of Sasa borealis are most frequent and abun- types of forests that are always dominated by the latter. dant at the mid-elevations, i.e., 800 to 1,200 m, and plants Furthermore, S. borealis occurs more frequently in favor gentle slopes near valleys and lower slopes. They late-successional mixed stands of Q. mongolica—Abies also show a preference for a northern rather than a south- holophylla that are located on moist, gentle slopes. ern aspect, probably because the former is relatively moist Once S. borealis has become established on a site, it will (Lee et al. 1996). Kong (2001) has shown that this species remain very abundant regardless of environmental condi- tends to grow better at higher elevations because winter tionsorthe speciesoftrees with whichit isassociated. snows provide protection against cold, dry conditions. On Therefore, this scenario can influence forest dynamics, in- Mt. Jiri, this species appears in patches that occupy large cluding regeneration, for at least several decades (Makita Table 2 Plant species diversity, richness, and evenness as a function of growth form in the herb stratum, based on abundance (% cover) of Sasa borealis. Data are means ± standard error Parameter Cover of S. borealis (%) < 5 5~10 10~25 25~50 50~75 75~100 No. of plots 338812 12 Species diversity Tree 1.06 ± 0.20 1.43 ± 0.33 1.05 ± 0.28 1.65 ± 0.22 1.23 ± 0.17 0.65 ± 0.23 Shrub 1.25 ± 0.18 1.03 ± 0.29 1.07 ± 0.23 0.77 ± 0.19 1.04 ± 0.16 0.92 ± 0.19 Herb 1.88 ± 0.26 1.59 ± 0.34 1.49 ± 0.19 0.69 ± 0.18 0.54 ± 0.13 0.31 ± 0.12 Species richness Tree 3 ± 1 5 ± 1 3 ± 1 6 ± 1 4 ± 1 3 ± 1 Shrub 5 ± 1 4 ± 0 4 ± 1 3 ± 0 3 ± 0 3 ± 1 Herb 31 ± 6 10 ± 3 16 ± 3 8 ± 3 10 ± 2 6 ± 2 Species evenness Tree 1.00 ± 0.00 0.90 ± 0.10 0.75 ± 0.16 1.00 ± 0.00 0.92 ± 0.08 0.47 ± 0.14 Shrub 0.84 ± 0.16 0.69 ± 0.15 0.75 ± 0.13 0.66 ± 0.16 0.83 ± 0.10 0.79 ± 0.11 Herb 0.56 ± 0.08 0.70 ± 0.05 0.54 ± 0.04 0.39 ± 0.07 0.22 ± 0.04 0.15 ± 0.04 Cho et al. Journal of Ecology and Environment (2018) 42:9 Page 6 of 7 1998). In Japan, S. kurilensis dominates beech (Fagus cre- Biodiversity Institute 2017). In forests on the mainland, in- nata) forests and probably has a strong effect on beech re- cluding Korean national parks, S. borealis dominates large generation because thick coverage by S. kurilensis prevents portions of the herb stratum where Q. mongolica is the the beech seedlings from rooting firmly in the forest floor. most prevalent tree species. Its impact is enormous not Cerny et al. (2013) have shown that S. borealis inhibits only for species diversity but also for forest dynamics. species diversity in Korean national parks. Our current Therefore, designating such invader as ‘Disturbing Species’ findings support that conclusion. For example, we found should be seriously considered. The most recent rare, that species diversity within the herb stratum is signifi- nationwide event of synchronized massive flowering by cantly reduced as the abundance of S. borealis increases. this species peaked in 2015 (Cho et al. 2017). Taking Moreover, the extent of species diversity is lower for advantage of the fact that the culms of S. borealis decline herbaceous plants than for any of the other growth immediately after flowering, managers should quickly take forms recorded near the forest floor. The greater con- the opportunity to implement methods of ecological tributors to species diversity in forests are herbaceous control to restore biodiversity in Korean forests. plants. On the Korean Peninsula, approximately 77% of the 4,050 plant taxa are herbaceous (Choung et al. Conclusions 2015). Park et al. (2012) have reported that the number We explored the physical habitats and forest communi- of understory plant species and the biodiversity index ties in which S. borealis occurs and determined the are low on Mt. Jiri, a region where the coverage by S. dominance of this species on other plants. It was found borealis is > 90%. We believe that S. borealis inhibits the commonly at mid-elevational ranges, on gentle, usually establishment of canopy tree species. Species richness lower, and near valley northern slopes. This plant cov- also declines as the shoot