1 INTRODUCTION

The genus Meconopsis, commonly known as Himalayan or blue poppies, is a group of herbaceous alpine ecosystem plant species native to the Himalayas. This diverse genus comprises over 70 species within the Papaveraceae family (Xiao & Simpson, 2017). Bhutan is a habitat for more than 18 Meconopsis species, including the notable Meconopsis gakyidiana (Tosh. Yoshida, Yangzom and D. G. Long, 2017), which holds significance as the country's national flower. Previously, this species was misidentified as Meconopsis grandis (Prain, 1896).

Amongst the 18 Meconopsis species found in Bhutan, Papaver bhutanicum (Yoshida & Grey-Wilson, 2012), formerly known as Meconopsis bhutanica, is particularly significant due to its rarity, endemic nature and status as a critically endangered species (International Union of Conservation of Nature and Natural Resource [IUCN], 2017; Yoshida & Grey-Wilson, 2012). This Bhutan poppy is confined to Jigme Dorji National Park (JDNP), around Tshophu Lake. Initially classified as a subspecies of Meconopsis discigera in 1995 (Prain, 1906), it was not until 2012 that the species was accurately identified as a distinct entity (Yoshida & Grey-Wilson, 2012). Characterised by its extremely limited distribution range, the Bhutan poppy has been documented in a few specific locations, such as Barshong (potentially referring to Yaklela), Bongtela and Tshophu (Yoshida & Grey-Wilson, 2012).

Alpine ecosystems thrive beyond the treeline, exhibiting remarkable richness in plant ecosystems (Korner, 2002). In the Himalayas, these ecosystems boast abundant native and endemic biodiversity, providing a habitat for numerous specialised and geographically range-restricted species (Chettri et al., 2010; Dhar, 2002). However, these ecosystems are also amongst the most vulnerable and sensitive to the impacts of land use and climate change, primarily due to the temperature limitations that influence species survival (Huber et al., 2013; Vanneste et al., 2017). With global warming, there is an anticipated upward movement of species from lower elevations into alpine and subalpine environments. This shift poses significant threats, potentially resulting in habitat shrinkage, increased risk of cryophilic plant extinction, disruption of current species composition and effects on both physical and biological environmental conditions (Beniston, 2003; Parmesan & Yohe, 2003; Pauli et al., 2003; Wiens, 2016). Rare species that have a restricted distribution range and are native to alpine regions face a higher risk of extinction due to limited opportunities for upward migration.

Ecologists use various criteria to define species rarity, with certain rare species exhibiting variability in their local presence. A species might be widely distributed but rare in specific locations, locally abundant but with restricted distribution or scarce in specific localities despite a broad geographic range (Rabinowitz, 1981). The rarity of certain species is intricately linked to their life history traits, such as dependency on disturbances or specific pollinators (Bissessur et al., 2019; Kaye et al., 2001). Rare species play a disproportionate role in contributing to regional community diversity (Chapman et al., 2018). They significantly enhance ecosystem functioning, often in ways that cannot be substituted by a more common species (Winter et al., 2013). Rarity extends beyond numerical abundance or spatial extent; it encompasses the unique ecological roles these species play in their environments (Winter et al., 2013). Increasingly rare and endemic plant species such as the Bhutan poppy warrant special conservation concern as they are more susceptible to disturbances, thereby facing a higher risk of extinction (Coelho et al., 2020; Gaston, 1998).

The objectives of this study were as follows: (1) identify and document different growing sites of the Bhutan poppy; (2) assess and catalogue floristic composition in the Bhutan poppy growing sites; (3) investigate environmental variables affecting the growth of the Bhutan poppy; (4) predict the potential distribution of the Bhutan poppy in JDNP; and (5) assess anthropogenic threats to Bhutan poppy conservation. The anticipated results aim to significantly contribute to informed management and conservation strategies for the Bhutan poppy within the national park.

