J Ornithol (2012) 153 (Suppl 1):S3–S14

DOI 10.1007/s10336-011-0768-0

REVIEW

Bird migration and the conservation of the global environment

Hiroyoshi Higuchi

Received: 5 March 2011 / Revised: 29 July 2011 / Accepted: 4 October 2011 / Published online: 10 December 2011
Ó Dt. Ornithologen-Gesellschaft e.V. 2011

Abstract I have collaborated with Asian and American Introduction

scientists on satellite-tracking the migration of birds in East
Asia for nearly 20 years. We have tracked the migration of Migratory birds encounter many problems during their
about 20 bird species, including cranes, storks, swans and migration. These include habitat destruction, hunting,
hawks. We have used the results in a variety of applica- chemical pollution and collisions with aircraft. These
tions, from showing migration routes and the relative problems may reduce the chance of survival or reproduction
importance of each staging site to more advanced analyses of birds. Habitat destruction leads to habitat and food loss in
including using various data overlays to examine habitat breeding, staging or wintering areas (Askins 2000). Hunting
use and the connectivity and network structure of migration and chemical pollution reduce the chance of survival or
pathways. We have also studied the effects of climate reproduction of the birds (Kerlinger 1995; Colborn et al.
change on population trends of swans satellite-tracked 1996). In collisions with aircraft, they may not only lose
from their wintering areas in Japan to their breeding ground their own lives but also cause a heavy loss of human lives
in Russia. Satellite-tracking is a powerful research tool to (Leshem and Bahat 1999). Migratory birds may also carry
study the detailed migration routes, seasonal differences in some infectious disease viruses such as West Nile fever and
migration pattern, locations of important sites, and the avian influenza (Tambyah and Leung 2006; LaDeau et al.
conservation issues that migratory birds encounter. 2007). The infected birds may lose their own lives or spread
Migratory birds establish a link not only among natural the viruses over a wide area. Therefore, it is important to
environments in different countries along their migration study their migration routes, stopover sites, destinations,
routes but also among people in different countries. Further migration patterns through time and habitat use.
interdisciplinary cooperation is needed to develop tracking In the early 1990s, the new technology of ‘satellite-
technology, and more international collaboration is tracking’ became available for studying bird migration
required to promote migration studies. (Higuchi 2010). In this technology, once we deploy satel-
lite transmitters, called platform transmitter terminals
Keywords Climate change  Conservation  East Asia  (PTTs), on the birds, we can receive information on their
Migration  Satellite-tracking locations over time through the Internet from the Argos
worldwide tracking and environmental monitoring service.
At least two satellites are operational at any time; these
move through an 850-km trajectory above the earth’s sur-
face at a speed of one orbit every 100 min. Data received
Communicated by John Wingfield. and stored by the satellites are transmitted to ground sta-
tions in the US and France, and then transmitted to the
H. Higuchi (&) Argos Global Processing Centers, where the data are con-
Laboratory of Biodiversity Science, Graduate School of
verted into latitudinal and longitudinal position information
Agricultural and Life Sciences, The University of Tokyo,
Bunkyo-ku, Tokyo 113-8657, Japan (see Olival and Higuchi 2006; Higuchi 2010, for details on
e-mail: higuchi@es.a.u-tokyo.ac.jp the satellite-tracking system). Using satellites as research

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tools enables data to be recorded over large spatial scales, was expected to fall off through deterioration 2–3 years
far greater than the range capabilities of more traditional after deployment.
telemetry systems. We categorized location data into seven Location
For nearly 20 years, I have collaborated on satellite- Classes (LC) with respect to accuracy: from Z (least
tracking bird migration with Russian, Mongolian, Chinese, accurate), to B, A, 0, 1, 2 and 3 (most accurate) (Keating
Korean, Indian and American scientists (Higuchi et al. et al. 1991; Service ARGOS 1994). Accuracies for the least
1991, 1992, 2004; Higuchi and Pierre 2005; Yamaguchi accurate location classes, A, B and Z, could not be esti-
and Higuchi 2008; Higuchi 2010). Satellite-tracking is mated using the ARGOS system. In general, we used LC
especially well suited to Asian-based research because of 1–3 for data analysis, which are reported with one standard
the extremely large land area, sensitive political situations deviation accuracies of 350–1,000 m, 150–350 m, and
and the many urgent conservation problems in the region. \150 m, respectively. We included LC 0, A, B and Z data
We have satellite-tracked the migration of about 20 species only when they were spatially and temporally close to LC
of cranes, storks, swans, geese, ducks and hawks. We are 1–3 location estimates.
interested in migration routes, migration patterns through
time and habitat use of threatened birds in East Asia, with
the aim of contributing to the conservation of focal species Migration routes identified
and their habitats.
In this article, I review the results obtained from our The migration routes of certain species have been well
work, focusing on migration routes, important areas for studied, and some of the examples are introduced here. The
migratory birds, and the effect of climate change on the groups treated are ducks, swans, cranes and hawks.
population of migratory birds. I will discuss the links
among natural environments in different countries along Ducks
their migration routes as well as among human lives in
different countries, and will describe future issues con- Mallards Anas platyrhynchos were tracked from many
cerning the relationship among the birds, the environment regions in Japan (Fig. 1). Migration routes differed greatly,
and human activities. This article draws from and extends not only among individuals from different wintering sites
Higuchi (2010), adding further information. but also among individuals from the same wintering site,
although Mallards from the same wintering sites followed
the same general migration routes.
Transmitters and their deployment One Mallard that departed from northern Hokkaido, the
northernmost main island of Japan, moved along the Kuril
We used satellite transmitters or platform transmitter ter- Islands and reached the Kamchatka Peninsula in Far
minals (PTT) made by NTT, North Star Science and Eastern Russia. Six Mallards from central Japan traveled
Technology, and Microwave Telemetry, which weighed no northward and crossed the Sea of Japan. All six of these
more than 3% of the target species’ body weight. The birds reached the southeastern area of Far Eastern Russia.
transmission frequencies of satellite transmitters were set at One bird reached northern Khabarovsk (51°220 N,
401.65 MHz ± 30 kHz. Duty cycles were set with the 137°020 E), and then turned east and reached the north end
desired length of tracking period in mind for battery- of Sakhalin Island.
powered PTTs (e.g., Higuchi et al. 2004). A solar-powered Mallards from southern Japan traveled northward, and
battery can be expected to last 2–3 years but maybe less, most crossed the Sea of Japan just like the Mallards from
depending on the bird species being tracked and on envi- central Japan. However, some birds went north along the
ronmental conditions. eastern coastline of the Korean Peninsula. Most birds
We deployed the PTT on the bird’s back with a harness. stayed near the border between North Korea and China.
Our harness consisted of two Teflon-treated ribbons, which Three birds moved farther inland and reached points near
were sewn to each of the two anterior corners of the PTT. the border between Inner Mongolia (China) and Russia. In
The ribbons met at the keel of the bird’s sternum, where some cases, birds exhibited a sharp change in direction
they crossed and passed through a small tube and were during migration. After crossing the Sea of Japan directly,
sewn together with a surgical suture (Nagendran et al. one Mallard moved northward from the north end of the
1994) or nylon thread. We expected the PTTs to fall off coastline of North Korea, reached the border between
once the thread deteriorated over 6 months to a year if Russia and China in northern Heilongjiang Province
attached with a surgical suture, or 2–3 years if attached (45°390 N, 132°450 E) and then turned sharply west and
with a nylon thread. For swans, we attached the PTT to a finally arrived at the border between Russia and China in
neck collar, which weighed 70–80 g total. The neck collar southern Chitinskaya (49°250 N, 119°370 E).