height of S. kurilensis increases ered more than 50% of the surface mostly where Q. (Kudo et al. 2011). Kim (2009) has determined that spe- mongolica dominates, particularly in late-successional cies diversity decreases as the density of S. quelpaertensis mixed stands of Q. mongolica, other deciduous species, populations increases in shrubby areas of Jeju Island. and the coniferous Abies holophylla. Species diversity Although it might be difficult to explain how Sasa hin- declined significantly as the abundance of S. borealis in- ders plant species diversity, certainly its monopolizing of creased in the herb stratum. The same trend was noted physical space and resources is a key factor. As an ever- for the species richness and species evenness. These green plant, members of this genus block light from findings clearly demonstrate that S. borealis is a weed reaching the forest floor throughout the year (Kudo et al. pest and severely hinders species diversity. Authorities 2011;Parket al. 2012). Researchershavealsosuggested should be implementing various measures for ecological that S. quelpaertensis (Kim et al. 2007)and S. cernua (Li et control to take advantage of declining chance after the al. 1992) have allelopathic effects on their competitors. recent synchronized massive flowering of S. borealis. Furthermore, patches of Sasa can provide habitat for small mammals, who might consume larger seeds and indirectly Abbreviations prevent the regeneration of trees (Abe et al. 2001). ANOVA: Analysis of variance; SPSS: Statistical Package for Social Science Historically, S. borealis had been widely used in the pro- Funding duction of mats, baskets, and “Jori” a type of strainer that This study was supported by Basic Science Research Program through the separates soil particles from the grains when cooking rice. National Research Foundation of Korea (NRF) funded by the Ministry of In fact, Jori was used in this manner during the Joseon Education (C1013696-01-01), Korea Ministry of Environment and National Institute of Ecology as National Long-Term Ecological Research Project Dynasty, as recorded in “Imwon Gyeongjeji” (Agricultural (NIE-Strategy Research-2017-02), and 2016 Research Grant from Kangwon Economy) (Chung 2012), but might date back even further National University (D1000654-01-01). because rice has been eaten in Korea since the Three States period, which was much earlier than the Joseon Availability of data and materials The datasets during and/or analyzed during the current study are available Dynasty. However, automation replaced Jori in the 1970s. from the corresponding author on reasonable request. Since then, plants of S. borealis have not been harvested for Jori but instead have invaded nearby abandoned or dis- Authors’ contributions turbed fields and forests. Simultaneously, those forests SC analyzed the data and wrote the manuscript draft; KL built up the have been disrupted by logging and slash-and-burn farm- database and performed the community analysis; YC planned and revised the manuscript. All the authors approved the manuscript. ing practices, resulting in huge open areas that are vulner- able to expansion by this weedy species (Lee 2010). Ethics approval and consent to participate On Jeju Island, authorities are implementing various Not applicable. measures, e.g., horse grazing and cutting, to restore the level of plant species diversity that has been diminished by Competing interests the presence of S. quelpaertensis (Northeastern Asia The authors declare that they have no competing interests. Cho et al. Journal of Ecology and Environment (2018) 42:9 Page 7 of 7 Publisher’sNote Jang, H. T., Park, W. J., Kim, N. C., & Park, J. M. (2012). 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Distribution, abundance, and effect on plant species diversity of Sasa borealis in Korean forests

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Abstract

