41

Migration of Birds in East Asia with Reference to
the Spread of Avian Influenza
Noriyuki YAMAGUCHI* and Hiroyoshi HIGUCHI
Laboratory of Biodiversity Science, School of Agriculture and Life Sciences,
The University of Tokyo
1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan.
*e-mail: noriyuki@es.a.u-tokyo.ac.jp

Abstract
Avian influenza, highly pathogenic avian influenza, in particular, is now one of the most serious infectious diseases of poultry and wild birds. It is suspected that wild bird may spread the viruses widely. Humanand material movements, however, are also candidates for spreading the viruses. To evaluate the relative
contribution of wild birds, precise movement data of potential host species are needed. Satellite tracking is a
powerful technique for studying bird movements on middle (within a country) to large (global) scales. We
review satellite tracking studies on migratory birds such as cranes, storks, waterfowl and hawks in Asia, anddiscuss the contribution of such research to examining the role of wild birds in the spread of LPAI/HPAI inthis area.
Key words: avian influenza, infectious disease, migration, migratory birds, satellite tracking

1. Introduction
Avian influenza, in particular highly pathogenic
avian influenza (HPAI), is now one of the most serious
infectious diseases for poultry and wild birds, since theviruses cause outbreaks and a high risk of fatality(Subbarao et al., 1998; Alexander, 2000; Fouchier et al.,
2004; Liu et al., 2005; Olsen et al., 2006). HPAI
emerges by switching from low pathogenic avian influenza (LPAI) through repeated transmissions among
poultry or in live bird markets (Webster et al., 1992;
Alexander, 2000; Hulse-Post et al., 2005). Waterfowl
are common reservoirs of LPAI (Alexander, 2000;
Munster et al., 2005; Olsen et al., 2006) and most exhibit long distance migration between their breeding andwintering grounds, resulting in the spread of LPAI overa wide range (Olsen et al., 2006). Some raptors can also
be carriers of LPAI/HPAI, because they can become
secondary carriers by preying on infected poultry or
wild birds. Some raptor species also migrate long
distances.
Wild birds are a suspected cause of the spread of
HPAI throughout the world (Alexander, 2000; Gilbert
et al., 2006; Olsen et al., 2006), especially Asia (Li et al.,
2004; Chen et al., 2006), but there are several otherpossible pathways for the spread of viruses. They include the movement of infected poultry, the use of theirfeces in fish farming bait and agricultural fertilizer, there-use of inadequately cleaned transportation crates andGlobal Environmental Research
12: 41-54 (2008)
printed in Japanthe movement of caged wild birds in trade (Bulter, 2006;
BirdLife International, 2007). In order to evaluate therelative contribution of wild birds to the spread of HPAI,
precise movement routes and movement patterns ofpotential host birds as well as trading routes of poultry
and wild birds should be examined. This basic information is also useful for studying the spread of other infectious diseases such as West Nile fever (Rappole et al.,2000).
Satellite tracking is a powerful research technique
for studying bird movements on middle (within a country) to large (global) scales, because it allows individual
birds to be tracked anywhere in the world nearly realtime (Cohn, 1999; Webster et al., 2002; Higuchi &Pierre, 2005). From the locations obtained, we can know
the precise migration routes, the temporal schedule ofmigration and the relative importance of stopover sites
based on the number of birds visited and their length ofstay. In Asia, satellite tracking studies have been carriedout intensely from the 1990s and a lot of information on
migration of cranes, storks, waterfowl and raptors has
been gathered (e.g., Higuchi et al., 1994, 1996, 1998,
2004b, 2005; Kanai et al., 1997, 2000, 2002).
Here, we review these migration studies based onsatellite tracking and discuss the possible contribution ofsuch studies to the elucidation of the role of wild birds
in the spread of LPAI/HPAI. Most of the species
included in this review have been studied well.
©2008 AIRIES42

N. YAMAGUCHI and H. HIGUCHI

2. Satellite Tracking System
To track a focal individual, researchers need to
deploy a satellite transmitter (platform transmitter terminal [PTT]) on it. PTTs are usually attached to the backof the birds with a harness system. The harness consistsof two Teflon-treated ribbons, which are sewn to each of
the two front corners (toward the head of the bird) of the
PTT. The ribbons meet at the bird’s breastbone, where
they are crossed, passed through a small tube and sewn
together with a thread. Then the ribbons are sewn toeach of the backside corners of the PTT. The PTT is
expected to fall off when the thread wears out after
attachment (usually 2-3 years). The PTTs used are madeby NTT (Nippon Telegraph and Telephone Corporation),
Toyo Communication Equipment, Microwave Telemetry,and North Star Science and Technology. They neverweigh more than 4% of the deployed individual’s bodyweight. The weight of the smallest PTT model used in
the study was 12 g, and the size was 43 × 18 × 14 mmwith an antenna of 178 mm, which could be attached torelatively small duck species (for example the pintail
Anas acuta and Eurasian wigeon Anas penelope). PTTs
operate on internal batteries or solar power. Researchers
can set duty cycles with the desired length of the
tracking period in mind, and satellites are used to detectand collect location data. The transmission frequencies
of PTTs are set at 401.650 MHz ± 30 kHz. The message
from a PTT to a satellite includes a preliminary
synchronization sequence, statement of message length,

