Reintroduction（2011）1:31 – 36

INVITED ARTICLE

Captive propagation, habitat restoration, and reintroduction ofOriental White Storks (Ciconia boyciana) extirpated in South Korea* Shi-Ryong Park1, Jongmin Yoon1 and Su-Kyung Kim1
Abstract Reintroduction of wildlife that is extinct or

Key words Captive breeding, Habitat management,

extirpated in its ecological range becomes a new conser-

Korea Institute of Oriental White Stork Reintroduction

vation tool to restore the status of historic biodiversity in

Research Center, Reintroduction biology

ecosystems. However, reintroduction projects often meetthe uncertainty of successful results due to a lack of scientiﬁc knowledge on how the system previously worked.

Introduction

To minimize the reintroduction failure, successful captive

Reintroduction is an intended movement of wildlife

propagation should be followed by a series of assessing

into a part of its innate range to restore the status of thehabitat quality for the target species in reintroduction sites

historically extirpated population (Seddon et al. ₂₀₀₇;

before and after releases. The purpose of the present paper

Armstrong and Seddon ₂₀₀₈). Ecologists and wildlife

is to describe the past, present, and future efforts of Ori-

managers, in several decades, have not only sought toental White Stork (Ciconia boyciana) reintroduction inconserve currently viable populations but also attemptedSouth Korea. The species is listed as a globally endan-

to reintroduce individuals to previously damaged popula-

gered bird species currently breeding only in Russia andtions. However, the restoration projects often lack scien-

partially in China, and it has been extirpated in Japan andtifically manageable knowledge on how the system

South Korea more than a decade ago. Reintroduction of aworked previously with the interesting species and how astork population was recommended in Japan and the

population after releases will self-sustain in a given eco-

Korea peninsula. The last stork individual was translo-

system (McNab ₁₉₈₃). Successful reintroduction requires

cated and died in a zoo in 1994 so that Korea Institute ofa series of careful pre-release studies that include success-Oriental White Stork Reintroduction Research Center

ful captive breeding tightly linked with veterinary man-

(KIOWSRRC) was launched in 1996. Our captive breed-agement, habitat management of reintroduction sites, pre-ing effort tightly linked with veterinary management

release training programs, and future demography studies

yielded near one hundred captive storks in the facility up(Armstrong and Seddon ₂₀₀₈). The Oriental White Storkto dates. Prior to reintroduction, a wide range of GIS-

(Ciconia boyciana; hereafter stork), one of the large andrelated analyses using past breeding habitat information

long-lived stork family Ciconiidae, is listed as Endangered,determined reintroduction sites, which habitat quality forwhich status became deteriorated even from a Threatened

future releases began to be managed and restored. The

species in IUCN Red List of Threatened Species in ₁₉₉₄

pre-release training program is also scheduled prior to the(BirdLife International ₂₀₀₈). Now the four-related coun-ﬁrst reintroduction of 2013. The signiﬁcance of the rein-

tries in East Asia began to recognize the fast need of con-troduction projects in South Korea is to not only restore

servation acts on the remaining stork population.

the extinct population in their historic breeding ranges but

Historically the breeding stork populations were ranged

also augment the total size of the endangered metapopula-from Russia, northern China to Japan and the Korea pen-tion of storks in one of its historic regions.

insula (Luthin ₁₉₈₇). The last remaining breeding area forthe majority of the globally decreasing stork populations

₁

Korea National University of Education, Korea Institute ofOriental White Stork Reintroduction Research Center, San ₇,
Darak-ri, Gangnae-myon, Cheongwon-gun, Chungbuk, South
Korea ₃₆₃-₇₉₁* E-mail:currently become limited to the Amur-Heilong basin
ﬂoodplains along the border of Russia (Simonov andDahmer ₂₀₀₈). In the mean time, the sizes of stork populations both breeding in Russia (V. Andronov, personal
31

Reintroduction（2011）1:31 – 36

communication) and wintering in China (L. Z. Zhou, per-ably after breeding in Russia still visit the west coast of

sonal communication) have been critically decreasing,the Korea peninsula for wintering (Tomek ₁₉₉₉; Park andwhich was intensively discussed in the International Sym-

Cheong ₂₀₀₂; see Fig. ₁). Korea Institute of Oriental White

posium on Conservation of Oriental White Stork＇s Habitat

Stork Reintroduction Research Center (KIOWSRRC) was

and Population held in Hefei, Anhui, China of ₂₀₁₀. Nev-

established in ₁₉₉₆ to restore the extirpated stork popula-ertheless, the status of this species in the Korea peninsulation in South Korea, starting with a series of stork imports

was described as not uncommon prior to Korea War infrom foreign countries for captive propagation and cur-₁₉₅₀–₁₉₅₃ (Campbell ₁₈₉₂) where Austin (₁₉₄₈) also

rently planning on the reintroduction of storks into thedepicted that individual stork nests were at least ₁₀₀ m

wild. The purpose of the present manuscript is to describe

apart at the rate of one nest to one village (i.e., fairly high₁) captive breeding effort and ₂) habitat management ofbreeding densities as a non-colonial breeder; Fig. ₁).

reintroduction sites, and ₃) reintroduction plans, followed

Although it became listed as Natural Monument No. 199by ₄) future directions in the stork reintroduction projectby Cultural Heritage Administration of Korea as well as

conduced in South Korea.

