Global Ecology and Conservation 30 (2021) e01771

Contents lists available at ScienceDirect

Global Ecology and Conservation

journal homepage: www.elsevier.com/locate/gecco

Bird diversity and conservation threats in Jigme Dorji National Park,

Pema Dendup a,*, Leki Wangdi a, Yenten Jamtsho a, Pema Kuenzang a, Dorji Gyeltshen b, Tashi Tashi a, Ugyen Rigzin a, Yeshey Jamtsho a, Rinzin Dorji a, Rinzin Dorji a, Yonten Jamtsho a, Choki Lham a, Bep Tshering a a Jigme Dorji National Park, Department of Forests and Park Services, Ministry of Agriculture and Forests, Royal Government of Bhutan, Gasa, Bhutan b Tashigang Territorial Forest Division, Department of Forests and Park Services, Ministry of Agriculture and Forests, Royal Government of Bhutan, Tashigang, Bhutan

ARTICLE INFO ABSTRACT

Keywords: The diversity of populations serve as a strong indicator for the overall health of an ecosystem. Abundance This study was aimed to understand and document bird diversity in different forest types and its Bhutan conservation threats in Jigme Dorji National Park, Bhutan. Across the period of winter 2019 through autumn 2020, we used MacKinnon lists to collect data on birds along a total of 535.92 km Diversity transects (existing trails and roads) within the altitudinal range of 1300 – 5100 m inside the park. Habitat Richness A total of 12363 individuals of birds belonging to 59 families, 143 genera, and 272 were recorded. Two vulnerable species (Chestnut-breasted Partridge and Wood ) and six near- threatened species (Bearded Vulture, Himalayan Vulture, River , Satyr Tragopan, Yellow-rumped Honeyguide and Ward’s Trogon) as per IUCN Red List have been recorded. The survey also recorded 57 migratory bird species as per Birdlife International. Of the forest types surveyed, highest species richness index was recorded in subtropical forest (17.4) followed by warm temperate (16.7), cold temperate (16.2), cool temperate (13.3), and rhododendron scrub (12.7). During the survey, five species were recorded as new species to the park (Wood Snipe, Yellow Wagtail, Pink-browed Rosefinch,and Spotted Bush Warbler) with one species being a new record for the country (Desert Wheatear). The large number of species recorded reveals the importance of the national park to serve as a critical habitat for birds. To conserve this rich bird diversity of the national park, we suggest better management of habitats through reduction in habitat destruction, conservation awareness programmes and enhanced monitoring of illegal activities.

1. Introduction

Birds are an important constituent of natural ecosystem and are a vital part of the food chain (Paulsch and Müller-Hohenstein, 2008; Whelan et al., 2008). Bird diversity and richness has been related to accessibility to open fields( Wuczynski´ et al., 2011; Zuria and Gates, 2012; Morelli, 2013), and forest edges (Batary et al., 2014), habitat fragmentation (Bhatt and Joshi, 2011), habitat quality

* Corresponding author. E-mail address: [email protected] (P. Dendup). https://doi.org/10.1016/j.gecco.2021.e01771 Received 12 March 2021; Received in revised form 16 August 2021; Accepted 20 August 2021 Available online 21 August 2021 2351-9894/© 2021 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license

(http://creativecommons.org/licenses/by-nc-nd/4.0/). P. Dendup et al. Global Ecology and Conservation 30 (2021) e01771

(Caprio et al., 2011), landscape changes (Wretenberg et al., 2010; Fischer et al., 2011; Morelli, 2013), farming systems (Morelli, 2013; Smith et al., 2014), types of vegetations (Kissling et al., 2010) and climate (Wuczynski´ et al., 2011; Zuria and Gates, 2012; Morelli, 2013). Birds are the indicator species to signal quality of forest habitats (Moning and Müller, 2008) and are responsive to habitat structure changes (MacArthur and MacArthur, 1961) and are thus helpful guides to conservation management at regional and landscape levels (Canterbury et al., 2000; O’Connell et al., 2000). Anthropogenic activities in many parts of the world have resulted in large-scale habitat destruction, fragmentation, and degra­ dation. The deleterious effects on bird diversity warrants an assessment on the impacts of such activities on the ecosystem (Wiens, 1995; O’Connell et al., 2000; Chettri et al., 2001; McLaughlin, 2011; Bregman et al., 2014). The eastern Himalaya is an area known for rich biodiversity (CEPF, 2005; CEFP, 2007), encompassing three distinct biogeo­ graphical realms: Indo-Malayan, Palaearctic, and Sino-Japanese. The Himalayan mountain system is known for its remarkable bio­ logical diversity (Sinha et al., 2019), and the eastern Himalaya in particular is identified as a Priority I Endemic Bird Area (Birdlife International, 2001). The region supports 22 restricted-range bird species (Stattersfield et al., 1998; Jathar and Rahmani, 2006; Acharya and Vijayan, 2010) and represents one of the largest accumulations of globally threatened birds in Asia (Acharya and Vijayan, 2010). Bhutan is nestled in the heart of the eastern Himalaya and is a biodiverse region recognized as a conservation priority area (Olson and Dinerstein, 1998; Stattersfieldet al., 1998; Myers et al., 2000; Hoekstra et al., 2005). More than half (51.44%) of the country’s total geographical area is under a protected area network consisting of five national parks, four wildlife sanctuaries, one strict nature reserve, one botanical park and eight biological corridors (DoFPS, 2011). Protected areas have been established for protection of globally threatened species, ecosystem restoration, recreation and help sustain ecosystem services to the communities (Oli et al., 2013). Encompassing an area of 4374.06 km2 in the northwestern part of the country, Jigme Dorji National Park (JDNP) is the second- largest protected area in Bhutan. The park is the ecosystem representation of the upper Himalayan region, Palearctic biogeographic realm and is known for diverse ecological and altitudinal gradients providing habitat to a rich diversity of floraand fauna, including birds (Thinley et al., 2014). Of 23 Important Bird and Biodiversity Areas (IBA) in the country, JDNP is the largest (390,000 ha) IBA in Bhutan known to provide safe home to critically endangered (CR) species such as the White-bellied Heron Ardea insignis and en­ dangered (EN) Pallas’s Fish Eagle Haliaeetus leucoryphus (BirdLife International, 2021). At the landscape level, the JDNP provides connectivity to Jigme Khesar Strict Nature Reserve (JKSNR), Jigme Singye Wangchuck National Park, Wangchuck Centennial National Park and Royal Botanical Park. In the realm of international transboundary conservation, JDNP provides crucial connectivity to the Kanchenjunga Conservation Complex in northeast and eastern via JKSNR (NCD, 2008) (Fig. 1). The study aimed to answer the following questions: (1) What are the different types of bird species present in the national park; (2) Which forest type has the maximum bird diversity; and (3) What are the existing conservation threats to birds in JDNP?