the PTT ID number, and the sensor data or othermessage data. Each message lasts 360 to 920
milliseconds, according to the length of the message.
Location and time data are received through internetor on disks sent from the ARGOS Service in France(https://www.argos-system.org/). ARGOS uses Polar
Orbiting Environmental Satellites (POES) of the US
National Oceanic and Atmospheric Administration(NOAA, Fig. 1). At least two satellites are operational at
any time. The trajectory of the satellites is 850 km above
the earth’s surface at a speed of one orbit every 100 min.
Data received and stored by the satellites are transmitted
to ground stations in the USA and France, usually once
per orbit, and then transmitted to the ARGOS Global
Processing Centers. The data are converted into latitudinal and longitudinal position information here. It takes
as little as 1-2 h from the time the satellite receives thesignals from a PTT to the time the researcher obtain thelocation and record time data on the ground.
The location of each PTT is estimated from Doppler
shifts in frequency, and there are some positional errors
for longitudinal and latitudinal data. Argos provides anestimate of location accuracy (Argos, 1996). The location classes or LCs are classified as 3, 2, 1, 0, A, B and
Z. They state that accuracy is within 150 m for LC3,
between 150 m and 350 m for LC 2, between 350 m and1,000 m for LC 1, and over 1,000 m for LC 0, with 1
standard deviation of the positional error in both latitudinal and longitudinal axes. Location accuracies for LCs
A, B and Z are unspecified by ARGOS.

3. Migration Routes and Main Stopover Sites
of Water Birds and Raptors in Asia

Fig. 1 Mechanisms of satellite tracking with the ARGOS
system. (reprinted from Higuchi (1994) withpermission from Yomiuri Shinbun, drawn by
M. Shigehara.)

3.1 Swans
Three swan species occur in Asia. Of these, thetundra swan Cygnas columbianus and whooper swan
Cygnas cygnas have been satellite tracked. Tundraswans breed in the polar region and move to East Asia
to winter. Whooper swans breed across North Asia andwinter in East Asia (Wild Bird Society of Japan, 1993).
3.1.1 Tundra swans
Higuchi et al. (1991) tracked the spring migration offour (three males and one female) tundra swans from
Lake Kuccharo in 1990. The lake is not a wintering site
for the tundra swan, but one of the major stopover sites
where a few thousand to more than 10,000 swans stayduring spring and autumn migrations. All four swans
migrated along similar routes. They went north along
Sakhalin, and stopped over in northern Sakhalin or
around the mouth of the Amur River. One female was
successfully tracked to the mouth of the Kolyma River,which was in the breeding range of the arctic region(Fig. 2). It is suggested that the mouth of the Amur
River and the east and west coasts of northern Sakhalin(51.5-51.6ºN, 143.3-143.9ºE and 51.4-51.6ºN, 142.0ºE,
respectively) are important stopover sites for the swans,since a half of the birds stayed at each location forseveral to nearly 14 days.

Migration of Birds in East Asia

43

3.1.2 Whooper swans
The spring migration of whooper swans was successfully satellite-tracked in 1994 and 1995 (Kanai et al.,1997). A total of 15 swans (six birds in 1994 and ninebirds in 1995) were tracked from the Kominato sea
coast (40.94ºN, 140.98ºE), northern Honshu, Japan,
which is a well-known wintering site of whooper swans.
Of these, eight individuals were successfully tracked totheir breeding ground in Russia. They migrated from
Kominato to their breeding sites via southern Hokkaido,
northeastern Hokkaido, Sakhalin and the lower Amur
River. The presumable breeding sites were distributed
over the lower Amur River, the north coast of the
Okhotsk Sea, middle reaches of the Indigirka River, andthe lower Kolyma River (Figs. 3a, b). The Tokachi River(42.74-42.92ºN, 143.40-143.65ºE), Aniva Bay (46.5146.78ºN, 142.24-143.38ºE) and the lower Amur River
(52.19-53.20ºN, 139.46-140.80ºE) were the important
stopover sites for the swans. About a half of the trackedswans rested in these areas for two to 40 days, and two
tracked swans spent the summer on the lower Amur
River.
SymbolIndividual Number

Sex

Fig. 2 Spring migration routes of tundra swans tracked from
Lake Kuccharo, northern Japan in 1990. (reprinted
from Higuchi et al. (1991) with permission fromYamashina Institute for Ornithology.)(a)3.2 Geese
The greater white-fronted goose Anser albifrons has
one of the greatest circumpolar breeding ranges of thewaterfowl. A subspecies wintering in East Asia is the
Pacific white-fronted goose A. a. frontalis, which breeds
from Hudson Bay in eastern Canada to the YukonKuskokwim Delta of western Alaska, across the Pacific
Rim into Siberia as far west as the Kolyma River(b)

Fig. 3 Spring migration routes of whooper swans tracked from Kominato, northern Japan in 1994 (a), and1995 (b). (reprinted from Kanai et al. (1997) with permission from the Wild Bird Society of Japan.)44