Background: Sasa borealis (Hack.) Makino, a clonal dwarf bamboo, is widespread in Korean forests. Although S. borealis is native to that country, its growth habit can cause considerable harm when occupying particular areas where it dominates and influences those forested communities. However, few reports have described the extent of its inhibitory effects on the vigor of co-existing plant species. Therefore, we investigated the distribution, abundance, and diversity of other plant species in the communities where this plant occurs in the east-central forests on the Korean Peninsula. Results: S. borealis was most commonly found at an elevational range of 800 to 1,200 m, on gentle, usually lower, and near valley northern slopes. Out of the 13 forest communities based on 447 forest stands that we surveyed, S. borealis was detected in eight communities, mostly where Quercus mongolica dominates. In particular, it was more common in late-successional mixed stands of Q. mongolica, other deciduous species, and the coniferous Abies holophylla. Because of their ability to expand rapidly in the forest, this plant covered more than 50% of the surface in most of our research plots. Species diversity declined significantly (F =78.7, p = 0.000) as the abundance of S. borealis increased in the herb stratum. The same trend was noted for the total number of species (F =18.1, p = 0.000) and species evenness (F =91.5, p =0.000). Conclusions: These findings clearly demonstrate that S. borealis is a weed pest and severely hinders species diversity. Authorities should be implementing various measures for ecological control to take advantage of declining chance after the recent synchronized massive flowering of S. borealis. Keywords: Dwarf bamboo, Quercus mongolica forest, Native weedy pest, Synchronized massive flowering Background Ulleung Island, Jeju Island, and in North Korea, respect- Sasa borealis (Hack.) Makino is a native plant species that ively (Lee 2003). belongs to Bambusoideae. It can be found on almost any This evergreen dwarf bamboo shows a clonal habit. mountain in Korea, including national parks (Lee and Lim Once established, the plants annually produce new 2002), and has been reported from the southern to the ramets (culms) on their long, thin rhizomes (Makita northern regions, e.g., Mts. Baegun, Wolchul, Jiri, Naejang, 1998) and grow approximately 1 to 2 m tall. Because of Deogyu, Sobaek, Chiak, Odae, and Seorak (Ahn et al. 2004; the physiological integration between connected Oh et al. 2005; Choung et al. 2009;Kim 2012;Parketal. rhizomes, they can overcome resource deficiencies 2012; Cerny et al. 2013). Although three other species of (Saitoh et al. 2002). In addition, their very shade-tolerant Sasa—S. kurilensis, S. quelpaertensis,and S. coreana—grow nature means that they can occupy the forest floor and in Korea, their populations are isolated and found only on become dominant as their populations increase infinitely (Yuruki et al. 1987; Park et al. 2012). Consequently, the density of aboveground evergreen shoots is high * Correspondence: yschoung@kangwon.ac.kr throughout the year while their thick, round rhizomes Department of Biological Sciences, Kangwon National University, completely also occupy the underground space. These Chuncheon 24341, South Korea attributes make the plants very competitive within the Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Cho et al. Journal of Ecology and Environment (2018) 42:9 Page 2 of 7 lower strata of a forest, and pure patches can be main- on Natural Resources in Korean National Parks (Choung tained for long periods (Oshima 1961; Nakashizuka et al. 2004). Those studies of 447 forested plots in the 1988; Hiura et al. 1996; Narukawa and Yamamoto 2002). east-central portion of the Korean Peninsula focused on In Japan, plants within the Sasa genus are regarded as the period of 1992 to 2014 and covered most of Gangwon serious weed pests (Li et al. 1992). In the 1950s, the Province and part of Chungcheong Province, including Japanese Forestry Research Institute reported that Danyang and Jecheon. Four variables were examined as approximately 50% of the area in Japanese national parks potential factors in determining the establishment and was covered with these plants, and that they accounted spread of S. borealis: elevation, slope, topography, and as- for 90% of the coverage in Hokkaido (Oshima 1961). On