The endangered red panda (Ailurus fulgens): Ecology and conservation approaches across the entire range

Biological Conservation 220 (2018) 112–121

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Review

The endangered red panda (Ailurus fulgens): Ecology and conservation approaches across the entire range Arjun Thapaa,b, Yibo Hua,c, Fuwen Weia,b,c,

T

⁎

a

Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, 1-5 Beichenxi Road, Chaoyang, Beijing 100101, China International College, University of Chinese Academy of Science, Beijing, China c Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, China b

A R T I C L E I N F O

A B S T R A C T

Keywords: Anthropogenic activities Foraging ecology Habitat specialist Molecular ecology

The red panda (Ailurus fulgens), a vegetarian member of the order Carnivora, is distributed in Nepal, India, Bhutan, Myanmar, and China. Many populations occur at low densities in small fragmented forest patches and face pressure from habitat loss, degradation, and fragmentation, poaching, and developmental activities. Most studies have taken place in China and Nepal; few studies have been conducted in the other countries, creating a gap in documentation. Therefore, there is an urgent need to increase our knowledge regarding the ecology of the red panda and its threats. Based on literature regarding the red panda, we attempt to summarize the progress in research on its current distribution, ecology, and existing threats in the wild, highlight conservation approaches and recommend future directions. Recent studies have focused on wild populations; however, earlier studies emphasized captive. China and Nepal have a wider elevational range in red panda distribution (2000–3800 m) compared to other countries. Bamboo mixed subtropical and temperate forest and other associated variables, including a relatively high cover of bamboo, shrubs, and canopy, high densities of fallen logs, relatively steep slopes, and proximity to water sources, are ecologically important in the habitat. Due to differences in methodologies, prior estimates on population size and habitat area have varied. The genetic diversity of red pandas is high in China, but a lack of such data in other range countries makes subspecies classification unclear. Movement, microbiota, pathogens, and threats have been insufficiently documented; thus, we recommended extensive research in these areas. Furthermore, regional cooperation in research, data sharing, and policy implementation are urgently needed to protect wild panda populations.

1. Introduction The red panda (Ailurus fulgens), a member of the order Carnivora, is an arboreal vegetarian mammal that depends almost mainly on a bamboo diet (Wei et al., 1999; Yonzon and Hunter, 1991). The red panda occupies a highly specialized niche, primarily inhabiting bamboo understories in temperate and conifer forest types and areas adjacent to broadleaf forests in Nepal, India, Bhutan, Myanmar and China (Choudhury, 2001; Dorji et al., 2012; Kandel et al., 2015; Pradhan et al., 2001; Reid et al., 1991; Sharma and Belan, 2009; Wei et al., 1999; Yonzon, 1989; Yonzon and Hunter, 1991), and a separate population may occur in Meghalaya, India (Choudhury, 2001). Ailurus fulgens fulgens (Himalayan subspecies) and Ailurus fulgens styani (Chinese subspecies) are believed to be two subspecies based on morphological evidence and the geographical barrier of the Nujiang River (Glatston, 1994; Wei et al., 1999). However, this classification and geographical

boundary are debated and have remained unclear due to insufficient genetic evidence from the westernmost biogeographical ranges (Hu et al., 2011). Relied on skull morphometric data and other secondary information (comparative photographs of specimen of known origin), Groves (2011) thought that these two subspecies should update as two distinct species: Ailurus fulgens from the Himalayan and Ailurus styani from Yunnan, Sichuan, southeastern Tibet and Myanmar (Groves, 2011). However, these pieces of evidence are premature to justify distinct species due to limited sample size and lack of genetic evidence. Especially, genetic study of the Himalayan red panda would be very critical to justify taxonomic classification. Habitat loss, fragmentation, and degradation are major threats to wild red pandas (Pradhan et al., 2001; Wei et al., 1999; Yonzon and Hunter, 1991). These factors have accelerated declines in wild populations, and the species has been listed as Endangered by IUCN (Glatston et al., 2015). Red panda population has plausibly declined by

⁎ Corresponding author at: Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, 1-5 Beichenxi Road, Chaoyang, Beijing 100101, China. E-mail address: [email protected] (F. Wei).

https://doi.org/10.1016/j.biocon.2018.02.014 Received 10 November 2017; Received in revised form 2 February 2018; Accepted 9 February 2018 0006-3207/ © 2018 Elsevier Ltd. All rights reserved.