N. YAMAGUCHI and H. HIGUCHI

Fig. 4 Spring migration routes of white-fronted geese tracked from Lake Izunuma andUchinuma wetland, northeastern Japan in 1994. The solid squares and Figure
numbers refer to the figures in Takekawa et al. (2000). (reprinted fromTakekawa et al. (2000) with permission from the Association of International
Research Initiatives for Environmental Studies.)(Cramp & Simmons, 1977; Mooij et al., 1999). The
number of wintering sites of the geese is limited, although the population size is quite large, numberingwell over one million (Ely & Dzubin, 1994). The major
wintering areas in Asia are found in China, Korea andJapan (Miyabayashi & Mundkur, 1999).
Takekawa et al. (2000) reported the migration routes
from Lake Izunuma and the Uchinuma wetland(38.75ºN, 141.12ºE), in northern Japan (Fig. 4). They
deployed PTTs on ten adult males and satellite tracked
eight working PTT-deployed geese in 1994. After moving to western Hokkaido, they crossed the Sea of
Okhotsk directly and seven birds reached the west coastof the Kamchatka Peninsula. Of these, four geese stayed
there and probably bred there. The other three birds
went further north and went northeast of Kamchatka
reaching the southern Chukchi Autonomous Region at
Khatyrka Lake (62.25ºN, 175.17ºE) and the Pekul’ney
Lakes (62.60ºN, 176.01ºE). They probably bred there.
The important stopover sites for the geese were
Hachirogata Lagoon in Akita Prefecture, Japan (40.00ºN,
140.57ºE), Utonai-ko Lake in Hokkaido, Japan (42.42ºN,
141.42ºE), Miyajimanuma Lake in Hokkaido, Japan(42.42ºN, 141.42ºE), and Kharchinskoye Lake on the
Kamchatka Peninsula, Russia (56.53ºN, 160.18ºE). Their
duration of stay ranged from one to 34 days.
In the spring of 2007, four white-fronted geese weresatellite tracked from Izumo, Shimane Prefecture, western Honshu. They crossed the Japan Sea directly toreach the east coast of North Korea (Fig. 5). Unfortunately, the PTTs stopped functioning there, but theresults showed that there is another migration route ofthis species leaving Japan.

RussiaFig. 5 Spring migration routes of white-fronted geese tracked
from Izumo, western Honshu, Japan in 2008.

Migration of Birds in East Asia

3.3 Ducks
Ducks are the most common reservoirs of LPAI(Alexander, 2000; Munster et al, 2005; Olsen et al.,2006), and we particularly need to study their migrationroutes and moving patterns. However, there have been
no published satellite tracking studies that report on
migration routes of ducks in Asia. We and our collaborators have tracked three species of Anas ducks (mallards(Anas platyrhynchos), pintails and Eurasian wigeons)from Japan. The details will be published elsewhere, but
we can summarize their migration as follows.
Mallards were tracked from four wintering sites(Hokkaido, Saitama, Nagasaki and Miyazaki prefectures). Most birds went north, crossing the Japan Sea
directly except for one bird from Hokkaido; it went
north along the Kuril Islands. The destinations were
widely scattered around inland of northern China andFar East Russia. The stopover sites were also distributed
over a broad range (Yamaguchi et al., in press (a)).
Pintails were tracked from Hokkaido and Saitama
Prefectures. They reached probable breeding sites in thenorth of the Kamchatka Peninsula, crossing the Okhotsk
Sea directly. The stopover sites were distributed overJapan, the northern coast of the Okhotsk Sea, and theKamchatka Peninsula.
Eurasian wigeons were tracked from Miyazaki
Prefecture. They went north inland in southeastern
Russia or along Honshu, Hokkaido, and Sakhalin
Islands in contrast to mallards and pintails, most ofwhich went north by crossing the sea directly. The stopover sites were distributed mainly over southeastern
Russia, Japan, Sakhalin Island and the northern coastline of the Okhotsk Sea.

Fig. 6 Spring migration routes of mallards tracked from
Miyazaki, southern Kyushu, Japan from the winterof 2006 to the Spring of 2007.

45

There were great differences in migration routes ofindividual ducks from any wintering site, and the number and location of stopover sites also differed amongindividuals. However, most of the ducks heading for Far
Eastern Russia crossed the Sea of Japan directly and a
few individuals traveled through the Korean Peninsula(e.g., the migration routes of Mallards from Miyazaki(32.04ºN, 131.48ºE) as shown in Fig. 6). Stopover sites
were distributed over a broad area in North Korea,
northern China, Mongolia, Far Eastern Russia and Japan.
It should be noted that we found that there were some“hub” stopover sites, that is, ducks from different wintering sites shared the same stopover sites (Yamaguchi
et al., in press (a)). This finding may be important for
estimating and predicting the circulation and spread of
LPAI/HPAI in East Asia.
3.4 Cranes
Most cranes migrate long distances and use wetlands,
grasslands and farmland for their stopover and winteringsites. These open habitats are shared by ducks, therefore
cranes risk being secondary carriers through the
fecal-oral route from LPAI-infected ducks (Webster,1992).
3.4.1 Demoiselle cranes
The demoiselle crane Anthropoides virgo breeds
across the Eurasian Continent from eastern Europe andsouthern Ukraine to northeastern China. The wintering
areas are in Africa and the Indian subcontinent. The
migration routes from three breeding sites in Russia(Daursky Nature Reserve: 50.18ºN, 115.30ºE), Mongolia(Har Us Lake: 48.11ºN, 91.87ºE) and Kazakhstan (Kopacity: 43.50ºN, 75.77ºE) have been studied by Kanai et al.
(2000). In 1995, they deployed PTTs on ten cranes atDaursky Nature Reserve, nine cranes at Har Us Lake,and two cranes at Kopa city. Of these, four cranes (onefrom Kazakhstan and three from Mongolia) werecompletely tracked to their wintering grounds, and theFig. 7 Autumn migration routes of demoiselle cranes tracked
from Daursky Nature Reserve, Russia, Har Us Lake,
Mongolia and Kopa, Kazakstan in 1995. (reprinted
from Kanai et al. (2000) with permission from the
Association of International Research Initiatives forEnvironmental Studies.)

