Maling bamboo (Yushania maling) overdominance alters forest structure and composition in Khangchendzonga landscape, Eastern Himalaya

The Khangchendzonga Landscape (KL), a part of ‘Himalayan Biodiversity Hotspot’, is known for its unique biodiversity assemblage. In recent years, the KL is experiencing threats to biodiversity due to the biological overdominance of native Maling bamboo (Yushania maling). In the present study, we investigated the impacts of the overdominance of Y. maling on the forest composition of Singalila National Park (SNP), Eastern Himalaya, India. Elevational habitats 2400 to 3400 m asl were sampled by laying 69 (10 m × 10 m) forest plots including 51 bamboo plots and 18 non-bamboo plots. Bamboo plots showed significantly (p < 0.05) low species richness and density in both shrub and herb layers which further manifested the low seedling density. Generalized Additive Model (GAM) estimated a significant (p < 0.0001) decline in species richness and density with increasing bamboo density in SNP. Our study projects the overdominance of Y. maling has a significant negative impact on forest structure and composition. Therefore, management of invasiveness of Y. maling is essential through its optimized removal from the protected areas and utilization in making handicrafts, paper industries etc. to create ecological and economic benefits. Further long-term studies assessing the impacts of Y. maling overdominance on forest ecosystems and soil dynamics are recommended.

Biodiversity provides numerous essential services to society; the survival and socio-economic activities of people largely depend upon various natural resources. Forests, hitherto, are considered to provide renewable resources and ecosystem services that support life on the planet 1-3 . However, invasion of invasive alien species [4][5][6] and over expansion/dominance of native plant species [7][8][9] alter the composition and structures of natural forests, which mostly manifested by the loss of biodiversity at the global scale 10 . Besides, an overabundance of native herbaceous species can appear as dominant element in the forest ecosystem 11,12 . That may disturb the composition and dynamics of the forest ecosystem adversely. Studies revealed that the expansion of bamboo has altered the overall forest composition and dynamics of many ecosystems 6,[13][14][15] .
Bamboo, the fastest growing plant also referred as 'green gold' , offers incredible economic, cultural and ecological benefits. Owing to its cheap and plentiful availability, bamboo is also known as 'poor man's timber' 16 and especially used as a substitute of the wood 17 and as food product in numerous cases for human [18][19][20] and wildlife 21,22 . Communities extensively use bamboos, for various household purposes such as supporting poles, flooring, frames, partitions, ceiling, walls, thatching, tying, roofing, making doors and windows frames, etc. 23,24 . Various traditional items and modern decorative are crafted from bamboos. Worldwide, they represented by about 1400 species and 107 genera, consisted 79 genera representing 1200 species of woody bamboo, and 28 genera representing 180 species of herbaceous bamboo 6 . India stands second largest diversity center for bamboos after China 25 and possess 136 species of bamboo belonging to 18 genera and encompasses over 13.96 million ha occupying 17.3% of the total forest and tree cover of the country 26 (National Bamboo mission, 2022). Over 84
Concerning the bamboo shoot density across the plots, we estimated the changes in species richness for trees, shrubs, and herbs (Table 4). Our results projected a significantly (p < 0.0001) declining trends for shrubs (β = − 0.0026; SE = 0.0005; R 2 = 53.61) and a non-significant decline for trees and herbs ( Fig. 1) (Fig. 2). The model predicted a significant decrease in the richness of shrubs (2-3 species) with an increase of 1000 shoots of bamboo per 100 m 2 area (Table 4). Also, the model projected significant decline in species density with increasing 1000 shoots of bamboo for shrubs (28-30 individual) and herbs  individual) per 100m 2 area. Nevertheless, we did not observe the trends for a change in the species richness of trees and herbs, and density of trees (p > 0.05), which indicates recent overdominance of Y. maling in the area. The GAMs projected the species richness and density of tree saplings and seedlings along with the bamboo (shoot) density (Table 5). GAM showed a non-significant decline in the species richness of tree saplings (β = − 0.0024; SE = 0.0002; R 2 = 22.70) and a significant (p < 0.00001) decline seedlings (β = − 0.0014; SE = 0.0002;  Table 3. Comparison of species richness and density of saplings and seedlings of trees between bamboo and non-bamboo plots. Mean values ± SE of the vegetation parameters calculated and compared between bamboo and non-bamboo plots using t-test for independence samples.

