The long-tailed goral (Naemorhedus caudatus) is a member of the tribe Rupicaprini in the subfamily Caprinae (An, 2006). The distribution of this species ranges from the northern to central Baekdoodaegan mountain range in South Korea (Choi & Park, 2004; 2005; Yang, 2002). The goral has been listed as an endangered species (Ministry of Environment, 2004) and a natural monument (No. 217; Cultural Heritage Administration of Korea, 1999) by the South Korean government. Internationally, this species is also considered endangered (Baillie & Groombridge, 1996). Commercial trade of this species is prohibited in countries signatory to the Convention on International Trade in Endangered Species (Hutton & Dickson, 2000). The population size of the goral has gradually decreased to fewer than 800 individuals because of illegal hunting, overexploitation, habitat destruction, and habitat fragmentation in South Korea (Ministry of Environment, 2002; Yang, 2002).

In particular, habitat fragmentation is a major issue in the conservation of the goral. For wild populations, habitat fragmentation has caused decreased connectivity, i.e., the degree to which the landscape facilitates or impedes movement between resource patches (Coulon et al., 2004; Taylor et al., 1993). Heterogeneity caused by fragmentation can create natural barriers against population movement, because unfavorable habitats do not provide cover against predators or because distances between suitable patches are greater than can be rapidly crossed (Arnold et al., 1993). Therefore, the movement ability of wild animals may be altered by habitat fragmentation. Such changes can have negative consequences for wildlife populations, partially due to the reduction of gene flow between populations, which leads to greater inbreeding and loss of genetic diversity within fragments (Coulon et al., 2004; Frankham et al., 2002). Fragmentation can even lead to the extinction of species, and many studies on habitat fragmentation have focused on fragmentation created by barriers, such as roads, islands, and settlements (Burkey, 1989; Coulon et al., 2004; Soulé et al., 1992). In the case of wild goral in South Korea, few studies have hitherto been conducted on the ecology and genetics of this species (Choi & Park, 2004; 2005). Suitable goral habitats are expected to significantly decline and/or disappear from South Korea in this century (Lee et al., 2019).

Collecting elusive animal samples (e.g., tissue, blood, etc.) in the wild is difficult, but non-invasive sampling methods could overcome such constraints (Kohn & Wayne, 1997). Fecal sampling is the most frequently used method of obtaining wildlife DNA (Wehausen et al., 2004). As a useful genetic marker in non-invasive wildlife research, the mitochondrial cytochrome b gene has been used for phylogenetic, population, and forensic investigations (Parson et al., 2000). The nucleotide sequence of this gene contains species-specific information. Furthermore, the cytochrome b gene is located on the mitochondrial genome, making it suitable for forensic PCR-based mitochondrial DNA typing. Taxonomic researches—using invasive samples—based on mitochondrial genes, such as cytochrome b (An, 2006; Min et al., 2004) gene or D-loop (An, 2006) region have been conducted on the goral in South Korea. A population study on the goral was recently performed using invasive samples based on 12 microsatellite loci (Choi et al., 2015). For the first time to my knowledge, the present study assessed the phylogenic status and genetic diversity of the long-tailed goral inhabiting South Korea via a simple method using non-invasive fecal samples.


Samples and DNA extraction

A total of 64 goral fecal samples were collected from the wild (n=40) in Soraksan National Park, Injae, Gangwon Province, and a goral farm (n=24) in Yanggu, Gangwon Province, South Korea, during summer (July 4 and 6) 2005 and winter (December 16 and 17) 2006 (Table 1; Fig. 1). The samples were frozen at –70°C until experimentation. Genomic DNA was extracted from fecal samples using the method developed by Gerloff et al. (1995). Additional sequences (n=28) were obtained from a previous study (An, 2006). In total, I obtained 36 sequences (10, 17, and 9 for non-Soraksan, Soraksan, and unknown population, respectively; Table 1). All sequences were obtained from different goral individuals identified in another study (B.J. Kim, unpublished data).