46

N. YAMAGUCHI and H. HIGUCHI

other nine cranes (three from Russia and six from
Mongolia) gave partial information on their migrationroutes (Fig. 7).
The crane from Kazakhstan reached western India
via the west side of the Hindu Kush Mountains (4,700 masl) and Pakistan. The cranes from Mongolia alsoarrived in western India, going through the Tarim Basin,
Qing-Zang Heights and Himalaya Mountains (more than
5,000 m asl). All PTTs deployed on the cranes in Russia
ceased functioning before the birds reached their wintering grounds, but three cranes were confirmed to arrive at
Qinghai Lake, Qinghai Province, China. Since themigration route from Russia appeared to move toward
western India, the cranes that breed in Daursky may
migrate to western India over the Himalayas like thecranes from Mongolia.
These results suggest that there are two migrationroutes for demoiselle cranes in central Asia: one flying
directly over the Himalaya Mountains, and the otherdetouring around the Hindu Kush Mountains. The
important stopover sites were Barkol Lake (43.6643.77ºN, 92.95-93.23ºE), Lop Nur Lake (41.04-41.31ºN,
90.30-90.39ºE), Yakatograk and Yeyik (36.76-38.49ºN,
83.18-86.95ºE), and the Keriya River (37.81ºN, 81.88ºE).
3.4.2 Red-crowned cranes
The red-crowned crane Grus japonensis breeds onlyin Northeast Asia, where two populations are confirmed:
one on the island of Hokkaido (Japan) and the other on
the continent. While the Hokkaido population is nonmigratory, the continental population travels for a long
distance between breeding and wintering grounds. Their
breeding areas are remnants of large wetlands inNortheast China and in the extensive wetlands along theAmur River in Far Eastern Russia. They winter at
Yancheng National Biosphere Reserve, the Yellow Rivermouth delta (Chan, 1999), the Demilitarized Zone
(DMZ) and coastal areas of the Korean Peninsula.
Higuchi et al. (1998) satellite tracked the autumn
migration of this species from Khingansky Nature
Reserve in 1993 and Lake Khanka Nature Reserve in1993 and 1994, respectively (Fig. 8). Three cranes captured at Khingansky and eleven cranes captured at Lake
Khanka were fitted with PTTs. Of these, two from
Khingansky and seven from Lake Khanka were tracked
the entire migration to their wintering grounds. The
cranes from Khingansky and Lake Khanka exhibited
different migration routes. The route from Khingansky
led to coastal China via Heilongjiang Province, Bohai
Bay, Tangshan City and the Yellow River estuary. The
route from Lake Khanka led to the Korean Peninsula via
the Tumen River and the river mouth at Odaejinnodongjagu. The important stopover sites were Panjin(40.90ºN, 121.50-127.90ºE), Tangshan (39.10-39.20ºN,
118.80-119.00ºE), the Yellow River estuary (37.3037.80ºN, 118.80-119.00ºE), Yangcheng (33.00-33.40ºN,
120.60-120.90ºE), Tumen River (42.40-42.60ºN, 130.60130.80ºE), Kumya (39.41-39.5ºN, 127.30-127.50ºE),
Anbyon (39.00-39.10ºN, 127.50-127.60ºE), and Cholwon(38.20-38.30ºN, 127.10-127.30ºE).

longitude

Fig. 8 Autumn migration routes of red-crowned cranes tracked
from Lake Khanka, Far Eastern Russia in 1993 and 1994,
and from Khingansky Nature Reserve, southeastern Russia
in 1993. Drawn from Higuchi et al. (1998).

Tamura et al. (2000) also tracked five cranes fromwetlands along the Amur River in Far Eastern Russia in
1998 and 1999. They also confirmed that there were tworoutes; one led to Yangchen Beach of coastal China andthe other led to the Korean Peninsula. They suggested
other important stopover areas for the cranes: the Amur
River basin (49.0-50.1ºN, 127.6-130.4ºE), Liao Riverdelta (41.0ºN, 121.8ºE), and the Han/Imjin estuary(37.6ºN, 126.6ºE).
Higuchi (2001) reported on the autumn migration of
three cranes from Blagoveshchensk and one from
Khingansky in Russia in 1998 and 1999. Three of thefour cranes reached Chenjiagang and Yangcheng,coastal China through Heilongjiang Province, Bohai
Bay and the Yellow River basin. The remaining one
from Khingansky headed for Liaoyuan, Jilin Province,
China. After arriving there, it went to the Korean
Peninsula and wintered in the Hangang River estuary(Fig. 9a). Of the four cranes, one bird that wintered in
Yangcheng was successfully tracked the following
spring. The bird went north via Bohai Bay as in theautumn migration, then moved more inland than it did inautumn, and returned to Khingansky (Fig. 9b). This
study first confirmed the spring migration route of thisspecies and the breeding population in Khingansky having at least two different wintering sites.
3.4.3 White-naped and hooded cranes
The white-naped crane Grus vipio and the hooded
crane G. monacha breed in southeastern Russia andnorthern China, and many white-naped cranes and theMigration of Birds in East Asia

majority of hooded cranes winter at Izumi (32ºN, 125ºE)
on Kyushu Island, southern Japan. The site is managed
by Ministry of the Environment and the local government, which provide grain and fish for the cranes. Thereis an epidemic risk of infectious diseases, since more