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National Park (Pradhan et al., 2001). Records of red pandas are known from eight protected areas in the state of Sikkim (Ghose and Dutta, 2011). Red panda with cubs was captured in camera-trap that setup in different locations in Kyongnosla Alpine Sanctuary of East Sikkim (Khatiwara and Srivastava, 2014). Similarly, they have been recorded in the Twang district in Arunachal Pradesh (Chakraborty et al., 2015; Srivastava and Dutta, 2010). Noteworthy, a red panda carcass was found in the highest elevation 4325 m in Twang district (Dorjee et al., 2014). The carcass may be carried here by predators in higher elevation. Choudhury (2001) reported hide of red panda in the village closer to Nokrek and Balpakram national parks in Garo Hills in Meghalaya (Choudhury, 2001). Yet, there has been no recent authentic report of red panda sighting (indirect evidence of fecal pellets) or scientific study of red panda in that district (Ghose and Dutta, 2011). Except Choudhury's (2001) report, there is no any further scientific exploration on this issue. Duckworth (2011) elaborated that the red panda skins found could be the descendant of previous captive pandas released by tea planter when they had departed that area. Due to great difference in ecological conditions with current distribution range, it would be premature to accept the existence of wild pandas based on this information in Meghalaya (Duckworth, 2011). A ground based field survey in Meghalaya is urgently need for investigation the signs of wild pandas. The occurrence of the red panda has been confirmed in 13 districts, including Haa, Thimphu, Paro, Punakha, Wangdiphodrang, Gasa, Trongsa, Zhemgang, Bumthang, Mongar, Lhuntse, Trashigang and Trashiyangtse, in Bhutan (Dorji et al., 2012). Field-based studies have confirmed the presence of red pandas in the Jigme Dorji, Jigme Singye Wangchuck and Thrumshingla national parks, the Bumdeling and Sakteng wildlife sanctuaries and the Toorsa Strict Nature Reserve and biological corridors connecting these reserves (Dorji et al., 2012). In China, its distribution is confined to Sichuan, Yunnan, and Tibet (Wei et al., 1999; Wei et al., 2014). A Population and Habitat Viability Assessment (PHVA) document indicated that the red panda could be distributed in 88 counties in five provinces, Sichuan, Yunnan, Tibet, Qinghai and Gansu, with 43.8% of the habitat in Sichuan; however, populations in Qinghai and Gansu have not been recorded. The subspecies A. f. styani is confined to the Sichuan province and northeastern Yunnan, whereas A. f. fulgens occurs in both the Tibet and Yunnan provinces in China (Wei et al., 1999). The distribution status is poorly known in Myanmar, and red pandas have only been confirmed in Hkhakaboraz National Park, Hponkanrazi Wildlife Sanctuary, and other places including Emaw Burn, Nam Tamai, Taron valley in closer border of Yunnan (Rabinowitz and Khaing, 1998). Globally, the estimated potential red panda habitat is approximately 142,400 km2, with China alone accounting for more than half of the area (Choudhury, 2001), but recent modeling-based estimates indicate 47,000 km2 (Kandel et al., 2015). Recent estimates of habitat in Sichuan, Yunnan and Tibet are 17,228.3 km2, 10,634.1 km2 and 9574.1 km2, respectively (Wei et al., 2014). Due to inconsistent methodologies, the estimated potential red panda habitat area varies (Table 1). Earlier estimated population is approximately 16,000–20,000 red pandas in the wild; 5000–6000 occur in China, and the remaining 5000–7000 are distributed in other range countries (Choudhury, 2001). Recent assessment based on the IUCN Red List indicates that the red panda population may be as low as 10,000 individuals in the wild (Glatston et al., 2015).

50% over last three generations and this decline is continuing (Glatston et al., 2015). However, any estimate of the total red panda population is likely to be inaccurate, as the red panda inhabits five countries, and occurrence records are scant and patchy. Most studies to date have relied on the observation of indirect signs, such as feces, pugmarks and feeding (Pradhan et al., 2001; Wei et al., 1999; Yonzon and Hunter, 1991), and consultation with experts and local communities in small units (Jnawali et al., 2012; Wei et al., 2014). There is a spatial bias in terms of the areas where most studies have been conducted. Studies have mainly been concentrated in parts of Sichuan in China and in the eastern part of Nepal, so there remains a huge area of the species' range where a few or no studies have been performed so far, such as the western part of Nepal, part of Arunachal Pradesh, part of Tibet, part Yunnan and norther Myanmar. However, little empirical research has been carried out in limited areas in the landscape, which have been sparsely documented. There are still many gaps in the current knowledge regarding red pandas, including in relation to several aspects of the species' ecology, population parameters (e.g., population size, density, mating system, and dispersal pattern), behavior, pathology, genetics, isotopes, gut microbiota diversity and geographic demarcation of subspecies. To provide a thorough summary of what is known to date, here we performed a comprehensive review of the existing literature relevant to red panda studies in the wild habitats of its range countries. Our aims in this paper are to summarize the current scientific progress on the distribution and ecology of this species, update the existing threat status of the wild population and clarify the recommendations for future conservation efforts. Additionally, this paper provides a synthesis of prior conservation approaches and future directions that would be beneficial to scientific communities focused on other species and protected area managers to implement effective conservation measures. 2. Status and species ecology 2.1. Distribution and population status The published information regarding the red panda is limited in comparison to that pertaining to other high altitude-dwelling species, such as the giant panda (Ailuropoda melanoleuca), snow leopard (Uncia uncia), and Himalayan musk deer (Moschus leucogaster), which are the iconic species of pristine mountainous ecosystems. The distribution of the red panda is restricted to isolated habitat patches in the mountainous regions of five Asian countries: Nepal, India, Bhutan, Myanmar and China (Choudhury, 2001; Pradhan et al., 2001; Wei et al., 1999; Yonzon et al., 1991) (Fig. 1). Mountainous protected areas, including Langtang National Park (LNP), Makalu Barun National Park (MBNP), Rara National Park (RNP), Sagarmatha National Park (SNP), Annapurna Conservation Area (ACA), Gaurishankar Conservation Area (GCA), Kanchenjunga Conservation Area (KCA), Manaslu Conservation Area (MCA), and Dhorpatan Hunting Reserve (DHR), are the major habitats of red panda in Nepal (Jnawali et al., 2011; Jnawali et al., 2012; Williams, 2003; Yonzon, 1989). However, > 77% of red panda habitats lie beyond protected areas (Jnawali et al., 2011) and are under increasing anthropogenic threats, which is a serious conservation challenge. Recent surveys recorded the occurrence of red pandas in the Bhojpur, Dolpa, Jumla, Jajarkot, Kalikot, Khotang, Lamjung, Rolpa, Ramechhap, and Sindhupalchowk districts, which represent habitats outside protected areas (Bhatta et al., 2014; Bista et al., 2017b; Thapa et al., 2013). In India, red panda occurrence records have been confirmed in West Bengal, Sikkim, Arunachal Pradesh, and possibly Meghalaya (Choudhury, 2001). The Singalila and Neora Valley national parks are protected areas in West Bengal that harbor good red panda habitat, and detailed studies have been carried out in these areas (Pradhan et al., 2001). A prior study found a density of one panda per 3.9 km2 distributed within a range of elevation of 2600–3600 m in Singalila

