1. bookTom 32 (2021): Zeszyt 1 (March 2021)
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30 May 2013
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The resilience of Rubiaceae to anthropogenic factors: a case study from the Himalayan range of Western Bhutan

Data publikacji: 31 Mar 2021
Tom & Zeszyt: Tom 32 (2021) - Zeszyt 1 (March 2021)
Zakres stron: 13 - 20
Informacje o czasopiśmie
License
Format
Czasopismo
eISSN
2353-8589
Pierwsze wydanie
30 May 2013
Częstotliwość wydawania
4 razy w roku
Języki
Angielski
INTRODUCTION

Since not all plant species exhibit similar responses to the disturbance regime (Onaindia et al. 2004), it is imperative to understand what kind of disturbance regimes are detrimental or helpful and how various plant species respond to different types of disturbance regimes. For instance, the natural disturbances are thought as an integral part of the ecosystem (Dale et al. 2000) since they may also act as the drivers of plant species diversification (Lorimer and White 2003), while the human-driven disturbance is believed to cause exploitation of biological resources and impact species diversity to a great extent (Abadie et al. 2011). Predominantly, anthropogenic disturbances are supposed to cause greater biodiversity alteration than the one that occurs under natural conditions (Kumar and Ram 2005). On the contrary, human-driven disturbances are on the rise along with the escalating demand for forest resources (Hasenauer et al. 2012), resulting in inadvertent destruction to various plant species. Consequently, it is crucial to study the response of different plant species to different types of disturbance regimes because the consequences may be devastating for those plant species that are on the verge of extinction or endemic in nature.

The influence of anthropogenic factors on plant species diversity has been studied with reference to the Rubiaceae family as this family has been described as better fitted to be used in the ecological analysis (Delprete and Jardim, 2012). Furthermore, the Rubiaceae is described as a family exhibiting high endemism further aggravated by ecological sensitivity (Barbhuiya et al., 2014). Additionally, the species in Rubiaceae are less diverse (Davis and Bridson, 2007) and exhibit higher rate of susceptibility to extinction owing to the presence of at least 72% of the genera with lesser than 10 species further exacerbated by the presence of 211 monotypic genera of the total 620 genera (Davis et al., 2009).

Bhutan with 71% of land under forest coverage (DoFPS 2016) characterized by a high density of species richness (Bruggeman et al. 2016) that are thriving against 89.6% of the population relying on forest resources for their day livelihood (MoLHR 2011) provides ideal conditions for the study concerning the influence of anthropogenic factors on the plant species composition. Furthermore, the recognition of Bhutan as part of a global biodiversity hotspot (Myers et al. 2000) under the imminent anthropogenic threat driven by the historic human land use system and the associated disturbance regime (Siebert and Belsky 2014) provides a wide range of habitat—from disturbed to intact—for the plant species to occupy. It, therefore, creates an ideal site for the study.

Hence, this study endeavors to investigate the resilience of Rubiaceae species to anthropogenic factors. In particular, the study aims to (i) explain the variation of Rubiaceae species diversity based on the prevalence of anthropogenic factors and (ii) discuss the resilience of Rubiaceae to human disturbances.

MATERIALS AND METHODS
Study area

The study was conducted along Phuntsholing-Thujaydrak and Dagachu-Dagala range within the altitudinal gradient of 300–3900 m asl. (Figure 1). Both the study area encompasses the tropical, subtropical, warm-temperate, cool temperature, and subarctic zones based on the vegetation zonation of Bhutan by Ohsawa (1987). The study areas are characterized by the presence of roads, hydropower constructions, settlements, cultivation, abandoned lands, religious sites, and trekking trails, thereby, manifesting high variability of habitat—from pristine to disturbed. Furthermore, the landscape is characterized by sharp ridges, hills, valleys, thick forests, and alpine scrub and meadows.

Figure 1

A map showing the study sites. (A) A map of Bhutan; (B) Map of Dagana, Chukha, and Thimphu districts; (C) Phuntsholing–Thujaydrak study area; (D) Dagachu–Dagala study area

The climate data for the past 10 years recorded at the weather stations located in the study areas, obtained from the National Center for Hydrology and Meteorology, Thimphu Bhutan, show a high variation in annual mean precipitation, relative humidity, the maximum and minimum temperature in the study sites (Figure 2). The high variability of climate, topography, elevation, and rock composition fosters the presence of high biodiversity in both the study areas.

Figure 2

The summary of mean annual rainfall, relative humidity (RH), maximum, and minimum temperature of the study area during the period of 2008–2017; (A) Phuntsholing–Thujaydrak area; (B) Dagachu–Dagala area

Study design and data collection

Based on the ocular inspection and reconnaissance survey, the study areas were pigeonholed into three as undisturbed forests (UDF), semi-disturbed forests (SDF), and highly disturbed forests (HDF). The portion of the forest where anthropogenic factors are completely absent or showing evidence of some minor disturbances lacking potential risk to deplete or alter the native state of the habitat is categorized as undisturbed forests. The forest zone experiencing timber extraction, tree felling, litter extraction, fuelwood collection, and cattle grazing is defined as semi-disturbed forests. The area characterized by settlement, road and hydro-power plant constructions, cultivated land, an abandoned area with early vegetation succession, trekking routes, and farmlands is defined as highly disturbed forests.