Discussion
In our study in SNP, the plots invaded by bamboo (Y. maling) showed the low species richness and density of the shrubs, herbs, and tree seedlings as compared to the non-bamboo plots. These results indicate that the abundance of bamboo restricts the richness and density of the shrubs and herbs species and hinders tree regeneration in the forests. A supportive study on the expansion of dwarf bamboo in Japan 9 showed the negative relationship between bamboo density and herb species richness. Also, studies have suggested altering forest structure and dynamics, revealing lower density of trees and lower species diversity, by the overabundance of bamboo in Brazilian Atlantic forest 15 . Such evidences signifies that the high degree of bamboo dominance over a long period may effectively alter the forest composition and structures. Our analysis of the effect of the bamboo overdominance on the forest composition in SNP and the results drawn from GAM vividly estimated the significant decline in the richness of shrubs and herbs and further predicted that, with increasing 1000 shoots of bamboo per 100 m 2 , there would be an adverse change in the species richness of shrubs (2-3 species). Also, changes in the richness of tree seedlings, (1-2 species) were estimated with 1000 shoots of bamboo. Similarly, disadvantageous changes of density of shrubs (28-30 individual) and herbs (1943-1969 individual), tree saplings (23-25 individual) and tree seedlings (141-145 individual) were estimated with increasing the 1000 shoots of bamboo in 100 m 2 area significantly. The GAMs predictions indicate that the abundance of bamboo has negatively influenced the richness of shrubs, herbs and tree saplings and tree seedlings. Concurrently, the density of shrubs, herbs, tree saplings and tree seedlings in SNP, as the physical and physiological stresses of bamboo, may cause the reduction of the tree seedlings' richness 15 . Further, it is suggested that the dominance of bamboo reduces the tree regeneration and the undergrowth vegetation, and their thick layer of litter affects the tree seedling regeneration negatively causing alternations in the plant community composition and species diversity 39 . Another supportive study from Southwest China suggested that the high density of bamboo Fargesia nitida greatly decreases understory species richness especially shrubs 40 . However, the expansion of a dominant native species may threaten other native forest species and enables invasion of non-native species in herbs and shrubs layers 7 .
The rapid overdominance of bamboo species (Y. maling) in SNP has consequently indicated the alteration in forest composition when compared with non-bamboo plots. Here, we recorded the widespread extension of bamboo reaching upto 3300 m asl, which is commonly observed in the Temperate broadleaved forests, and expanded across the Temperate Coniferous broad-leaved forests. We observed excellent bamboo growth under tree species like Quercus spp., Rhododendron spp., Eurya spp., Symploccus spp., Vitex heterophyllum and Abies densa accompanying various shrub species because of its tremendous adaptability and excellent resource use (light) capability in different habitats 41 . They expand through their rhizomes and survive over several decades in many forest types and thus have raised concerns about the regeneration of tree seedlings and the diversity of shrubberies and herbaceous species 13,[42][43][44] . Consequently, some studies have suggested controlling and managing the invasion of bamboos by applying moderate grazing. That can control forest structures to some extent thereby reducing the density and height of the bamboos and creating favorable conditions for the regeneration of other species 42,45,46 .
Additionally, our results reveal a positive alteration in species richness of shrubs, herbs, and tree seedlings and in density of tree, shrubs, herbs and tree seedlings while, negative change in tree saplings richness and density of tree saplings and bamboo (stems). Previous study from similar region resulted negative correlation between species richness of woody species and elevation 47 however, contradictory results as adverse change in species richness along the elevation emerged from the mountains of China 48 . The change in species richness and density may be due to difference in climatic, physiographic and edaphic factors 2,49 .
In general, bamboos offer major ecosystem services, providing livelihood opportunities and supplying food resources to humans and wild fauna. These uses are wide-ranging, like tender shoots eaten as vegetable, the leaves Table 4. Estimated changes in species richness and density of trees, shrubs and herbs with respect to bamboo density in the Singalila National Park. ne Non eligible (as the R 2 value is < 1).    50,51 . Also, the species offers various uses in constructive purposes, linking directly to the livelihood of the forest fringe communities. Simultaneously, bamboo may provide opportunities for carbon farming and carbon trading 16,52 and supports the increasing organic matters in soil 53 . Nonetheless, as per the National Park rule and regulations, the community people around SNP are restricted to use bamboo and other resources for the commercial purposes. The invasiveness of native bamboo species (Y. maling) in SNP might have resulted, due to, i) ban on grazing and shifting shepherd communities outside the park area, ii) restriction on harvesting bio-resources for the forest fringe communities, iii) global climate change, and iv) limited management measures, etc. The management of bamboos by controlling their expansion in the areas of high bamboo density could be an appropriate forest restoration approach. It is understood that the bamboos have great potential for the rapid growth and forming complex dominant structures in the forests. The sustainable utilization of bamboos by the local communities would be suggestive especially in the PAs, not only in Darjeeling Himalaya but also in the entire eastern Himalayan forests. Such uses of bamboos can be encouraged, in order to, (i) limit its uncontrolled extension further inside the forests, (ii) decrease extraction pressure in other forest wood species, (iii) revitalize the local bamboo-based traditional handicrafts and linking with livelihood alternatives and (iv) remove bamboo clumps form affected areas, which can be used as a planting material in waste land restoration purpose. Besides, the growing ecotourism in the region demands the supply of various ethnic products for which the bamboo resources become the best option as an alternative livelihood. The bamboo should be used in such a way that the negative impacts of its current expansion on the other species could be limited.

