Introduction

Within the 40 species (Gilbert et al., 2006) included in the 16 genera of mammals classified as the Order artiodactyla Family Cervidae, the sika deer, classified as 'Cervus nippon', is said to comprise 16 subspecies, although this is a point of contention among scholars. Of the 16 subspecies, 6 subspecies are locally endangered or near-extinction (Cervus nippon centralis, C. n. grassianus, C. n. keramae, C. n. mandarinus, C. n. taiouanus, C. n. pseudaxis) while the other 10 subspecies (C. n. kopschi, C. n. pulchellus, C. n. sichuanicus, C. n. hortulorum, C. n. mageshimae, C. n. mantchuricus, C. n. nippon, C. n. yakushimae, C. n. yesoensis, C. n. pulchellus) have been reported worldwide in places such as Taiwan, Japan, and Europe as well as on the Korean peninsula (Groves, 2006; Harris, 2015; Schmid et al., 1993).

The sika deer (Cervus nippon ssp.) population in Europe was brought to France in 1890 and the Czech Republic in 1891 for hunting and zoo exhibitions. Individuals that had escaped or been released adapted to their new environment. As a result, the sika deer population spread across continental Europe (McCullough et al., 2009) where it was classified as an invasive species due to genetic disturbance resulting from interbreeding with wild individuals, ecosystem disturbance caused by excessive consumption of plants, and economic loss due to agricultural damage. Continuous efforts, such as regulating the import and proliferation of sika deer, have been made to reduce their adverse impact (McCullough et al., 2009; McLaughlan et al., 2014; Vilà et al., 2010).

Sika deer have also caused problems in other places. Japan, the deer’s native habitat, implemented the Conservation and Management Plan for Sika Deer (CMPS4) to prevent damage from overpopulation of the species (Ijima et al., 2015; Kaji et al., 2010). The population of Cervus nippon ssp. across the entire region of Hokkaido was controlled between 2013 and 2017 (Ijima et al., 2015).

In South Korea, a large number of sika deer (Cervus nippon ssp.) were imported from Japan and Taiwan for velvet antlers and deer blood from 1956 to 1975, but the import of deer has only been suspended since the 1997 IMF crisis (Woo et al., 2008). Furthermore, the endemic species of Korea, C. n. hortulorum (called ‘spotted deer'), has been locally extinct since 1940 due to indiscriminate poaching for medicinal purposes and the mammals relief project during the Japanese colonial period. Only a small number of wild individuals have been known to inhabit the region around Baekdusan Mountain (Won & Smith, 1999). As a result, C. n. hortulorum was designated as Class I endangered wildlife in 2005 (Ministry of Environment, 2005). Therefore, the wild sika deer populations currently found in South Korea are judged to be the escaped/released/abandoned exotic deer imported before 1997. However, two other subspecies of sika deer can be found in Korea: Formosan sika deer (C. n. taiouanus; Hwang et al., 2014) in Songnisan National Park and Honshu sika deer (C. n. centralis; Moon et al., 2016) in Geumodo Island district, Nam-myeon of Dadohaehaesang National Park.

In this study, sika deer populations, confirmed to exist in Taean-eup, Taean-gun, South Chungcheong Province, were investigated where civil complaints were raised due to damage caused by the exotic deer. Individuals from a population overseen by the Agency for Defense Development (ADD) had escaped and damaged rice paddy fields in the surrounding area. This study aimed to identify the characteristics of the population through a subspecies-level phylogenetic analysis, analysis of the population size, and investigation of the damage done by the invasive deer. Additionally, the ecological characteristics of the exotic sika deer and possible problems were investigated through a literature review to provide useful reference data for the establishment of a management plan.

Materials and Methods

History of the exotic sika deer in the study area

The ADD’s site, about 330 ha, is classified as a military protection zone and has a structure surrounded by double barbed wire for security, making it a difficult environment to escape. The breeding of the exotic sika deer began in the 1980s when two pairs of male and female exotic sika deer, their age and species unknown, were donated to the ADD’s site. In the early stages of breeding, they were confined in cages with managed feeding, but as the number of individuals increased rapidly, they were released within the site. However, when the control was loosened, some individuals escaped by destroying a part of the barbed wire structure. Exotic sika deer appeared in Taean-eup, Taean-gun, South Chungcheong Province, and caused civil complaints due to damage to cultivated land. Through exploration and field surveys, these deer were identified as the ADD escapees. The escaped individuals have had a damaging impact on the surrounding cultivated land and private houses.