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Fig. 1 Spring migration routes

of Mallards Anas platyrhynchos
satellite-tracked from a wide
range of Japan in 2005–2007.
Based on the data used by
Yamaguchi et al. (2008)

A total of 102 Pintails Anas acuta deployed with PTTs major stopover sites where thousands to more than 10,000
migrated from Japan and made landfall elsewhere (Hupp swans stay during their spring and autumn migrations. All
et al. 2011). Most Pintails migrated first to Sakhalin or four swans migrated along similar routes. They went north
Kamchatka. Many Pintails that migrated to Sakhalin sub- along Sakhalin and stopped over in northern Sakhalin or
sequently moved to stopovers in Kamchatka or the Mag- around the mouth of the Amur River. One female was
adan region facing the Okhotsuk Sea, with a small number successfully tracked to the mouth of the Kolyma River,
migrating along the Kolyma River in Russian tundra. A which was in the breeding range of the arctic region. In
small number of Pintails (4) remained on Sakhalin during 2009, another seven Whistling Swans were tracked again in
the summer. Pintails that reached Kamchatka either spring from Lake Kuccharo. They took similar routes,
directly from Japan or via Sakhalin made non-stop trans- migrating north along Sakhalin and stopping over in some
oceanic flights of at least 1,200 km. areas of Sakhalin and around the mouth of the Amur River.
From Kamchatka, most Pintails next migrated to They finally reached the area around the mouth of the
Chukotka and the surrounding areas, northeastern end of Kolyma River (Fig. 2).
the Far Russia, although 32% of the Pintails that arrived in Thus, the mouth of the Amur River and the east and
Kamchatka remained there during summer. Pintails that west coasts of Sakhalin (51.5–51.6°N, 143.3–143.9°E and
migrated to Magadan and the surrounded areas primarily 51.4–51.6°N, 142.0°E, respectively) appear to be important
next migrated along the Kolyma River, although 6 of the stopover sites for the swans.
21 Pintails that arrived in Magadan remained there for the The spring migration of eight Whooper Swans Cygnus
summer. cygnus was successfully satellite-tracked to their breeding
Differences in migration routes of Pintails that sum- ground in Russia in 1994 and 1995 (Kanai et al. 1997). The
mered in different regions were apparent. Pintails that swans were released from the Kominato sea coast (40.94°N,
arrived at summer sites in Kamchatka and Chukotka 140.98°E), northern Honshu, Japan, a well-known wintering
migrated almost exclusively through Kamchatka, either site of the swans. They migrated through southern Hokkaido,
directly from Japan or via Sakhalin Island. northeastern Hokkaido, Sakhalin and the lower Amur
River. The presumed breeding sites were distributed along
Swans the lower Amur River, the north coast of the Okhotsk Sea,
the middle reaches of the Indigirka River, and the lower
Four Whistling Swans Cygnus columbianus were tracked Kolyma River. Their breeding ground was located in more
from Kuccharo Lake (45.17°N, 142.33°E) in 1990. The southern areas than that of the Whistling Swans. The
lake is not a wintering site for the swan, but one of the Tokachi River (42.74–42.92°N, 143.40–143.65°E), Aniva

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118.53–118.98°E) and Wuhan (31.15–31.20°N, 116.18–