2.2. Habitat ecology Habitat ecology is a widely covered research area in panda studies and is a major component of species-specific conservation tools. Subtropical and temperate forests constitute a broad habitat range for red pandas (Yonzon et al., 1991; Yonzon, 1989), but survival of a distinct sole population may occur in a warm climate, i.e., in tropical forest in Meghalaya at elevations of 700–1400 m (Choudhury, 2001). Roberts and Gittleman (1984) recorded an altitudinal range for the 113

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Fig. 1. Geographical range of the red panda Ailurus fulgens (Dark green color: built in MaxEnt Model). Red panda occurrence records: Red dots represent indirect sign, yellow squares represent sighting, and blue triangles represent museum specimens. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

densities of fallen logs and tree stumps in Bashania faberi bamboo forest. In Singalila National Park, Pradhan et al. (2001) concluded that relatively high bamboo cover, bamboo height, and canopy cover were significant components of habitat used by red pandas. Red pandas were strongly associated with old-growth Bhutan fir (Abies densa) forest dominated by a dense cover of Yushania and Arundinaria bamboo and high densities of fallen logs and tree stumps at ground level and high densities of trees, dead snags, and rhododendron shrubs in the midstory (Dorji et al., 2012; Dorji et al., 2011). Most of the animal's feces were observed close to water (Dorji et al., 2011; Pradhan et al., 2001; Yonzon, 1989; Zhang et al., 2011; Zhang et al., 2006; Zhou et al., 2013), which indicates that proximity to water sources is major habitat requirement for the red panda throughout its entire range. A habitat suitability analysis indicated that forest type, bamboo, canopy, fallen logs, bamboo density, elevation, slope, aspect and distance to water are variables that have important roles (Table 2).

animal of 2200–4800 m; however, Choudhury (2001) suggests it can be found at 1500–4800 m. We compiled species occurrence records (< 3000 occurrence records) throughout the range that were recorded in various field studies and museum records. The altitudinal distribution is wider, between 2000 and 3800 m (average 2800 m), in China than in other countries. Furthermore, occurrence data showed an average altitudinal range below 3000 m in China and Myanmar, whereas it was above 3000 m in other countries, such as Nepal, India, and Bhutan (Fig. S2, Supporting Information). In addition to variation in climate and topography, the habitat of red pandas includes different vegetation compositions, including evergreen forests, evergreen and deciduous mixed broad-leaf forests, deciduous forests, deciduous and coniferous mixed forests, and coniferous forests with associated bamboo thicket understories (Wei et al., 1999; Yonzon et al., 1991). Yonzon and Hunter (1991) classified the habitats of red pandas into five types at a fine scale: fir-jhapra, rhododendron, broad-leaved-raate, birch and alpine scrub; only fir-jhapra was preferred in Langtang National Park. Wei et al. (1995) found that red pandas occurred at sites on steeper slopes and with higher densities of fallen logs, shrubs, and bamboo culms in Yele Reserve. Similarly, Zhang et al. (2004) recorded that the animal preferred habitats with higher

2.3. Foraging ecology Their elusive behavior, arboreal habits, and habitat in remote and inaccessible mountain terrain make it difficult to directly encounter red

Table 1 Summary of estimated habitat (km2) of red panda by different studies. Authors

Categories

Nepal

India

Bhutan

Myanmar

China

Variables

This study (Predictive model)

Total (threshold ≥0.22) Probability ≥0.5 – 912 Total 49.1% used Total High quality Total High quality Total predicted Expert

20,150

7142

12,407

12,623

82,653

Presence records (Nepal, India, Bhutan, Myanmar, and China), bioclimatic, topographic (slope, aspects)

15,721 – – 16,700 8200 35,44 592 20,397 3612 22,400 1,7400

6529 – – 25,500 12,500 8330 – 40,400 18,969 5700 3200

12,171 – – 10,900 5400 3600 900 21,284 12,979 900 600

9195 – – 13,000 6400 – – 27,627 12,979 5000 2900

63,005 37,436.5 – 76,300 37,400 154,200 121,400 298,000 139,700 13,000 8100

Wei et al. (1999) Yonzon et al. (1997) Choudhury (2001) PHVA (2010/2013) Mahato (2010) Kandel et al. (2015)

114

Forest cover, country boundary Forest types, topographic, annual precipitation Forest cover, country boundary Expert view Presence records (Nepal only), bioclimatic, topographic Presence records (Nepal only), bioclimatic, topographic

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Table 2 Degree of habitat suitability analysis. Factors

Degree of suitability

Strengthen of evidence

Highly

Suitable

Marginally

Unsuitable

Bamboo Forest Deciduous broadleaf forest

Bamboo Forest Evergreen broadleaf forest, mixed evergreen and deciduous broadleaf forest –

No bamboo No forest Brush, grassland, cropland, no vegetation

**** **** ****

Forest age

Bamboo Forest Coniferous forest, mixed coniferous and deciduous broadleaf forest Old growth forest (primary)

–

****

Elevation (m) Slope (0) Aspect

2800–3200 > 30–45 North, North East

> 45 –

> 4000 – –

*** *** **

Canopy Fallen logs Bamboo height (m) Bamboo density Distance to water (m)

25–50 High density 1.0–2.5 < 25–50 < 100

< 25 Low density – > 75, < 25 250–500

– – – No bamboo > 500

*** *** ** *** ***

Bamboo distribution Forest distribution Forest types

Old growth forest (primary) 3200–3600 20–30 North, West, Southern > 50 High density 1.5–3.0 50–75 100–250