Phylogenetic analysis

As for the exotic sika deer inhabiting the country, with the introduction of many different subspecies, farmed individuals escaping into the wild, and frequent interbreeding between wild and farmed populations, classification of species or subspecies based on visual observation is difficult. Therefore, in this study, subspecies identification was conducted by performing DNA sequencing using samples of antlers, hair roots, and feces collected from the exotic sika deer settled in the region.

Samples of feces, hair, and antlers collected from deer in Taean were used for DNA sequencing. Feces were sampled by scraping the surface of the feces with a knife, hair was sampled by cutting the hair root, and antlers were sampled by scraping the basal burr (the site of antler growth) with a knife (Table 1). DNA sequencing of cytochrome b (CytB) gene (1,140 bp) was performed with the QIAamp DNA Micro Kit (Qiagen). No DNA was isolated in the feces samples (Fig. 1), but DNA sequencing was possible in the hair and antler samples.

Survey on population size and damage status

Through the field survey of ADD, the population size was identified through the examination of footprints and visual observation of sika deer inhabiting the site. The characteristics of the main habitat and plants resources were also investigated. Additionally, researchers visited nearby private farmhouses around the site to conduct interviews and surveys on specific cases of damage caused by the escaped deer.

Investigation on the necessity of sika deer management by literature review

Through a literature review, the ecological characteristics of individuals and the possibility of pathogenic infection were investigated. The need for sika deer management to prevent their escape and dispersal was investigated by analyzing the current status of sika deer farms.

Results and Discussion

Phylogenetic analysis

The result indicated that all samples were from an identical species. Through analysis of a phylogenetic tree, it is thought that the exotic deer introduced to the ADD’s site was ‘Cervus nippon yesoensis Heude, 1884’, a subspecies of Japanese sika deer (Fig. 2). The Korean names of Cervus nippon yesoensis are ‘에조(meaning Yezo deer)’, ‘북해도사슴(meaning Hokkaido dear)’, and ‘홋카이도사슴(meaning Hokkaido dear)’, and the English names are 'Yezo sika deer', 'Yezo sika' or 'Ezo sika deer'.

The Yezo deer originated from Hokkaido, Japan, but its migration within the country is restricted due to the nature of Japan as an archipelago, limiting the distribution of the deer to Hokkaido. The deer inhabits various types of land such as forests and grasslands, can adapt to different climatic zones, and is known as a species with a strong tolerance to cold climate (McCullough et al., 2009; Ohtaishi, 1986). In the past, the population declined sharply due to hunting, and the species went nearly extinct, requiring protection. However, due to excessive proliferation of the species, it currently damages crops and negatively affects the ecosystem. Accordingly, Japan implemented from 2000 to 2012 the first stage of the CMPS to control the sika deer population (Ijima, 2015; Kaji et al., 2010).

This study is the first of its kind to identify escaped Yezo deer in the wild in South Korea using phylogenetic analysis. The finding was confirmed by Ecological Studies of Alien Species of the National Institute of Ecology (Park et al., 2020).

Population size and damage status

The two pairs of male and female exotic sika deer introduced to the ADD site in the late 1980s bred on the site and adapted well to the climate of Taean. The number of individuals rapidly increased to 280 in 2018. Around 10 groups of Yezo deer, consisting of a range of 8 to 53 individuals, respectively, were confirmed to inhabit the ADD’s site. The main habitat of the large group was located in an area of large grassland near drinking water sources such streams and ponds. Pennisetum alopecuroides, Glycine soja, Persicaria perfoliata, Crassocephalum crepidioides, and Camellia japonica’s fruit were used as resources for the sika deer.

Yezo deer are herbivores feeding on extensive range of herbage, consuming herbaceous plants, twigs of trees, bark and fallen leaves (Fukuda et al., 2015; McCullough et al., 2009; Takafumi et al., 2015). Their feeding behavior and rubbing of antlers on trees damaged landscaped trees, flowing plants and herbaceous layers in forests as well as caused tree deaths on the ADD’s site (Fig. 3). Due to frequent movement of the herd, there was a risk of slope failure caused by soil loss on the slopes at the edge of the forest on the ADD’s site. Furthermore, there have been reports that the escaped individuals from the ADD’s site invaded a rice paddy field after rice planting in Taean and caused destruction and economic loss in 2019 and 2020 (Park et al., 2020).