116.20°E). The main stopover sites along the route to Izumi
were Lake Khanka and the Three River Plain.
Higuchi et al. (1998) studied the autumn migration of
Red-crowned Cranes Grus japonensis from Khingansky
Nature Reserve in 1993 and from Lake Khanka Nature
Reserve in 1993 and 1994 (Fig. 4). Two from Khingansky
and seven from Lake Khanka were tracked for their entire
migration to the wintering grounds. The cranes from Khin-
gansky and Lake Khanka had 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
Odaejin-nodongjagu. The important stopover sites were Panjin
(40.90°N, 121.50–127.90°E), Tangshan (39.10–39.20°N,
118.80–119.00°E), the Yellow River Estuary (37.30–37.80°N,
118.80–119.00°E), Yangcheng (33.00–33.40°N, 120.60–
120.90°E), the Tumen River (42.40–42.60°N, 130.60–
130.80°E), Kumya (39.41–39.5°N, 127.30–127.50°E),
Anbyon (39.00–39.10°N, 127.50–127.60°E), and Cholwon
(38.20–38.30°N, 127.10–127.30°E).
In 1998 and 1999, another five cranes were tracked from
wetlands along the Amur River in the Russian Far East
(Tamura et al. 2000). There were two routes, one of which
led to Yangchen Beach on the coast of China, and the other
to the Korean Peninsula. Tamura et al. (2000) suggested
other important stopover areas for the cranes: the Amur
Fig. 2 Spring migration of Whistling Swans Cygnus columbianus
satellite-tracked from Lake Kuccharo, northern Japan in 2009 River basin (49.0–50.1°N, 127.6–1303.4°E), the Liao River
delta (41.0°N, 121.8°E), and the Han/Imjin Estuary
Bay (46.51–46.78°N, 142.24–143.38°E) and the lower (37.6°N, 126.6°E).
Amur River (52.19–53.20°N, 139.46–140.80°E) were Eleven Siberian Cranes Grus leucogeranus were tracked
important stopover sites for the swans. About half the from the lower Indigirka River (71°N, 144–148°E) in the
tracked swans rested in these areas for 2–40 days. autumn of 1995–1996 (Kanai et al. 2002). All the cranes
migrated along a similar route. They moved to Poyang
Cranes Lake via the Qiqihar-Baicheng area, the Shuangtaize River
delta and the Yellow River delta. These four areas (the
In 1992–1993, nine White-naped Cranes Grus vipio were Qiqihar-Baicheng area, Aumannykan area, Shuangtaizi
successfully tracked to their breeding grounds (Higuchi et al. River delta and Yellow River delta) are considered to be
1992, 1996; Higuchi and Minton 2000). Two routes were the most important stopover sites.
identified: one led to the Three River Plain in northeastern
China via the Korean DMZ, Kumya and Sonbong in North Hawks
Korea, and Lake Khanka in China; the other led to the
Zhalong National Nature Reserve in northeastern China via Seven Grey-faced Buzzards Butastur indicus were tracked
the DMZ (Fig. 3a). The autumn migration was tracked by between their breeding and wintering grounds (Higuchi, in
Higuchi (1994) and Higuchi et al. (2004). Eleven cranes were preparation). In spring, the buzzards departed from their
tracked from Daursky Nature Reserve (50°N, 115°E), wintering sites in southern South-West Islands, in south-
Khingansky Nature Reserve (49°N, 129°E) and Muraviovka ernmost Japan. They traveled northward along the island
Wildlife Refuge (49.92°N, 127.60°E) in south-central Rus- chains stretching to Kyushu, the southernmost main island
sia in 1991–1993. They reached Poyang Lake in China of Japan. Then they veered east and crossed the island of
(28.95–29.20°N, 115.86–116.10°E) and Izumi in Japan Shikoku to reach Honshu, the largest main island of Japan.
(Fig. 3b). The main stopover sites along the route to Poyang After that, the routes diverged and the birds headed for
Lake were the mouth of the Yellow River (37.44–37.69°N, different breeding sites in Honshu. We could track two

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Fig. 3 Spring migration routes in 1992 and 1993 (a), and autumn tracked for 11 cranes from Daursky Nature Reserve, Muravivka
routes in 1991–1993 (b) of White-naped Cranes Grus vipio. The Wildlife Refuge, and Khingansky Nature Reserve. From Higuchi
spring migration was successfully tracked for 9 cranes from Izumi, et al. (1996), (2004), and Higuchi (2010)
southern Kyushu, Japan. The autumn migrations were successfully

successive spring migrations of three birds. The two spring terminal points differed among individuals. After reaching
routes were very similar and all the birds returned to the Sumatra, 18 birds changed their travel direction to the
same breeding sites. For the bird breeding in Niigta, central northeast. Only 2 individuals arrived in the Philippines,
Honshu, there were only 1 or 2 days difference in the through Borneo, and 16 individuals ended their migration
departure and arrival dates between the years. on Borneo and the surrounding islands. The other 10
In autumn, the buzzards retraced the route they had moved along the Malay Archipelago and ended their
taken the previous spring. The buzzards breeding in migration at Bankga Island, central Java, and Flores
Tochigi, central Honshu, for instance, flew along the Island, respectively.
Pacific coast and reached Kyushu via Shikoku. The birds of The spring migration was continuously tracked for 22 of
Niigata on the Sea of Japan coast, on the other hand, the 28 honey-buzzards (Fig. 5b). From their wintering sites
migrated through the mountainous regions in central to the end of the Malay Peninsula, the birds mainly fol-
Honshu, and flew across Shikoku into Kyushu. All the lowed the same routes used during autumn migration. They
birds flew through the southernmost Peninsula in Kyushu migrated northwestward along the Malay Archipelago and
on their migration to the South-West Islands. One bird was the Malay Peninsula, then moved to inland China after
tracked down to northern Taiwan, and another bird reached going north through Thailand, Laos, and Vietnam. The
as far as the Batan Islands in the northern Philippines. routes in inland China were located north of those used
Since 2003, Higuchi et al. (2005) and Yamaguchi et al. during the autumn migration, before the birds reached the
(2008) have tracked the migration of 28 Oriental Honey- end of Korean Peninsula. Unlike during the autumn
buzzards Pernis ptilorhynchus from central and northern migration, the birds detoured around the East China Sea by
Japan. Their migration route was totally different from going down through the Korean Peninsula and crossing the
that of Grey-faced Buzzards. In autumn, after departing Korean/Tsushima Strait to reach Japan. Before travelling to
their breeding areas in Japan, they migrated west across China, all the birds stopped for several weeks in Southeast
about 700 km of the East China Sea, then moved through Asia.
inland China, Vietnam, Laos and Thailand and reached As a consequence, individual honey-buzzards visited
the Malay Peninsula (Fig. 5a). All the birds continued most or sometimes all East Asian countries during their
moving from the Malay Peninsula, but the directions and complete migration cycle of autumn and spring.