Endangered Species Level 1 by Korea Ministry of Environment, the last breeding pair remained in South Korea
until the male was killed by a careless hunter in ₁₉₇₁, andCaptive propagation and veterinary management

then the widowed female was translocated to and lived in

We have run the captive breeding project with import-

Seoul Zoo until ₁₉₉₄. To our knowledge, the population

ing a total of ₃₈ storks periodically from Russia, Germany,of breeding storks ranged in the Korea peninsula has

and Japan since ₁₉₉₆ (i.e., ₂₆ individuals from Russia,

become extirpated more than a decade ago presumably

four individuals from Germany, and eight individuals

due to Korea War and elongated habitat loss. Similarly,

from Japan), resulting in a total of ₉₆ viable storks in thethe latest breeding status of the North Korea population

facility up to dates (Fig. ₂). Three types of enclosures

has been reported as very scarce and sporadic until ₁₉₇₇

were maintained in the stork Reintroduction facility: ₁)(Tomek ₁₉₉₉). Finally, the signiﬁcance of the reintroduc-large public enclosures, ₂) breeding enclosures, and ₃)

tion project has been strongly recommended in Japan andlarge semi-natural habitat enclosures. First, to establish

South Korea (Luthin ₁₉₈₇). Since the last breeding stork

breeding pairs, individuals were naturally induced topair was lost in South Korea in ₁₉₇₁, the small number ofinteract with each other in two larger enclosures. Second,

storks (i.e., approximately ₁₀ to ₂₀ individuals) presum-

breeding pairs were translocated to each nesting area withnesting materials and a nesting pole prior to reproduction

Fig. ₁. The approximate distribution of breeding and non-breeding oriental white storks (Ciconia boyciana) prior to the extirpation in the Korea peninsula with its current wintering range only
in South Korea (S. K. Kim, unpublished data).
32

Fig. ₂. The progress of the captive propagation made by Korea
Institute of Oriental White Stork (Ciconia boyciana) Reintroduction Research Center in South Korea. Bars denote numbers of
captive storks imported from Russia, German, and Japan, ﬂedged
successfully, and dead in ₁₉₉₆–₂₀₁₀.

Park et al.: Stork reintroduction in South Korea

Table ₁. Reproductive rates of captive oriental white storks (Ciconia boyciana)＇ nests in Korea
Institute of Oriental White Stork Reintroduction Research Center, South Korea in ₁₉₉₆ – ₂₀₁₀. Data
are limited only to the ﬁrst breeding attempts and rates without assisted parental care in captivity.
Fledging success indicates the success that a nest produces at least one ﬂedgling.
Reproductive
rates
Mean
±₁·SE (n)Clutch size

Incubation
period (days)

Hatching
success

Nestling period(days)

Fledgenumbers

Fledging
success

₄.₂₇
₀.₁₇ (₃₀)

₂₉.₉₂
₂.₁₅ (₂₆)₀.₉₀
₀.₀₇ (₂₁)₅₅.₉₁
₃.₉₃ (₁₁)₂.₀₈
₀.₃₁ (₁₃)₀.₉₂
₀.₀₈ (₁₃)(i.e., total ₂₅ breeding cages) when they exhibited courtHere, storks with other member of Family Ciconiidae are

Pre-release habitat management of reintroduction
sites

not sexually dimorphic, resulting in a common misidenti-

The ecological evaluation of reintroduction sites is one

ﬁcation for sexing while establishing pairs due to a falseof crucial issues in reintroduction biology. First, we sur-sign of courtship (King ₁₉₉₀). To identify correct sexes in

veyed the past breeding sites through intensive literature

captivity, a non-invasive method for sexing was devel-

and face-to-face interviews with local people to find

oped using bill morphology from high-resolution photog-

potential reintroduction sites (Kim ₂₀₀₉a; Park et al.

raphy (Cheong et al. ₂₀₀₇); another simple and universal

₂₀₁₀), which was intended to be close to the originality ofsexing method was found using a multiplex polymerase

its historic range for reintroduction (Armstrong andchain reaction (PCR) for storks as well as other avian