pect. The abundance of all plant species in each plot was Jeju Island in Korea, S. quelpaertensis covers approxi- analyzed by the Braun-Blanquet dominance scale for each mately 76% of the northern slopes at Mt. Halla National of four strata, based on plant height: (1) tree (T1), > 8 m Park, from 400 m up to the top. These circumstances tall; subtree (T2), 5∼8 m; shrub (S), 1∼5 m; and herb (H), are especially threatening to the survival of rare plant < 1 m. The number of plots where S. borealis presented species such as Empetrum nigrum var. japonicum, Genti- was 76 with either 15 m × 15 m (46) or 20 m × 20 m (30). ana chosenica, Primula modesta var. hannasanensis, and We first conducted a cluster analysis to classify vegeta- Ranunculus borealis in subalpine zones (Northeastern tion types, using cover data transformed by the Asia Biodiversity Institute 2017). square-root arcsign (Peck 2016) and then determined The current massive flowering cycle for S. borealis began the frequency and abundance of S. borealis within com- nationwide in 2013 (Cho et al. 2017). As a typical mono- munities. Those communities were named according to carpic plant, culms in the flowering patches tend to die off the one or two dominant tree species (cover > 50%) and within 1 year. Therefore, this type of reproductive event other species that were deemed to be significant indica- has an enormous effect on the vegetation dynamics of a tors, as revealed by an analysis by Peck (2016). From our forest dominated and suppressed by Sasa. Although it may 447 plots, 642 taxa were identified (Lee 2015). be too early to determine whether this event enables other Speciesdiversity wasevaluated by stratum, and S. species to regenerate naturally or allows S. borealis to borealis abundance (% cover) was assessed within the re-populate a site, this phenomenon gives us the opportun- herbaceous stratum. For species diversity using the ity to investigate whether a species that normally inhibits same size 46 plots (15 m × 15 m each), we applied diversity in South Korean forests might also experience its the Shannon-Weiner index (H′ = −∑ p log p ), where i e i own natural decline on such a large spatial scale. p represented relative cover. Species evenness (E)was In Korea, the Act on the Conservation and Use of Bio- calculated as E =H′/log S (S number of species), logical Diversity has been enacted to preserve and protect while species richness was defined as the number of biodiversity by designating some plants, including invasive individual species on a plot. The growth form was re- aliens, as ecosystem-disturbing species (Ministry of Envir- corded for each species, as we have previously de- onment 2017). Although S. borealis is native to that coun- scribed (Choung et al. 2012). For this, the categories try, we believe that its growth habit can cause considerable of tree, shrub, and herb respectively included trees harm when occupying particular areas where it dominates and subtrees; shrubs, vines, prostrate woody plants, and influences those forested communities. Under such and subshrubs; and herbs and climbing herbs. conditions, the diversity of other plant species appears to Differences among plots and strata were examined by be very low. However, these scenarios have not yet been of- one-way ANOVA, followed by a Bonferroni post hoc ficially documented or quantified in Korea. Our research analysis. Regression analysis was used to investigate the goals were to explore the physical habitats and forest com- responses of diversity indices based on S. borealis coverage. munities in which S. borealis occurs and to determine how All data were examined with SPSS software (SPSS 2013; plant species diversity is affected by the dominance of this ver. 22). species. These findings could then be used to develop strat- egies for ecological control and manipulation. Results Methods Distribution and abundance for Sasa borealis We used a database incorporating information that we The most common habitats for Sasa borealis were had gathered previously in our National Ecosystem Survey determined by examining site conditions (Fig. 1). Our for the Ministry of Environment (Choung et al. 1997, plot surveys revealed plants of that species on 76 of 1998; Choung and Oh 1999; Choung and Hong 2001; 447 plots. This species was less likely to occur in the Choung et al. 2002, 2003; Choung and Lee 2012;Choung elevational classes of lowlands (100 to 240 m) and and Kim 2013), plus data collected for Korea Long-term highlands (1,360 to 1,555 m) and was more common Ecological Research (Choung et al. 2013) and the Survey (61.9% of all plots) at elevations of 800 to 1,200 m. Cho et al. Journal of Ecology and Environment (2018) 42:9 Page 3 of 7 Fig. 1 Frequency of Sasa borealis in Korean forests. In each panel, gray bars indicate relative distribution (%) of 447 investigated plots; green bars, relative distribution (%) of 76 plots in which S. borealis occurs. LS, lower slope; MS, middle slope; US, upper slope Plants of S. borealis preferred more gentle slopes, i.e., S. borealis occurring forest communities 0° to 47°, and were not found in steeper areas. In par- The 447 plots were classified into 13 communities (domin- ticular, this species was most frequently counted ant—dominant_other significant indicator species): Quercus (40.8%) on slopes ranging from 20° to 30°, followed by variabilis—Pinusdensiflora_Ulmusmacrocarpa, Q. variabi- 30° to 40° (33% of all plots where it occurred). Overall, lis—Q. dentata_Spodiopogon sibiricus, P. densiflora—Q. these plants tended to be more common, topologically, variabilis_Q. serrata, P. densiflora_Rhododendron mucro- on near valleys and lower slopes (61.6%) and were less nulatum, P. densiflora_Rubus crataegifolius, P. densiflora— frequent on ridges and mountain tops. With regard to Juglans mandshurica_Persicaria filiformis, Q. mongolica— the aspect variable, S. borealis was more common on Carpinus laxiflora_Lindera obtusiloba, Q. mongolica_Sy- northern slopes (315°~45°) and relatively less frequent neilesis palmata, Q. mongolica_R. schlippenbachii, Q. mon- on southern and western slopes. golica—Abies holophylla_S. borealis, Q. mongolica_Lychnis Of the 76 plots containing S. borealis,those plants cognata, Q. mongolica—Fraxinus mandshurica_Philadel- covered more than half of the surface on 58% of those phus schrenckii,and Q. mongolica—Betula ermanii_Cacalia plots. This high spread value was rare for species found praetermissa. in the herbaceous layer in general. Because of its clonal Of these 13, S. borealis appeared within eight of them habit, the average coverage and standard deviation for (Fig. 2). Except for the P. densiflora—Q. variabilis_Q. ser- plots with S. borealis were 53.3 and 31.7, and abun- rata community (no. 3 in Fig. 2), Quercus mongolica was dance did not differ significantly among classes for any the dominant species, occurring on 96% of all plots. The of the four variables (Table 1). highest coverage by S. borealis, 61%, was measured in the Cho et al. Journal of Ecology and Environment (2018) 42:9 Page 4 of 7 Table 1 Percent coverage of Sasa borealis plants according to site variables of elevation, slope, topography, and aspect Elevation Slope Topography Aspect Class (m) Cover (%) Class (°) Cover (%) Class Cover (%) Class (°) Cover (%) 200~400 53.5 ± 12.3 (8) ≤ 10 59.8 ± 9.9 (8) Valley 62.7 ± 6.9 (13) 315~45 57.1 ± 5.6 (30) 400~600 34.0 ± 19.4 (4) 10~20 58.4 ± 11.1 (8) Lower slope 55.7 ± 6.5 (23) 45~135 59.6 ± 7.2 (18) 600~800 62.2 ± 9.0 (13) 20~30 48.9 ± 6.1 (31) Middle slope 55.8 ± 9.7 (13) 135~225 57.1 ± 9.2 (15) 800~1000 53.1 ± 5.1 (29) 30~40 57.2 ± 7.1 (21) Upper slope 41.3 ± 6.6 (23) 225~315 28.9 ± 7.9 (10) 1000~1200 53.1 ± 8.6 (18) 40~50 46.6 ± 10.7 (8) Ridge and top 65.8 ± 21.8 (4) 1200~1400 42.0 ± 20.0 (4) Data are means ± standard error, with number of plots shown in parentheses. Aspect for three plots were not determined Q. mongolica—Abies holophylla_S. borealis community trend was noted for the total number of species (F = (no. 10 in Fig. 2, right side). That particular community is 18.1, p = 0.000) and species evenness (F = 91.5, p = considered relatively late-successional (Lee 2015), where 0.000). This was especially true when S. borealis covered Q. mongolica co-dominates with Tilia amurensis, Abies more than 75% of the surface