Fig. 1. Location of study site. (a) Location of Bhutan in , situated between in the North and India in the South. (b) Kan­ chenjunga Landscape encompassing parts of Nepal, Bhutan and India. (c) Protected area network of Bhutan. Protected areas in blue colour and biological corridors in rose colour. JDNP: Jigme Dorji National Park, WCNP: Wangchuck Centennial National Park, JSWNP: Jigme Singye Wangchuck National Park, RMNP: Royal National Park, PNP: Phrumsengla National Park, BWS: Bomdeling Wildlife Sanctuary, SWS: Sakteng Wildlife Sanctuary, JWS: Jomotsangkha Wildlife Sanctuary, PWS: Phibsoo Wildlife Sanctuary, JKSNR: Jigme Khesar Strict Nature Reserve, RBP: Royal Botanical Park. (d) The elevation map of JDNP.

2 P. Dendup et al. Global Ecology and Conservation 30 (2021) e01771

2. Methods

2.1. Study area

JDNP spatially extending 27o33’N–28o15’N and 89o14’E–90o22’E (Fig. 1) with a varied altitudinal gradient (1200 to >7000 m) has rich biodiversity (Thinley et al., 2014) within the fivemajor ecosystem types classifiedfor Bhutan (Ohsawa, 1987). The fivemajor forest types are subtropical forest (ST) (1000–2000 m), warm temperate forest (WT) (2000–2500 m), cool temperate forest (CT) (2500–3000 m), subarctic/cold temperate forest (CO) (3000–4000 m) and rhododendron scrub (RS) (>4000 m) (Fig. 2). JDNP is considered as the water tower of Bhutan as the four primary river systems of the country The Pachu, The Wangchu, The Phochu and The Mochu, originate from within the park. The park has four distinct seasons: winter (December - February); spring (March–May); summer (June–August); and autumn (September - November). JDNP is rich in floral and faunal diversity. The past management plan has documented over 1434 vascular plants, 50 mammal species, 313 bird species, 22 reptiles, 15 amphibians, 87 butterflies, and 17 dragon and damselflies (Thinley et al., 2014). Recently, Dendup et al. (2020) reported the presence of 371 bird species in the park. After the publication of “Birds of Jigme Dorji National Park: A photographic fieldguide for the park visitors” (Dendup et al., 2020), 36 additional species of birds have been recorded. As of today, the total bird species count for the park stands at 407 (Dendup et al., 2021). The recording of globally threatened species such as one CR species (White-bellied Heron Ardea insignis), two EN species (Pallas’s Fish Eagle Haliaeetus leucoryphus and Steppe Eagle Aquila nipalensis), three vulnerable (VU) species (Black-necked Crane Grus nigricollis, Chestnut-breasted Partridge Arborophila mandellii and Wood Snipe nemoricola) and seven near-threatened (NT) species (Bearded Vulture Gypaetus barbatus Himalayan Vulture Gyps himalayensis, Northern Lapwing vanellus, River Lapwing Vanellus duvaucelii, Satyr Tragopan Tragopan satyra, Yellow-rumped Honeyguide Indicator xanthonotus and Ward’s Trogon Harpactes wardi) and other charismatic pheasants like Himalayan Monal Lophophorus impejanus and Blood Pheasant Ithaginis cruentus only indicates the importance of the national park in context of bird conservation in the country (Dendup et al., 2020, 2021; IUCN, 2021).

2.2. Field survey and data collection

We identified and traversed 384.96 km of existing trails and 156.96 km of district and feeder roads (hereafter, trails and roads known as transects) across five different forest types within the altitude of 1300–5100 m as our transect to survey birds in JDNP (Fig. 2). The bird survey was carried out in November - December 2019 in the lower elevations and September - October 2020 in the higher elevations. The lower elevation transects primarily sampled bird species representation for the central, south, and southeastern parts of

Fig. 2. Survey transects (dotted lines represents existing trails and solid dark lines represents roads) across different forest types in JDNP. The five major ecosystem types are based on classifications made for Bhutan (Ohsawa, 1987).

3 P. Dendup et al. Global Ecology and Conservation 30 (2021) e01771 the park while the high elevation transects sampled northwestern, west, north, north-central and northeastern parts of the park. The survey was not carried out continuously across all seasons because from January – mid April, most of the passes remain blocked due to heavy snow. While in the monsoon season, bird detectability is affected by heavy rainfall. MacKinnon species listing method was used as the method is considered time-efficient,cost-effective and numerous lists of species can be collected from one-time rapid assessment for birds (MacKinnon and Phillipps, 1993; DoFPS, 2020). The MacKinnon method however is not suitable for estimating species densities or for estimating populations (Bibby et al., 2000). Two types of listings were done for different habitats. In the case of ST, WT and CT, 20 bird species were listed in chronological order of detection with no repetitions of species, while in CO and RS, 10 species were listed following same protocol as in ST, WT and CT. Due to rain and foggy weather, different timing was used to collect data (for ST 8.00 AM–5.00 PM, WT 6.00 AM–5.00 PM, CT 7.00 AM–5.00 PM, CO 6.00 AM–6.00 PM, and RS 6.00 AM–5.00 PM). The survey team used a pair of binoculars (Nikon Aculon A211 8 ×42) for bird scanning and identification, and a Garmin etrex 20x for collecting location and altitude information. The field surveyors received extensive training on field survey and data recording methodology both before and during survey works. Training on fieldsurveys included, but was not restricted to, techniques for identificationand detection of birds, forest types identification and strategies to minimize surveyors’ effect on bird detection. The data recording training included appropriate adoption of MacKinnon bird listing methods and fillingin data forms. The training was provided irrespective of fieldsurveyors ’ level of experiences. To effectively record the species inhabiting a habitat, direct sighting of birds and indirect evidence (seasonal call, mating and breeding calls, alarm calls, feathers, dead remains, and droppings) were used. For direct sighting, species were identified and the number counted and recorded. In the case of indirect signs, we identifiedthe species while recording only one individual against the species identified. Species identificationwas based on the fieldguide book to the Birds of Bhutan (Inskipp et al., 1999), a fieldguide book to the Birds of the Indian Subcontinent (Grimmett et al., 2011) and Birds of Jigme Dorji National Park: A photographic fieldguide for the park visitors (Dendup et al., 2020). Recent changes in species have been adopted from Grimmett et al. (2019). In the case of bird calls, pre-recorded bird songs were used for species identification (Bird Songs of Bhutan, produced by UWICER).