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Differences in migration routes between seasons

Migration routes sometimes or often differ between spring

and autumn, as shown in the case of the Oriental Honey-
Buzzards. Why did the birds take such different migration
routes at different seasons? Important factors are probably
the weather and the distribution and abundance of their
main foods.
We hypothesized that weather conditions, particularly
wind conditions, were the primary cause of the seasonal
difference in the migration routes of the Oriental Honey-
buzzards. Yamaguchi et al. (in preparation) thought that the
key area causing the seasonal difference was the East
China Sea stretching about 700 km between the western
end of Japan (Goto Islands of Kyushu) and eastern end of
China (mouth of the Yangtze River). Because honey-
buzzards usually fly by soaring and gliding, it would be
difficult for them to traverse the 700-km water barrier
without the benefit of tailwinds and thermals. Our analysis
confirms the presence of relatively strong and stable
northeasterly or north-northeasterly winds blowing over the
East China Sea during the autumn. In contrast, wind
directions are not stable in the East China Sea or Korea/
Fig. 4 Autumn migration routes of Red-crowned Cranes Grus Tsushima Strait during the spring.
japonensis tracked from Lake Khanka, Far East Russia in 1993 and The birds probably use relatively strong winds to tra-
1994, and from Khingansky Nature Reserve, southeastern Russia in verse the oceans. The estimated wind strengths at the
1993. Two cranes from Lake Khanka and seven from Khingansky
satellite locations of migrating individuals over the East
Nature Reserve were tracked, but only a few route lines are shown
here because some routes greatly overlapped. From Higuchi et al. China Sea or the Korea/Tsushima Strait were greater than
(1998) and Higuchi (2010) the mean wind strength at each altitude, except over the
Korea/Tsushima Strait during the spring season. These

Fig. 5 Autumn (a) and spring (b) migration routes of 28 Oriental the migration of the same respective individual. In the spring migration,
Honey-Buzzards Pernis ptilorhynchus tracked between 2003 and 2009. the sites where the honey-buzzards stayed for more than 7 days are
Each different color in the autumn and spring migration routes indicates shown by larger circles. From Higuchi (2010) and further information

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results suggest that it would be beneficial for the honey- military and construction workers. Apparently the level of
buzzards to cross the East China Sea directly by soaring control within the two areas leads to an environment with
and gliding in autumn and to detour around the sea to avoid less disturbance than areas outside these zones. Adjacent to
unstable wind conditions in spring. Furthermore, our data the northern border of the DMZ, North Korea does not
show that, while crossing the East China Sea in autumn, maintain a zone similar to the CCZ, and thus the cranes
each bird travelled in strong tail winds and avoided bad may find too much disturbance in areas directly adjacent to
weather conditions, such as headwinds and rainfall. The the DMZ on the north side, as they do south of the CCZ in
birds occasionally travelled in unfavorable weather condi- South Korea.
tions (weak or headwinds), particularly when passing Habitat protection is relatively assured along the DMZ,
through the Korean Peninsula and the Korea/Tsushima as people cannot enter the DMZ or develop land there.
Strait in spring. Thus, the DMZ functions as a nature reserve or a nature
The autumn migration route across the East China Sea is sanctuary. However, if reunification is achieved on the
likely to have evolved in response to the specific weather Korean Peninsula, key sites will require enforced and
conditions over the sea. meaningful protection to ensure the continued presence of
breeding and wintering cranes (Higuchi et al. 1996, 2004;
Higuchi and Minton 2000).
Important migration areas identified We usually say that there are no national borders for
migratory birds. However, while national borders have no
We can evaluate the importance of stopover, wintering or biological significance, the DMZ is clearly extremely
breeding site based on the number of birds visiting and/or important for birds migrating through East Asia.
length of stay. This information can be used to recommend Using satellite-tracking data on Oriental White Storks
conservation strategies for threatened species and their migrating from southern Russia to southern China, Shi-
habitats. Areas identified as important are likely to be mazaki et al. (2004a) evaluated the importance of the
significant for conservation of the focal species, and can be location of stopover sites by quantifying how well con-
allocated conservation priority accordingly. nected the sites were at which birds spent time during
For example, in China, satellite-tracking data have been migration. They suggested that the stopover sites situated
used to identify the following important stopover and on the shores of Liaodong Bay, Bohai Bay and Laizhou
wintering sites for Siberian Cranes, Red-crowned Cranes, Bay in eastern China are less connected within the network
White-naped Cranes, and Oriental White Storks Ciconia than the other sites used along the migration route. This
boyciana: Bohai and Liaodong Bays, Poyang Lake, the implies that these seashore stopover sites are at higher risk
Three Rivers Plain, Tianjin, the Qiqihar Baicheng area and
the Yellow River delta (Higuchi et al. 1996, 1998, 2000,
2004; Kanai et al. 2000; Tamura et al. 2000). Tracking data Panmunjom Cholwon Kumya Lake Khanka Others
have identified insufficiently protected areas that are 62 29 42 85 28 41 76 17 17
important to cranes and storks, and have helped promote 100
the conservation of these areas.
Data on the number of visiting individuals and the
Total migration days (%)