Species-specific PCR amplification and sequencing

Partial sequences of the mitochondrial cytochrome b gene (337 bp) from the fecal samples were amplified via PCR using a new Korean goral-specific primer set developed in this study (NCF: 5’-atgatcaacatccgaaaaac-3’; NCR: 5’-ataggagggattaccccaata-3’). The PCR analysis was carried out using a 25 µL reaction volume containing 4 µL DNA template, 1X PCR buffer (iNtRON Inc., Seongnam, Korea), 2 mM MgCl2, 0.2 mM dNTP, 0.1 µM of each primer, 2.5 µg bovine serum albumin (Promega Inc., Madison, WI, USA), and 1.25U i-Star Taq polymerase (iNtRON Inc.). PCR amplification was performed in a PTC-100 Thermal Cycler (MJ Research, Inc., Watertown, MA, USA) as follows: initial denaturation for 3 minutes at 94°C, followed by 45 cycles (at 94°C for 60 second, 46°C for 45 second, and 72°C for 60 second) and a final extension for 3 minutes at 72°C. The PCR products were resolved through electrophoresis on 2% agarose gel, stained by ethidium bromide, and visualized under an ultraviolet illuminator. Of the 64 PCR samples, we selected 18 from the captive and wild populations, respectively, for sequencing (Table 1). Thirty-six PCR products were purified using a QIAquick Gel Purification Kit (QIAGEN Inc., Valencia, CA, USA). Purified PCR products were sequenced using the forward primer in an ABI PRISM 3100 Genetic Analyzer (Applied Biosystems Inc., Foster City, CA, USA). We only used 310 out of 337 bp for our sequence analyses.

Data analysis

In total, we used 36 sequences for data analysis (Table 1). The phylogenetic relationships between the haplotypes of gorals and serows were reconstructed via the neighbor-joining method (Saitou & Nei, 1987) using the Kimura 2-parameter model (Kimura, 1980). As outgroup, corresponding mitochondrial cytochrome b gene sequences of one goat (accession no. D84201) and one sheep (accession no. D84205) were chosen to root the phylogenetic tree (Douzery & Randi, 1997). Confidence in the estimated relationship was determined using the bootstrap approach (Felsenstein, 1985) obtained through 1,000 replicates using the same model as mentioned above. Bootstrap analyses and phylogenetic reconstruction were conducted using MEGA version 3.1 (Kumar et al., 2004). In addition, a minimum-spanning network was created combining goral haplotypes using TCS software (Clement et al., 2000). To determine goral genetic diversity, three haplotype sequences were aligned and edited using BIOEDIT version ( http://www.; Hall, 1999). Sequences that varied by at least one nucleotide were considered different haplotypes. Haplotype and nucleotide diversity were calculated according to Nei (1987), and the neutral molecular evolution hypothesis was tested according to Tajima (1989) and Fu and Li (1993) using DNASP version 4.10.9 ( Rozas et al., 2003).


Three goral haplotypes defined by only two polymorphic sites were found (Table 2). The polymorphic sites were a synonymous transversion (Ala, GCA/GCC) and a synonymous transition (Asp, GAC/GAT), and no insertion or deletion existed (Fig. 2). The haplotype (H) frequencies of H1, H2, and H3 were 0.056, 0.917, and 0.028, respectively, in the total Korean goral population. Among the three haplotypes, H2 was found in the non-Soraksan (1), Soraksan (0.882), and unknown (0.889) populations, but H1 was restricted to the Soraksan population (0.118), and H3 only occurred in the unknown population (0.111; Fig. 3). The frequency of H2 was similar in the non-Soraksan (1) and Soraksan (0.882) populations, excluding the unknown population (Fig. 3). I also tested the neutral evolution hypothesis for the Korean goral, and neither Tajima’s D value nor Fu and Li’s D value showed strong selective sweeps in this species (Table 2).

The consensus neighbor-joining tree was reconstructed with the three haplotypes and other reference sequences and rooted by two outgroup species, such as goat and sheep (Fig. 4). The three haplotypes formed a separate cluster from those of Chinese and Himalayan gorals but not from the Russian goral (Fig. 4). The latter showed one of the three Korean goral haplotypes (H2). Furthermore, TCS generated a 95% parsimony haplotype network for the Korean, Chinese, and Himalayan goral haplotypes (Fig. 5). The network showed a clearly separated distribution pattern between the Korean goral and Chinese and Himalayan gorals (Fig. 5). The haplotype diversity was 0.160 in the total population and ranged from 0 in the non-Soraksan population to 0.221 in the Soraksan population (Table 2). The nucleotide diversity was 0.053% in the total population and differed slightly between the non-Soraksan (0%) and Soraksan (0.071%) populations (Table 2).