Necessity of management

The average height, length, and weight of Yezo deer are 105.2 cm, 112.6 cm, and 126.9 kg for stags, and 94.8 cm, 103.9 cm, and 83.9 kg for does. Yezo deer are classified as the largest deer in size among subspecies of sika deer (Suzuki et al., 2001). Their extensive feeding behavior and large size are expected to cause negative ecological impact on the surrounding area when individuals from deer farms escape. Their size poses a risk on the road where road kills and accidents can incur further costs. Yezo deer may also compete for food and habitat with other Cervidae, such as the roe deer (Capreolus pygargus) and water deer (Hydropotes inermis). Moreover, because there are many individuals within the ADD’s site, damage to structures such as the barbed wire on the site, and the resulting maintenance and repair costs, may continue. As for the sika deer, a higher taxa of Yezo deer, there have already been reports of ecological damage in Europe through interbreeding with phylogenetically related species, competition with Odocoileus virginianu (Artiodactyla), excessive feeding, and antler rubbing. Furthermore, due to excessive disturbance by understory herbage feeding and frequent movement, there is a risk of soil loss and slope collapse in some steep slopes.

Yezo deer may interbreed with C. n. hortulorum, whose presence in South Korea was confirmed in the past, C. n. taiouanus inhabiting Songnisan National Park, and C. n. centralis inhabiting and Dadohaehaesang National Park. However, since C. n. hortulorum is regarded as in a state of local extinction, the possibility of interbreeding is thought to be low. The sika deer bred in deer farms are considered to be hybrids imported from Japan and Taiwan, and it is thought that interbreeding may be possible if there are escaped or released individuals.

The respective deer populations inhabiting the Hidaka, Daisetsu, and Akan regions of Hokkaido, the native habitat of the Yezo deer, were confirmed to have low rates of inter-population migration and interbreeding, although these populations are not geographically isolated (McCullough et al., 2009). The population in Hokkaido migrates according to snow, distribution of draft bamboo, distribution of highly preferred food, and the cover of conifers (Ijima, 2015; McCullough et al., 2009).

Ten species of parasites and three species of ectoparasites were observed in the Yezo deer population inhabiting Hokkaido (Kitamura et al., 1997). Half of the population about 47.5% was identified as the host of Toxoplasma gondii, the pathogen of toxoplasma (Hoshina et al., 2019) (Table 2). There are five zoonotic pathogens hosted by sika deer (Cervus nippon spp.). Special attention is required as that the deer can become a carrier of Borrelia burgdorferi, the pathogen of Lyme disease (which is fatal to humans), Cryptosporidium parvum, the pathogen of cryptosporidiosis, and the rabies virus, the cause of rabies (Wardeh et al., 2015). Parasitic mites were identified in the Yezo deer population of ADD, but the individuals infected with mite-induced diseases were not identified.

Subspecies information is not available for the sika deer individuals in the 1,732 nationwide deer farms, so it is difficult to predict the probability of Yezo deer escapes. However, considering there are 12,235 individuals registered as sika deer (Ministry of Agriculture, Food and Rural Affairs, 2019) (Table 3), there is a possibility that these farmed sika deer may be introduced into the wild due to escape from poor management and farm closures.

Since the velvet antler yield per unit weight for Yezo deer is smaller than other species such as red deer and elk (Woo et al., 2008), it is expected that the population of Yezo deer may be replaced by that of red deer or elk. In addition, due to the decrease in the price of velvet antler because of the increase in its import, making stable income generation from the velvet antler business difficult, the numbers of deer farms and individuals of sika deer have continued to decrease since 2000 (Ministry of Agriculture, Food and Rural Affairs, 2019). Therefore, it is considered necessary to identify the phylogenetic information on the subspecies of sika deer farms nationwide and establish a management plan to distinguish exotic sika deer from C. n. hortulorum which is the second grade endangered species of wild fauna and flora of the ministry of environment.

Sika deer was introduced into Korea for breeding, warfare, and economic purposes, but escaped due to negligence in management or was discarded due to economic deterioration and was released into the natural ecosystem. Currently, in Korea's natural ecosystem, various subspecies of sika deer are found inhabiting various regions across the country, including Jeju Island and Songnisan National Park.