2 MATERIALS AND METHODS

2.1 Study area

The research was carried out at three distinct sites within JDNP: Tshophu, Tshophu base and Jichudrakey base, located in Soe Gewog, Lingzhi Dungkhag, Thimphu Dzongkhag (Figure 1). JDNP, spanning from 27°33′ N–28°15′ N to 89°14′ E–90°22′ E, is the second-largest of Bhutan's 11 protected areas, inclusive of the Royal Botanical Park, covering an extensive area of 4374.06 square kilometres. The park is renowned for its diverse altitudinal gradient (1200–>7000 m), its representation of the upper Himalayan ecosystem and the Palaearctic biogeographic realm and its rich biodiversity (Dendup, Dorji, Jamtsho, Wangchuk, Tshering et al., 2021). The park experiences four distinct seasons (winter, spring, summer and autumn) and is characterised by five different forest types, including subtropical forests, warm temperate forests, cool temperate forests, cold temperate forests and rhododendron scrubs.

Additionally, JDNP is the origin of four major rivers—The Pachu, The Wangchu, The Phochu and The Mochu—contributing significantly to the country's water resources and hydropower. The Pachu originates from within the study area. The park's rich biodiversity includes over 1434 vascular plants, 50 mammal species, 414 birds, 22 reptiles, 15 amphibians, 87 butterflies and 17 species of dragons and damselflies (Dendup, Dorji, Jamtsho, Wangchuk, Tshering et al., 2021). The national park is home to more than 5000 residents across 138 villages. The park's importance is further accentuated by its role as a habitat for eight species of blue poppies, including the critically endangered M. bhutanica (Papaver bhutanicum) (Figure 2), alongside M. horridula (Hook. f. & Thomson, 1855), M. bella (Prain, 1894), M. simplicifolia (D. Don/G. Don, 1831), M. primulina (Prain, 1896), M. paniculata (D. Don/Prain, 1896), M. villosa (Hook. f/G. Taylor, 1934) and M. sherriffii (G. Taylor, 1937).

3 RESULTS

3.1 Species diversity and environmental variables in the study site

A total of 202 plots, each measuring 2 × 2 m, were surveyed across three distinct sites: Tshophu, Tshophu base and Jichudrakey base. The sites were situated at altitudes ranging from 4351 to 4494 m, with a mean of 4418 m (SD = 24.7). Amongst these plots, nine were situated on rocky scree devoid of vegetation cover and were consequently excluded from the analysis. The descriptive statistics for both the species data and environmental variables are detailed in Table 1. In the remaining 193 plots, the presence of the Bhutan poppy and other alpine plants was documented in two primary habitats:  Alpine scree and Alpine meadow.

Table 1. Descriptive statistics (minimum, maximum, mean and standard deviation) of environmental variables and species richness and abundance in the study site (Tshophu, Tshophu base and Jichudrakey base) (n = 193).

Habitat	Minimum	Maximum	Mean ± SD
Alpine scree (n = 188)
Environmental variables
Elevation (m)	4310	4553	4406.5 ± 55.3
Slope (deg)	15	50	33.6 ± 6.4
Aspect (deg)	0	355	182.9 ± 93.3
Rock cover (%)	10	99	85 ± 18.3
Bare soil cover (%)	0	60	4.8 ± 9.8
Shrub cover (%)	0	30	1.2 ± 4.3
Herb cover (%)	0	70	8.8 ± 10.2
Species richness and abundance
Richness	1	10	3.8 ± 1.6
Abundance	1	170	44.4 ± 34.1
Alpine meadow (n = 5)
Environmental variables
Elevation (m)	4335	4474	4410.8 ± 53.0
Slope (deg)	0	39	23.4 ± 16.1
Aspect (deg)	25	353	137 ± 153.1
Rock cover (%)	0	40	22 ± 16.4
Bare soil cover (%)	0	65	30 ± 28.5
Shrub cover (%)	0	40	8 ± 17.9
Herb cover (%)	5	100	40 ± 40.5
Species richness and abundance
Richness	3	5	4.2 ± 1.1
Abundance	84	151	110.2 ± 27.3