in a plot. In that case, the holophylla,and Acer pseudosieboldianum.In addition to diversity index for the herb stratum was as low as 0.536, several other tree species, its tree stratum or the shrub which then limited the availability of water and nutrients stratum in this community is occupied by Rhododendron to plants in the canopy. However, diversity within the shillipenbachi and Lindera obtusiloba. tree, subtree, and shrub strata did not tend to be corre- Among the eight communities in which S. borealis lated with the dominance of S. borealis. Although the di- grows, that species covered more than 50% of the forest versity of shrub species tended to decrease as the floor in five of them (Fig. 2). For the remaining three frequency of S. borealis rose, this trend was not statisti- communities, lower overall coverage by those plants was cally significant and possibly resulted, instead, because due to less amenable site conditions, including a lower of the limited sample size. elevation, an upper slope facing south (no. 8), an upper In the herb stratum, H′ values for herbaceous species slope or ridge at high elevation (nos. 11 and 13), or the were significantly reduced as the abundance of S. borea- purity of the Q. mongolica stands that precluded compe- lis increased (F = 45.8, p = 0.000; Table 2). When cover- tition from other species. age by that species was > 75%, the diversity index in such plots was as low as 0.314. In particular, the number Effect of S. borealis on plant species diversity, based on of herbaceous species averaged 31 when S. borealis stratum and growth form abundance was < 5% but totaled only six when Sasa At the plot level, values for species diversity declined sig- coverage was > 75% (F = 45.8, p = 0.000). Similar trends nificantly (F = 78.7, p = 0.000) as the abundance of S. were noted for species evenness and total number of borealis increased in the herb stratum (Fig. 3). The same species (F = 65.8, p = 0.000). The species diversity of tree Fig. 2 Left, frequency of Sasa borealis in 13 communities identified from surveys of 447 total plots. Right, abundance (% cover) of S. borealis plants in communities shown on left. On right, error bars indicate significant differences at p < 0.05. Communities: 1, Quercus variabilis—Pinus densiflora_Ulmus macrocarpa;2, Q. variabilis—Q. dentata_Spodiopogon sibiricus;3, P. densiflora—Q. variabilis_Q. serrata;4, P. densiflora_Rhododendron mucronulatum;5, P. densiflora_Rubus crataegifolius;6, P. densiflora—Juglans mandshurica_Persicaria filiformis;7, Q. mongolica—Carpinus laxiflora_Lindera obtusiloba;8, Q. mongolica_Syneilesis palmata;9, Q. mongolica_R. schlippenbachii; 10, Q. mongolica—Abies holophylla_S. borealis; 11, Q. mongolica_Lychnis cognata; 12, Q. mongolica—Fraxinus mandshurica_Philadelphus schrenckii; and 13, Q. mongolica—Betula ermanii_Cacalia praetermissa Cho et al. Journal of Ecology and Environment (2018) 42:9 Page 5 of 7 Fig. 3 Plant species diversity (H′), richness, and evenness as a function of Sasa borealis abundance (% cover) in 4 strata. Data points are mean values. Strata: T1, tree; T2, subtree; S, shrub; H, herb and shrub species in the herb stratum also tended to be areas of slopes, ranging from lower valleys to mountain lower, but those differences were not significant due to tops. The same observations have been reported by Ji and the small sample size. Park (2008)and Park (2013). Jang et al. (2012)have sug- gested that the distribution of S. borealis is similar to that Discussion of Q. mongolica because the former can appear in various Populations of Sasa borealis are most frequent and abun- types of forests that are always dominated by the latter. dant at the mid-elevations, i.e., 800 to 1,200 m, and plants Furthermore, S. borealis occurs more frequently in favor gentle slopes near valleys and lower slopes. They late-successional mixed stands of Q. mongolica—Abies also show a preference for a northern rather than a south- holophylla that are located on moist, gentle slopes. ern aspect, probably because the former is relatively moist Once S. borealis has become established on a site, it will (Lee et al. 1996). Kong (2001) has shown that this species remain very abundant regardless of environmental condi- tends to grow better at higher elevations because winter tionsorthe speciesoftrees with whichit isassociated. snows provide protection against cold, dry conditions. On Therefore, this scenario can influence forest dynamics, in- Mt. Jiri, this species appears in patches that occupy large cluding regeneration, for at least several decades (Makita Table 2 Plant species diversity, richness, and evenness as a function of growth form in the herb stratum, based on abundance (% cover) of Sasa borealis. Data are means ± standard error Parameter Cover of S. borealis (%) < 5 5~10 10~25 25~50 50~75 75~100 No. of plots 338812 12 Species diversity Tree 1.06 ± 0.20 1.43 ± 0.33 1.05 ± 0.28 1.65 ± 0.22 1.23 ± 0.17 0.65 ± 0.23 Shrub 1.25 ± 0.18 1.03 ± 0.29 1.07 ± 0.23 0.77 ± 0.19 1.04 ± 0.16 0.92 ± 0.19 Herb 1.88 ± 0.26 1.59 ± 0.34 1.49 ± 0.19 0.69 ± 0.18 0.54 ± 0.13 0.31 ± 0.12 Species richness Tree 3 ± 1 5 ± 1 3 ± 1 6 ± 1 4 ± 1 3 ± 1 Shrub 5 ± 1 4 ± 0 4 ± 1 3 ± 0 3 ± 0 3 ± 1 Herb 31 ± 6 10 ± 3 16 ± 3 8 ± 3 10 ± 2 6 ± 2 Species evenness Tree 1.00 ± 0.00 0.90 ± 0.10 0.75 ± 0.16 1.00 ± 0.00 0.92 ± 0.08 0.47 ± 0.14 Shrub 0.84 ± 0.16 0.69 ± 0.15 0.75 ± 0.13 0.66 ± 0.16 0.83 ± 0.10 0.79 ± 0.11 Herb 0.56 ± 0.08 0.70 ± 0.05 0.54 ± 0.04 0.39 ± 0.07 0.22 ± 0.04 0.15 ± 0.04 Cho et al. Journal of Ecology and Environment (2018) 42:9 Page 6 of 7 1998). In Japan, S. kurilensis dominates beech (Fagus cre- Biodiversity Institute 2017). In forests on the mainland, in- nata) forests and probably has a strong effect on beech re- cluding Korean national parks, S. borealis dominates large generation because thick coverage by S. kurilensis prevents portions of the herb stratum where Q. mongolica is the the beech seedlings from rooting firmly in the forest floor. most prevalent tree species. Its impact is enormous not Cerny et al. (2013) have shown that S. borealis inhibits only for species diversity but also for forest dynamics. species diversity in Korean national parks. Our current Therefore, designating such invader as ‘Disturbing Species’ findings support that conclusion. For example, we found should be seriously considered. The most recent rare, that species diversity within the herb stratum is signifi- nationwide event of synchronized massive flowering by cantly reduced as the abundance of S. borealis increases. this species peaked in 2015 (Cho et al. 2017). Taking Moreover, the extent of species diversity is lower for advantage of the fact that the culms of S. borealis decline herbaceous plants than for any of the other growth immediately after flowering, managers should quickly take forms recorded near the forest floor. The greater con- the opportunity to implement methods of ecological tributors to species diversity in forests are herbaceous control to restore biodiversity in Korean forests. plants. On the Korean Peninsula, approximately 77% of the 4,050 plant taxa are herbaceous (Choung et al. Conclusions 2015). Park et al. (2012) have reported that the number We explored the physical habitats and forest communi- of understory plant species and the biodiversity index ties in which S. borealis occurs and determined the are low on Mt. Jiri, a region where the coverage by S. dominance of this species on other plants. It was found borealis is > 90%. We believe that S. borealis inhibits the commonly at mid-elevational ranges, on gentle, usually establishment of canopy tree species. Species richness lower, and near valley northern slopes. This plant cov- also declines as the shoot height of S. kurilensis increases ered more than 50% of the surface mostly where Q. (Kudo et al. 2011). Kim (2009) has determined that spe- mongolica dominates, particularly in late-successional cies diversity decreases as the density of S. quelpaertensis mixed stands of Q. mongolica, other deciduous species, populations increases in shrubby areas of Jeju Island. and the coniferous Abies holophylla. Species diversity Although it might be difficult to explain how Sasa hin- declined significantly as the abundance of S. borealis in- ders plant species diversity, certainly its