The species absence and presence examination were done at every 200 m elevation interval covering all the three forest types mentioned above. In this manner, a total of 38 sites, 19 sites in each study area, were set up for investigation. For every encounter of Rubiaceae species, an approximate quadrat in the manner of 10 × 10 m, 5 × 5 m, and 1 × 1 m was laid for tree, shrub, and herb species, respectively. The information on the quadrat number, species count in each quadrat, the forest type, altitude, latitude, and longitude was recorded in the field datasheet. The Rubiaceae species observed in other areas were also included in the list following the same protocol of assessment as detailed above. The data collection was done from February to December to cover the whole flowering period.

The in situ and ex situ methods of specimen identifications were adopted using the Flora of Bhutan (Grierson and Long 1999) and other available taxonomic literature. The methods of Bridson and Forman (1992) were used to prepare voucher specimens and deposited at the National Herbarium, Serbithang, Thimphu, Bhutan.

Data analysis

The species diversity in each forest type was calculated using Shannon-Wiener and Simpson diversity index. The climate data and species density (mean and stand deviation) were calculated through direct computation in Microsoft Excel 2007. A between-group one-way analysis of variance (ANOVA) was performed using Statistical Package for the Social Science (SPSS) version 24 to evaluate the significance of species diversity in different forest types.

RESULT

A total of 54 Rubiaceae species, consisting of 11 tree species, 22 shrub species, and 21 herb species, belonging to 41 genera were recorded from the study sites (Table 1). The percentage species composition was higher for semi-disturbed forests at 40.4% (51 species) against 30.4% (38 species) in undisturbed forests and 28.8% (36 species) in highly disturbed forests. In general, the Shannon-Wiener and Simpson diversity analysis revealed highest diversity for semi-disturbed forests, H = 0.94 (tree), 0.927 (shrub), and 0.946 (herb), D = 0.898 (tree), 0.937 (shrub), and 0.941 (herb), followed by undisturbed forests, H = 0.950 (tree), 0.831 (shrub), and 0.709 (herb), D = 0.910 (tree), 0.913 (shrub), and 0.876 (herb). The lowest diversity recorded was in the highly disturbed forest, H = 0.774 (tree), 0.751 (shrub), and 0.873 (herb), D = 0.852 (tree), 0.886 (shrub), and 0.925 (herb) (Figure 2).

The species density of the Rubiaceae in three different forest types based on the prevalence of anthropogenic factors (UDF: undisturbed forests, SDF: semi-disturbed forests, HDF: highly disturbed forests, SD: standard deviation)