2.3. Data analysis

Using survey data, analysis on (a) richness index (R1), (b) diversity index (H’), and (c) cumulative species accumulation richness in each ecosystem was carried out. We performed logistic regression using Poisson distribution to model bird abundance as a function of altitude to predict the altitude at which there is maximum bird abundance. A similar logistic regression of bird abundance as a function of survey efforts was carried out to study if more survey effort led to the detection of more bird abundance. Statistical analysis was carried out in R v. 3.5.1 (R Core Team, 2018).

2.3.1. Richness index (R1) The Richness index is the total number of species in a community, and where the value depends on the sample size of the area and the survey effort to achieve it. The Richness index (R1) is calculated using the Margalef equation (Margalef, 1958).

R = (S-1)(1)/Ln(N) (1)

Where: R: index of species richness. S: number of species observed. N: number of individuals (all species observed). Ln: natural logarithm value. There are three classifications of Margalef richness index values namely low species richness (R < 2.5), medium species richness (2.5 > R < 4) and high species richness (R > 4). For the five major ecosystem types covered during the survey, species richness accumulation curves were generated using ecosystem type as a function of total time of the survey (cumulative effort). Species richness is thus assumed as an approximate number of different bird species present in an ecosystem during the period of the survey. The data were processed using Microsoft Excel.

2.3.2. Diversity index (H’) Diversity index is intended to determine the distribution of individuals between types found, assuming; H’= Zero if there is only one type in the sample data collected, and H’ = Maximum if there are as many types as possible. Diversity index (H ’), using the Shannon - Weiner equation (Shannon and Weaver, 1963) ni ni H′ = Σ log N N (2) Where: H’ = the Shannon diversity index. ni = number of individuals of the species. N = number of individuals of species.

4 P. Dendup et al. Global Ecology and Conservation 30 (2021) e01771

There are three classifications; low diversity (H’ < 1), medium diversity (1 > H’ < 3) and high diversity (H’ > 4).

2.3.3. Ecosystem templates used Ecosystem and habitat types were identified using the ecosystem classification developed by Oshawa (1987) (Table 1).

3. Results

3.1. Bird diversity and significance of JDNP

The bird survey in JDNP was completed by trekking and enumerating data through five major forest types along an altitudinal gradient of 1300 – 5100 m. The cumulative survey effort was 644.56 hrs and the total transect length was 535.92 km (Table 2). The current survey recorded 12363 individuals, across 272 bird species belonging to 143 genera and 59 families. Of the 272 identifiedbird species, 57 were migratory species (BirdLife International, 2021; Additional file1). The mid-altitude ranges represented highest species richness with the maximum number of species ranging between 2000 and 3000 m (156 species belonging to 94 genera and 45 families), followed by the range between 3000 and 4000 m (137 species belonging to 79 genera and 41 families), and finallythe range between 1300 and 2000 m (135 species belonging to 85 genera and 45 families). The least number of species (110 species belonging to 65 genera and 31 families) were found in the highest range (4000–5100 m). Such higher numbers in mid-altitudes and lower numbers towards lower and higher altitude suggest a unimodal relationship between species richness and altitude (Fig. 3). The current survey at the national level recorded six totally protected species (Arborophila mandellii, Tragopan satyra, Gallinago nemoricola, Corvus corax, Harpactes wardi and Lophophorus impejanus) listed in Schedule I (Sch 1) of the Forest and Nature Conservation Act (FNCA) of Bhutan, 1995. In global context, two VU species (Arborophila mandellii and Gallinago nemoricola) and six NT species (Gypaetus barbatus, Gyps himalayensis, Vanellus duvaucelii, Tragopan satyra, Indicator xanthonotus and Harpactes wardi) were recorded. The survey recorded five bird species new to the park with one being new to the country and they are; Yellow wagtail Motacilla flava, Wood Snipe Gallinago nemoricola, Desert Wheatear Oenanthe deserti (new to the country), Pink-browed Rosefinch Carpodacus rodochroa, and Spotted Bush Warbler Bradypterus thoracicus.

3.2. Richness index

The Margalef Richness Index Value (R1) revealed that all the forest types had high species richness. The richness index value indicated that the ST forests (17.41) supported the highest number of bird species richness. The WT forests ecosystem (16.67) is the second richest in supporting birdlife, followed by CT (16.18), CO (13.29) and RS (12.71). In the case of species abundance, RS (3571) had the highest followed by CO (3487) forest. CT forest had the lowest species abundance (940) (Fig. 4). The three most abundant species (Snow Pigeon, Alpine Chough and Black-faced Laughingthrush) ranged between 400 and 800 observed individuals and accounted for 15.56% of the total bird abundance. Thirteen species were observed between 200 and 300 individuals (Rufous-vented Tit, Large-billed Crow, Red-billed Chough, Green-backed Tit, Olive-backed Pipit, Stripe-throated Yuhina, White-throated Laughingthrush, Nepal Fulvetta, Grey-crested Tit, Blood Pheasant, Rufous-winged Fulvetta, Black Bulbul, Striated Laughingthrush) accounting for 25.58% of the total bird abundance. Sixty-two species, representing 22.30% of total bird abundance had two or fewer individuals detected and are some of the rarest species in the park. Among these rare species are Chestnut-breasted Partridge, Ward’s Trogon, River Lapwing, Long-tailed Shrike, Grey-capped Pygmy Woodpecker, Asian Brown Flycatcher, Asian-barred Owlet, Tibetan Blackbird, Common Quail, Brown , Desert Wheatear, Indian Pond Heron, Pheasant-tailed Jacana, Wood Snipe, Solitary Snipe, Lesser Yellownape, Northern Goshawk, Snowy-browed Flycatcher, Slaty-bellied Tesia, Lesser Coucal, Eurasian , Great , Brown Wood-owl, Blue-bearded Bee-eater, Black-crowned Night-heron, Black-chinned Yuhina and Bonelli’s Eagle. The overlap of lower altitude species was high towards mid-altitude (2000 – 3000 m) but gradually decreased with an increase in altitude (Table 3). Eighteen species (6.47% of the total bird abundance) were most common and are found widely distributed across the whole forest ecosystem with species under the family Muscicapidae as most dominant (Table 4). The bird abundance was highest around 3200 – 3300 m altitude, decreasing with increasing altitude (Table 5).

Table 1 Forest types and vegetation communities in different altitudes.