47

than 10,000 cranes gather in a limited area of Izumi.
In 1992-1993, nine white-naped cranes were successfully tracked to their breeding grounds (Higuchi
et al, 1992; Higuchi et al., 1996; Higuchi & Minton
2000). Two routes were observed: one led to the Three
(a)

(a)

Vladivostok

(b)
(b)

Fig. 9 (a) Autumn migration routes of red-crowned cranes
tracked from Blagoveshchenk and Khingansky
Nature Reserve, southeastern Russia in 1998 and
1999, and (b) autumn and spring migration routes ofa red-crowned crane (ID 21502) tracked from
Khingansky Nature Reserve in 1999.

Fig. 10 (a) Spring migration routes in 1993, and (b)autumn routes in 1991-1993 of white-naped
cranes. The spring migration was tracked from
Izumi, southern Kyushu, Japan. The autumn
migrations were tracked from Daursky Nature
Reserve, Muravivka Wildlife Refuge, andKhingansky Nature Reserve in 1991, 1992 and1993, respectively. (reprinted from Higuchi et al.
(1996) and Higuchi et al. (2004b) with permission
from Blackwell publishing.)

48

N. YAMAGUCHI and H. HIGUCHIRiver Plain in China via the DMZ, Kumya and Sonbong
in North Korea, and Lake Khanka in China; the otherled to Zhalong National Nature Reserve in China via theDMZ (the routes observed in 1993 are shown in
Fig. 10a). Higuchi et al. (1992) tracked four hooded
cranes from Izumi and succeeded to track two cranes toDaursky
Nature Reserve

Fig. 11 Spring and autumn migration routes of hooded
cranes tracked in 1992 from Izumi, Kyushu, southern
Japan and Daursky Nature Reserve, Southern Russia,
respectively. (drawn using location data in Higuchi
et al. (1992) and Higuchi et al. (1994))

their breeding grounds in 1992. One crane went throughthe Korean Peninsula after resting on Fukune Island(32.73ºN, 128.68ºE), then reached the Three River Plain.
This individual probably bred there. The other passed
through Nagasaki (32.53ºN, 129.23ºE), the Korean
Peninsula, and Fuchin (46.18ºN, 131.46ºE), then restedon the Three River Plain. After leaving that, it continued
north and reached Imeni Poliny Osipenko (53.61ºN,
132.90ºE), the probable breeding site (Fig. 11).
The fall migrations of both species were tracked by
Higuchi et al. (1994) and Higuchi et al. (2004b). Fourteen, three, and one white-naped cranes were fitted with
PTTs at Daursky Nature Reserve (50ºN, 115ºE),
Khingansky Nature Reserve (49ºN, 129ºE) and
Muraviovka Wildlife Refuge (49.92ºN, 127.60ºE),
respectively, in south-central Russia in 1991-1993, andeleven cranes were successfully tracked to their wintering grounds, Poyang Lake in China (28.95-29.20ºN
115.86-116.10ºE) and Izumi in Japan (Fig. 10b). The
main stopover sites along the route to Poyang Lake werethe mouth of the Yellow River (37.44-37.69ºN,
118.53-118.98ºE) and Wuhan (31.15-31.20ºN, 116.18116.20ºE). The main stopover sites along the route to
Izumi were Lake Khanka and the Three River Plain. For
hooded cranes, two individuals were fitted with PTTs at
Daursky Nature Reserve in 1992 and one of the birds
was tracked to its wintering site, Poyang Lake (Fig. 11).
The bird rested at Taoman (45.09-45.13ºN, 123.20123.40ºE), the mouth of the Yellow River and Xihekou(31.47-31.56ºN, 116.32-116.43ºE).
3.4.4 Siberian cranes
The Siberian crane Grus leucogeranus is one of themost endangered bird species in the world. The population size is only 2,500 to 3,000 and the IUCN designates
this species “Critically Endangered” (BirdLife Interna-

Fig. 12 Autumn migration routes of Siberian cranes tracked from the lower Indigirka
River, northwestern Russia in 1995 and 1996. (reprinted from Kanai et al.
(2002) with permission from Bkackwell Publishing.)