Species name Density (Mean + SD)
UDF SDF HDF
Trees Ceriscoides campanulata Roxb. 1.3 + 0.5 2.3 + 1.9 2.3 + 1.9
Hymenodictyon flaccidum Wall. 2.0 + 0.8 2.5 + 0.3 0
Ixora undulata Roxb. 0 2.3 + 1.0 1.3 + 0.5
Tarenoidea wallichi Hook.f. 1.3 + 0.5 0 0
Wendlandia coriacea DC. 3.0 + 0.8 3.3 + 1.3 2.3 + 0.9
Wendlandia grandis Cowan. 2.8 + 0.9 2.3 + 1.5 0
Wendlandia heynei Stantapau & Marchant. 4.0 + 0.8 4.5 + 1.3 2.8 + 1.7
Wendlandia puberula DC. 3.0 + 0.8 4.3 + 2.2 2.3 + 1.5
Wendlandia speciosa Cowan. 1.8 + 0.9 2.0 + 0.8 0.5 + 0.6
Wendlandia tinchoria DC. 2.5 + 0.6 3.0 + 0.8 1.5 + 0.6
Wendlandia wallichi Wight & Arnott. 2.3 + 0.9 1.3 + 0.9 0
Shrubs Catunaregam longispina Link. 2.0 + 0.8 1.5 + 0.6 0
Chassalia curvifolia Wall. 9.3 + 1.0 8.3 + 1.2 0
Himalrandia tetrasperma Roxb. 3.5 + 1.0 4.0 + 1.8 2.8 + 0.9
Leptodermis amoena Springate. 1.8 + 0.9 3.0 + 1.4 5.8 + 0.9
Leptodermis kumaonensis Parker. 2.3 + 0.5 3.8 + 1.7 1.8 + 1.0
Leptodermis stapfiana Winkler. 1.3 + 0.5 2.8 + 1.7 0
Luculia grandifolia Ghose. 0.8 + 0.5 1.3 + 0.5 0
Luculia gratissima (Wall.) Sweet. 3.8 + 1.3 1.8 + 0.9 1.8 + 0.9
Morinda angustifolia L. 0 5.8 + 1.3 2.0 + 0.8
Mussaenda frondosa L. 0 2.3 + 0.5 0.5 + 0.6
Mussaenda glabra Vahl. 2.5 + 1.3 3.5 + 1.3 2.3 + 1.3
Mussaenda macrophylla Wall. 0 1.8 + 1.0 3.8 + 1.0
Mussaenda roxburghii Hook.f. 0 4.8 + 1.7 5.3 + 2.8
Mycetia longifolia (Wall.) Kuntze. 7.0 + 1.8 0 0
Neohymenopogon parasiticus Wall. 5.5 + 1.3 4.0 + 1.8 0
Oxyceros fasciculata Roxb. 3.0 + 2.2 1.3 + 0.5 0
Pavetta subcapitata Hook.f. 3.8 + 1.8 5.8 + 1.3 0
Psilanthus bengalensis (Sc.) Leroy. 0 6.8 + 1.7 2.8 + 1.7
Rubiaceae sp. (Pentas) 5.8 + 1.1 4.0 + 1.8 0
Spemadictyon suaveolons Roxb. 0 9.5 + 1.3 9.3 + 1.7
Uncaria scandens (Sm.) Hutchinson. 1.3 + 0.5 1.8 + 1.0 1.0 + 0.8
Uncaria sessilifructus Roxb. 1.8 + 0.9 1.3 + 0.5 1.5 + 0.6
Herbs Argosteamma sarmentosum Wall. 8.3 + 2.6 4.0 + 2.6 0
Argosteamma verticillatum Wall. 9.8 + 2.2 5.8 + 2.8 0
Galium aparine L. 5.8 + 1.0 4.8 + 0.9 5.3 + 2.6
Galium asperuloides Edgeworth. 0 7.3 + 2.6 2.8 + 1.3
Galium craticulatum Mill. 3.0 + 0.8 3.5 + 1.7 3.8 + 0.9
Galium sp. 0 7.5 + 1.3 3.0 + 1.8
Hedyotis auricularia L. 0 3.3 + 1.5 4.3 + 0.9
Hedyotis scandens Roxb. 0 5.3 + 1.7 4.0 + 0.8
Hedyotis verticillata (L.) Lam. 0 5.3 + 2.6 4.0 + 1.4
Neonatis ingrata Lewis. 0 9.0 + 2.2 9.5 + 2.1
Oldenlandia corymbosa L. 0 1.5 + 0.7 3.8 + 0.9
Ophiorrhiza fasciculata Roxb. 10 + 1.8 9.8 + 0.9 0
Ophiorrhiza mungos L. 10 + 0.8 9.8 + 1.7 0
Ophiorrhiza rugosa Wall. 5.3 + 1.5 4.8 + 1.7 0
Paederia foetida L. 3.8 + 1.0 5.8 + 1.7 4.3 + 1.5
Richardia brasillensis Gomes. 0 0 9.5 + 1.9
Rubia cordifolia auct. 2.3 + 1.3 2.8 + 1.0 2.0 + 0.8
Rubia manjith Roxb. 0 2.5 + 1.3 2.8 + 1.7
Rubia sikkimensis Kurz. 1.8 + 0.9 1.8 + 0.9 1.5 + 0.6
Spemacocea latifolia Aublet. 0 5.8 + 2.1 6.0 + 2.6
Spermacoce mauritiana Gideon. 0 5.5 + 3.5 6.3 + 1.3

In addition, a between-group one-way analysis of variance (ANOVA) was performed to evaluate the relationship between Rubiaceae species richness and diversity with the forest type (highly disturbed forests, semi-disturbed forests, and undisturbed forests). It is apparent that the moderate level of disturbance was associated with the highest mean level of species diversity (M = 15.63, SD = 10.02), and the highest level of disturbance was associated with the lowest mean level of species diversity (M = 9.30, SD = 10.12) as shown in Figure 3. The assumption of homogeneity of variances evaluated based on Levene's F test, F (2, 159) = 0.239, p = 0.788 was found tenable.

Figure 3

The diversity of trees, shrubs, and herbs in undisturbed forests (UDF), semi-disturbed forests (SDF), and highly disturbed forests (HDF) analyzed using Shannon-Wiener and Simpson diversity index

Figure 4

The species richness and diversity mean and 95% confidence interval across forest types

An independent between-group analysis of variance revealed a statistically significant difference between groups, F(2, 159) = 5.687, p = 0.004, η2 = 0.067. However, based on the conventions for interpreting effect size (Cohen 1988), the magnitude of the difference between a mean score and the effect size was very small. The post-hoc analysis with Tukey's HSD, to evaluate the differences among three group means, revealed a statistically significant differences in Rubiaceae species diversity between undisturbed forest (M = 10.22, SD= 11.43) versus semi-disturbed forest (M = 15.63, SD = 10.02), p = 0.023, and semi-disturbed forests (M = 15.63, SD = 10.02) versus highly disturbed forests (M = 9.30, SD = 10.12), p = 0.006. On the contrary, the undisturbed forests versus highly disturbed forests did not show statistically significant differences, p = 0.892.