*** High strength, ** Medium strength, and * Weak strength.

important sites or barriers to movement (Seidler et al., 2015). Due the crepuscular and nocturnal behavior of red pandas (Johnson et al., 1988), they are difficult to track and follow; therefore, the collaring technique provides good insight for advanced scientific exploration in terms of movement ecology. Compared to the sympatric giant panda, very limited research covers the movement ecology of red pandas, which has particularly focused on animal home ranges and daily activity patterns (Johnson et al., 1988; Yonzon, 1989). To monitor the movement and activity patterns of female red pandas, radio telemetry was first carried out in Wolong Nature Reserve in 1984, which resulted in an estimated 481 ± 312 m, and 4.3 km2 average daily movement distance and home range, respectively (Johnson et al., 1988). After a few years, an adult male and female panda were radio-collared in the same reserve, resulting in 235 ± 169 m being recorded for the female and 325 ± 210 m for the male (Reid et al., 1991). Yonzon (1989) collared six red pandas in LNP, estimating 1–1.5 km2 and 1.7–9.6 km2 ranges for females and males, respectively (Table S2, Supporting Information). Additionally, in Fengtongzhai Reserve, six adult red pandas (three males and three females) were collared in 2002, and the daily movement was estimated at 460.9 ± 329.5 m and 431.5 ± 307.8 m for males and females, respectively (Wei and Zhang, 2011).

pandas in their natural habitats; thus, the majority of studies have relied upon indirect signs, such as feces, feeding signs and pugmarks in the snow (Choudhury, 2001; Wei et al., 1999; Yonzon and Hunter, 1991). The collection of fresh feces is a good means for exploring the dietary composition of the red panda, which is estimated by the weight of the dry matter or the proportional occurrence or frequency of food items (Wei et al., 1999) using macroscopic or microhistological techniques. In addition to Bhutan and Myanmar, dietary studies have been conducted in Nepal (Panthi et al., 2015; Sharma et al., 2014; Thapa and Basent, 2015; Yonzon, 1989), India (Pradhan et al., 2001) and China (Wei et al., 1995), identifying 16, 5 and 4 food plants, respectively (Table S1, Supporting Information). The red panda is a diet specialist (Yonzon, 1989) and mainly depends on bamboo for nutrients and other trace food items, such as berries and other fruits, which occur infrequently in different seasons. The red panda feeds on bamboo leaves (68.5%), shoots (18%), fruits of Sorbus sp. (8.4%) and other mushroom and berry mixed with leaf or shoot of bamboo in LNP (Yonzon, 1989). Similarly, Thapa and Basent (2015) found eight plant species consumed by red pandas, which were categorized into bamboo (> 90% Thamnocalamus aristata), trees, herbs, shrubs, mosses and unidentified in the same national park. Pradhan et al. (2001) found that Arundinaria aristata (34.86–53%) and Arundinaria maling (36.18–48.16%) were stable food items of red pandas in Singalila National Park in the Eastern Himalayas. Wei et al. (1995) recorded that red pandas feed on new shoots of Qiongzhuea macrophylla in spring but also occasionally feed on Yushania glauca in Mabian Reserve. In addition to bamboo, the fruits of other species, such as Prunus pilosiuscula, Prunus sp., Rubus foliolosus, R. innominatus, R. flosculosus, Rosa sericea, Sorbus koehneana, Ribes meyerri, R. tenue, and R longiracemosum, are eaten by red pandas in the reserves in China (Wei and Zhang, 2011).

2.5. Molecular ecology Across its range countries, genetic studies of red panda have flourished in both wild and captive populations. Due to the obstacles and challenges of collecting genetic samples, such as blood and muscles, from endangered species, noninvasive genetic sampling is considered to be a good method and has been successfully deployed for red panda fecal samples (Guo et al., 2011; Hu et al., 2011). Although population estimates of red pandas have not been well documented using molecular techniques, microsatellite-based fecal genotyping could identify individuals for population estimates (Guo et al., 2011). Such noninvasive methods would have higher accuracy than prior conventional practices (forest cover and ecological densities) used to estimate populations (Choudhury, 2001; Jnawali et al., 2012; Pradhan et al., 2001; Wei et al., 1999; Yonzon and Hunter, 1991). A Bayesian coalescent simulation based on microsatellite data detected red panda population declines (Hu et al., 2011) and suggested a declining population trend consistent with field survey studies. Analyses based on mitochondrial DNA (mtDNA) and microsatellites demonstrated high levels of genetic diversity in red pandas (Hu et al., 2011; Liu et al., 2005; Su et al., 2001). Multiple studies consistently

2.4. Movement ecology Because of advancements in recent technologies and the analytical power in tracking animals, the field of movement ecology has developed rapidly and has been more widely implemented in recent decades (Tomkiewicz et al., 2010). Linking movement ecology to conservation has several implications for the future management of wildlife, such as improving our understanding of important habitats for wildlife and the area traversed by wide-ranging species (Hebblewhite and Haydon, 2010), enabling managers to implement actions across the entire movement path, e.g., flyway approaches for birds and butterflies (Howard and Davis, 2009), and to identify threats, e.g., the loss of 115

