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Bird diversity and conservation threats in Jigme Dorji National Park, Bhutan

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  • Jigme Dorji National Park

Abstract and Figures

The health and diversity of bird populations serve as a strong indicator for the overall health of an ecosystem. This study was aimed to understand and document bird diversity in different forest types and its 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 transects (existing trails and roads) within the altitudinal range of 1300 – 5100 m inside the park. A total of 12363 individuals of birds belonging to 59 families, 143 genera, and 272 species were recorded. Two vulnerable species (Chestnut-breasted Partridge and Wood Snipe) and six near-threatened species (Bearded Vulture, Himalayan Vulture, River Lapwing, 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.
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Global Ecology and Conservation 30 (2021) e01771
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/).
Bird diversity and conservation threats in Jigme Dorji National
Park, Bhutan
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
Keywords:
Abundance
Bhutan
Birds
Diversity
Habitat
Richness
ABSTRACT
The diversity of bird populations serve as a strong indicator for the overall health of an ecosystem.
This study was aimed to understand and document bird diversity in different forest types and its
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
transects (existing trails and roads) within the altitudinal range of 1300 5100 m inside the park.
A total of 12363 individuals of birds belonging to 59 families, 143 genera, and 272 species were
recorded. Two vulnerable species (Chestnut-breasted Partridge and Wood Snipe) and six near-
threatened species (Bearded Vulture, Himalayan Vulture, River Lapwing, Satyr Tragopan,
Yellow-rumped Honeyguide and Wards 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, ve species were recorded as new species to the park (Wood Snipe,
Yellow Wagtail, Pink-browed Rosench, 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 elds (Wuczy´
nski 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: pemadndp@gmail.com (P. Dendup).
Contents lists available at ScienceDirect
Global Ecology and Conservation
journal homepage: www.elsevier.com/locate/gecco
https://doi.org/10.1016/j.gecco.2021.e01771
Received 12 March 2021; Received in revised form 16 August 2021; Accepted 20 August 2021
Global Ecology and Conservation 30 (2021) e01771
2
(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 (Wuczy´
nski 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; OConnell 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; OConnell 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 identied as a Priority I Endemic Bird Area (Birdlife
International, 2001). The region supports 22 restricted-range bird species (Statterseld 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; Statterseld et al., 1998; Myers et al., 2000; Hoekstra et al., 2005). More than half (51.44%) of the countrys total
geographical area is under a protected area network consisting of ve 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 km
2
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 ora and 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) Pallass 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 India and eastern Nepal 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 southeast Asia, situated between China 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.
P. Dendup et al.
Global Ecology and Conservation 30 (2021) e01771
3
2. Methods
2.1. Study area
JDNP spatially extending 27
o
33N28
o
15N and 89
o
14E90
o
22E (Fig. 1) with a varied altitudinal gradient (1200 to >7000 m)
has rich biodiversity (Thinley et al., 2014) within the ve major ecosystem types classied for Bhutan (Ohsawa, 1987). The ve major
forest types are subtropical forest (ST) (10002000 m), warm temperate forest (WT) (20002500 m), cool temperate forest (CT)
(25003000 m), subarctic/cold temperate forest (CO) (30004000 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 (MarchMay); summer
(JuneAugust); and autumn (September - November).
JDNP is rich in oral and faunal diversity. The past management plan has documented over 1434 vascular plants, 50 mammal
species, 313 bird species, 22 reptiles, 15 amphibians, 87 butteries, and 17 dragon and damselies (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 eld guide 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 (Pallass 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 Gallinago nemoricola) and seven near-threatened (NT) species (Bearded Vulture Gypaetus barbatus Himalayan Vulture Gyps
himalayensis, Northern Lapwing Vanellus vanellus, River Lapwing Vanellus duvaucelii, Satyr Tragopan Tragopan satyra, Yellow-rumped
Honeyguide Indicator xanthonotus and Wards 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 identied 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 ve different forest types within the altitude of 13005100 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 ve
major ecosystem types are based on classications made for Bhutan (Ohsawa, 1987).