Seddon ₂₀₀₈). A total of ₂₆ past breeding sites were foundspecies (Han et al. ₂₀₀₉a, ₂₀₀₉b). In captivity, both males

in Chungcheong-do and Gyeonggi-do (Fig. ₃). Contrast-

and females contributed for reproduction including nest

ing the landcover characteristics of the used breeding sites

building, egg incubation, and post-hatching nestling carein the past to the randomly selected unused sites using(Cheong et al. ₂₀₀₆). Artiﬁcial incubation, cross-fostering,

remote-sensing data with a GIS-based tool, the potential

or hand-rearing chicks were also applied when parents did

reintroduction sites that exhibited higher percentages of

not exhibit appropriate parental behaviors on occasion

paddy ﬁelds, grasslands, and closed to urbanized area

during the incubation or nestling period (Cheong ₂₀₀₅).

were narrowed down (Kim et al. ₂₀₀₈; Kim ₂₀₀₉a). The

Since the ﬁrst captive breeding in ₁₉₉₆, storks pairs haveselection of the ﬁrst reintroduction sites (Dae-ri, Kwangsi-

produced a total of ₇₆ viable ﬂedges up to dates (Table ₁,

meyon; ₃₆°₃₂′₄₂.₃₅″N, ₁₂₆°₄₇′₀₅.₇₇″E) did not also occur

ship displays among socially interacting individuals.

see also Fig. ₂). During the period of captive propagation,
diagnosis and treatment of disease in captive storks havebeen monitored by the veterinary medical center in
Chungbuk National University since ₂₀₀₅. The team ofthe veterinary medical center established a diagnosis
method for abnormal health conditions in captive storks(Han et al. ₂₀₀₉c; Han et al. in prep.). Third, one large
top-open enclosure provided a semi-natural habitat wherea ﬂock of captive storks after being clipped their primary
ﬂight feathers were allowed to compete for supplied foodresource and experience a variety of foraging areas thatdiffered in vegetation and water depth as a part of prelease training for future reintroduction.
Fig. ₃. Historic breeding sites of oriental white storks (Ciconia
boyciana) in Gyeonggi-do, Chungcheongbuk-do, andChungcheongnam-do, South Korea. Dots indicate locations ofbreeding sites, based on literature surveys (ﬁlled dots) and faceto-face interviews (opened dots; Kim ₂₀₀₉b).


33

Reintroduction（2011）1:31 – 36

without the ﬁnancial and political supports of Yesan Prov-

Similarly, the habitat use of herons and egrets varied

ince and Cultural Heritage Administration of Korea inthroughout the year, depending upon food availability in₂₀₀₉. The selected habitats in the reintroduction region

paddy ﬁelds and riparian areas in South Korea (Choi et al.

were re-examined by a series of ecological evaluations,

₂₀₀₇, ₂₀₀₈). However, more data on food availability andincluding the assessment of wetland biodiversity, agricul-

habitat quality on reintroduction sites are critically needed

tural types (i.e., pesticide-used vs. ecologically friendly

prior to stork releases.

agriculture), hydrology with pollution level, topography,
distance to rivers, and total available area for reintroduced
Storks in South Korea are known to be a representative

Pre-release behavioral training and reintroduction
planof wetland species foraging in primarily paddy ﬁelds,

We established a pre-release behavioral training andriparian areas, and various types of wetlands in the past

reintroduction plan for captive storks in addition to habitat(Park et al. ₂₀₁₀). The reintroduction sites occupy mainly

management. Here, captive-bred animal training prior tolarge and connected patches of paddy ﬁelds where foodreleases is known to play a crucial role in survival rate ofavailability is anticipated to one of the major habitat

reintroduced animals (Sutherland ₁₉₉₈; Griffin et al.

requirements for breeding storks. However, the current₂₀₀₀). An experimental pre-release of captive storks into

project lacks sufﬁcient knowledge on the breeding ecol-a large bird cage containing various habitat types withogy of storks due to the historically early extirpation innatural prey items supplied from the reintroduction sites

South Korea. Instead, we have attempted to investigate

is anticipated to facilitate the ﬂying and foraging ability

and manage food availability in association with agricul-of captive storks prior to reintroduction (K. Naito, per-tural methods and habitat types for future reintroduction

sonal communication). Subsequently, small numbers ofsites. For example, more mudﬁsh (Misgrnus and Channa

captive pairs (i.e., less than ten individuals) are scheduled

species), potential food sources for breeding storks in

to be released into the reintroduction sites in ₂₀₁₃, based

reintroduction sites, and higher biodiversity were found inon the progress of the current habitat restoration effort.

the paddy ﬁelds with the mixed characteristics of shallow

These release sizes should be carefully considered because

ponds, water ﬂows for the movements of fresh-water ﬁsh,storks generally maintain large home ranges during theand ecologically friendly agricultural methods without thebreeding season (Jiguet and Villarubias ₂₀₀₄), and ele-

history of pesticide use (Cho ₂₀₁₀; Ra ₂₀₁₀). In addition,vated numbers of breeding pairs per area can also elicit ashallow-water paddy ﬁelds appeared to contain more tad-negative density dependent feedback effect on reproduc-poles and mudﬁsh compared to other types of wetlands intive rates (Denac ₂₀₀₆). To minimize this likelihood, we

the reintroduction sites (Sung et al. ₂₀₀₈; Kim ₂₀₀₉b).

still try to ﬁnd an optimal level of how establishment

storks.