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have motivated the development of Ex situ environments to maintain healthy populations (Bertelsen et al., 2010; Panayotova-Pencheva, 2013; Pradhan et al., 2011; Xie et al., 2011); however, there is little knowledge regarding parasites and infectious diseases in wild populations. Additionally, a high infant mortality rate was recorded in a wild red panda (Yonzon, 1989); the causes of this phenomenon are still unclear but may be the result of infectious disease. Some studies have addressed parasites in wild populations of red pandas, particularly in Nepal (Bista et al., 2017a; Lama et al., 2015; Sharma et al., 2016; Shrestha and Maharjan, 2015a; Shrestha and Maharjan, 2015b) (Table S4, Supporting Information). A recent study recorded seven different protozoan, cestode, nematode, trematode and coccidian species (Bista et al., 2017a; Sharma et al., 2016). Numerous infectious diseases have been reported in captive red panda population that were caused by parasites, bacterial, fungal and virus. The red panda is highly susceptible to infectious disease. The most significant infectious agent appear to be canine distemper virus that has been reported earlier (Bush and Roberts, 1977). Particularly in the Himalaya, transhumance grazing is a good practice of livestock rearing, which has high risk in disease transmission to wild animals. Livestock guarding dogs increase with herder numbers, which have high chance to encroach red panda habitat, contact between dogs that could increase such viral infection in red panda. Even all the livestock guarding dogs in red panda habitat are vaccinated again this disease, the chance that it will enter and spread in wild red panda population with disastrous consequences are high (Glatston et al., 2015). A proper understanding of wildlife disease is essential to maintain healthy wild population; otherwise, it would be turned into the biggest threat to wild red pandas.

showed that for the Chinese panda populations, there is high mtDNA control region (CR) haplotype diversity (h = 0.93, (Su et al., 2001); h = 0.95, (Li et al., 2005); h = 0.924, (Hu et al., 2011) (Table S3, Supporting Information). Captive red panda in European's zoos have high haplotype diversity (h = 0.91) that indicates importance of good genetic management in the early years of breeding programs (Schäfer and Reiners, 2017; Schäfer et al., 2016). Captive red panda population has low observed heterozygosity (0.60) and inbreeding coefficient (0.05) in Padamja Naidu Himalayan Zoological Park, India (Kumar et al., 2016) but genetic assessment of wild red panda population in the Himalayan regions has not been carried out. With the development of microsatellite isolation techniques, red panda-specific microsatellite markers have been increasingly developed (Liang et al., 2007; Liu et al., 2005; Wu et al., 2009; Zhang et al., 2008), which are valuable genetic resources for conservation genetics studies of red pandas. A few studies have attempted to explore subspecies differentiation using mtDNA markers but have failed to detect significant lineage divergence (Hu et al., 2011; Liu et al., 2005; Su et al., 2001). No significant mtDNA-based phylogeographic structure has been found for red pandas, which suggests historically wide gene flow among populations (Hu et al., 2011). However, microsatellite data reveal three genetic clusters, Gaoligong-Tibet, Xiaoxiangling and Qionglai-Liangshan, in China, reflecting significant genetic differentiation and limited gene flow among the clusters (Hu et al., 2011). Thus, the classification of subspecies and the geographical boundaries of red pandas need further reassessment combining morphological and genetic analysis using representative samples from its distributional range. 2.6. Gut microbiota

2.8. Existing threats to populations Advances in microbiological studies over the past decade have revealed a significant role of gut microbial symbionts in host immunity, nutrient use, and disease, and genome sequencing has elevated the progress in research (Wei et al., 2015b). Prior studies include 16S ribosome RNA gene sequencing and shotgun sequencing techniques to understand human gut microbiome diversity (Turnbaugh et al., 2006); these methods have also been adopted in wild animals to explore the adaptation and evolution of gut microbiomes, for instance, in the giant panda (Wei et al., 2015b). Several studies have focused on the gut microbiota of the giant panda (Li et al., 2015; Wei et al., 2015b; Xue et al., 2015; Zhu et al., 2011). However, little is known about the gut microbiota of the red panda (Kong et al., 2014). Phylogenetically, both red and giant pandas are carnivores but underwent a dietary switch to become highly specialized bamboo herbivores and are therefore interesting species for studying the evolution of gut microbiotas (Li et al., 2015). Recently, studies have suggested the divergent evolution of gut microbiotas in pandas and found that the two panda species harbor distinct gut microbiotas (Li et al., 2015). However, these results need further clarification due to the limited number of species studied. Distinct bacterial communities have been recorded between wild and captive red panda populations, suggesting higher community diversity, richness and evenness in wild populations (Kong et al., 2014). Furthermore, phylogenetic analysis shows that a considerable number of bacterial OTUs are related to cellulose degraders (Kong et al., 2014).

Based on the literature, we compiled threats that directly or indirectly affect the red panda and its habitats in its range countries and indexed them based on the number of papers. There are 13 different types of threats to the red panda, including both anthropogenic and natural threats (Fig. 2). Habitat loss and degradation, poaching and illegal trade, developmental activities, and illegal herbal plant collection are the major threats to red pandas. Other threats are forest fire, killing by guard dogs, tourist disturbance, bamboo flowering, high infant mortality, small and fragmented populations, weak law enforcement, and inadequate awareness. The red panda faces high threats in Himalayan countries, including Nepal, India, and Bhutan, whereas there are very low threats to panda populations in China. Poaching of red pandas is dramatically increasing in Nepal; however, its consequences are still unclear. Wildlife Crime Unit at Central Investigation of Nepal seized 52 red panda hides from different places in Nepal between 2013 and 2017. In 2016 and 2017, the highest number of red panda illegal trade cases (< 25) was reported (Damber Bist personal comm.) but motive is mysterious. Many confiscated persons with red panda hides were villagers, thus conservation awareness, and strict legal punishment (heavy fine with Jail) are possible solution to controlling poaching and illegal trade (Prof. Shah personal comm.). In addition, author reported two dead red pandas in the snare trap at Langtang National Park in December 2016. Ghose and Dutta (2011) reported that poaching is second direct threat to red panda survival in India, and added further motivation for hunting is purely for sport and skin, which is traded locally in an illegal way. Red panda skin has not been seized in China last 7–8 years. However, wildlife smugglers were sentenced in jail for trading wild panda in southwestern China while transporting six panda (three dead) from natural habitat in 2016. Recently, six live red pandas confiscated in Loas after being transported from Yunnan in 2018 (January), but unclear about the original habitat from where they were captured. Sharma et al. (2014) suggest that livestock grazing adversely affects red panda habitat use in Rara National Park. However, red pandas may forage in areas with steeper slopes, which livestock cannot access (Wei et al., 2000), and there is no