The Korean long-tailed goral is a species in the tribe Rupicaprini, subfamily Caprinae, and family Bovidae (An, 2006). Within the tribe Rupicaprini, gorals and serows are classified as Naemorhedus and Capricornis, respectively (Mead, 1989; Nowak, 1999; von Dolan, 1963). In contrast, Groves and Grubb (1985) suggested that serows should also be classified as Naemorhedus (Corbet & Hill, 1992; Grubb, 1993). Few studies have hitherto reported genetic differences between the two genera (An, 2006; Min et al., 2004). The present study also showed similarities in the phylogenetic status of the two genera based on the neighbor-joining tree (Fig. 4) and maximum spanning network (Fig. 5). The Korean goral should be classified as a genus distinct from Capricornis. In addition, the Korean and Russian gorals have the same haplotype and clustered within the same clade (Fig. 4). However, the Chinese goral (N. caudatus) has relatively higher genetic variation than the Korean and Russian gorals do and therefore clustered with the Himalayan goral (N. goral; Fig. 4). This result agreed with those of previous studies (An, 2006; Min et al., 2004). For the reasonable solution of this taxonomical issue, more samples of Chinese and Russian gorals in eastern China and Russia adjacent to Korean habitats are necessary.

Based on the partial mitochondrial cytochrome b gene sequences (310 bp), only three haplotypes were found for the Korean goral (Table 2). The sequence divergence between these haplotypes was 0.4% for the total population (Table 2). Min et al. (2004) found only two haplotypes (Korean goral types a and b) in partial cytochrome b sequences (646 bp) of the species, with a 0.16% sequence divergence. According to a more recent study on the Korean goral (An, 2006), seven haplotypes (A) of complete mitochondrial cytochrome b gene sequences were identified (N. caudatus KG-a, b, c, d, e, f, and g), but the sequence divergence (ps) ranged from 0 to 0.4%. Furthermore, the haplotype (h=0.323) and nucleotide (π=0.053%) diversity of the species according to the present results were low (Table 2). In contrast, other ungulate species, such as moose (Alces alces; 403 bp; A=8; ps=0.2-1.8%; h=0.56-0.60; π=0-0.3%; Hundertmark et al., 2002), western red deer (Cervus elaphus; complete 1,140 bp; A=21; ps=1.86±0.22%; h=0.98±0.02; Ludt et al., 2004), and eastern red deer (C. elaphus; complete 1,140 bp; A=13; ps=1.27±0.020%; h=0.98±0.03; Ludt et al., 2004), showed relatively high genetic diversity in their mitochondrial cytochrome b gene sequences.

The population structure of the long-tailed goral has been rarely studied despite it being one of the most endangered species in South Korea. Yang (2002) reported that the total population consisted of many small, fragmented populations. Choi and Park (2004; 2005) indicated that Korean goral populations are isolated by local highways or forest trails in one of its main habitats. Using invasive sampling based on 12 microsatellite loci (n=68 gorals), Choi et al. (2015) recently reported that the goral population in the lower northeastern regions of South Korea was distinct from the upper northeastern population. The genetic integrity and individual identification of goral in Soraksan National Park were studied using non-invasive sampling based on the mitochondrial D-loop region (n=38 fecal samples) and nine microsatellite loci (Jang et al., 2020). This study is the first to report results of the phylogenic relationship and genetic diversity of the Korean goral compared with those of other species using non-invasive fecal samples. In particular, non-invasive molecular genetic studies using fecal samples could provide more information to support the conservation of South Korean goral populations.


This work was supported in part by Korea Environment Industry & Technology Institute (KEITI) through The Decision Support System Development Project for Environmental Impact Assessment, funded by Korea Ministry of Environment (MOE) (No. 2020002990009), and by the National Institute of Ecology (NIE), funded by Korea Ministry of Environment (MOE) (No. NIE-C-2020-04). This work was also partially supported by the Research Institute for Veterinary Science and the Brain Korea 21 Program for Veterinary Science, Seoul National University. The author thanks Prof. H. Lee and Prof. Y. .J. Won for supporting this experiment. The author also thanks many field surveyors for their participation in fecal collection.

Conflict of Interest

The authors declare that they have no competing interests.



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Figures and Tables
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Fig. 1

Map of Gangwon province, South Korea. Baekdoodaegan mountain range is located in Gangwon province, the main distribution range of Korean goral (Naemorhedus caudatus). Soraksan National Park is isolated from other areas by local highways and human settlements. The national park, including Mt. Sorak, consists of four different areas, namely Injae, Gosung, Yangyang, and Sokcho.

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Fig. 2

Alignment of partial sequences of mitochondrial cytochrome b gene of Korean goral (Naemorhedus caudatus) and closely related species. Dots represent same base as those of haplotype 1. Two polymorphic sites were found in Korean goral.

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Fig. 3

Haplotype frequencies of partial mitochondrial cytochrome b gene in Gangwon province, South Korea. Non-Soraksan population samples were collected from Yanggu (YG), Donghae (DH), and Samcheok (SC), and Soraksan population samples were collected from Injae (IJ), Gosung (GS), and Yangyang (YY). Three allele frequencies were found for each population. No information from samples was obtained from unknown population. n, sample size.

