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Ecological Research
Volume 13 Issue 3 Page 273  - October 1998
doi:10.1046/j.1440-1703.1998.00271.x
 
Satellite tracking of the migration of the red-crowned crane Grus japonensis
Hiroyoshi Higuchi, Yuri Shibaev, Jason Minton, Kiyoaki Ozaki, Sergey Surmach, Go Fujita, Kunikazu Momose, Yuria Momose, Mutsuyuki Ueta, Vladimir Andronov, Nagahisa Mita & Yutaka Kanai

Autumn migration routes of red-crowned cranes, Grus japonensis, from two continental east Asian sites were documented in detail by satellite tracking. Two routes were identified: a 2200 km western route from Russia's Khingansky Nature Reserve to coastal Jiangsu Province, China; and a 900 km eastern route from Lake Khanka (Russia) to the Korean Peninsula and the Demilitarized Zone. The most important rest-sites were identified as Panjin Marsh (China), coastal mudflats south-east of Tangshan City (China), the Yellow River mouth (China), Tumen River mouth (North Korea/China/Russia), Kumya (North Korea) and Cholwon (Korean DMZ). Movements within the wintering range were also recorded, including complex commuting between sites by individual cranes and patterns of daily movements within sites. These data should prove useful for conservation of the flyway.

 INTRODUCTION Go to: GO down

The red-crowned crane Grus japonensis (P.L.S. M・ler) of east Asia is listed as an endangered species by Collar et al. (1994). It is closely associated with wetlands, which are being converted for agricultural use at a rapid rate throughout Asia (Hussain 1994). Red-crowned cranes breed only in north-east Asia, where they have two separate populations. On the island of Hokkaido (Japan), there is an estimated 600 non-migratory cranes (ECRPT 1993). The continental population, estimated at 1100-1450 individuals (Meine & Archibald 1996), migrates from breeding grounds in the China, Mongolia and Russia to the Korean Peninsula and coastal China.

Two migration routes of continental red-crowned cranes have been hypothesized from observations of migration sites and wintering grounds (Williams et al. 1986; Pae & Won 1994; Shibaev & Surmach 1994), but detailed information on the routes and their crucial stopover sites has not been available, partially due to difficulties in coordinating research efforts. Two hundred and twenty-nine red-crowned cranes were captured and banded between 1981 and 1996 in Russia and China, but only 11 have been re-sighted or recovered outside the banding areas (K. Ozaki, unpubl. obs.; Xu et al. 1995). This illustrates the difficulties in studying the species' migration routes using traditional methods.

As migratory cranes may pass through several different countries, they are an excellent subject to study by satellite tracking, which has been used in several successful studies to overcome logistical or environmental difficulties in studying long-distance movements of birds (e.g. Jouventin & Weimerskirch 1990; Nowak et al. 1990; Higuchi et al. 1996).

In the present study, red-crowned cranes migrating from two breeding sites in continental Asia were located by satellite during their autumn migrations. They revealed the timing of their movements and the exact locations of stopover sites. In this paper, we report the detailed migration routes, distances and days spent for migration, local movements between wintering sites, and important sites judged from the frequency of use of each site.

 STUDY AREA AND METHODS Go to: GO up down

Capture sites

Red-crowned cranes were captured in Russia at Khingansky Nature Reserve in 1993, and at Lake Khanka Nature Reserve in 1993 and 1994.

Khingansky Nature Reserve lies along the Amur River downstream of the Bureya River confluence in the Russian Far East, near Blagoveschensk City. The nature reserve, with the closely associated Ganukan Wildlife Refuge, protect 145 000 ha of marshlands and 5690 ha of lake.

Lake Khanka Nature Reserve is on the shores of Lake Khanka in the south-east of the Russian Far East, north of Vladivostok. The reserve has a core protected area of 38 000 ha, and a buffer zone of 73 500 ha. Lake Khanka is on the border with China, where the Xingkai Lake National Nature Reserve also protects some breeding habitat for red-crowned cranes.

Cranes captured

At the study sites, adult cranes which were flightless due to molting were captured with the aid of helicopters. In July 1993, one crane was captured at Khingansky, and two at Ganukan Refuge. Those cranes were marked with platform transmitter terminals (PTT) and released immediately. At Lake Khanka, seven cranes were captured in July 1993 and four cranes in July 1994. They were marked with PTT and released immediately. All of the 14 cranes were adults belonging to different families.

Transmitter and harnessing

Transmitters used in this study were developed by the Nippon Telegraph and Telephone Corporation (NTT). Two types of transmitter, T-2038 and T-2050, were attached to cranes in Lake Khanka, but only the T-2050 was used at Khingansky.

All PTT were attached to the back of cranes with Teflon-treated ribbon. The type T-2038 was 133 x 33 x 23 mm in size with an antenna of 200 mm, and weighed 120 g including harness (15 g), which is about 1.5% of the body weight of an adult red-crowned crane. The type T-2050 was 60 x 40 x 30 mm in size with an antenna of 180 mm, and weighed about 95 g including its harness (15 g), which is about 1.2% of the body weight of an adult red-crowned crane.

The frequency of transmission from PTT in 1993 and 1994 was 6 h active and 12 h inactive, and the pulse interval was 60 s. The battery life was expected to be 6 months for all transmitters. The actual battery life varied among transmitters.