DISCUSSION

In total, these results suggest that the prevalence of a moderate form of disturbance enhances species diversity of Rubiaceae. Similar findings, though not for Rubiaceae species, were reported by other researchers (Connell 1978; Shrestha et al. 2013; Rahman et al. 2009) claiming higher plant diversity in the forest characterized by an intermediate level of disturbance. Nonetheless, a higher disturbance regime in the form of complete habitat alteration or destruction is compatible neither for species conservation nor for diversification. The higher species diversity recorded in the forest experiencing a moderate level of disturbance regime could be ascribed to creation of ample gap for increased light penetration to the forest floor and reduced competition (Pedreira et al. 2000). In contrast, lower species diversity in the undisturbed forest and highly disturbed forest could be construed as a restriction triggered by increased competition in the former and amplified degrees of stress to the species diversification in the latter condition. While the phenomenal diversity of Rubiaceae in the semi-disturbed forest is unusual for the family that has been described as ecologically sensitive and rare in the secondary forest (Davis et al. 2009), the creation of suitable and variable micro-habitat (Brosofske et al. 2001) from disturbed to intact in the semi-disturbed forest may have enhanced diversity.

The detection of higher woody Rubiaceae diversity in the undisturbed forest indicates a higher rate of tolerances of the woody Rubiaceae to the competition as well as the ability to compete at par with other woody species. Along these lines, the dominance of herbaceous Rubiaceae in the highly disturbed forests could signal higher resource availability for the herbs and lesser competition from superior species like trees and shrubs. Correspondingly, the higher diversity of shrubby Rubiaceae in the semi-disturbed forest describes the ability of the shrub to take advantage of the overstory openings and grow into the layer where light is available. Such a pattern of species diversity variation based on the life form is observed due to the influence of higher vegetation layers like overstory trees on the distribution and abundance of subordinate species like shrubs and herbs (McKenzie et al. 2000).

The findings also suggest that the impact of anthropogenic factors on Rubiaceae species diversity is inconsistent. The species like Argostemma Wall., Mycetia Reinwardt., and Chassalia Poiret. are confined mostly to the nondisturbed areas while the distribution of Ceriscoides (Hook.f.) Tirvengadum, Himalrandia Yamazaki, and Uncaria Schreber, Leptodermis Wall. ranges from highly disturbed forests through the semi-disturbed forest into the undisturbed forests. And it is interesting to note that the Rubia L., Mussaenda L., Spemacocea L., and Oldenlandia L. are diverse in highly disturbed forests. Furthermore, the dominance of Rubia manjith Roxb. in swidden and secondary forests and their absence in undisturbed forests testify the importance of a disturbance regime for the existence and diversification of some species. In general, species showing a higher rate of adaptability to different environmental and ecological conditions may exhibit a higher probability of survival in the world where disturbance regimes are on the rise. On the other hand, species showing higher confinement to natural habitat may experience a higher risk of extinction.

The effect of anthropogenic factors on the diversity of endemic and endangered Rubiaceae species requires further investigation. The presumed sensitivity of Rubiaceae to the ecological disturbance and the vulnerability of endemic and monotypic Rubiaceous species, calculated at 34.5% of genera (211 monotypic genera) to extinction (Davis et al. 2009) is a cause of concern requiring thorough investigation and documentation. However, the current research findings contradict this proposition revealing higher Rubiaceae diversity in the semi-disturbed forest. Such contradictory findings could be associated with the absence of endemic species in the current survey or may have been obscured by the research design.

Since plants exhibit species-specific tolerances and adapt based on the suitability of conditions (Kikvidze et al. 2005), not all the species would respond equally to the disturbance regimes. For that matter, the effect relies upon the type and intensity of disturbances that may augment or reduce diversity. Thus, there is a need for a careful examination of the impact of different anthropogenic factors on the resilience of different species of Rubiaceae.

CONCLUSION

The diversity of Rubiaceae species, as revealed by Shannon-Wiener and Simpson diversity index, further validated by in between-group one-way ANOVA analysis is higher in the forest experiencing an intermediate form of disturbances. The finding suggests that the tolerance of species to the disturbance regime is specific, and it, therefore, defines habitat preferences of different species. Ultimately, the survival rate and extinction risk of the species may be defined by the adaptive potential of the species to varying conditions created by anthropogenic influences.

Subsequently, striking a good balance between the forests managed through the influence of human activities and keeping the virgin forest intact is found imperative to ensure the continuance of the species diversity of Rubiaceae.