Migration of Birds in East Asia

tional, 2000). The cranes breed in northern Russia,
between the Yana and Kolyma River, and most of themwinter on Poyang Lake in southern China (Meine &Archibald, 1996).
The autumn migration route was tracked from thelower Indigirka River (71ºN, 144-148ºE) in 1995-1996(Kanai et al., 2002). Of thirteen cranes marked in the
two years, five cranes were tracked over their entire
migration routes and six cranes were tracked for part oftheir routes. All the cranes migrated along a similarroute (Fig. 12). All successfully tracked cranes moved
to Poyang Lake via Qiqihar-Baicheng area, theShuangtaize River delta, and the Yellow River delta. The
four areas (Qiqihar Baicheng area, Aumannykan area,
Shuangtaizi River delta, and Yellow River delta) areconsidered to be the most important stopover sites.
3.5 White storks
Stork species are one of the largest water birds anduse a relatively varied range of habitats, including not
only wetlands but also agricultural lands. Thus, thisstork species would have a potential for contact withpoultry. In East Asia, one stork species, the Orienral
white stork Ciconia ciconia occurs. This species
migrates for a long distance from Far Eastern Russia
and northern China to southeastern China.
The autumn migration routes were reported by
Higuchi et al. (2000) and Tamura et al. (2000). They
successfully satellite tracked thirteen storks from theAmur region (49.21-59.96ºN, 127.66-129.97ºE) andKhabarovsk (48.56-49.28ºN, 134.27-135.56ºE) in 19981999 (the routes observed by Higuchi et al. (2000) is
shown in Fig. 13a). The birds from the Amur region
moved mainly through Qi-Xin Lake (30.31-30.33ºN,
113.84-113.87ºE), the Nenjiang River (44.64-48.57ºN,
121.84-126.32ºE) and Bohay Bay (37.33-39.87ºN,
118.64-119.42ºE), then wintered at Poyang Lake or the
East Donting Hu Nature Reserve (29.41-29.52ºN,
112.73-112.80ºE), which are very important wintering
areas for numerous wetland birds. The birds from
Khabarovsk reached their wintering area at Shenjin
Lake along the Yangtze River (30.80ºN, 117.11ºE) or
Poyang Lake mainly via the Tangwang River (49.4647.18ºN, 130.47-131.16ºE) and Bohai Bay. In addition
to the main stopover sites, the storks stopped several
times enroute with daily movements ranging from 1 to
10 km during most of the migration period. Thisbehavior of short flights during migration is quite
unique in this species.
The autumn and spring migrations were successfully
tracked for a stork in 1998-1999 (ID 20821, Fig. 13b).
The route and stopover sites of the spring migration
were similar to those of the autumn migration from thewintering site to the Nenjiang River, although thesummering area in 1999 differed from that in 1998.
3.6 Raptors
Raptors are not considered to be the major reservoirsof LPAI. However, they may carry LPAI/HPAI viruses

49(a)Khabarovsk

Vladivostok

Yangtze River(b)

Khabarovsk

Vladivostok

Yangtze River

Fig. 13

Autumn migration routes of Oriental white
storks tracked from the Amur region, southern
Russia in 1998 and 1999 (a), and autumn andspring migration route of ID 20821 (b) in 1999
to 2000. Autumn routes were drawn using
location data in Higuchi et al. (2000).

for a short period through preying on infected wild birds
and poultry. In fact, an HPAI (H5N1 type) infectedmountain hawk-eagle Spizaetus nipalensis was recorded
in Kumamoto, Japan (Kumamoto Prefectural Government, press materials). Some raptors travel for long
distances between their breeding and wintering grounds.
Therefore, the species may convey viruses for somedistance, depending on the duration of viruses retainedin migrating birds.

50

N. YAMAGUCHI and H. HIGUCHI

3.6.1 Steller’s sea eagles
The migration of the Steller’s sea eagle Haliaeetus
pelagicus was satellite-tracked by Meyburg & Lobkov(1994) and Ueta et al. (2000). Ueta et al. (2000) tracked
the autumn and spring migration of the eagle from Japan.
They tracked seven and four eagles from Nemuro
Peninsula (43.33ºN, 145.67ºE), eastern Hokkaido, Japan
in 1995 and Oshima Peninsula (42.25ºN, 140.25ºE),
southern Hokkaido in 1996, respectively. In total, nineeagles were successfully tracked in the two years.
Of the birds from Nemuro Peninsula, apart form one
eagle, which migrated along the Kuril Islands to
Onekotan Island south of Kamchatka Peninsula, all the
tracked eagles moved north to Lake Kuccharo or
Wakkanai, at the north end of Hokkaido, and crossed to
Sakhalin. They migrated north along Sakhalin and spent
the summer in northern Sakhalin or on the nearby continental seacoast. One eagle was tracked through the next
autumn migration. The bird retraced its spring route,although its route between southern Sakhalin and theShiretoko Peninsula is not known because we wereunable to obtain its location data during that period(Fig. 14).
The birds from the Oshima Peninsula moved to
Wakkanai or Lake Kuccharo in northern Hokkaido, andcrossed the La Perouse Strait to Sakhalin. After arriving
on Sakhalin Island, their routes were similar to those of
the birds from Nemuro Peninsula. There were no major
stopover sites used by most of the eagles (M. Ueta, pers.
com.).
3.6.2 White-tailed sea eagles
The spring and autumn migrations of two whitetailed sea eagles Haliaeetus albicilla were successfully
tracked from Oshima Peninsula, southern Hokkaido,
Japan in the 1995-1996 seasons (Ueta et al., 1998). In
the spring migration, the eagles moved from southern