Broad Forest Types Altitude Vegetation communities (m)

Subtropical forest (ST) 1000–2000 Castanopsis tribuloides, Schima wallichii, Quercus glauca, Lithocarpus elegans, Q. semiserrata, Castanopsis hystrix, Litsea elongata, Quercus lamellosa, Persea clarkeana, Pinus roxburghii Warm temperate forests (WT) 2000–2500 Castanopsis hystrix, Quercus lamellosa, Q. semiserrata, Lithocarpus elegans, Acer campbelii, Magnolia campbelii, Sorbus cuspidata, Alnus nepalensis, Quercus griffithii, Rhododendron arboretum, Schima wallichii Cool temperate forests (CT) 2500–3000 Tsuga dumosa, Picea spinulosa, Pinus wallichii, Quercus semecarpifolia, Acer campbellii Cold temperate (subarctic) 3000–4000 Abies densa, Juniperus recurva, J. indica, J. squamata, Larix grifithii, Cupressus corneyana forests (CO) Rhododendron scrub (arctic) >4000 Rhododendron nivale, R. setosum. R. anthopogon, R. lepidotum forests (RS)

5 P. Dendup et al. Global Ecology and Conservation 30 (2021) e01771

Table 2 Information on the area, survey effort, transect length and altitude in each forest type.

Variables Subtropical Warm Temperate Cool Temperate Cold Temperate Rhododendron Scrub

Area (square km) 66.26 143.47 208.34 835.14 1596.87 Total hours surveyed 74.59 70.44 61.18 192.06 246.29 Transect length (km) 60.52 61.68 20.91 148.38 244.44 Alt_m (Min) 1351 2002 2503 3040 4001 Alt_m (Max) 1998 2498 2997 4000 5094

Fig. 3. Total number of bird individuals represented by Family, Genera and Species across altitudinal gradient in Jigme Dorji National Park.

Species abundance was positively dependent on survey effort, with more survey efforts leading to detection of a greater number of individuals (y = 11.47x + 993.59, r2 = 0.72, n = 4, p < 0.05) (Fig. 5).

3.3. Species richness in each ecosystem

Species richness was highest in ST (135) followed by CO (133), WT (129), RS (105) and CT (92). The cumulative species richness curve for each forest type is shown in Fig. 6.

3.3.1. Subtropical forest ecosystem (1000–2000 m) The ST forest ecosystem is the smallest forest ecosystem represented in the park. It covers an area of 66.26 km2 corresponding to 1.51% of the total park area within an elevation range of 1351–1998 m. In the ST zone, a total of 135 bird species including Chestnut- breasted Partridge Arborophila mandellii (VU, Sch1) and Yellow-rumped Honeyguide Indicator xanthonotus (NT) were recorded. The cumulative species richness curve (Fig. 6) does not approach asymptote, indicating that more bird species would be found in this ecosystem.

3.3.2. Warm temperate forest ecosystem (2000 – 2500 m) The WT forest ecosystem is the second smallest forest ecosystem represented in the park. It covers an area of 143.47 km2 corre­ sponding to 3.28% of the total park area within an elevational range of 2002–2498 m. A total of 129 bird species inclusive of River Lapwing Vanellus duvaucelii (NT), Lemon-rumped Honeyguide Indicator xanthonotus (NT), Ward’s Trogon Harpactes wardi (NT, Sch1) and Satyr Tragopan Tragopan satyra (NT, Sch1) were recorded during the survey. The cumulative species richness curve (Fig. 6) somewhat approaches asymptote and flattens, indicating that the survey was reasonably complete.

6 P. Dendup et al. Global Ecology and Conservation 30 (2021) e01771

Fig. 4. A total number of bird species detected in each family across different forest types.

3.3.3. Cool temperate forest ecosystem (2500–3000 m) The CT forest ecosystem of the JDNP has coverage of about 208.34 km2 corresponding to 4.76% of the total park area within an elevational range of 2503–2997 m. It is the third-largest ecosystem available in the park but has the lowest bird diversity as compared with the other four ecosystems represented in the park. A total of 92 species of birds were recorded with Satyr Tragopan Tragopan satyra (NT, Sch1) and Chestnut-breasted Partridge Arborophila mandellii (VU, Sch1). Here too, the cumulative species richness curve (Fig. 6) almost approached asymptote, which indicates that very minimal or no new bird species would be found in this ecosystem with an increase in survey effort.

7 P. Dendup et al. Global Ecology and Conservation 30 (2021) e01771

Table 3 The number of lower altitude species overlap with high altitude species. The bold figures are the total species detected in each habitat.

Number of species overlap across habitat type

Habitat Type ST (1000 – 2000 m) WT (2000–2500 m) CT (2500–3000 m) CO (3000–4000 m) RS (>4000 m)

ST (1000–2000 m) 135 84 62 46 29 WT (2000–2500 m) 129 67 58 39 CT (2500–3000 m) 92 49 33 CO (3000–4000 m) 133 83 RS (>4000 m) 105

Table 4 Most common and widely distributed bird species across habitat in the national park.

Family Common name Scientific name Individuals detected

Muscicapidae Blue-fronted frontalis 187 Blue Whistling Thrush Myophonus caeruleus 53 Plumbeous Water Redstart Rhyacornis fuliginosus 38 Phylloscopidae Lemon-rumped Warbler Phylloscopus chloronotus 127 Tickell’s Leaf Warbler Phylloscopus affinis 86 Leiothrichidae Black-faced Laughingthrush Garrulax affinis 442 Corvidae Large-billed Crow Corvus macrorhynchos 287 Motacillidae Olive-backed Pipit Anthus hodgsoni 258 Oriental Turtle Dove Streptopelia orientalis 85 Muscicapidae White-capped Water Redstart Chaimarrornis leucocephalus 83 Prunellidae Rufous-breasted Accentor Prunella strophiata 60 Motacillidae Rosy Pipit Anthus roseatus 54 Nectariniidae Green-tailed Sunbird Aethopyga nipalensis 50 Dusky Warbler Phylloscopus fuscatus 28 Cettiidae Chestnut-crowned Bush Warbler Cettia major 21 Cinclidae Brown Dipper Cinclus pallasii 20 Fringillidae Dark-breasted Rosefinch Carpodacus nipalensis 19 Accipitridae Eurasian Sparrowhawk Accipiter nisus 14

Table 5 Summary of logistic regression (Poisson distribution) models indicating mean beta, standard errors (SE) of beta, lower CI and upper CI for altitude influencing bird abundance.

Parameters Mean β SE (β) 2.50% 97.50%

(Intercept) 2.398 9.595 2.209 2.585 Altitude 1.502 6.689 1.94 2.816 Altitude^2 -3.347 1.07 -5.449 -1.254

Fig. 5. The abundance of birds increases with the increase in survey effort. Star represents the total number of individuals detected.

8 P. Dendup et al. Global Ecology and Conservation 30 (2021) e01771

Fig. 6. Cumulative species richness curve obtained as a result of cumulative hours surveyed in each different habitat in two seasons.