P. Dendup et al.
Global Ecology and Conservation 30 (2021) e01771
4
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-efcient, 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 AM5.00 PM, WT 6.00 AM5.00 PM, CT 7.00 AM5.00 PM, CO 6.00
AM6.00 PM, and RS 6.00 AM5.00 PM). The survey team used a pair of binoculars (Nikon Aculon A211 8 ×42) for bird scanning and
identication, and a Garmin etrex 20x for collecting location and altitude information.
The eld surveyors received extensive training on eld survey and data recording methodology both before and during survey
works. Training on eld surveys included, but was not restricted to, techniques for identication and detection of birds, forest types
identication and strategies to minimize surveyors effect on bird detection. The data recording training included appropriate
adoption of MacKinnon bird listing methods and lling in data forms. The training was provided irrespective of eld surveyorslevel 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 identied and the
number counted and recorded. In the case of indirect signs, we identied the species while recording only one individual against the
species identied.
Species identication was based on the eld guide book to the Birds of Bhutan (Inskipp et al., 1999), a eld guide book to the Birds
of the Indian Subcontinent (Grimmett et al., 2011) and Birds of Jigme Dorji National Park: A photographic eld guide for the park visitors
(Dendup et al., 2020). Recent changes in species taxonomy have been adopted from Grimmett et al. (2019). In the case of bird calls,
pre-recorded bird songs were used for species identication (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 classications 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 ve 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)
H= Σni
Nlog ni
N(2)
Where:
H=the Shannon diversity index.
ni =number of individuals of the species.
N=number of individuals of species.
P. Dendup et al.
Global Ecology and Conservation 30 (2021) e01771
5
There are three classications; 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 identied using the ecosystem classication developed by Oshawa (1987) (Table 1).
3. Results
3.1. Bird diversity and signicance of JDNP
The bird survey in JDNP was completed by trekking and enumerating data through ve 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
identied bird species, 57 were migratory species (BirdLife International, 2021; Additional le 1). 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 nally the
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 (40005100 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 ve bird species new to the park with one being new to the country and they are; Yellow wagtail Motacilla
ava, Wood Snipe Gallinago nemoricola, Desert Wheatear Oenanthe deserti (new to the country), Pink-browed Rosench 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, Wards Trogon, River Lapwing, Long-tailed Shrike, Grey-capped Pygmy Woodpecker, Asian Brown Flycatcher, Asian-barred
Owlet, Tibetan Blackbird, Common Quail, Brown Accentor, 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
Woodcock, Great Parrotbill, Brown Wood-owl, Blue-bearded Bee-eater, Black-crowned Night-heron, Black-chinned Yuhina and
Bonellis 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
(m)
Vegetation communities
Subtropical forest (ST) 10002000 Castanopsis tribuloides, Schima wallichii, Quercus glauca, Lithocarpus elegans, Q. semiserrata, Castanopsis hystrix,
Litsea elongata, Quercus lamellosa, Persea clarkeana, Pinus roxburghii
Warm temperate forests (WT) 20002500 Castanopsis hystrix, Quercus lamellosa, Q. semiserrata, Lithocarpus elegans, Acer campbelii, Magnolia campbelii,
Sorbus cuspidata, Alnus nepalensis, Quercus grifthii, Rhododendron arboretum, Schima wallichii
Cool temperate forests (CT) 25003000 Tsuga dumosa, Picea spinulosa, Pinus wallichii, Quercus semecarpifolia, Acer campbellii
Cold temperate (subarctic)
forests (CO)
30004000 Abies densa, Juniperus recurva, J. indica, J. squamata, Larix grithii, Cupressus corneyana
Rhododendron scrub (arctic)
forests (RS)
>4000 Rhododendron nivale, R. setosum. R. anthopogon, R. lepidotum
P. Dendup et al.
Global Ecology and Conservation 30 (2021) e01771
6
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, r
2
=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 (10002000 m)
The ST forest ecosystem is the smallest forest ecosystem represented in the park. It covers an area of 66.26 km
2
corresponding to
1.51% of the total park area within an elevation range of 13511998 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 km
2
corre-
sponding to 3.28% of the total park area within an elevational range of 20022498 m. A total of 129 bird species inclusive of River
Lapwing Vanellus duvaucelii (NT), Lemon-rumped Honeyguide Indicator xanthonotus (NT), Wards 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 attens, indicating that the survey was reasonably complete.