Figure 1

A map showing the study sites. (A) A map of Bhutan; (B) Map of Dagana, Chukha, and Thimphu districts; (C) Phuntsholing–Thujaydrak study area; (D) Dagachu–Dagala study area
A map showing the study sites. (A) A map of Bhutan; (B) Map of Dagana, Chukha, and Thimphu districts; (C) Phuntsholing–Thujaydrak study area; (D) Dagachu–Dagala study area

Figure 2

The summary of mean annual rainfall, relative humidity (RH), maximum, and minimum temperature of the study area during the period of 2008–2017; (A) Phuntsholing–Thujaydrak area; (B) Dagachu–Dagala area
The summary of mean annual rainfall, relative humidity (RH), maximum, and minimum temperature of the study area during the period of 2008–2017; (A) Phuntsholing–Thujaydrak area; (B) Dagachu–Dagala area

Figure 3

The diversity of trees, shrubs, and herbs in undisturbed forests (UDF), semi-disturbed forests (SDF), and highly disturbed forests (HDF) analyzed using Shannon-Wiener and Simpson diversity index
The diversity of trees, shrubs, and herbs in undisturbed forests (UDF), semi-disturbed forests (SDF), and highly disturbed forests (HDF) analyzed using Shannon-Wiener and Simpson diversity index

Figure 4

The species richness and diversity mean and 95% confidence interval across forest types
The species richness and diversity mean and 95% confidence interval across forest types

The species density of the Rubiaceae in three different forest types based on the prevalence of anthropogenic factors (UDF: undisturbed forests, SDF: semi-disturbed forests, HDF: highly disturbed forests, SD: standard deviation)

Species name Density (Mean + SD)
UDF SDF HDF
Trees Ceriscoides campanulata Roxb. 1.3 + 0.5 2.3 + 1.9 2.3 + 1.9
Hymenodictyon flaccidum Wall. 2.0 + 0.8 2.5 + 0.3 0
Ixora undulata Roxb. 0 2.3 + 1.0 1.3 + 0.5
Tarenoidea wallichi Hook.f. 1.3 + 0.5 0 0
Wendlandia coriacea DC. 3.0 + 0.8 3.3 + 1.3 2.3 + 0.9
Wendlandia grandis Cowan. 2.8 + 0.9 2.3 + 1.5 0
Wendlandia heynei Stantapau & Marchant. 4.0 + 0.8 4.5 + 1.3 2.8 + 1.7
Wendlandia puberula DC. 3.0 + 0.8 4.3 + 2.2 2.3 + 1.5
Wendlandia speciosa Cowan. 1.8 + 0.9 2.0 + 0.8 0.5 + 0.6
Wendlandia tinchoria DC. 2.5 + 0.6 3.0 + 0.8 1.5 + 0.6
Wendlandia wallichi Wight & Arnott. 2.3 + 0.9 1.3 + 0.9 0
Shrubs Catunaregam longispina Link. 2.0 + 0.8 1.5 + 0.6 0
Chassalia curvifolia Wall. 9.3 + 1.0 8.3 + 1.2 0
Himalrandia tetrasperma Roxb. 3.5 + 1.0 4.0 + 1.8 2.8 + 0.9
Leptodermis amoena Springate. 1.8 + 0.9 3.0 + 1.4 5.8 + 0.9
Leptodermis kumaonensis Parker. 2.3 + 0.5 3.8 + 1.7 1.8 + 1.0
Leptodermis stapfiana Winkler. 1.3 + 0.5 2.8 + 1.7 0
Luculia grandifolia Ghose. 0.8 + 0.5 1.3 + 0.5 0
Luculia gratissima (Wall.) Sweet. 3.8 + 1.3 1.8 + 0.9 1.8 + 0.9
Morinda angustifolia L. 0 5.8 + 1.3 2.0 + 0.8
Mussaenda frondosa L. 0 2.3 + 0.5 0.5 + 0.6
Mussaenda glabra Vahl. 2.5 + 1.3 3.5 + 1.3 2.3 + 1.3
Mussaenda macrophylla Wall. 0 1.8 + 1.0 3.8 + 1.0
Mussaenda roxburghii Hook.f. 0 4.8 + 1.7 5.3 + 2.8
Mycetia longifolia (Wall.) Kuntze. 7.0 + 1.8 0 0
Neohymenopogon parasiticus Wall. 5.5 + 1.3 4.0 + 1.8 0
Oxyceros fasciculata Roxb. 3.0 + 2.2 1.3 + 0.5 0
Pavetta subcapitata Hook.f. 3.8 + 1.8 5.8 + 1.3 0
Psilanthus bengalensis (Sc.) Leroy. 0 6.8 + 1.7 2.8 + 1.7
Rubiaceae sp. (Pentas) 5.8 + 1.1 4.0 + 1.8 0
Spemadictyon suaveolons Roxb. 0 9.5 + 1.3 9.3 + 1.7
Uncaria scandens (Sm.) Hutchinson. 1.3 + 0.5 1.8 + 1.0 1.0 + 0.8
Uncaria sessilifructus Roxb. 1.8 + 0.9 1.3 + 0.5 1.5 + 0.6
Herbs Argosteamma sarmentosum Wall. 8.3 + 2.6 4.0 + 2.6 0
Argosteamma verticillatum Wall. 9.8 + 2.2 5.8 + 2.8 0
Galium aparine L. 5.8 + 1.0 4.8 + 0.9 5.3 + 2.6
Galium asperuloides Edgeworth. 0 7.3 + 2.6 2.8 + 1.3
Galium craticulatum Mill. 3.0 + 0.8 3.5 + 1.7 3.8 + 0.9
Galium sp. 0 7.5 + 1.3 3.0 + 1.8
Hedyotis auricularia L. 0 3.3 + 1.5 4.3 + 0.9
Hedyotis scandens Roxb. 0 5.3 + 1.7 4.0 + 0.8
Hedyotis verticillata (L.) Lam. 0 5.3 + 2.6 4.0 + 1.4
Neonatis ingrata Lewis. 0 9.0 + 2.2 9.5 + 2.1
Oldenlandia corymbosa L. 0 1.5 + 0.7 3.8 + 0.9
Ophiorrhiza fasciculata Roxb. 10 + 1.8 9.8 + 0.9 0
Ophiorrhiza mungos L. 10 + 0.8 9.8 + 1.7 0
Ophiorrhiza rugosa Wall. 5.3 + 1.5 4.8 + 1.7 0
Paederia foetida L. 3.8 + 1.0 5.8 + 1.7 4.3 + 1.5
Richardia brasillensis Gomes. 0 0 9.5 + 1.9
Rubia cordifolia auct. 2.3 + 1.3 2.8 + 1.0 2.0 + 0.8
Rubia manjith Roxb. 0 2.5 + 1.3 2.8 + 1.7
Rubia sikkimensis Kurz. 1.8 + 0.9 1.8 + 0.9 1.5 + 0.6
Spemacocea latifolia Aublet. 0 5.8 + 2.1 6.0 + 2.6
Spermacoce mauritiana Gideon. 0 5.5 + 3.5 6.3 + 1.3