A total of 57 alpine plant species were documented during the survey, averaging 3.8 species per plot (SD = 1.5) and a total abundance of 8905 individuals (Tshophu = 5869, Tshophu base = 2066 and Jichudrakey = 970), with a mean of 42.3 individuals per plot (SD = 35.5). These plants belonged to 24 different families, with Asteraceae being the most prevalent (17.5%), followed by Papaveraceae (12.3%). Notably, 46% of the families comprised only one species.

In terms of species distribution, Tshophu exhibited higher species richness and abundance compared to Jichudrakey base and Tshophu base (Figure 3). Species richness was positively and significantly correlated with slope (p = 0.001), rock cover (%) (p = 0.049), bare soil cover (%) (p = 0.045) and herb cover (%) (p = 0.037), while the species abundance was positively and significantly correlated to slope only (p = 0.007).

A significant difference in species richness was observed between Tshophu and Jichudrakey base (95% confidence interval [CI] = 0.589–2.306, p = 0.000), as well as between Tshophu base and Jichudrakey base (95% CI = 0.335–2.242, p = 0.004). However, the difference in species abundance across study sites was nonsignificant (p = 0.350).

The diversity analysis revealed that Tshophu site exhibited the highest species diversity with a Shannon diversity index (H') of 1.00, followed by Tshophu base (H' = 0.95) and Jichudrakey base (H' = 0.76). Despite the relatively high species diversity indices across the study sites, the species richness accumulation curve suggests that the survey effort was not exhaustive (Figure 4 and Table 2).

Table 2. Summary of the number of survey samples conducted in each site and the completeness of the survey samples.

Site	Sample size	Completeness
Jichudrakey base	22	0.941
Tshophu base	51	0.959
Tshophu	120	0.967

The observed sampling shortfall in the study indicates an incomplete representation of species diversity within the surveyed areas. Specifically, a shortfall of approximately 6% at Jichudrakey base, about 4% at Tshophu base and roughly 3% at Tshophu (Table 2). To address this, extrapolating species richness to the asymptote provides a more comprehensive estimate of species diversity for each study site. The results of this extrapolation are detailed in Table 3.

Table 3. Summary of extrapolated species richness at survey asymptotes across different study sites.

		Estimate		Standard error
Site	Extrapolated richness	2.5%	97.5%	2.5%	97.5%
Jichudrakey base	15	16.99	18.81	1.43	2.35
Tshophu base	27	30.6	34.84	1.76	3.1
Tshophu	43	49.43	58.86	2.39	4.65

3.3 Bhutan poppy current and future distribution in JDNP

Under the current climate conditions, the species distribution model for the Bhutan poppy revealed approximately 37.29 square kilometres of suitable habitat within JDNP. However, future climate projections for the Years 2041–2060, based on the ssp245 climate scenario, anticipate a decline of approximately 33% in this distribution area, with a shift towards the northeastern part of the national park. Intriguingly, the climatic model for the period 2061–2080, also under ssp245, suggests an 8% increase in distribution area, with the shift maintaining its direction towards the northeast (Figure 5).

4 DISCUSSION

The exploration of species distribution, including that of the Bhutan poppy, is subject to diverse factors, encompassing inadequate species records, restricted empirical data, sampling biases and variations in sampling techniques. The intensity of sampling is anticipated to fluctuate, with easily accessible areas often acknowledged for their diverse species richness (Joshi & Joshi, 2021; Ladle & Hortal, 2013).