2.7. Pathogens Emerging infectious diseases are threatening the survival of many endangered species, including red pandas; thus, it is essential to understand how disease affects small isolated wildlife populations for the implementation of effective management strategies. Parasitic infections are ubiquitous in wildlife, livestock and human populations, and healthy ecosystems are often parasite rich (Cable et al., 2017). Red pandas are known to be highly susceptible to parasitic infection, which has a tremendous impact on their population dynamics (Bista et al., 2017a; Lama et al., 2015). Therefore, red panda pathogenic studies 116

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Fig. 2. Existing threat status of red panda.

3.1.2. Population and habitat viability assessment and species conservation strategy A series of PHVA workshops have been conducted in the red panda ranges countries of Nepal (2010), China (2012), India (2013), with additional discussion including participants from Bhutan and Myanmar, each devoted to red panda conservation planning for the different populations in each country (Jha et al., 2014; Jnawali et al., 2012; Wei et al., 2014). The workshops aim to identify habitats, distribution ranges, the degree of habitat fragmentation, and existing threats to red pandas at the national scale using advances in knowledge from expert biologists, desktop review and Vortex computer model simulation. Finally, the workshops establish a vision and develop goals, objectives and actions needed to achieve this vision.

competition for bamboo food resources between pandas and livestock (Yonzon, 1989), but livestock have had a role in reducing overall bamboo abundance through trampling. Livestock grazing likely also reduces bamboo abundance and availability in red panda habitat (Williams, 2003). Small-scale resource use, bamboo extraction and livestock grazing were found to negatively affect panda occurrence in Dhorpatan Hunting Reserve in Nepal, which indicated major threats in the study area (Panthi et al., 2017). Red pandas face threats from developmental activities (e.g., road construction), the harvesting of timber, bamboo and minor forest products, livestock grazing, inefficiently managed tourism, guard dogs, and snares (for musk deer and pheasants) in Bhutan (Dorji et al., 2012). Deforestation, habitat fragmentation, population isolation, poaching, and bamboo flowering are the dominant threats affecting its sustainable survival in China (Wei and Zhang, 2011) and also in other ranges countries.

3.1.3. Human resource development and institutional strengthening Small-scale wildlife monitoring and patrolling activities are conducted at a local level in different panda range countries; however, regional-level coordination is lacking. Conservation organizations (e.g., the World Wildlife Fund) in partnership with government authorities have provided technical skills to park managers, forest rangers, and local communities to monitor and patrol endangered fauna. Protected Areas have ensured the protection of red panda within and outside PAs by establishing corridor among PAs, buffer zones and specific conservation zones. In Nepal, protected area governing authorities have designed buffer zone areas in all the PAs in which red pandas are distributed, and have contributed to protecting large areas of panda habitat. Similarly, Bhutan has designed a network of corridors among all PAs that encompasses good panda habitat beyond PAs under effective protection (Wangchuk, 2007). In the Himalayas, community-based red panda monitoring and Community-Based Anti-Poaching Units have been established to monitor wildlife in mountainous PAs where human resources are inadequate (Acharya and Dhakal, 2012). For example, an Anti-Poaching Unit has been established in Langtang National Park, a prime habitat of red pandas, to control illegal hunting and the poaching of wild fauna, and community-based red panda monitoring has been established in the park. Outside PAs, the Red Panda Network (RPN) began conservation initiatives in the eastern part of Nepal in 2007 through research and community-based monitoring with the coordination and mobilization of Community Forest User Groups (CFUGs) (Williams et al., 2011). The red panda is the state animal of Sikkim state in India, which has focused attention in its conservation. Red panda conservation activities are carried out in collaboration with the Forest, Environment and Wildlife Management Department (FEWMD), Government of Sikkim, and the World Wildlife Fund-India. Similarly, other institutions, such as the

3. Conservation approaches and future directions 3.1. Prior conservation approaches 3.1.1. Management plan/action plan (national and regional) Management plans include “protected areas” in red panda range countries with an aim to protect red pandas and other sympatric endangered species. For effective conservation, the trend of PA establishment is increasing, and various approaches, such as designing corridors, managing community conservation sites, and community forestry, are practiced in the landscape where pandas are distributed. The management plan of Langtang National Park (1976–1980) recommends a separate red panda conservation zone in LNP for red panda protection in Nepal. The site-specific species action plan Red Panda Conservation Plan for LNP and its Buffer Zone in Nepal (2010–2014) was implemented with an aim to achieve five objectives. However, this plan was not able to achieve its target objectives successfully. Over the past year, red panda conservation action plan for Nepal has been drafted; however, its implementation is still in process. Conservation action plan that specific to red panda has not developed fully in the range countries, but conservation actions are addressed by incorporating in biodiversity conservation plan of the respective countries. Therefore, it is essential to develop a national and regional action plan to protect the red panda and its habitat to update scientific studies, habitat management, and conservation outreach and improve policy and partnership development.

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implementation of specific management and conservation actions.