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Fig. 4

Consensus neighbor-joining tree of mitochondrial cytochrome b haplotypes of Korean goral (Naemorhedus caudatus) and closely related species. Tree was computed using Kimura-2-parameter distance matrix of haplotypes and was rooted using goat (Capra hircus D84201) and sheep (Ovis aries D84205) sequences as outgroups. Haplotypes 1, 2, and 3 were obtained from Korean goral. Nemorhaedus caudatus RG, Russian goral; Nemorhaedus caudatus U17861, Chinese goral; Naemorhedus goral HG, Himalayan goral; Capricornis crispus D32191, Japanese serow; C. sumatraensis DQ459334, Indian serow.

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Fig. 5

A 95% parsimony network of five goral haplotypes obtained via our sequence and previous sequence data. Each haplotype is represented by an oval, the size of which is proportional to haplotype frequency. Group A involved 27 Korean goral haplotypes (H1, H2, and H3) and one Russian goral haplotype (H2). Group B, separate from Group A, included Chinese and Himalayan goral haplotypes (CG and HG, respectively). Two groups differed with a large sequence variation. Each branch connecting haplotypes represents single mutation event. ---, 15 substitutions between H2 and CG; ◦, unsampled haplotypes.

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Table 1


No. Sample Haplotype Sample Individual Sampling site Reference
N=24 Non-Soraksan population
1 Cgrb1612 H2 Feces A Yanggu This study
2 Cgrb1613 A
3 Cgrb1614 A
4 Cgrb1617 A
5 Cgrb1618 A
6 Cgrb1619 A
7 Cgrb1620 A
8 Cgrb1621 A
19 Cgrb1622 C
10 Cgrb1623* C
11 Cgrb1624* A
12 Cgrb1625* B
13 Cgrb1626 C
14 Cgrb1629* D
15 Cgrb1630 A
16 Cgrb1633 D
17 Cgrb1634 D
18 Cgrb1635 A
19 KG09* Tissue - An (2006)
20 KG12* -
21 KG02* - Samcheok
22 KG03* -
23 KG23* -
24 KG30* - Donghae
N=31 Soraksan population
1 Cgrb1640 H1 Feces - Injae This study
2 Cgrb1641 -
3 Cgrb1642 -
4 Cgrb1643 H2 -
5 Cgrb1645* E
6 Cgrb1646 -
7 Cgrb1647 H1 -
8 Cgrb1653 H2 -
9 Cgrb1654* F
10 Cgrb1655* H1 G
11 Cgrb1659 H2 -
12 Cgrb1660* H
13 Cgrb1665 -
14 Cgrb1666 H
15 Cgrb1668 H
16 Cgrb1669 -
17 Cgrb1671 -
18 Cgrb1673 -
19 KG05* Tissue - An (2006)
20 KG17* -
21 KG18* H1 -
22 KG19* H2 -
23 KG20* -
24 KG26* -
25 KG27* -
26 KG28* -
27 KG02* - Gosung
28 KG03* -
29 KG16* -
30 KG29* Blood -
31 KG10* Tissue - Yangyang
N=9 Unknown population
1 KG01* H2 Tissue - Everland Zoo An (2006)
2 KG04* -
3 KG11* -
4 KG13* -
5 KG14* -
6 KG21* -
7 KG22* H3 -
8 KG24* -
9 KG25* -
N=7 Others
1 Russian goral RG Tissue - Russia An (2006)
2 Chinese goral CG GenBank - China U17861
3 Himalayan goral HG DNA - Singapore Zoo An (2006)
4 Indian serow IS GenBank - India DQ459334
5 Japanese serow JS - Japan D32191
6 Goat (outgroup) G - D84201
7 Sheep (outgroup) S - D84205

*Fecal samples used in this study. A, B, C, D, E, F, G, and H were previously identified as individuals via microsatellite genotyping analysis (B.J. Kim, unpublished data).

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Table 2

Summarized statistics for cytochrome b variation in Korean goral populations (Naemorhedus caudatus)

Statistics Population

Non-soraksan Soraksan Unknown Total
N 10 17 9 36
A 1 2 2 3
h 0 0.221 0.222 0.160
ps 0 0.300 0.600 0.400
π 0 0.071 0.072 0.053
Tajima’s D NA –0.491 (P>0.05) –1.088 (P>0.05) –1.284 (P>0.05)
Fu and Li’s D NA 0.677 (P>0.05) –1.190 (P>0.05) –0.800 (P>0.05)

N, fecal sample size; A, number of haplotypes in each population; h, haplotype diversity; ps, sequence divergence (%); π, nucleotide diversity (%); NA, not available.