3.3.4. Cold temperate forest ecosystem (3000–4000 m) The CO forest ecosystem is the second largest ecosystem coverage represented in the park. It covers an area of 835.14 km2 cor­ responding to 19.09% of the total park area from the elevation of 3040 – 4000 m. A total of 133 species were recorded including Vulture Gypaetus barbatus (NT), Himalayan Vulture Gyps himalayansis (NT), Satyr Tragopan Tragopan satyra (NT, Sch1), Wood Snipe Gallinago nemoricola (VU, Sch1) and Himlayan Monal Lophophorus impejenus (Sch1). The cumulative species curve is fully asymptotic and thus indicates that this ecosystem has been thoroughly surveyed and no new species will be detected with an increase in survey effort (Fig. 6).

3.3.5. Rhododendron scrub ecosystem (>4000 m) RS ecosystem is the largest in the park with 1596.87 km2 corresponding to 36.55% within an elevation range of 4001–5094 m. In this ecosystem, the bird species recorded is second lowest with only 105 species. Bearded Vulture Gypaetus barbatus (NT), Himalayan Vulture Gyps himalayansis (NT) and Northern Raven Corvus corax (Sch 1) have been recorded in the ecosystem. However, the cu­ mulative species richness curve (Fig. 6) continues to rise, and this indicates that with more survey efforts, more new species are ex­ pected. The RS ecosystem is also reported to host the majority of dead tree snags which are very useful as wildlife habitat.

3.4. Diversity index

The Shannon-Weiner Diversity Index (H’) value revealed that CT forest (4.82) had the highest bird diversity, followed by WT (4.02) and ST (4). CO forest (3.87) and RS forest (3.60) had medium species diversity.

4. Discussion

The significance and importance of the park for birdlife conservation is enormous. Besides recording two VU and six NT species during the current study, the park has additionally recorded one CR species Ardea insignis, two EN species Haliaeetus leucoryphus and Aquila nipalensis, one VU species Grus nigricollis and one NT species Vanellus vanellus. The national park has a total of 407 species accounting for approximately 55% of the country’s total bird species (Dendup et al., 2020, 2021). The presence of the relatively higher number of globally threatened species (13 species) and >50% of the country’s bird species in the JDNP indicates that the mosaic of forest ecosystems at varying altitude are essential habitat for bird survival. JDNP has 1% of the total area under water bodies, 12% under broadleaf forest, 34% conifer forest, 33% snow cover and glaciers and 20% scree and rock outcrops (Thinley et al., 2014; Dendup et al., 2021). Each of these habitats may be preferred by different bird species across different seasons. The presence of 57 migratory species observed in this study reveals the importance of JDNP to serve as critical winter or summer grounds. Tadorna ferruginea, the winter visitor of the park, comes in highest abundance while the low land bird Hydrophasianus chirurgus is the summer visitor, recorded at two occasions at an altitude above 4000 m. Birds migrate between different spatial area in response to climate change, avoidance of harsh winters, site productivity, connectivity to breeding grounds and dietary preferences (Newton, 2008; Somveille et al., 2015).

9 P. Dendup et al. Global Ecology and Conservation 30 (2021) e01771

Habitats in the lower elevations had high bird richness and diversity, increasing until the mid-altitude (2000 – 3000 m), followed by a gradual decline towards the higher elevations. Our results were consistent with the commonly reported unimodal relationship between species richness and altitude (Colwell et al., 2008; McCain and Grytnes, 2010; Basnet et al., 2016). The maximum predicted bird richness occurred approximately at 3200 – 3300 m. The recording of high species richness and diversity in the lower elevation may be related to the ideal biophysical environment such as warm temperature, better nesting sites, habitat diversity (including agriculture farms), availability of food, and better cover from predators (Rahbek, 2005; McCain, 2009). Abundant agricultural farmlands may provide ample opportunity for birds to efficientlyforage at these lower elevations. The lower- to mid-latitude area of the national park has diverse vegetation cover, agricultural land, and hot-warm climatic conditions, all also possibly contributing to species richness. The meteorological data in the park for last 10 years (2010 – 2020) revealed that the park experienced an average of minimum 0.7 oC to a maximum of 20.93 oC with an average rainfall of low 0.1 millimeters (mm) to high of 9.7 mm (Dendup et al., 2021) which in turn has provided birds with ideal climatic conditions. Many fruit-bearing trees and floweringvegetations are planted along these altitudes providing abundant food for the bird populations. Most of the threatened bird species such as Satyr Tragopan, Yellow-rumped Honeyguide, River Lapwing, Ward’s Trogon, and Chestnut-breasted Partridge are recorded below 3200 m and therefore, forest ecosystem within these altitudes should be conserved. The decrease in species richness and abundance in higher altitude could be due the decrease in temperature and vegetation resulting from shorter growing seasons, and low availability of food and nesting sites (Herzog et al., 2005; Basnet et al., 2016; Katuwal et al., 2016). However, proper management of forest habitats above 3000 m should also be taken into consideration as they too shelter other threatened bird species such as Himalayan Monal, Himalayan Vulture, Bearded Vulture and Wood Snipe. Species abundance was positively and significantlydependent on survey efforts. More survey effort resulted in a higher number of species detected. For an average of 129 h of survey effort, we predict that about 2474 individuals of birds could be observed in JDNP. However, the result of the species cumulative accumulation curve indicates the incompleteness of the current survey. Except for CO forest, none of the species’ richness curves appropriately approach asymptote, meaning that each of the remaining forest types were under-sampled in this survey. Dendup et al. (2021), reported a total number of bird species of 407 in the national park, suggesting that the current bird survey has under-recorded species richness by 33.16%. However, it must be understood that such gaps will remain inherent in future surveys as well because species detection is dependent on time (survey time and seasonality), space (habitat use by species and movement, behavioral characteristic of species) and observer’s fatigue (Lardner et al., 2019). Repeated surveys during different seasons will help fillsuch knowledge gaps. It is expected that the bird diversity checklist for JDNP will continue to increase with continued survey, albeit at a lower rate than in previous reports as the preponderance of species have likely already been identifiedto date. As MacArthur and Wilson (1967) reported that the factors determining bird diversity within the given area include (but not limited to) vastness of the space, diversity in habitat, degree of isolation and disturbance, it is possible that the species number does not increase as the landscape changes.