Khangchendzonga Conservation Committee (KCC) and Singdrabong Khangchendzonga Eco-Friendly Society (SKES), have actively joined at the local level (Ghose and Dutta, 2011). With the support of WWFIndia, people of the local community have demarcated Pangchen Lumpo Muchat Community Conservation Area and Pangchen Lakhar Community Conservation Area to conserve the rare flora and fauna in Pangchen Valley (Chakraborty et al., 2015). The red panda is not included on the list of the key protected animal project in China (Wei et al., 2011). Conservation initiatives have been increasing to protect wild fauna and flora through the implementation of various projects, such as the Natural Forest Protection Project (NEPP), Grain to Green Project, National Wildlife Conservation and Natural Reserves Construction Project, and China Rural Energy Enterprise Development (Wei et al., 2011). The Chinese government has invested in huge efforts to protect the habitat of giant pandas (Wei et al., 2015a) that would beneficial for both panda species. Due to sympatric habitat dwellers with giant panda, the red pandas can certainly benefit much from the mentioned projects that are devoted to nature conservation.

3.2.2. Establishment of coordination/partnerships among organizations and nations regarding red panda conservation Due to the multinational range of distribution of the red panda in five Asian countries, it is essential to instill cooperation among all these countries based on internationally accepted acts, such as the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), which regulates the export and import of animals and their body parts. To secure a viable population of red pandas in the landscape, there is an urgent need for national and international coordination and cooperation in the methodological advancement of survey techniques, quality in data generation and data sharing. Various governmental/non-governmental institutions and organizations are working in their respective panda range countries; however, a common pool of shared data is scant. There is even variation in field survey methodologies due to the lack of the regional development of standard survey and monitoring protocols. Recently, the government of Nepal developed a national-level red panda monitoring protocol (MFSC, 2015), which needs further field implementation and validation. Because of its large amount of red panda habitat, highquality research and experiences, and experts, China could initiate a focal coordination and cooperation partnership in the landscape. Furthermore, panda range countries should coordinate with captive population holders (zoos) around the globe to raise conservation funds. Almost all red pandas that are living in captivity in Europe, America, and other countries originate from the Himalayas (Nepal and India) and China. To strength coordination among captive breeders and range countries, Red panda Global Species Management Plan (GSMP) was approved in 2013, which needs further effective implementation to protect wild populations and balance genetic diversity level at Ex-situ and In-situ.

3.1.4. Field implementation Other mammals, such as the giant panda, have garnered great attention in terms of conservation, and national-scale censuses and regular monitoring have been conducted over certain time intervals in China (Wei et al., 2015a). Similarly, national censuses on rhinoceros (Subedi et al., 2013) and royal Bengal tiger populations have been conducted in Nepal as well as a tiger census in Bhutan (Tempa, 2017). In Nepal, the Department of Forest and Department of National Park and Wildlife Conservation of Nepal's government carried out a survey of the distribution status of red pandas at a national scale in 2016, which has added further positive efforts in panda conservation. The Red Panda Network (RPN) has trained people of the local community as Forest Guardians and has been monitoring the red panda populations in three districts in eastern Nepal since 2007 (Mahato et al., 2011; Williams et al., 2011).

3.2.3. Initiation of transboundary conservation/establishment of biological corridors/extension of protected areas China shares a large amount of red panda habitat across its international borders with Nepal, India, Bhutan, and Myanmar. Thus, China could initiate collaborative research approaches with neighboring countries to secure viable populations across such border habitats. Recent studies have suggested that Nyirong, Nalyam and Dinggye have good potential red panda habitat across their borders with Nepal and Tibet; however, no field exploration studies have been conducted. Furthermore, we recommended field surveys to be carried out in these mountain ranges in Yunnan Province in China: Shangri La, Meili Snow Mountain, Chall Snow Mountain, the Gaoligong Mountains, Baima Snow Mountain, and Biluo Snow Mountain. The initiation of transboundary conservation efforts among transboundary countries through the Sino-Nepal, Sino-Bhutan, Sino-Myanmar-India and Sino-Myanmar regions could help to establish international coordination in biodiversity conservation.

3.1.5. Enforcement of laws and regulations Most of the panda range counties have focused much attention on protecting wildlife and have launched a series of laws and regulations to protect wild flora and fauna in their nations. The conservation of rare and endangered species, such as the red panda, is reflected in various conservation policies in summaries for the different countries presented in Table S5 (Supporting Information). The laws, acts, and regulations effectively protect rare and endangered animals throughout the range for the most part; however, illegal hunting and poaching still increasing in a few localities. 3.2. Future directions 3.2.1. Establishment of a regional database and upgrading the knowledge of the ecology of wild panda populations Large red panda habitats in the landscape need to be explored using advanced science-based techniques. Due to insufficient published information, it is difficult to ascertain true presence of red pandas in the warm climate of Meghalaya, which has been a debatable issue. We recommended that there is an urgent need for field survey to investigate current distribution status of the red panda in Meghalaya by protected areas authority of India. Potential habitat in the different areas, for instance, the western biogeographic distribution limit, including western Nepal, most of Tibet, and Yunnan, need further field surveys. Information about the red panda is very scant in Myanmar. Studies on population parameters (such as population size, density, mating system, and dispersal patterns), pathogens (particularly canine distemper virus), microbiota, and isotope ecology should be conducted in wild panda populations. The assessment of genetic diversity should be required throughout the species' range, which will allow the