ABADIE JC, MACHON N, MURATET A, PORCHER E (2011) Landscape disturbance causes small-scale functional homogenization, but limited taxonomic homogenization, in plant communities. Journal of Ecology. 99, 1134–1142, doi: 10.1111/j.1365-2745.2011.01851.x. ABADIEJC MACHONN MURATETA PORCHERE 2011 Landscape disturbance causes small-scale functional homogenization, but limited taxonomic homogenization, in plant communities Journal of Ecology 99 1134 1142 10.1111/j.1365-2745.2011.01851.x Otwórz DOISearch in Google Scholar

BARTELS SF, CHEN HYH (2010) Is understory plant species diversity driven by resource quantity or resource heterogeneity? Ecology, 91, 1931–1938. BARTELSSF CHENHYH 2010 Is understory plant species diversity driven by resource quantity or resource heterogeneity? Ecology 91 1931 1938 10.1890/09-1376.1 Search in Google Scholar

BRIDSON D, FORMAN L (1992) The Herbarium Handbook, 3rd ed.; Royal Botanic Garden, Kew, UK. 10: 1900347431. BRIDSOND FORMANL 1992 The Herbarium Handbook 3rd ed. Royal Botanic Garden Kew, UK 10: 1900347431. Search in Google Scholar

BROSOFSKE KD, CHEN J, CROW TR (2001) Understory vegetation and site factors: implications for a managed Wisconsin landscape. Forest Ecology and Mangement, 146, 75–87. BROSOFSKEKD CHENJ CROWTR 2001 Understory vegetation and site factors: implications for a managed Wisconsin landscape Forest Ecology and Mangement 146 75 87 10.1016/S0378-1127(00)00447-3 Search in Google Scholar

BRUGGEMAN D, MEYFROIDT P, LAMBIN EF (2016) Forest cover changes in Bhutan: Revisiting the forest transition. Applied Geography,, 67, 49–66. BRUGGEMAND MEYFROIDTP LAMBINEF 2016 Forest cover changes in Bhutan: Revisiting the forest transition Applied Geography 67 49 66 10.1016/j.apgeog.2015.11.019 Search in Google Scholar

COHEN J (1988) Statistical Power Analysis for the Behavioral Sciences, 2nd ed.; Lawrence Erlbaum Associates, USA, pp.110. COHENJ 1988 Statistical Power Analysis for the Behavioral Sciences 2nd ed. Lawrence Erlbaum Associates USA 110 Search in Google Scholar