The Bhutan poppy, classified as a rare and critically endangered species (IUCN, 2017), lacks comprehensive information about its distribution and occurrence. The Bhutan poppy was only identified in 2012 as a distinct species from M. discigera (Yoshida & Grey-Wilson, 2012). Historical knowledge suggests its presence in specific locations within Lingzhi Dungkhag, namely, Barshong, Bongtela, Tshophu and Yaklela (Yoshida & Grey-Wilson, 2012). In the recent survey, aside from the Tshophu area, the presence of the Bhutan poppy was noted at the Jichudrakey base and Tshophu base, although it was not found in Bongtela. Due to logistical constraints, its presence in Yaklela and Barshong could not be verified either.

The richness and abundance of plant species exhibited a stronger correlation with physical environmental factors like slope, rock cover and bare soil cover rather than with biological environmental factors. This contradicts findings from other studies, which highlighted different influencing factors (Dorji et al., 2018; Kaarlejarvi & Olofsson, 2014; Meineri et al., 2012). Both richness and abundance responded positively to physical environmental variables, possibly influenced by microclimate heterogeneity. Steeper slopes and increased rock cover may enhance exposure to sunlight, wind and moisture, influencing soil moisture and drainage, critical factors for alpine plant adaptation (Bliss, 1962). At higher elevations, where moisture content is reduced, there is a noticeable decrease in species evenness compared to lower elevations (Dorji et al., 2016).

The presence of the Bhutan poppy was significantly associated with aspect (southwest), consistent with other studies (Winkler et al., 2016). It is well-documented that in the Northern Hemisphere, plant diversity tends to be higher on east and south-facing slopes. These aspects provide a warmer microclimate compared to northern slopes at similar elevations, primarily due to greater sunlight exposure, which facilitates plant growth (Perring, 1959). This aspect-related preference is also observed in the Bhutan poppy growing, especially in the Tshophu area, which is known to receive more sunlight (Yoshida & Grey-Wilson, 2012).

The Bhutan poppy, recognised as a critically endangered plant species by the IUCN (2017), holds a distinct classification as a Schedule II species under the Forest and Nature Conservation Act of Bhutan 2023 (FNCA 2023) (RGoB, 2023). The IUCN defines a species as critically endangered when there is a reduction in population size of ≥90% over the previous 10 years or three generations (IUCN, 2012). This study identified three primary threats within the study area: grazing, trampling and harvesting. Grazing and trampling by yaks, horses and mules were found in 92% of the surveyed plots, while signs of harvesting were observed in 45% of the plots. Similar conservation threats were reported in the Jigme Khesar Strict Nature Reserve in a study on the white poppy (M. superba, Prain 1896) (Wangyal et al., 2023). The livelihood of the people in Soe Gewog revolves around yak rearing and the transportation of goods, with the area housing approximately 2186 livestock (yaks, horses and mules) (Dendup, Dorji, Jamtsho, Wangchuk, Gyeltshen et al., 2021). The grazing of these livestock in the Bhutan poppy habitat inevitably leads to trampling, which can be devastating for these rare plants. Trampling has a detrimental impact on plant survival, causing damage to reproductive parts and potentially resulting in reproductive arrest. Given the monocarpic nature of the Bhutan poppy (Yoshida & Grey-Wilson, 2012)—completing its life cycle within 1 year and flowering and seeding only once (Kiefer et al., 2019)—any damage to these plants can be particularly consequential. The slow regeneration rate of the species, combined with the potential for complete reproductive failure due to trampling, underscores the need for urgent conservation measures to protect this rare and ecologically significant species.

Beyond ecological concerns, the Bhutan poppy is also valued for its medicinal properties, with people reportedly collecting the entire plant. The utilisation of medicinal plants is a crucial aspect of human reliance on biodiversity, providing essential benefits (Hamilton, 2004). However, overharvesting poses a significant threat to these valuable species, potentially leading to genetic loss and jeopardising their survival (IUCN, 1993).