3.2.4. Sympatric species conservation (SSC) Many rare and endangered mammals, including Himalayan musk deer (Moschus sp.), the Asian black bear (Ursus thibetanus), the Nepal gray langur (Semnopithecus schistaceus), the common leopard (Panthera pardus), the giant panda, the golden monkey (Rhinopithecus roxellana), and the takin (Budorcas taxicolor), are sympatric with red pandas in its range countries. Sympatric species conservation efforts would benefit the protection of these mammals when conservation attention is focused on the red panda and its habitat. We suggest that the red panda could act as a model species to initiate SSC at the landscape level. 3.2.5. Community conservation areas and community-based monitoring A large portion of red panda habitat lies outside protected areas (PAs); for instance, 77% of red panda habitat lies beyond PAs in Nepal (Jnawali et al., 2011) and is under high pressure from threats. 118

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poaching and illegal trade, developmental activities, and illegal herbal plant collection are the major threats to this species. The red panda faces big threats in Himalayan regions, including Nepal, India, and Bhutan, which might be due to low conservation capacity, illegal trade, poor awareness, and the lack of policy implementation. Still, poaching and the illegal trade of red pandas, as well as other wild species, are inherently challenging in the Himalayan region. The species still faces an uncertain future due to the impacts of human activities, thus justifying its classification as Endangered on the International Union for Conservation of Nature's Red List. Mass conservation awareness and strict law enforcement would be the best solutions to address threats relevant to poaching and illegal hunting in the Himalayas. Due to insufficient genetic data from the entire range, subspecies classification is questionable, but this is a fundamentally important taxonomic issue that should be addressed through multidisciplinary studies using modern morphological and genomic tools. We recommend extensive studies on other important aspects, including movement, microbiota, isotopes, pathogens, and threat-minimizing mechanisms. To improve conservation management for red panda survival, it would be useful to obtain detailed information on the current management status and its role in sustaining panda populations within protected areas, which are insufficiently documented. In addition, a large proportion of panda habitats lies outside protected areas, suggesting that alternative conservation approaches, such as designing corridors, implementing community-managed forestry, and establishing special conservation sites, should be initiated. The red panda is distributed multinationals, which suggests an urgent need to initiate regional coordination and cooperation in research, a common data hub and policy implementation to ensure the long-term survival of this species in habitats at regional and local scales. Supplementary data to this article can be found online at https:// doi.org/10.1016/j.biocon.2018.02.014.

Designing new PAs is not always feasible, and alternative conservation approaches, such as the establishment of new biological corridors, community conservation sites, community-managed forestry, and special species conservation sites, are essential to protect habitat. Priorities and benefit sharing rights belonging to local communities could make such conservation options outside PAs effective. Furthermore, establishing community-based monitoring at a local level would increase the effectiveness of conservation. Various income-generation options in local communities would deliver positive messages regarding conservation and aid in the long-term stability of monitoring activities. Such conservation actions have been implemented in the eastern part of Nepal with aims to protect 25% of Nepal's red panda habitat (Williams et al., 2011); however, an impact assessment is lacking. 3.2.6. Conservation education and awareness It is important to educate and increase awareness regarding red panda conservation among local communities, national governments and international audiences. Local people, including herders, hoteliers, and trekking guides, are not aware of the conservation importance of the red panda; therefore, the launching of awareness-increasing programs throughout its range is urgently needed (Shah and Thapa, 2012). The effectiveness of conservation management is increased by adopting local community-based monitoring programs that involve local people, such as herders, farmers, park rangers, and members of forest user groups (Williams et al., 2011). Recent studies suggest that 90% of respondents had positive attitudes toward red panda conservation in the Nepal Himalayas and further suggested that awareness programs focused on school children and community groups would be effective in increasing positive attitudes toward panda conservation (Sharma et al., 2017). Most villagers within the range of red panda habitat in India are not aware of the legal status of the species; thus, the conservation of red pandas could benefit from awareness programs (Choudhury, 2001). We recommend developing conservation toolkits (such as posters, brochures, booklets, hoarding boards) including information about the ecology and conservation significance of the species.

Acknowledgements

4. Conclusion

We thank the CAS-TWAS Presidential Fellowship Program for providing PhD fellowship to first author (Thapa A.) The National Key Program of Research and Development, Ministry Science and Technology of China (2016YFC0503200) and the National Science Foundation of China (31470441) supported this work. We thank to Dr. Sunita Pradhan, Tulsi Ram Subedi, and Pemba Dinup for recent red panda occurrence database access. We thank to Prof. Karan Bahadur Shah and Damber Bista for providing recent update on Nepalese national red panda survey and illegal trade trend information in Nepal Himalaya.

In this review, we have summarized the current knowledge regarding the red panda in its range countries, including its habitat ecology, foraging ecology, movement ecology, molecular ecology, microbiota, parasites and threat status. Despite all efforts, it was impossible to compare the results obtained regarding the estimated area of habitat and population size due to inconsistent methodologies. China has lead the attempts in the red panda research, with particular successes in molecular ecology, which has suggested that the non-invasive analysis of fecal DNA would help in estimates of wild panda populations. However, research activities in other countries have relied on surveys of the distribution of red pandas and habitat assessments based on feces as an indirect sign. Most recent studies have focused on wild populations, including their habitat ecology, feeding, parasites and genetic information; however, there have been limited attempt in terms of other aspects. Red panda habitat is composed of different forest types, including evergreen forests, evergreen and deciduous mixed broad-leaf forests, deciduous forests, deciduous and coniferous mixed forests, and coniferous forests mixed with different bamboo species are the dominant red panda habitats. Other important habitats are associated with a relatively high cover of bamboo, shrubs and canopy, high densities of fallen logs, relatively steep slopes, and proximity to water sources. More than 90% of the diet of red pandas is composed of the stable food source of bamboo, and trace amounts of other plant species, including fruiting plants, are also included in the red panda diet. Recent studies suggested evolution of gut microbiotas in pandas, which harbor distinct gut microbiotas. We have analyzed the general threats to red pandas in various regions, revealing 13 different types of threats. Habitat loss and degradation,

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