duration of their stays show that Panmunchom and Chol- 75

won along the Korean DMZ are particularly important sites
for migrating cranes in East Asia (Higuchi et al. 1996,
2004; Higuchi and Minton 2000). All White-naped Cranes 50
tracked over the entire course of their spring migration
stopped at one or more DMZ sites. Seven of the nine cranes
tracked spent more than half their total migration period 25
there (Fig. 6). Higuchi et al. (1998) also showed another
aspect of the importance of the DMZ for Red-crowned
Cranes. In Cholwon, along the DMZ, no satellite locations
0
were received from outside the DMZ or the Civilian 1 2 3 4 5 6 7 8 9
Control Zone (CCZ), in which land use and movements of Individuals
people are less controlled than in the DMZ. The DMZ and
Fig. 6 Percent of migration days spent at each staging site for nine
CCZ provide an area of relatively little disturbance. The
successfully tracked White-naped Cranes in spring 1992 and 1993.
DMZ is of course completely off limits to civilians, and the The numbers above the columns are the total days in migration of
CCZ to the south has controlled use by farmers, the each crane. Higuchi et al. (1996)

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of being isolated from the network of sites occupied on wintering population count data in Japan. The results are
migration. Shimazaki et al. (2004b) also modeled a stay summarized as follows.
site network as an abstraction of the storks’ potential Whistling Swans arrive in Japan during autumn to
migration routes from their breeding sites to wintering sites overwinter, and return to northern Russia in spring. Since
(Fig. 7), and applied network analysis techniques for 1975, a nationwide count survey of Anatidae around Jan-
exploring how the loss of stopover sites could affect the uary 15 has been conducted (Ministry of the Environment
links between breeding and wintering sites. The results 1975–2008). The results show that the population of the
revealed that the number of potential migration routes wintering swans across the country was 1,745 in 1975 but
could decrease exponentially as more stopover sites were began increasing rapidly in the 1980s and reached 40,485
lost under some specific patterns of attrition. It is suggested (approximately 23 times more) in 2008 (Fig. 8). Niigata
that, if the seashore stopover sites facing Bohai Bay in prefecture showed a significant increase in its swan popu-
eastern China were lost, the storks’ migration routes would lation. The population of the swans there was only 69 in
be fragmented, and the wintering sites along the Yangtze 1975 but reached 16,277 (approximately 236 times more)
River in southeastern China would be isolated (Fig. 7b). in 2008, accounting for 40% of the total across the country.
This work provides insights into the requirements for a Satellite-tracking has shown that Whistling Swans
conservation framework that includes a well-connected wintering in Japan breed near Chaun Bay and the mouth of
network of appropriate habitats between breeding and the Kolyma River in Russia, as described above. The swans
wintering locations. lay eggs mainly in May and June. In autumn, they migrate
down to Lake Kuccharo and Lake Ohnuma, Hokkaido, in
the northernmost part of Japan, and fly to all the other parts
Migratory birds and climate change of Japan. When migrating north to their breeding areas,
they return to Lake Kuccharo and Lake Ohnuma in
Higuchi et al. (2009) studied the effect of climate change northern Hokkaido during March through May.
on the population trends of Whistling Swans, combining In order to show the effects of climate change on the
migration routes obtained from satellite-tracking and swan population, we analyzed the relationship between the

Fig. 7 The stay site network of Oriental White Storks Ciconia boyciana: a the network assumed with no staging sites removed; b the network
assumed following removal of four sites facing Bohai Bay. From Shimazaki et al. (2004a, b)

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50,000
45,000
Whole Japan
40,000
Population

35,000
Niigata Pref.
30,000
25,000
20,000
15,000
10,000
5,000
0
1970 1975 1980 1985 1990 1995 2000 2005

Fig. 8 Population trends of Whistling Swans wintering in Japan.