monopolizing of creased in the herb stratum. The same trend was noted physical space and resources is a key factor. As an ever- for the species richness and species evenness. These green plant, members of this genus block light from findings clearly demonstrate that S. borealis is a weed reaching the forest floor throughout the year (Kudo et al. pest and severely hinders species diversity. Authorities 2011;Parket al. 2012). Researchershavealsosuggested should be implementing various measures for ecological that S. quelpaertensis (Kim et al. 2007)and S. cernua (Li et control to take advantage of declining chance after the al. 1992) have allelopathic effects on their competitors. recent synchronized massive flowering of S. borealis. Furthermore, patches of Sasa can provide habitat for small mammals, who might consume larger seeds and indirectly Abbreviations prevent the regeneration of trees (Abe et al. 2001). ANOVA: Analysis of variance; SPSS: Statistical Package for Social Science Historically, S. borealis had been widely used in the pro- Funding duction of mats, baskets, and “Jori” a type of strainer that This study was supported by Basic Science Research Program through the separates soil particles from the grains when cooking rice. National Research Foundation of Korea (NRF) funded by the Ministry of In fact, Jori was used in this manner during the Joseon Education (C1013696-01-01), Korea Ministry of Environment and National Institute of Ecology as National Long-Term Ecological Research Project Dynasty, as recorded in “Imwon Gyeongjeji” (Agricultural (NIE-Strategy Research-2017-02), and 2016 Research Grant from Kangwon Economy) (Chung 2012), but might date back even further National University (D1000654-01-01). because rice has been eaten in Korea since the Three States period, which was much earlier than the Joseon Availability of data and materials The datasets during and/or analyzed during the current study are available Dynasty. However, automation replaced Jori in the 1970s. from the corresponding author on reasonable request. Since then, plants of S. borealis have not been harvested for Jori but instead have invaded nearby abandoned or dis- Authors’ contributions turbed fields and forests. Simultaneously, those forests SC analyzed the data and wrote the manuscript draft; KL built up the have been disrupted by logging and slash-and-burn farm- database and performed the community analysis; YC planned and revised the manuscript. All the authors approved the manuscript. ing practices, resulting in huge open areas that are vulner- able to expansion by this weedy species (Lee 2010). Ethics approval and consent to participate On Jeju Island, authorities are implementing various Not applicable. measures, e.g., horse grazing and cutting, to restore the level of plant species diversity that has been diminished by Competing interests the presence of S. quelpaertensis (Northeastern Asia The authors declare that they have no competing interests. Cho et al. Journal of Ecology and Environment (2018) 42:9 Page 7 of 7 Publisher’sNote Jang, H. T., Park, W. J., Kim, N. C., & Park, J. M. (2012). Use of Arundinaria munsuensis Springer Nature remains neutral with regard to jurisdictional claims in Y. Lee as revegetation plant materials of damaged slopes. Journal. Korean published maps and institutional affiliations. Environmental Research and Technology, 15,133–140 (in Korean). Ji, H. Y., & Park, J. H. (2008). Analysis of water retention capacity at Sasa borealis stands Author details in Jirisan National Park. J. Korean Env. Res. & Reveg. Tech, 11,1–11 (in Korean). Department of Biological Sciences, Kangwon National University, Kim HC. Ecological characteristics and management methods of Sasa Chuncheon 24341, South Korea. National Institute of Ecology, Seocheon quelpaertensis Nakai. Jeju National University, Ph.D. thesis. Jeju. 2009. (in 33657, South Korea. Korean). Kim, H. C., Go, J., Song, J., Kang, J., Woo, S., Kim, T., & Song, C. (2007). 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Journal of Ecology and EnvironmentSpringer Journals

Published: Jun 1, 2018

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