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.
P. Dendup et al.
Global Ecology and Conservation 30 (2021) e01771
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3.3.3. Cool temperate forest ecosystem (25003000 m)
The CT forest ecosystem of the JDNP has coverage of about 208.34 km
2
corresponding to 4.76% of the total park area within an
elevational range of 25032997 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.
Fig. 4. A total number of bird species detected in each family across different forest types.
P. Dendup et al.
Global Ecology and Conservation 30 (2021) e01771
8
Table 3
The number of lower altitude species overlap with high altitude species. The bold gures are the total species detected in each habitat.
Number of species overlap across habitat type
Habitat Type ST (1000 2000 m) WT (20002500 m) CT (25003000 m) CO (30004000 m) RS (>4000 m)
ST (10002000 m) 135 84 62 46 29
WT (20002500 m) 129 67 58 39
CT (25003000 m) 92 49 33
CO (30004000 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 Scientic name Individuals detected
Muscicapidae Blue-fronted Redstart Phoenicurus frontalis 187
Blue Whistling Thrush Myophonus caeruleus 53
Plumbeous Water Redstart Rhyacornis fuliginosus 38
Phylloscopidae Lemon-rumped Warbler Phylloscopus chloronotus 127
Tickells Leaf Warbler Phylloscopus afnis 86
Leiothrichidae Black-faced Laughingthrush Garrulax afnis 442
Corvidae Large-billed Crow Corvus macrorhynchos 287
Motacillidae Olive-backed Pipit Anthus hodgsoni 258
Columbidae 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
Locustellidae Dusky Warbler Phylloscopus fuscatus 28
Cettiidae Chestnut-crowned Bush Warbler Cettia major 21
Cinclidae Brown Dipper Cinclus pallasii 20
Fringillidae Dark-breasted Rosench 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
inuencing 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.
P. Dendup et al.
Global Ecology and Conservation 30 (2021) e01771
9
3.3.4. Cold temperate forest ecosystem (30004000 m)
The CO forest ecosystem is the second largest ecosystem coverage represented in the park. It covers an area of 835.14 km
2
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 km
2
corresponding to 36.55% within an elevation range of 40015094 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 signicance 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 countrys 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 countrys 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).
Fig. 6. Cumulative species richness curve obtained as a result of cumulative hours surveyed in each different habitat in two seasons.
P. Dendup et al.
Global Ecology and Conservation 30 (2021) e01771
10
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 efciently forage 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
o
C to a maximum of 20.93
o
C 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 owering vegetations 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, Wards 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 signicantly dependent 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 speciesrichness 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 observers fatigue (Lardner et al., 2019). Repeated surveys during
different seasons will help ll such 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
identied to 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 signicance, 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 ve years (2016 2020) a
total of 33,937.38 cubic meters of timber and rewood has 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-modied 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 countrys
size) and despite regular patrolling activities carried out by the park ofcials, 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 shing in these two rivers is of great concern to
conserving White-bellied Heron as it results to loss of prey.
P. Dendup et al.
Global Ecology and Conservation 30 (2021) e01771
11
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 identied 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 rewood 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 eld level ofcials, 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 rewood to
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 rewood as 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 identied as one of the IBAs for providing safe
home to critically endangered White-bellied Heron Ardea insignis and endangered Pallass 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 ndings of 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 nancial interests or personal relationships that could have appeared to
inuence the work reported in this paper.
Acknowledgements
We would like to thank all our eld staff especially, Mr. Karma Jangchuk, Mr. Dawa Penjor and Mr. Norbu Jamtsho for their help
during the eld works and arrangement of eld logistics. 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 rene this manuscript. This bird study
was funded by Bhutan For Life.
P. Dendup et al.
Global Ecology and Conservation 30 (2021) e01771
12
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.
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