From Higuchi et al. (2009)
Fig. 9 The relationship between air temperature in the breeding area
and the number of young Whistling Swans visiting Japan in winter.
population trends and meteorological factors from 1993 to Based on data from Koike and Higuchi (2009)
2005. We calculated the survival of the swans based on the
proportion of white- and gray-plumaged individuals in per year). Snowfall decreases with higher temperatures.
1 year and the previous year, and the best model, i.e., the The annual rates of temperature increase in these three
best set of factors explaining the survival rates was selected areas are much higher than the 0.02°C average annual rate
through the Generalized Linear Model (GLM) based on of temperature increase in the northern hemisphere.
Akaike’s information criterion (AIC). The results showed Therefore, it is likely that the population trend of
that the snowfall in the wintering area, the air temperature Whistling Swans is associated with the increase in tem-
in the breeding area and the air temperature in the staging peratures (climate change) in the breeding, staging and
area in spring affected the swan population. Namely, the wintering areas of Far East Asia.
survival of the swans increased with less snowfall in Jan-
uary to March in the previous year in Niigata, the wintering
area; with higher air temperatures during May and June of Migrating birds: linking nature and people in different
the previous year in Chersky, the breeding area, near the areas of the world
mouth of the Kolyma River (68.8°N, 161.3°E); and with
higher temperature during March and April in the previous During my research on migratory birds, I felt strongly that
year in Esashi (44.9°N, 142.6°E), the staging area located these birds establish a link not only among natural envi-
about 20 km from Lake Kuccharo. ronments in different countries along their migration routes
If snowfall in the wintering area decreases, the birds can but also among people in different countries. Here, I will
easily forage in paddy fields with more bare ground, discuss this link brought about by migratory birds and
increasing the survival of the swans. The increased tem- future issues concerning the relationship among the birds,
perature in the staging and breeding areas enables the the environment and human activities.
swans to obtain sufficient food for breeding at an early Each autumn and spring, enormous numbers of birds visit
stage, contributing to better survival and breeding success. many areas along their migration routes. During migration,
We also analyzed the relationship between the number the birds obtain food and other things in these areas. Pas-
of wintering young swans and meteorological factors. The serine birds eat insects and seeds in forests and grasslands,
data used for analysis were limited, but the results sug- while shorebirds take sandworms, shellfish and crabs in tidal
gested that more young visited in winter when tempera- flats. Hawks prey on insects, frogs and snakes in forests and
tures were higher in the breeding area the previous summer paddy fields; cranes, ducks and swans eat grass roots and
(Fig. 9). Probably, more young are produced in a warmer seeds in wetlands and aquatic plants near water. Birds cannot
summer and come to Japan for winter as a result. continue their migration without such foods.
The temperature during May and June from 1974 to On the other hand, migratory birds are thought to play
2007 in Chersky has increased by about 3.8°C in the past an important role in maintaining ecosystems in different
33 years (0.11°C per year). The temperature during the areas through their food habits. If only a limited number of
same period in Esashi increased by about 1.5°C (0.04°C migratory birds exist, the population of certain insects, for
per year). Snowfall during January through March in Nii- example, may drastically increase in forests or grasslands
gata decreased by about 1.4 cm in the past 33 years through unbalanced nature in the ecosystem. In tidal flats
(0.04 cm per year). The temperature during the same per- or lakes, specific algae may grow densely and pollute the
iod in Niigata advanced by about 2.6°C in 33 years (0.08°C water.

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These potential negative impacts are not well under- After many years, Pyong Oh became a professor at
stood. During the course of evolutionary history, however, Kyunghee University in South Korea. In May 1964, the
the ecosystems of different areas where many migratory Yamashina Institute for Ornithology in Japan received a
birds stopover could not have functioned well without the letter from North Korea via Moscow. The letter was sent
existence of these migratory birds. Therefore, the popula- from an ornithologist of the Biological Institute of the
tion decline of migratory birds arising from habitat Academy of Sciences. This letter said that he had found a
destruction in one area may cause an ecosystem to deteri- banded Daurian Starling at Moranbon Park in Pyongyang
orate in another distant stopover, breeding or wintering that had a Japanese ring, and asked where the bird had been
area. For example, the destruction of tropical rainforests in released.
southeast Asia may decrease the number of tropical The bird had actually been banded in Seoul, South
migratory birds that overwinter there and migrate to Japan Korea. It was Pyong Oh who had banded the bird. And it
in spring, resulting in unbalanced nature in forest ecosys- was Wong Hong, his father, who had inquired about the
tems in Japan. The destruction of tidal flats in Japan may bird from North Korea. Thus, his father realized that his
diminish the numbers of many shorebirds, and conse- son had grown up to be an ornithologist in the South.
quently cause wetland ecosystems to deteriorate in the Pyong Oh learned that his father was fine and continuing
Philippines, Australia or Russia. conducting bird research in the North. The bird’s ring
Elucidation of these issues is a challenging subject for established a contact between the father and the son who
the future development of ornithology and ecology. Geo- had not met nor corresponded for many years. The
graphically, natural environments in different regions and demilitarized zone still divides North and South Korea.
countries exist separately, but in fact, are linked by Birds, however, easily fly across this border. Thus, the
migratory birds. The conservation of these birds is not only Daurian Starling linked the father to his son even though
essential for their survival but also for the maintenance of the joy it provided was limited.
remote ecosystems, eventually leading to the conservation Migratory birds can be considered unique because there
of the entire global environment. are few creatures that act as such a link between people.
On the other hand, migratory birds also link people People living along the same migration route often share
along the migration routes. Many people visit places along information on these birds. Such information is important
the migration routes to observe migratory birds. Each day in understanding the current state of the birds, clarifying
during migration, hundreds or even thousands of people the relevant conservation issues, and making action plans
visit Shirakaba Pass in Nagano, Cape Irago in Aichi, and to solve their issues. By doing this, people share their
Cape Sata in Kagoshima, where Grey-faced Buzzards and delights and pleasures and realize the importance of con-
Oriental Honey-buzzards fly over during migration. These nections with each other.
people include not only hawk watchers but also many The benefits that migratory birds give us are of
members of the general public. The general public cannot extraordinary value. Research on bird migration or orni-
identify different hawk species but enjoy watching the thology that discovers such benefits is indeed a wonderful
migrating flocks, imagining their long journey for migra- field of science.
tion. Similarly, many people share the same experiences in
different countries along the migration routes. People in
Taiwan, Malaysia or Indonesia may enjoy watching the Future challenges
same flocks of the hawks that flew through Japan; in other
words, migrating birds link different people in remote Satellite-tracking proves to be a powerful research tool to
regions. study the migration of birds. Through this technology, we
The most remarkable example of migratory birds being can show the details of migration routes, seasonal differ-
a link between people is the case where a Daurian Starling ences in migration pattern, and relative importance of each
Sturnus sturninus became a link between an ornithologist of the staging sites. Satellite-tracking is also very useful for
and his son in North and South Korea, respectively. This clarifying the conservation issues that migratory birds
example is summarized below Higuchi (2005). encounter. Based on such information, we can make rea-
It was before 1950. Wong Hong, an ornithologist in sonable recommendations or good action plans for the
North Korea, and his youngest child, Pyong Oh, enjoyed conservation of focal species and their habitat (Higuchi
watching birds and making skins together. When the et al. 2004; Higuchi 2010).
Korean War began, the family was separated: the parents However, because of the weight of transmitters, satel-
stayed in North Korea, while Pyong Oh and the other lite-tracking can be conducted only on large and medium-
children went to South Korea. Afterwards, they could sized birds like cranes, swans, ducks, and hawks. As
neither see nor correspond with each other. transmitters become smaller, the number of bird species