4.1. Threats to bird conservation

Regardless national and global significance, the national park is faced with numerous challenges for biodiversity conservation. JDNP has 975 households with 5026 people living inside the national park leading to a population density of 21.68 people per square kilometer (Dendup et al., 2021). Habitat loss and fragmentation is the major threat to declining population of birds around the globe (Crosby, 1996; Pandit et al., 2007). In JDNP too, habitat loss and fragmentation as a result of inevitable development activities and demand on natural resources poses the greatest threat to wildlife conservation, including birds. In the period June 2020 – July 2021, JDNP has lost 52.813 ha of forest land for various developmental activities (Dendup et al., 2021). In the last fiveyears (2016 – 2020) a total of 33,937.38 cubic meters of timber and firewoodhas been supplied from the national park to the urban and rural communities living within the national park (Dendup et al., 2021). It is well known that forestland provides the most important bird habitat, globally accounting for 75% of all species while human-modified habitats are home to only 45% of the bird species (Birdlife International, 2008). In the current study, forestland had 48.11% of bird individuals recorded followed by shrubs (25.14%) and grassland (12.11%). The fewest number of birds were found around human habitation (0.11%). Continued unsustainable harvesting of natural resources from the forest can cause changes in vegetation structure and composition, leading to landslides and opening up of barren areas. This will in turn affect occupancy and resource use patterns of birds (Chettri et al., 2005). Poaching of wildlife, especially the musk deer is quite common in the park. Given the large size of the park (11.39% of the country’s size) and despite regular patrolling activities carried out by the park officials,musk deer traps are still encountered while on patrol. In the year 2016, a total of 400 musk deer snares were removed and two poachers apprehended by the park staff (Dendup et al., 2018). Musk deer traps and snares can also pose a serious threat to ground dwelling birds (Galliformes) such as Himalayan Monal Lophophorus impejenus, Blood pheasant Ithaginis cruentus, Kalij Pheasants Lophura leucomelanos and Satyr Tragopan Tragopan satyra. There are reports of Monal Pheasants getting trapped and killed in the musk deer snares (Dendup et al., 2018). The use of snares is reported to have high negative conservation implication as wildlife of any form are killed indiscriminately (Dendup et al., 2018). Fishing along the rivers of JDNP (Pachu, Wangchu, Mochu, Phochu and their tributaries) is also one of the major concerns for waterbird survival. In particular, Mochu and Phochu are reported to host the biggest and oldest known population of critically en­ dangered White-bellied Heron Ardea insignis in Bhutan (The Thrid Pole, 2021). Over fishingin these two rivers is of great concern to conserving White-bellied Heron as it results to loss of prey.

10 P. Dendup et al. Global Ecology and Conservation 30 (2021) e01771

4.2. Current conservation efforts

Despite JDNP being one of the most important landscapes for biodiversity conservation in the country and the region, the park is also under pressure from the increasing demand on natural resources. JDNP is one of the national parks in Bhutan incorporating the highest number of local communities. Because of the pressures on wildlife (including birds), the park management has devised several conservation efforts to protect threatened species and their habitat. JDNP has very recently revised its management plan giving top priority to monitoring of threatened species and habitat (Dendup et al., 2021) with several management zones created for more effective conservation. Four different zones, namely core zone (28.10%), transition zone (40.72%), multiple use zone (19.49%) and buffer zone (11.69%), have been designated in the park (JDNP, 2021). Given the presence of globally threatened species in the park, JDNP has also been identified as one of the largest IBAs in Bhutan (BirdLife International, 2021). Strong government policies, especially the Forest and Nature Conservation Act of Bhutan, 1995, and Forest and Nature Conser­ vation Rules and Regulations of Bhutan, 2017, provide a powerful legal framework for protecting and managing wildlife and habitat (DoFPS, 2017). Article 5 of the Constitution of Bhutan further emphasizes the requirements to maintain at least 60% of the total land under forest cover for all times to come (RGoB, 2009).

4.3. Conclusion

The forests of JDNP are an important habitat for a majority of bird species. However, these forests are vulnerable to over- exploitation as a result of increasing demand for firewood and timbers. The timber requirement and access to other natural re­ sources cannot be denied to the residents of the park; however, better-informed decisions have to be made by the park management and fieldlevel officials, especially while allotting standing trees and other NWFPs. While best-practiced silviculture must be applied during the marking of trees, individual trees must be assessed for nest cavities as these are potential nesting sites for owls and woodpeckers. In higher altitudes, many snag trees have been recorded. There is an utmost need to avoid allotting snags as firewoodto the local communities as they provide ideal micro habitat for owls and woodpeckers. Fruit- and cone-bearing tree species (Abies, Tsuga, Pinus, Persia, Morus) have to be cautiously marked for timber and firewoodas these trees are the main source of food for most of the frugivore birds. JDNP is home to many bird species in the country and the national park has been identifiedas one of the IBAs for providing safe home to critically endangered White-bellied Heron Ardea insignis and endangered Pallas’s Fish Eagle Haliaeetus leucoryphus (BirdLife International, 2021). With the recording of Black-necked Crane Grus nigricollis, Chestnut-breasted Partridge Arborophila mandellii, and Wood Snipe Gallinago nemoricola (Dendup et al., 2021), there is a need for Birdlife International to update the list of threatened species in the national park. Global conservation organizations such as Birdlife International should allocate resources and effort to areas such as JDNP to intensify successful conservation of bird species. Management of habitats and periodic monitoring of bird populations is very important to place strategic management prescription by the park management to help sustain bird population in the lanscape. Timely awareness programs on the importance of conserving birds and their habitat should also be provide to the communities residing in the national park.

5. Data limitations

Field data were collected at all times of the day; however, there are some limitations and imbalances in the data. In particular, because most of the data were collected during the day time, birds with nocturnal behaviour (such as owls and nightjars) are under- represented. Information on birds across the season is also under-represented as the current study was conducted from September through December. Furthermore, as most part of the national park is inaccessible due to rugged terrain, our survey transects have been along the existing trails and roads. Due to non-random sampling design, the findingsof bird diversity in different habitats in JDNP in the current study may be biased and under-represented. However, to minimize species richness biasness in the park from the current survey, we mentioned about the total number of bird species recorded till date. Information on total bird species of the park was collected from the current and past surveys. Except for the data collected from the current survey, we have not used the secondary data for analysis. Therefore, we request the viewers to draw a careful conclusion.

Declaration of Competing Interest

The authors declare that they have no known competing financialinterests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We would like to thank all our fieldstaff especially, Mr. Karma Jangchuk, Mr. Dawa Penjor and Mr. Norbu Jamtsho for their help during the fieldworks and arrangement of fieldlogistics. We would also like to thank Mr. Ugyen Penjor for guidance with statistical analysis. Special thanks to Ms. Anita Man and Mr. Shad Grunert for reviewing our revised manuscript. Finally, we would like to thank editor and the three anonymous reviewers for their invaluable comments which helped further refinethis manuscript. This bird study was funded by Bhutan For Life.