Species richness
Based on the information gathered from our case study from Khangchendzonga Landscape-India, appropriate management plans need to be developed, focusing on its sustainable harvesting system and identifying the threshold levels of extraction for conservation and sustainable utilization approaches. Furthermore, we suggest in-depth further studies on, (i) bamboo-based forest community structures and dynamics, (ii) changing the intensity of bamboos community growth with respect to climate change, (iii) monitoring ecological resilience with respect to the bamboos plantation and cultivation, and (iv) integrating mechanism of sustainable utilization of bamboo by the communities around PAs. Our study site, Singalila National Park (SNP), covers an area of 79 km 2 , extending within 27° 13′ 15″ N and 22° 1′ 46″ N latitude and 83° 1′ 91″ to 38° 7′ 54″ E longitude. SNP lies in transboundary with Nepal and India, and its northern part borders with Barsey Rhododendron Sanctuary of Sikkim. The study site represents sub-tropical to sub-alpine eco-climatic zones (2200 m to 3668 m asl) along the trekking corridor from the Gorkhey forest village to Phalut (Fig. 5). The diversified eco-climatic ranges provide various broad habitats and numerous microhabitats harboring the inclusive floral and faunal diversity. A prior permission to conduct this study was taken from the Department of Forests, West Bengal and all rules and regulations of protected areas (National Park) were followed during the study.

Methods
Sampling design. The study was undertaken along the stretch of 2400 m asl to 3400 m asl (temperate to sub-alpine zone) in SNP, across the Gorkhey-Phalut trekking corridor. In the region below 2400 m, the bamboo growth was sparse due to the anthropogenic activity including the extent of agricultural fields and the use of bamboo for various purposes by the people of the fringe villages. Along this elevation, we randomly sampled 69 plots to assess the community structure of the vegetation (tree, shrub and herbaceous species) within the assemblage of Y. maling, as the major understory growth including both bamboo and non-bamboo areas 55 . We adopted nested quadrat method for the study of species richness and density of trees, shrubs, herbs, tree saplings and tree seedlings within identified plots. We studied the tree species in 0.1 hectare (10 m ×10 m) Table 5. Estimated changes in species richness and density of saplings and seedlings with respect to bamboo density in the Singalila National Park.   www.nature.com/scientificreports/ plots, within which 25 m 2 (5 m × 5 m) plots exactly in the middle were selected to study shrubs, bamboos, and tree saplings. We laid two quadrats m 2 (1 m × 1 m) each in the alternative corners of the major plot to study tree seedlings and other herbaceous species. We considered mature trees having the girth size ≥ 30 cm (girth at breast height; 1.3 cm above the ground level); the saplings having girth of < 30 cm to ≥ 10 cm, while we regarded seedlings having collar girth < 10 cm /or collar diameter < 3.14 cm at the height of 1 cm from the ground level. In all the plots, we recorded total number and the respective diameters of each tree. Measuring tape was used to measure the tree/ sapling circumference, however, seedling diameter was measured with the help of digital  www.nature.com/scientificreports/ Vernier caliper (Model:CD-8 CS, Mituyoto, Japan). However, Small-to-medium sized woody perennial plants having profuse branching from the base were considered shrub. However, most annuals and few perennials with herbaceous stem were kept under herb layer. To understand the bamboo density responses over other forest communities (trees, shrubs, herbs, including seedling and sapling of trees), we recorded it in each random plot. Out of 69 major 0.1 ha plots, 51 were recognized with the occurrence of bamboo species and 18 plots without any presence of Y. maling. Plant species of each plot were identified using filed guide books and their identity was confirmed by consulting regional floras (Flowers of the Himalaya 56 ; Flora of Darjeeling Himalayas and Foothills: Angiosperms 57 ; Sikkim Himalayan Rhododendrons 58 ) and available herbarium records. The plant species nomenclature follows the Plant list (www. thepl antli st. org) an online database accessed on 01/01/2022. For the quantitative measure of species richness (tree, shrub, herb, sapling, and seedling) was calculated as the number of species per unit area 59 . We measured the density (number of individuals per unit area) for tree, shrub, herb, tree sapling, and tree seedling, simultaneously with Y. maling density. For bamboo density, shoots/culms were counted from each sampled plot.
Statistical analysis. Realizing the asymmetrical data structure (Non-Normal), we transformed the recorded data into arcsine format and applied independent sample t-test for comparing the mean of diversity and density of the trees, shrubs, herbs, and seedlings and saplings of trees between bamboo and non-bamboo plots. Finally, we retransformed the analysed arcsine data presented in the tables for interpretation.
To deal with nonparametric statistical analysis, Generalized Additive Model (GAM) was considered exceedingly suitable for ecological studies 60,61 . The GAM is a semi-parametric extension of GLM 62 and deals with highly non-linear and non-normal relationships between the response and the set of explanatory variables 63 . GAM includes the estimation of smoothing terms in the additive model and general algorithm added in the model as partial residuals (i.e. R j th set of partial residuals).
The partial residuals remove the effects of all the other variables from Y (depended variable i.e. richness and density of trees, shrubs, herbs, and saplings and seedlings of trees); therefore, the Y can be used to model the effects against X j (density of bamboo-Y. maling for all studied plots including non-bamboo plots as zero quantitative value). However, due to ranging wider variability and inconsistence series of data, the variables under study were indicated non-normal and non-linear data structure.