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that can be tracked is sure to increase. If additional Acknowledgments Many scientists were involved in the field
improvements are made to battery life and location accu- work, catching birds and deploying PTTs. They include V. Andro-
nov, G. Archibald, Y. Darman, P. L. Flint, G. Fujita, O. Goroshko, J.
racy, it will become possible to obtain even more detailed Harris, E. Hiraoka, N. Hijikata, J. W. Hupp, S. Javed, Y. Kanai, K.
tracking information for even longer periods of time. Konishi, H. Kuno, V. Krever, J. Minton, E. Morishita, M. Nagen-
Transmitters have been developed recently that use dran, K. Ozaki, M. Parilov, J. M. Pearce, P. Johanna, A. M. Ramey,
solar-powered batteries, which are expected to have a life F. Sato, T. Shimada, H. Shimazaki, R. Suwal, M. Tamura, K. Tokita,
K. Uchida, M. Ueta, and N. Yamaguchi. Yossi Leshem always
of at least 2–3 years. This type of transmitter can reduce provided insightful comments on my migration studies. Naoya Hi-
the weight of PPTs. The smallest solar-powered PTT jikata and Shigeto Koike helped with data analysis and preparing
weighs about 5 g, which is suitable to track birds in the some figures used in this article. Patricia Ormsby and Robert A.
150–200 g range, such as medium-sized terns and sand- Askins reviewed the draft of the manuscript. I thank all of them. The
satellite-tracking studies were funded by NEC, NTT, The Yomiuri
pipers. Efforts have also been made to integrate the global Shimbun, the Ministry of the Environment, the Ministry of Educa-
positioning system (GPS) with the Argos system, known as tion, Culture, Sports, Science and Technology, and the US Geo-
the Argos/GPS PTT. Unlike an Argos PTT, a location can logical Survey.
be specified using GPS systems as they receive coordinate
data from satellites. In an Argos/GPS PTT, location data
stored in the GPS are periodically retrieved through the References
Argos system.
GPS methods entail the use of many satellites, so they Askins RA (2000) Restoring North America’s birds: lessons from
landscape ecology. Yale University Press, New Haven
generally have greater location accuracy (to within dozens
Colborn T, Dumanoski D, Myers JP (1996) Our stolen future: are we
of meters with 1 standard deviation of the positional error) threatening our fertility, intelligence and survival? A scientific
than the Argos system (150–1,000 m), and can provide detective story. Dutton, New York
many measurements per unit of time. Argos/GPS PTTs Higuchi H (1994) Satellite tracking the migration of cranes. The
Yomiuri Shimbun, Tokyo (in Japanese)
also have the benefit of reducing satellite usage fees
Higuchi H (2005) Migration of birds based on satellite tracking
because the data are sent over a shorter period of time. studies. NHK Publishing, Tokyo (in Japanese)
Although the tracking technology of system is ideal, the Higuchi H (2010) Satellite tracking the migration of birds in eastern
smallest solar-powered Argos/GPS PTT still weighs 22 g. Asia. Br Birds 103:284–302
Higuchi H, Minton J (2000) The importance of the Korean DMZ to
Additional sensors can be used in conjunction with stan-
threatened crane species in northeast Asia. Global Environ Res
dard satellite-tracking PTTs. Integrated sensors are used to 4:123–132
corroborate location findings. They include ambient light Higuchi H, Pierre JP (2005) Satellite tracking and avian conservation
sensors to collect environmental data (e.g., temperature, air in Asia. Landscape Ecol Eng 1:33–42
Higuchi H, Sato F, Matsui S, Soma M, Kanmuri N (1991) Satellite
pressure, and altitude), or to record behavioral information
tracking of the migration routes of Whistling Swans Cygnus
(e.g., move or stay, heading and speed when the bird is columbianus. J Yamashina Inst Ornithol 23:6–12
flying). PTTs with such sensors are already available. Higuchi H, Ozaki K, Fujita G, Soma M, Kanmuri N, Ueta M (1992)
However, the addition of sensors increases PPT weight, Satellite tracking of the migration routes of cranes from southern
Japan. Strix 11:1–20
and the sensors may not function well in the field.
Higuchi H, Ozaki K, Fujita G, Minton J, Ueta M, Soma M, Mita N
We expect to see several improvements in future, (1996) Satellite tracking of white-naped crane migration and the
including the development of lightweight, high-perfor- importance of the Korean Demilitarized Zone. Conserv Biol
mance devices that can be used on smaller birds and pro- 10:806–812
Higuchi H, Shibaev Y, Minton J, Ozaki K, Surmach S, Fujita G,
duced at lower cost. As highly accurate, less expensive
Momose K, Momose Y, Ueta M, Andronov V, Mita N, Kanai Y
devices come into use, a dramatic increase in conservation (1998) Satellite tracking of the migration of the red-crowned
research on migrating birds can be expected. crane Grus japonensis. Ecol Res 13:273–282
Of course, satellite-tracking is not only the research tool Higuchi H, Nagendran M, Darman Y, Tamura M, Andronov V,
Parilov M, Shimazaki H, Morishita E (2000) Migration and
to study the migration of birds. If we combine satellite-
habitat use of oriental white storks from satellite tracking studies.
tracking results with other technologies such as radars and Glob Environ Res 4:169–182
Geographical Information Systems (GIS) including satel- Higuchi H, Pierre JP, Krever V, Andronov V, Fujita G, Ozaki K,
lite images, we will be able to obtain more detailed Goroshko O, Ueta M, Smirensky S, Mita N (2004) Conservation
using remote technologies: satellite-tracking white-naped cranes
information on migration strategies and necessary conser-
(Grus vipio) in Russia and Asia. Conserv Biol 18:136–147
vation recommendations. Regular banding schemes and Higuchi H, Shiu H-J, Nakamura H, Uematsu A, Kuno K, Saeki M,
field observations are also necessary to confirm conclusions Hotta M, Tokita K, Moriya E, Morishita E, Tamura M (2005)
derived from relatively small numbers of birds that have Migration of honey-buzzards Pernis apivorus based on satellite
tracking. Ornithol Sci 4:109–115
been satellite-tracked. Further international and inter-dis-
Higuchi H, Koike S, Shigeta M (2009) Effects of climate change on
ciplinary collaboration and cooperation will be required to phenology, distribution, and population. Chikyukankyo
promote such activities from now on. 14:189–198