CONNELL J (1978) Diversity in tropical rain forests and coral reefs. Science, 199, 1302–1310. CONNELLJ 1978 Diversity in tropical rain forests and coral reefs Science 199 1302 1310 10.1126/science.199.4335.1302 Search in Google Scholar

DALE VH, JOYCE LA, MCNULTY S, NEILSON RP (2000) The interplay between climate change, forests, and disturbances. The Science of the Total Environment, 262, 201–204. DALEVH JOYCELA MCNULTYS NEILSONRP 2000 The interplay between climate change, forests, and disturbances The Science of the Total Environment 262 201 204 10.1016/S0048-9697(00)00522-2 Search in Google Scholar

DAVIS AP, GOVAERTS R, BRIDSON DM, RUHSAM M, MOAT J, BRUMMITT NA (2009) A Global Assessment of Distribution, Diversity, Endemism, and Taxonomic Effort in the Rubiaceae. Ann. Missouri Bot. Gard., 96, 68–78. DAVISAP GOVAERTSR BRIDSONDM RUHSAMM MOATJ BRUMMITTNA 2009 A Global Assessment of Distribution, Diversity, Endemism, and Taxonomic Effort in the Rubiaceae Ann. Missouri Bot. Gard. 96 68 78 10.3417/2006205 Search in Google Scholar

Department of Forests and Park Services (DoFPS) (2016) Forest facts and figure. Department of forests and park services. Ministry of Agriculture and Forests. Royal Government of Bhutan, Thimphu, pp.3. Department of Forests and Park Services (DoFPS) 2016 Forest facts and figure Department of forests and park services. Ministry of Agriculture and Forests. Royal Government of Bhutan Thimphu 3 Search in Google Scholar

GRIERSON AJC, LONG DG (1999) Flora of Bhutan: Including a record of plants from Sikkim and Darjeeling, Volume 2 Part 2; the Royal Botanic Garden Edinburgh EH3 5LR, UK and the Royal Government of Bhutan, pp.733–834, 1 872291 43 0. GRIERSONAJC LONGDG 1999 Flora of Bhutan: Including a record of plants from Sikkim and Darjeeling, Volume 2 Part 2; the Royal Botanic Garden Edinburgh EH3 5LR, UK and the Royal Government of Bhutan 733 834 1 872291 43 0 Search in Google Scholar

BARBHUIYA, HA, DUTTA BK, DAS AK, BAISHYA A K (2014). The family Rubiaceae in Southern Assam with special reference to endemic and rediscovered plant taxa. Journal of Threatened Taxa, 6(4), 5649–5659. BARBHUIYAHA DUTTABK DASAK BAISHYAA K 2014 The family Rubiaceae in Southern Assam with special reference to endemic and rediscovered plant taxa Journal of Threatened Taxa 6 4 5649 5659 10.11609/JoTT.o3117.5649-59 Search in Google Scholar

DAVIS AP, BRIDSON DM (2007) Rubiaceae: Flowering Plants of the World. Royal Botanic Gardens, Kew. DAVISAP BRIDSONDM 2007 Rubiaceae: Flowering Plants of the World Royal Botanic Gardens Kew Search in Google Scholar

DELPRETE PG, JARDIM JG (2012) Systematics, taxonomy and floristics of Brazilian Rubiaceae: an overview about the current status and future challenges. Rodriguésia 63(1): 101–128. DELPRETEPG JARDIMJG 2012 Systematics, taxonomy and floristics of Brazilian Rubiaceae: an overview about the current status and future challenges Rodriguésia 63 1 101 128 10.1590/S2175-78602012000100009 Search in Google Scholar

HASENAUER H, PETRITSCH R, ZHAO M, BOISVENUE C, RUNNING SW (2012) Reconciling satellite with ground data to estimate forest productivity at national scales. Forest Ecology and Management, 276, 196–208. HASENAUERH PETRITSCHR ZHAOM BOISVENUEC RUNNINGSW 2012 Reconciling satellite with ground data to estimate forest productivity at national scales Forest Ecology and Management 276 196 208 10.1016/j.foreco.2012.03.022 Search in Google Scholar

KIKVIDZE Z, PUGNAIRE FI, BROOKER RW, CHOLER P, LORTIE CJ, MICHALET R (2005) Linking patterns and processing alpine plant communities: a global study. Ecology, 86, 1395–1400. KIKVIDZEZ PUGNAIREFI BROOKERRW CHOLERP LORTIECJ MICHALETR 2005 Linking patterns and processing alpine plant communities: a global study Ecology 86 1395 1400 10.1890/04-1926 Search in Google Scholar

KUMAR A, RAM J (2005) Anthropogenic disturbances and plant biodiversity in the forests of Uttaranchal, central Himalaya. Biodiversity and Conservation, 14, 309–331. KUMARA RAMJ 2005 Anthropogenic disturbances and plant biodiversity in the forests of Uttaranchal, central Himalaya Biodiversity and Conservation 14 309 331 10.1007/s10531-004-5047-4 Search in Google Scholar