Hokkaido to Sakhalin, went north along Sakhalin, thentraveled along the coast of the Okhotsk Sea and spent
the summer in the central or northern parts of theKamchatka Peninsula. The autumn migration routes
differed from the spring ones. The eagles migrated south
along the Kamchatka Peninsula and the Kuril Islands,
making a circuit of the Okhotsk Sea during the year (Fig.
15). The autumn migration routes were similar to thoseof the Steller’s sea eagles, but the spring migration routediffered between the two eagle species. It remains
unknown why white-tailed sea eagles wintering in
Hokkaido migrate along the circuit route and Steller’s
sea eagles wintering in the same area do not.
3.6.3 Oriental honey-buzzards
Higuchi et al. (2005) tracked three (two adultand one juvenile) oriental honey-buzzards Pernis
ptilorhynchus from Nagano prefecture, central Japan in2003 and 2004. The birds went westward and crossed
the East China Sea. After reaching China, the two adults
moved through inland China and the juvenile moved
along coastal China, until they reached Vietnam. The
migration route greatly differed among the individuals
from there (Fig. 16). One adult moved further south andwintered in central Java (7.1ºS, 108.1ºE). The other
adult bird made a detour. It went south from Vietnam
and reached the tip of the Malay Peninsula, then it
moved through Borneo Island. Finally, the bird arrived
in western Mindanao, Philippines (8.4ºN, 123.5ºE) andwintered there. The juvenile bird did not winter at aFig. 15
Fig. 14 Spring and autumn migration routes of a Steller’s
sea eagle tracked from Nemuro Peninsula, eastern
Hokkaido, Japan from 1995 to 1996. (reprinted
from Ueta et al. (2000) with permission fromBlackwell Publishing)Spring and autumn migration routes ofwhite-tailed sea eagles tracked from Oshima
Peninsula, southern Hokkaido, Japan from1995 to 1997. (reprinted from Ueta et al.
(1998) with permission from Blackwell
Publishing. Some toponyms have been
added by the authors)Migration of Birds in East Asia

51

Fig. 16 Autumn and spring migration routes of Oriental honey-buzzards tracked from Nagano, central Japan from 2003 to
2004. (reprinted from Higuchi et al. (2005) with permission from the Ornithological Society of Japan)

fixed site, but continued moving around in the southern
Malay Peninsula and part of Sumatra.
The spring migration was successfully tracked forthe adult that wintered in central Java. The bird retraced
its autumn route from the wintering site to the end of the
Malay Peninsula, then it moved through inland China,
but the route was located north of the autumn migration.
Unlike the autumn migration, the bird’s route made adetour around the East China Sea by traveling down
through the Korean Peninsula and crossing the
Korean/Tsushima Strait to reach Japan (Fig. 16).
The adult buzzard was tracked for two and a halfyears. Each year, it used the same breeding and wintering sites and the same stopover sites where it stayed formore than four days (Shiu et al., 2006). We have been
tracking other individuals, and have shown that the
migration route between Japan and the tip of the Malay
Peninsula is quite similar among adult individuals, butroutes to the wintering sites from there greatly differedamong individuals (Yamaguchi et al., in press (b)).
3.6.4 Grey-faced buzzards
Seven grey-faced buzzards were satellite-tracked
between their breeding and wintering grounds (Higuchi
et al., 2004a; Higuchi, 2005, Fig. 17a, b). In spring, thebuzzards departed from their wintering sites in Ishigaki,
Iriomote and Miyako Islands of the Sakishima Islands in
mid−late March and early April. They traveled northward along the Southwest Islands through the island
chains of Okinawa, Amami and Tokara into Kyushu, thesouthernmost main island of Japan. Then they veered
east and crossed the island of Shikoku to reach Honshu
directly or via Awaji Island. After that the routes
diverged and the birds headed for different breedingsites (Niigata, Nagano, Tochigi, Chiba, Ibaraki and
Fukushima Prefectures). One bird stopped in Kyushu,
however, and bred in Oita Prefecture (Fig. 17a; the routes

to Nagano, Ibaraki and Oita are not shown in the figure
due to scarce location data). We could track two successive spring migrations for three birds (Fig. 17a). The
two spring routes were very similar and all birds
returned to the same breeding grounds. For the bird
breeding in Kitakanbara, Niigata Prefecture, there were
only one or two-day differences in the departure andarrival dates between the years.
In autumn, the buzzards departed from the breedingsites in late August at the earliest and in early October at
the latest. Most of them retraced the route they hadtaken the previous spring. The buzzards breeding in
Tochigi and Chiba Prefectures, for instance, flew
through Shizuoka and Aichi Prefectures on the Pacificcoast into the Kii Peninsula and reached Kyushu via
Shikoku. The birds of Niigata along the Sea of Japan, on
the other hand, migrated through the mountainous
regions from Nagano to Gifu Prefecture, and passed
south of Lake Biwa in Shiga Prefecture. After that, theyflew across Shikoku via Awaji island into Kyushu. All
the birds flew through the Osumi Peninsula in southernmost Kyushu on their migration to the Southwest
Islands. One bird was tracked from Niigata Prefecture
down to northern Taiwan, and another bird from Tochigi
Prefecture reached as far as the Batan Islands of thePhilippines (Fig. 17b).

4. The Importance of Satellite Tracking Datafor the Study on the Spread of Infectious
VirusesSatellite tracking studies on water birds and raptors
have been accumulating the last two decades, andindividual-based migration routes, travel schedules andimportant stopover sites that are shared by many
individuals have been revealed for several species.

52

N. YAMAGUCHI and H. HIGUCHI

(a)

(b)

Fig. 17 (a) Spring migration routes of grey-faced buzzards
satellite-tracked from Ishigaki Island and Miyako
Island of the Sakishima Islands, southwestern Japan in
2002-2004, and (b) fall migration routes of grey- faced
buzzards satellite-tracked from Niigata, Tochigi and
Chiba Prefectures, central Honshu, Japan, in 2002 and2003.