The distribution of biodiversity is anticipated to be impacted by climate change, acting in conjunction with human-induced stressors like changes in land use, land fragmentation and degradation (Diffenbaugh & Field, 2013). Accurately predicting the impact of climate change on the habitats and geographic ranges of species of conservation concern is crucial (Kearney & Porter, 2009). In the current climate scenario, the suitable area for Bhutan poppy is 37.29 km². However, the future climate scenario (2041–2060) predicts a loss of about 33% of its distribution area, with a northward shift in its range. This aligns with studies reporting a decline in plant species richness from the equator to the poles due to climate change (Willig et al., 2003), particularly affecting alpine and arctic ecosystems (Hansen et al., 2001; Kittel et al., 2000). Interestingly, for the more distant future climate scenario (2061–2080), there is an anticipated 8% increase in Bhutan poppy distribution from its current range. The observed increase in the distribution range of the Bhutan poppy in this future climate scenario (2061–2080) can be ascribed to the utilisation of the same GCM (MPI-ESM1-2-HR) and the ssp245 global CO₂ emission scenario. This scenario forecasts a decline in carbon emissions by 2045. As 2080 approaches, the climate is anticipated to be comparatively cooler than in 2060, leading the model to project an expansion in species distribution range.

While an increase in suitable areas by the year 2061 is projected, the Bhutan poppy may experience more disturbances. The future habitat projection for the Bhutan poppy encompasses regions within JDNP, such as Laya, Lingzhi and Lunana. These areas stand out for their considerably higher human and livestock populations when compared to Soe, the current location of the Bhutan poppy. Notably, Lingzhi boasts a human population of 440, Lunana 812 and Laya 1090, in contrast to Soe's 219 individuals. Similarly, predicted livestock numbers are significantly higher in these projected areas: Lingzhi at 4249, Lunana at 4283 and Laya at 5832, all surpassing Soe's 2186 livestock (Dendup, Dorji, Jamtsho, Wangchuk, Gyeltshen et al., 2021). Given the anticipated growth in both human and livestock populations, the Bhutan poppy's survival prospects in this future scenario appear challenging, with an expected escalation in threats to its existence.

5 CONCLUSION

This study represents the first focused research on the rare and critically endangered Bhutan poppy (P. bhutanicum) and its associated plant species. Our investigation underscores the sparseness of Bhutan poppy distribution within a highly restricted range, confined to an area of <87 ha. To gain a more comprehensive understanding of its presence, further exploration is warranted, particularly in areas historically mentioned by Yoshida and Grey-Wilson (2012) and potential new locations like Gunglung in Soe Gewog. In the absence of Bhutan poppy sightings in these additional areas, it would be prudent to upgrade its conservation status in Bhutan from Schedule II to Schedule I in the FNCA 2023. Such an elevation would afford the species enhanced protection, acknowledging its ecological significance.

Despite their numerical scarcity, restricted range and fragile habitats, rare plants such as the Bhutan poppy play pivotal roles in ecosystems. Each species, with its distinct role, contributes to maintaining ecological balance and functionality. The loss of a rare plant can disrupt intricate ecological interactions, potentially triggering cascading effects throughout an ecosystem. Furthermore, rare plants contribute to the aesthetic allure of natural landscapes, rendering them valuable for ecotourism and recreational purposes.

Given the vital ecological functions performed by rare plant species, particularly the Bhutan poppy, there is an urgent imperative to conserve this critically endangered alpine plant. While challenges like habitat loss due to climate change may be beyond immediate control, our focus should pivot towards raising awareness amongst local communities about the potential repercussions of harvesting the entire plant. Through concerted conservation efforts and community engagement, we can strive to safeguard the existence of this rare and ecologically significant species.

AUTHOR CONTRIBUTIONS

Pema Dendup: Conceptualisation; methodology; investigation; formal analysis; project administration; software; visualisation; writing—original draft; writing—review and editing). Pema Kuenzang: Investigation; data curation; writing—review and editing. Tandin Dorji: Investigation; writing—review and editing. Wangchuk Wangchuk: Data curation; writing—review and editing.

CONFLICT OF INTEREST STATEMENT

The authors declare no conflicts of interest.