LORIMER CG, WHITE AS (2003) Scale and frequency of natural disturbances in the northeastern US: implications for early successional forest habitats and regional age distributions. Forest Ecology and Management, 185, 41–64. LORIMERCG WHITEAS 2003 Scale and frequency of natural disturbances in the northeastern US: implications for early successional forest habitats and regional age distributions Forest Ecology and Management 185 41 64 10.1016/S0378-1127(03)00245-7 Search in Google Scholar

MCKENZIE D, HALPERN CB, NELSON CR (2000) Overstory influence on herb and shrub communities in mature forests of western Washington, U.S.A. Canadian Journal of Forest Research, 30, 1655–1666. MCKENZIED HALPERNCB NELSONCR 2000 Overstory influence on herb and shrub communities in mature forests of western Washington, U.S.A. Canadian Journal of Forest Research 30 1655 1666 10.1139/x00-091 Search in Google Scholar

Ministry of Labour and Human Resource (MoLHR) (2011) Labour Force Survey 2010. Royal Government of Bhutan, Thimphu. Ministry of Labour and Human Resource (MoLHR) 2011 Labour Force Survey 2010 Royal Government of Bhutan Thimphu Search in Google Scholar

MYERS N, MITTERMEIER RA, MITTERMEIER CG, FONSECA GAB, KENT J (2000) Biodiversity Hotspots for Conservation Priorities. Nature, 403, 24. MYERSN MITTERMEIERRA MITTERMEIERCG FONSECAGAB KENTJ 2000 Biodiversity Hotspots for Conservation Priorities Nature 403 24 10.1038/3500250110706275 Search in Google Scholar

OHSAWA M (1987) Vegetation Zones in the Bhutan Himalaya. Life Zone Ecology of the Bhutan Himalaya; Laboratory of Ecology, Chiba University, Japan, pp.17. OHSAWAM 1987 Vegetation Zones in the Bhutan Himalaya Life Zone Ecology of the Bhutan Himalaya; Laboratory of Ecology, Chiba University Japan 17 Search in Google Scholar

ONAINDIA M, DOMINGUEZ I, ALBIZU I, GARBISU C, AMEZAGA I (2004) Vegetation diversity and vertical structure as indicators of forest disturbance. Forest Ecology and Management, 195, 341–354. ONAINDIAM DOMINGUEZI ALBIZUI GARBISUC AMEZAGAI 2004 Vegetation diversity and vertical structure as indicators of forest disturbance Forest Ecology and Management 195 341 354 10.1016/j.foreco.2004.02.059 Search in Google Scholar

PEDREIRA CGS, SOLLENBERGER LE, MISLEVY P (2000) Botanical composition, light interception, and carbohydrate reserve status of grazed ‘Florakirk’ bermudagrass. Agronomy Journal, 92, 194–199. PEDREIRACGS SOLLENBERGERLE MISLEVYP 2000 Botanical composition, light interception, and carbohydrate reserve status of grazed ‘Florakirk’ bermudagrass Agronomy Journal 92 194 199 10.2134/agronj2000.922194x Search in Google Scholar

RAHMAN MM, NISHAT A, VACIK H (2009) Anthropogenic disturbances and plant diversity of the Madhupur Sal forests (Shorea robusta C.F. Gaertn) of Bangladesh. International Journal of Biodiversity Science & Management, 5, 162–173. RAHMANMM NISHATA VACIKH 2009 Anthropogenic disturbances and plant diversity of the Madhupur Sal forests (Shorea robusta C.F. Gaertn) of Bangladesh International Journal of Biodiversity Science & Management 5 162 173 10.1080/17451590903236741 Search in Google Scholar

SHRESTHA KB, MAREN IE, ARNEBERG E, SAH JP, VETASS OR (2013) Effect of anthropogenic disturbance on plant species diversity in oak forests in Nepal, Central Himalaya. International Journal of Biodiversity Science, Ecosystem Services & Management, 9, 21–29. SHRESTHAKB MARENIE ARNEBERGE SAHJP VETASSOR 2013 Effect of anthropogenic disturbance on plant species diversity in oak forests in Nepal, Central Himalaya International Journal of Biodiversity Science, Ecosystem Services & Management 9 21 29 10.1080/21513732.2012.749303 Search in Google Scholar

SIEBERT SF, BELSKY JM (2014) Historic livelihoods and land uses as ecological disturbances and their role in enhancing biodiversity: An example from Bhutan. Biological Conservation, 177, 82–89, https://doi.org/10.1016/j.biocon.2014.06.015. SIEBERTSF BELSKYJM 2014 Historic livelihoods and land uses as ecological disturbances and their role in enhancing biodiversity: An example from Bhutan Biological Conservation 177 82 89 https://doi.org/10.1016/j.biocon.2014.06.015. 10.1016/j.biocon.2014.06.015 Search in Google Scholar

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