11 P. Dendup et al. Global Ecology and Conservation 30 (2021) e01771

Appendix A. Supporting information

Supplementary data associated with this article can be found in the online version at doi:10.1016/j.gecco.2021.e01771.

References

Acharya, B.K., Vijayan, L., 2010. Status and distribution of endemic and threatened birds of the Eastern Himalaya in , India. J. Threat. Tex. 2, 685–689. Basnet, T.B., Rokaya, M.B., Bhattarai, B.P., Münzbergova, Z., 2016. Heterogeneous landscapes on steep slopes at low altitudes as hotspots of bird diversity in a hilly region of Nepal in the central . PLoS ONE 11, e0150498. Batary, P., Fronczek, S., Normann, C., Scherber, C., Tscharntke, T., 2014. How do edge effect and tree species diversity change bird diversity and avian nest survival in Germany’s largest deciduous forest? For. Ecol. Manag. 319, 44–50. Bhatt, D., Joshi, K.K., 2011. Bird assemblages in natural and urbanized habitats along elevational gradient in Nainital district (western Himalaya) of Uttarakhand state, India. Curr. Zool. 57, 318–329. Bibby, C., Burgess, N., Hill, D., Mustoe, S., 2000. Bird Census Techniques. Academic Press, London. BirdLife International , 2021. Important Bird Areas fact sheet, 2021. http://www.birdlife.org/datazone/country/bhutan. (Accessed 27 July 2021). Canterbury, G.E., Martin, T.E., Petit, D.R., Petit, L.J., Bradford, D.F., 2000. Bird communities and habitat as ecological indicators of forest condition in regional monitoring. Conserv. Biol. 14, 544–558. Caprio, E., Chamberlain, D.E., Isaia, M., Rolando, A., 2011. Landscape changes caused by high altitude skipistes affect bird species richness and distribution in the Alps. Biol. Conserv. 144, 2958–2967. DoFPS, 2017. Forest and Nature Conservation Rules and Regulations of Bhutan, fourth ed. Ministry of Agriculture and Forests, Royal Government of Bhutan, Tashichho Dzong Thimphu. DoFPS, 2011. Forestry Development in Bhutan, Policies, Programmes and Institutions. Kuensel Corporation Limited, Bhutan. Bregman, T.P., Sekercioglu, C.H., Tobias, J.A., 2014. Global patterns and predictors of bird species responses to forest fragmentation: implications for ecosystem function and conservation. Biol. Conserv. 169, 372–383. CEPF , 2005. Ecosystem profile: Indo-Burma Hotspot, Eastern Himalayan region. Khatmandu: WWF, US-Asian Programme/Critical Ecosystem Partnership Fund. Chettri, N., Sharma, E., Deb, D.C., 2001. Bird community structure along a trekking corridor of Sikkim Himalaya: a conservation perspective. Biol. Conserv. 102, 1–16. Chettri, N., Jackson, R., Sharma, E., 2005. Birds of Khecheopalri and Yuksom-Dzongri trekking corridor west Sikkim. J. Hill Res. 18, 16–25. Colwell, R.K., Brehm, G., Cardelús, C.L., Gilman, A.C., Longino, J.T., 2008. Global warming, elevational range shifts, and lowland biotic attrition in the wet tropics. Science 322, 258–261. Crosby, M., 1996. Threatened birds in the eastern Himalayas. OBC Bull. 23, 21–23. Dendup, P., Namgay, N., Lham, C., 2018. Winter distribution and poaching of musk deer, Moschus chrysogaster and Moschus leucogaster in Jigme Dorji National Park, Bhutan. Int. J. Conservation Sci. 9, 193–198. Dendup, P. , Dorji, R. , Jamtsho, Y. , Wangchuk, W. , Tshering, B., Dorji, R. , 2021. Conservation Management Plan of Jigme Dorji National Park for the period July 2021 – June 2031. Biodiversity Conservation in Pursuit of Gross National Happiness. Dendup, P. , Dorji, S. , Dorji, R. , Wangdi, L. , Wangchuk, T. , Dorji, P. , Kuenzang, P. , 2020. Birds of Jigme Dorji National Park: A photographic fieldguide for the park visitors. Department of Forests and Park Services, Royal Government of Bhutan. DoFPS , 2020. Bhutan Bird Monitoring Protocol. Department of Forests and Park Services, Thimphu. Bhutan. Fischer, C., Flohre, A., Clement, L.W., Batary, P., Weisser, W.W., Tscharntke, T., Thies, C., 2011. Mixed effects of landscape structure and farming practice on bird diversity. Agric., Ecosyst. Environ. 141, 119–125. Grimmett, R., Inskipp, C., Inskipp, T., Allen, R., Bowley, A., Byers, C., Cole, D., Cox, J., Driessens, G., D’silva, C., Elliott, M., Franklin, K., Gale, J., Harris, A., Hayman, P., Nurney, D., Robson, C., Schmidt, C., Small, B., Wilczur, J., Worfolk, T., Woodcock, M., 2011. Birds of Indian Subcontinent. Christopher Helm, Soho Square, London, The United Kingdom. Grimmett, R., Inskipp, C., Inskipp, T., Sherub, 2019. Birds of Bhutan and the Eastern Himalaya. Christopher Helm, Soho Square, London,The United KingdoM. Herzog, S.K., Kessler, M., Bach, K., 2005. The elevational gradient in Andean bird species richness at the local scale: a foothill peak and a high-elevation plateau. Ecography 28, 209–222. Hoekstra, J.M., Boucher, T.M., Ricketts, T.H., Roberts, C., 2005. Confronting a biome crisis: global disparities of habitat loss and protection. Ecol. Lett. 8, 23–29. Inskipp, C., Inskipp, T., Grimmett, R., Byers, C., Cole, D., Cox, J., Driessens, G., D’Silva, C., Elliott, M., Frankling, K., Harris, A., Hayman, P., Robson, C., Wilczur, J., Worfolk, T., 1999. Birds of Bhutan. Christopher Helm, Soho Square, London, The United Kingdom. IUCN , 2021. The IUCN Red List of Threatened Species. Version 2020–3. 2021. https://www.iucnredlist.org. (Assessed 22 January 2021). Jathar, G.A., Rahmani, A.R., 2006. Endemic birds of India. Buceros 11, 5–53. JDNP , 2021. Management zones of Jigme Dorji National Park. Department of Forests and Park Services, Ministry of Agriculture and Forests. Damji, Gasa, Bhutan. Katuwal, H.B., Basnet, K., Khanal, B., Devkota, S., Rai, S.K., Gajurel, J.P., Scheidegger, C., Nobis, M.P., 2016. Seasonal changes in bird species and feeding guilds along elevational gradients of the central Himalayas, Nepal. PLoS One 11, e0158362. Kissling, W.D., Field, R., Korntheuer, H., Heyder, U., Bohning-Gaese, K., 2010. Woody plants and the prediction of climate-change impacts on bird diversity. Philos. Trans. R. Soc. B Biol. Sci. 365, 2035–2045. Lardner, B., Adams, A.A.Y., Knox, A.J., Savidge, J.A., Reed, R.N., 2019. Do observer fatigue and taxon bias compromise visual encounter surveys for small vertebrates? Wildl. Res. 46 (2), 127–135. MacArthur, R.H., MacArthur, J.W., 1961. On bird species diversity. Ecology 42, 594–598. MacArthur, R.H., Wilson, E.O., 1967. The theory of island biogeography. Monograph in Population Biology. Princeton University Press. MacKinnon, J. , Phillipps, K. , 1993. A field guide to the birds of Borneo: Sumatra. Margalef, R., 1958. Information theory in ecology. Gen. Syst. 3, 36–71. McCain, C.M., 2009. Global analysis of bird elevation diversity. Glob. Ecol. Biogeogr. 18, 346–360. McCain, C.M., Grytnes, J.-A., 2010. Elevational gradients in species richness. Encyclopedia of Life Sciences. John Wiley & Sons Ltd, Chichester, UK. McLaughlin, D.W., 2011. Land, food, and biodiversity. Conserv. Biol. 25 (6), 1117–1120. Moning, C., Müller, J., 2008. Environmental key factors and their thresholds for the avifauna of temperate montane forests. For. Ecol. Manag. 256, 1198–1208. Morelli, F., 2013. Relative importance of marginal vegetation (shrubs, hedgerows, isolated trees) surrogate of HNV farmland for bird species distribution in Central Italy. Ecol. Eng. 57, 261–266. Myers, N., Mittermeier, R.A., Mittermeier, C.G., Dafonseca, G.A., Kent, J., 2000. Biodiversity hotspots for conservation priorities. Nature 403, 853–858. Newton, I., 2008. The ecology of bird migration. Academic Press,, London, UK. Paulsch, D., Müller-Hohenstein, K., 2008. Bird species distribution along an altitudinal gradient in southern Equador and its functional relationships with vegetation structure. In: Beck, E., Bendix, J., Kottke, I., Makeschin, F., Mosandl, R. (Eds.), Gradients in a Tropical Mountain Ecosystem of Ecuador. Springer, Berlin Heidelberg, pp. 149–156. Rahbek, C., 2005. The role of spatial scale and the perception of large-scale species-richness patterns. Ecol. Lett. 8, 224–239. RGoB, 2009. The Constitution of the Kingdom of Bhutan. Kuensel Corporation Limited, Thimphu, Bhutan.