The sika deer inhabiting the site of the Defense Science Research Institute (ADD) located in Taean-eup, Taean-gun, Chungcheongnam-do investigated in this study was 1) feeding damage to herbs, shrubs and sub-trees, 2) Rubbing with altler to kill the tree. And due to their habit of migrating along forest edges 3) excessive soil loss on slopes, 4) destruction of herbaceous layers due to compaction, and finally 5) damage to infrastructure have been investigated. The population, which was two pairs (four individuals) in the 1980s, increased to about 280 in a survey in 2018, just 30 years later, and due to excessive density, it spread and invaded nearby cultivated land, affecting it.

Based on DNA analysis of the hair and cast antlers, it was identified as Cervus nippon yesoensis, a subspecies of sika deer, which is the first confirmed case of the subspecies in South Korea. Through previous studies, there are found that including Yezo sika deer, “C. n. centralis” in Songnisan National Park and “C. n. centralis” in Geumodo Island district of Dadohaehaesang National Park. Already, Songnisan National Park is applying catch management to control the growing “C. n. centralis” population in this country.

We have more than 1,700 deer farms across the country, so there is always a possibility that the bred deer may be leaked into the natural ecosystem due to the closure of the farm or negligence in management (Kim et al., 2016; Song et al., 2017; 2018). As studied in the case of the Yezo sika deer, it is necessary to establish a management plan to prevent the exotic sika deer from invading the natural ecosystem. Therefore, conducting a regional habitat survey at the subspecies level of sika deer will be the first step in establishing a plan and preventing further ecological damage.

Acknowledgments

This project is supported by a grant from the Korea Environment Industry & Technology Institute (201800227001 and NIE-D-2021-28) and National institute of Ecology (NIE-A-2021-08).

Acknowledgement

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

Samples collected from the physical training field (Left: feces, Right: hair).

pnie-3-2-115-f1.jpg
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Fig. 2

Subspecies of sika deer identified by DNA sequencing of cytochrome b gene (1,140 bp) and the result of phylogenic tree analysis (Ba et al., 2015).

pnie-3-2-115-f2.jpg
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Fig. 3

Observed sika deer population at the ADD (Agency for Defense Development) study site and their impact on vegetation. (A) Group of sika deer. (B) Footprint. (C) Damage by horn rubbing. (D) Damage by feeding.

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Table 1

Sampling method by type of samples and gene identification result

Type of sample Sampling method Gene identification result
Feces Scrape the surface with a knife for sampling Unidentified
Hair Cut the hair root for sampling Identified
Antler Scratching the basal burr with a knife for sampling Identified
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Table 2

Pathogenetic parasites hosted by sika deer and Yezo deer

Classification of parasites Scientific name Zoonotic infection Infection symptoms
Trematodes Dicrocoelium dendriticum * O -
Cestodes Anopolcephalidae gen. sp.* X -
Nematodes Gongylonema sp.*
Gongylonema pulchrum
-
Spiculopteragia houdemeri - -
Rinadia andreevae * - -
Ostertagia ostertagi * - -
Mecistocirrus sp.* -
Nematodirus heletianus * X -
Capillaria bovis* O Capillariasis
Trichuris sp.* O Diarrhea and vomiting in children
Ectoparasites Haemaphysalis japonica * O -
Solenopotes sp.* O -
Trichodectidae gen. sp.* O -
Conoidasida Cryptosporidium parvum *** O Cryptosporidiosis
Toxoplasma gondii ** O Toxoplasma
Bacteria Borrelia burgdorferi *** O Lyme disease
Virus Rabies sp.*** O Rabies virus
Fungi Trichophyton mentagrophytes *** O Tinea capitis
[i]

O, infected; X, not infected; △, rarely infected; -, no data available.

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Table 3

Number of deer farms and farmed deer population by region

Region Number of deer farms Number of farmed deer Number of farmed sika deer individuals
Seoul 1 10 10
Busan 9 87 73
Daegu 8 53 20
Incheon 25 318 298
Gwangju 4 244 89
Daejeon 7 90 67
Ulsan 32 482 373
Gyeonggi 290 4,142 2,361
Gangwon 146 2,237 1,580
Chungbuk 187 2,349 777
Chungnam 375 5,094 739
Jeonbuk 149 2,095 1,041
Jeonnam 126 2,879 1,322
Gyeongbuk 158 2,509 800
Gyeongnam 178 3,184 2,307
Jeju 22 575 317
Sejong 15 324 61