123
S14 J Ornithol (2012) 153 (Suppl 1):S3–S14

Hupp JW, Yamaguchi N, Flint PL, Pearce JM, Tokita K, Shimada T, Olival K, Higuchi H (2006) Monitoring the long-distance movement
Ramey AM, Kharitonov S, Higuchi H (2011) Variation in spring of wildlife in Asia using satellite telemetry. In: McNeely JA,
migration routes and breeding distribution of Northern Pintails MacCarthy TM, Smith A, Whittaker L, Wikramanayake ED
that winter in Japan. J Avi Biol 42:289–300 (eds) Conservation biology in Asia. Society for Conservation
Kanai Y, Sato F, Ueta M, Minton J, Higuchi H, Soma M, Mita N, Biology Asia Section, Kathmandu, pp 319–339
Matsui S (1997) The migration routes and important rest sites of Service ARGOS Inc (1994) User manual. CLS/Service Argos,
Whooper Swans satellite-tracked from northern Japan. Strix Toulouse
15:1–13 Shimazaki H, Tamura M, Higuchi H (2004a) Migration routes and
Kanai Y, Minton J, Nagendran M, Ueta M, Auyrsana B, Goroshko O, important stopover sites of endangered Oriental White Storks
Kovshar AF, Mita N, Suwal RN, Uzawa K, Krever V, Higuchi H (Ciconia boyciana) as revealed by satellite tracking. Mem Natl
(2000) Migration of demoiselle cranes in Asia based on satellite Inst Polar Res Special issue 58:162–178
tracking and fieldwork. Glob Environ Res 4:143–153 Shimazaki H, Tamura M, Darman Y, Andronov V, Parilov M,
Kanai Y, Ueta M, Germogenov N, Nagendran M, Higuchi H, Mita N Nagendran M, Higuchi H (2004b) Network analysis of potential
(2002) Migration routes and important resting areas of Siberian migration routes applied to identification of important stopover
cranes (Grus leucogeranus) that migrate from northeastern sites for Oriental White Storks (Ciconia boyciana). Ecol Res
Siberia and China as revealed by satellite tracking. Biol Conserv 19:683–698
106:339–346 Tambyah P, Leung P-C (2006) Bird flu: a rising pandemic in Asia and
Keating KA, Brewster WG, Key CH (1991) Satellite telemetry: beyond. World Scientific, New Jersey
performance of animal-tracking systems. J Wildl Manag Tamura M, Higuchi H, Shimazaki H, Oguma H, Darman YA,
55:160–171 Andronov VA, Nagendran M, Parilov M (2000) Satellite
Kerlinger P (1995) How birds migrate. Stackpole, Mechanicsburg observation of movements and habitat conditions of red-crowned
Koike S, Higuchi H (2009) Climate change and the life of birds. In: cranes and oriental white storks in East Asia. Glob Environ Res
Higuchi H, Kurosawa R (eds) Natural history of birds. Hokkaido 4:207–217
University Press, Sapporo, pp 205–219 (In Japanese) Yamaguchi N, Higuchi H (2008) Migration of birds in East Asia with
LaDeau SL, Kilpatrick AM, Marra PP (2007) West Nile virus reference to the spread of avian influenza. Glob Environ Res
emergence and large-scale declines of North American bird 12:41–54
populations. Nature 447:710–714 Yamaguchi N, Tokita K, Uematsu A, Kuno K, Saeki M, Hiraoka E,
Leshem Y, Bahat O (1999) Flying with the birds. Kal Press, Tel Aviv Uchida K, Hotta M, Nakayama F, Takahashi M, Nakamura H,
Nagendran M, Higuchi H, Sorokin AG (1994) A harnessing technique Higuchi H (2008) The large-scale detoured migration route and
to deploy transmitters on cranes. In: Higuchi H, Minton J (eds) the shifting pattern of migration in Oriental honey-buzzards
The future of cranes and wetlands. Wild Bird Society of Japan, breeding in Japan. J Zool 276:54–62
Tokyo, pp 57–60

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