12 P. Dendup et al. Global Ecology and Conservation 30 (2021) e01771

NCD , 2008. Biological Corridor Strategic Plan (2008–2013). Jigme Kheser Stricty Nature Reserve – Jigme Dorji National ParkCorridor, Western Bhutan. Kuensel Corporation Limited, Thimphu, Bhutan. O’Connell, T.J., Jackson, L.E., Brooks, R.P., 2000. Bird guilds as indicators of ecological condition in the central Appalachians. Ecol. Appl. 10, 1706–1721. Ohsawa, M. (Ed.), 1987. Life Zone Ecology of Bhutan Himalaya, 1987. Chiba University, Yayoicho, Chiba, Japan. Oli, K.P., Chaudhary, S., Sharma, U.R., 2013. Are governance and management effective within protected areas of the Kanchenjunga Landscape (Bhutan, India and Nepal)? Parks 19 (1), 25–36. Olson, D.M., Dinerstein, E., 1998. The Global 200: a representation approach to conserving the Earth’s most biologically valuable ecoregions. Conserv. Biol. 12, 502–515. Pandit, M.K., Sodhi, N.S., Koh, L.P., Bhaskar, A., Brook, B.W., 2007. Unreported yet massive deforestation driving loss of endemic biodiversity in Indian Himalaya. Biodivers. Conserv. 16, 153–163. R Core Team , 2018. R: A language and environment for statistical computing. Vienna:Austria. https://www.R-project.org (Accessed 25 November 2019). Shannon, C.E., Weaver, W., 1963. The mathematical theory of communication. The University of Illinois Press, Illinois. Sinha, A., Hariharan, H., Adhikari, B.S., Krishnamurthy, R., 2019. Bird diversity along riverine areas in the Bhagirathi Valley, Uttarakhand, India. Biodivers. Data J. 7, e31588. Smith, A.C., Francis, C.M., Fahrig, L., 2014. Similar effects of residential and non-residential vegetation on bird diversity in suburban neighborhoods. Urban Ecosyst. 17, 27–44. Somveille, M., Rodrigues, A.S.L., Manica, L., 2015. Why do birds migrate? A macroecology perspective. Glob. Ecol. Biogeogr. 1–11. Stattersfield, A.J., Crosby, M.J., Long, A.J., Wege, D.C., 1998. Endemic bird areas of the world: priorities for biodiversity conservation. BirdLife Conservation Series No. 7. BirdLife International, Cambridge. The Thrid Pole , 2021. World’s rarest heron on the brink in its last Himalayan stronghold. https://www.thethirdpole.net/en/nature/white-bellied-heron-threatened- in-bhutan/?__cf_chl_captcha_tk__=pmd_fe1e8685c758d977811ed404316d14bf4b76af2c-1628318047–0-gqNtZGzNAvijcnBszQii (Accessed 7 August 2021). Thinley, P. , Tharchen, L. , Dorji, R. , 2014. Conservation management plan of Jigme Dorji National Park for the period January 2015 – December 2019: Biodiversity conservation in pursuit of Gross National Happiness. Department of Forests and Park Services, Thimphu: Bhutan. Whelan, C.J., Wenny, D.G., Marquis, R.J., 2008. Ecosystem services provided by birds. Ann. N.Y. Acad. Sci. 1134, 25–60. Wiens, J.A., 1995. Habitat fragmentation: island v landscape perspectives on bird conservation. IBIS 137, 97–104. Wretenberg, J., Part, T., Berg, Å., 2010. Changes in local species richness of farmland birds in relation to landuse changes and landscape structure. Biol. Conserv. 143, 375–381. Wuczynski,´ A., Kujawa, K., Dajdok, Z., Grzesiak, W., 2011. Species richness and composition of bird communities in various fieldmargins of Poland. Agric., Ecosyst. Environ. 141, 202–209. Zuria, I., Gates, J.E., 2012. Community composition, species richness, and abundance of birds in field margins of central Mexico: local and landscape-scale effects. Agrofor. Syst. 87, 377–393.

13