These data could contribute to (1) the estimation andprediction of the potential geological extent and speedof spread of LPAI/HPAI and other infectious viruses
such as West Nile fever, (2) the extraction of areas thathave a high risk of virus transfer among wild birds orfrom wild birds to poultry or vice versa, and (3) theevaluation of the relative importance of the role of wild
birds in the spread of the viruses compared with that ofhuman trade activities.
We can calculate or simulate the extent and speed of
the spread of avian infectious viruses when suchinformation is available as migration routes, travel speed,
infectious rates among birds including intra- and inter-

species transmission, incubation periods of the virusesin birds, and survival rates of infected birds. Comparing
the spatio-temporal pattern of spread of the viruses
obtained from simulation with that observed, we could
test the hypothesis that the spread of the viruses ismainly due to the movements of wild birds. If theobserved speed and extent of spread of the viruses
among henneries cannot be explained only by the pattern of movement of wild birds, then the hypothesis
would be rejected. If the hypothesis is not rejected, weshould make quantitative estimations and predictions of
the potential risk of infections to vicinal henneries assoon as possible when HPAI occurrence is detected in ahennery.
From the satellite tracking data, we can detect thebreeding and wintering areas in which birds are highly
concentrated, and the stopover sites that are shared bybirds with different migration routes and destinations(i.e., “hub” stopover sites). These areas could be criticalto the spread of the viruses. We can also evaluate thedegree of interaction among poultry, humans and migratory birds at these critical locations by overlaying cultivated areas and locations of henneries around thosestopover sites using GIS techniques. Knowledge of thecongested breeding and wintering sites and hub stopoversites is also crucial to the conservation of species. We
should not damage those sites or birds based on incomplete data and inappropriate speculations, but should
monitor and preserve them.
So far, two pathways are suspected as a main causeof the spread of the HAPI viruses; movements of wild
birds and human activities (physical distribution).
Human activities include the movements of infected
poultry, use of their feces for fish farming bait andagricultural fertilizer, the re-use of inadequately cleaned
transportation crates and the movement of caged wild
birds in trade (BirdLife International, 2007; Bulter,2006). Poultry trade and physical distribution of infectedmaterials are likely to be the causes of the spread of
HPAI (Alexander, 2000). For example, the HPAI
(H5N1) virus outbreak that took place in Russia andKazakhstan during the summer of 2005 spread along
important trade routes that link western China to Russia,
rather than along any direct migration route of wild
birds (Gilbert et al., 2006). Moreover, for the H5N1
virus, there is no doubt that domestic waterfowl, specificfarming practices and the agroecological environment
have played a key role in the occurrence, maintenanceand spread of HPAI, because these factors promoteinteractions between poultry and wild birds (Gilbert
et al., 2006; Olsen et al., 2006).
On the other hand, Gilbert et al. (2006) concluded
that the spread of HPAI (H5N1) from Russia andKazakhstan to the Black Sea basin is consistent in space
and time with the hypothesis that anatid waterfowl
seeded the virus along their autumn migration routes.
However, the relative contribution of the two possible
pathways in the spread of the viruses has not been
evaluated at all. In order to elucidate this issue, satelliteMigration of Birds in East Asia

tracking data will be greatly useful, since the data
provide accurate, quantitative movement patterns ofindividual birds.

Acknowledgements
Lots of scientists were involved in the field workof catching birds and deploying PTTs. They include
T. Amano, V. Andronov, G. Archibald, B. Auyrsana, Y.
Darman, P. Flint, G. Fujita, S. Grmogenov, O. Goroshko,
J. Harris, E. Hiraoka, N. Hijikata, J. Hupp, H. Iizuka,
S. Javed, Y. Kanai, N. Kanmuri, S. Konno, A. Kovhsar,
H. Kuno, M. Kurechi, V. Krever, J. Minton, N. Mita, S.
Moriguchi, E. Morishita, M. Nagendran, H. Nakamura,
M. Okuyama, K. Ozaki, M. Parilov, J. Pierce, P. Johanna,
M. Saeki, F. Sato, H. Sato, T. Shimada, H. Shimazaki,
H-J. Shu, M. Soma, R. Suwal, K. Takagi, M. Tamura,
K. Tokita, K. Uchida, H. Uematsu, M. Ueta, and K.
Ushiyama. The satellite tracking studies were funded byNEC, NTT, Yomiuri Newspaper Company, Ministry of
the Environment, Ministry of Education, Culture, Sports,
Science and Technology, and the University of Tokyo
21st Century COE Program on Biodiversity and Ecosystem Restoration.
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Noriyuki YAMAGUCHI
Noriyuki YAMAGUCHI is an AssistantProfessor at the University of Tokyo. In
his PhD thesis at Kyushu University, hestudied adaptive sex ratio adjustment inbirds. After graduating from there, hestudied the evolution of life history andphenotypic traits in an island populationof birds as a JSPS post-doctoral fellow at
Rikkyo University. He also undertook
fieldwork in a tropical dry forest of northern Australia at that time. His
current research focuses on satellite tracking of birds.

Hiroyoshi HIGUCHI
Hiroyoshi HIGUCHI is a Professor of
Biodiversity Science at the University ofTokyo. He is interested in various aspects
of Environmental Sciences, ranging fromthe ecology and conservation of migratory
birds through the conflicts between wildlife and humans to the effects of climatechange on biodiversity. He has publishedmany books including “What’s Wrong with Crows!?” (Shogakkan, Tokyo)
and “Bird Migration – Satellite Tracking of Migratory Birds –” (NHKBooks, Tokyo). He has served as the Editor-in-Chief of Global
Environmental Research since 2006.

(Received 28 January 2008, Accepted 26 April 2008)