In addition to the assessment of food availability, weprobability will be improved by a combined effect ofalso plans to monitor the foraging ecology of other exist-

release sizes and habitat quality during the breeding anding members of the order Ciconiiformes such as the gen-non-breeding seasons. A survey of historical breedingera of Egretta and Ardea that exhibit a similar foraging

sites was evidence for an approximate range of ₅₀ and ₁₀₀

preference to storks in relation to differences in the struc-breeding stork pairs in South Korea (Kim ₂₀₀₉b), which

ture of paddy ﬁelds and agricultural methods in a large

is ideally aimed for the self-sustainable number of thescale throughout the year. Other studies paid attention to

reintroduced stork population close to its historical origi-

egrets and herons as an indicator species for predicting

nality. Nevertheless, numbers of releases in consecutive

habitat-specific food availability of storks in Japan

reintroductions should be determined after monitoring(Nakajima et al. ₂₀₀₆). It was found that major foraging

habitat-speciﬁc densities and vital rates of previously

habitats of egrets and herons tended to be paddy ﬁelds

released individuals along with the current status of habi-

during the breeding season and riparian areas near rivers

tat quality.

during the non-breeding season presumably due tochanges in the aquatic fauna throughout the year in Japan.
34Park et al.: Stork reintroduction in South Korea

Future directions
What ecological conditions for wildlife reintroductionof elementary and middle school students signiﬁcantly
yielded a positive attitude moving towards the signiﬁcance of wildlife conservation (Kim et al. ₂₀₁₀).

are needed for the future persistence of a newly estab-

Conclusively, our reintroduction effort of the extirpatedlished population would be a key question in reintroduc-stork population that previously bred in South Korea

tion biology. First, the reintroduction incidence of stork

along with the breeding population newly being estab-

individuals will be followed by an intensive monitoring

lished in Japan is likely to expand the total metapopula-for population demography to project its growth ratetion size of globally endangered storks in the world.

(Schaub et al. ₂₀₀₄) as well as a satellite-tracking effort

Based on the historical prediction of a directional stork

to estimate home range sizes and study habitat selection.

migration from the Korea peninsula to Japan (Y. Ohsako,

Second, an adaptive management strategy after reintro-

personal communication), the released stork population

duction will be also applied to assess how the system after

from South Korea may also interbreed with the stork

reintroduction will work in the current ecological condi-

population in Japan and facilitate the genetic diversity oftion (Sarrazin and Barbault ₁₉₉₆; Schreiber et al. ₂₀₀₄). It

storks in Japan in the near future.

is because a preliminary failure of reintroduction tends toprovide useful information on habitat requirements (e.g.,

Acknowledgements

food availability) for reproduction and survival of newly

The present study was carried out with the support ofestablished wildlife (Armstrong et al. ₂₀₀₇; see also

＂Cooperative Research Program for Agriculture Science

Armstrong and Seddon ₂₀₀₈). For example, this manage-and Technology Development (Project No. PJ₀₀₇₅₂₂)＂

ment strategy will be also allowed to estimate proper

provided by Rural Development Administration, South

habitat compositions through a series of food supplemen-

Korea.

tation experiments at reintroduction sites. Third, theextension of ecologically friendly agriculture in paddy
ﬁelds for storks＇ major foraging sites will be continued not
only at our reintroduction sites but also in potential areas
after the dispersion of releases during the breeding andnon-breeding seasons. Currently, a group of rice farmers
chose an eco-friendly agricultural method in a core partof reintroduction sites (i.e., approximately ₃₉,₀₀₀ m₂)
with a full support of Rural Development Administration
in South Korea. This method involves no use of chemicals, the year-around maintenance of shallow water depth(e.g., above ₈ cm), and biotope establishment connectedby water ﬂows for maintaining a wide range of aquatic
fauna in paddy ﬁelds. This agricultural movement throughnurturing young farmers with new intellectuals is expected
to attract more local rice farmers and also landlords in theregion of reintroduction sites. Lastly, we have offered awide range of environmental education programs for thesigniﬁcance of wildlife conservation and reintroduction
biology to local students in the reintroduction sites toimprove their fundamental knowledge and attitudes
towards future stork reintroduction. It was even found thata short-term environmental education program with the
topic of biodiversity and wildlife conservation for a group

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