Data analysis

Location classes ranged from zero to three (Service ARGOS 1994). The higher the location class, the more accurate the location. In a reported case of location data received from PTTs designed for tracking ungulate mammals and wolves, location classes one, two and three had a one standard deviation accuracy of 1188 m, 903 m and 361 m, respectively (Keating et al. 1991). According to Service ARGOS (1994), class one and two locations offer a one standard deviation accuracy of 1000 and 360 m, respectively, for stationary transmitters. Therefore, we assumed an accuracy of 1 km for all data of location class one and above, which means that we will not use satellite locations for movements within 1 km.

Location class zero data were included to show migration routes, when the locations were considered appropriate from the nearest tracking time and locations. They were, however, excluded from the analysis when more accurate locations were required.

The period of stay at a particular site was calculated as the difference between the first day of arrival at the site and arrival at the next site. Locations of the cranes are presented below as longitude and latitude, and represent the range of coordinates received during their stay in each area. The most southern and northern latitudes received, and the most western and eastern longitudes, were reported when more than one location was received.

The tracking period outlasted the migration period, and thereby provided data on the wintering period of individual cranes. From the migration period we recorded the pattern of migration through time and space, the location of rest sites and their relative use by tracked cranes. From the wintering period, we recorded daily movement patterns, and commuting by some individuals between wintering sites on the Korean Peninsula.

Habitat analysis

General habitat characteristics of stopover sites were obtained from published materials such as Scott (1989), Ma and Li (1994), Fan et al. (1994) and maps available from the National Imagery and Mapping Agency of the USA (formerly the Defense Mapping Agency). Landsat satellite images were used to show the habitats of the Demilitarized Zone (DMZ) on the Korean Peninsula.

 RESULTS AND DISCUSSION Go to: GO up down

Migration routes

Of the 13 cranes marked in 1993 and 1994, seven from Lake Khanka and two from Khingansky were tracked the entire distance to their wintering grounds (Table 1). A total of 4562 locations were obtained. About 30.0% of them fell into location class 0, 49.6% into class one, and 24.4% into classes two and three. The daily number of locations received from each individual ranged from 0 to 8, with a mean and standard deviation of 2.9 ア 1.6 (n = 1449).

Cranes captured at the two sites took different migration routes to the wintering areas (Fig. 1). The route from Lake Khanka led to wintering grounds on the Korean Peninsula, and a total of seven cranes were tracked the entire distance along this eastern route in 1993 (n = 5) and 1994 (n = 2). The route from Khingansky led to coastal China, and two cranes were tracked the entire distance along this western route in 1993.

On the eastern migration route from Lake Khanka, the seven successfully tracked cranes began migration from early to mid-November (Table 1). Cranes then flew about 300 km south-west to wetlands around the Tumen River (Russia), where six cranes stopped over for 1-2 days each between 6 and 19 November. Their locations were along the sea coast, wetlands and lakes near the national borders of Russia, China and North Korea (Fig. 1). Then cranes migrated south along the coast of North Korea to the river mouth at Odaejin-nodongjagu (41ー25'N, 129ー40'E), where they followed an inland river valley to the coastal city of Kimchaek in the south. At the river mouth and within this valley, five cranes stopped over at four sites for 1-3 days each between 9 and 22 November. After reaching the coast again at Kimchaek, they flew south along the coastline toward Kumya, arriving by 22 November.

All seven birds wintered in Kumya, Anbyon and Cholwon, which are within 125 km of each other. One individual wintered exclusively at Kumya (ID 20261), while four cranes (ID 20263, 20265, 20266, 20267) wintered exclusively at Cholwon after resting for 1-4 days at either Kumya or Anbyon. The other two cranes (ID 3622, 3623) followed a complex pattern of commuting between the three sites during the winter season. Movements during wintering will be treated in a following section.

None of the seven cranes on the eastern route rested at a single site for more than 4 days. The total migration distance on this route was 874.4 ア 62.3 (SD) km (range = 775.5-948.2 km) for the five cranes that did not show movement among the wintering areas (Table 1). The cranes took 5.6 ア 2.4 (SD) days (range = 3-9 days, n = 5) to migrate between breeding and wintering areas.

The two cranes (ID 20269, 20270) from Khingansky Nature Reserve, the head of the western migration route, began migration in early November (Table 1). After beginning migration, overnight rests were spent at separate sites within Heilongjiang Province (China). They flew to Panjin Marsh (China), at the head of Bohai Bay (Fig. 1), where they rested for 2-3 days and 6-7 days each between 7 and 15 November.

They next rested at coastal mud flats south of Tangshan City in China (Fig. 1), having arrived on the same day they departed Panjin, and were located here for 6-8 days between 9 and 17 November. The cranes flew across Bohai Bay to separate rest sites south of the Yellow River Estuary (Fig. 1). One crane (ID 20270) rested only 3 days before departing for the south, but the second crane (ID 20269) rested for 25 days between 18 November and 13 December. The cranes flew south until reaching the coastal area of Jiangsu Province (China), known as the Yangcheng Marshes, arriving on 22 November and 14 December, respectively. They wintered separately in coastal mud flats (Fig. 1).

The two cranes migrating from Khingansky traveled 2.5 times the mean distance of eastern migrants, 2241.8 km, and took more than 20 days (mean = 29.5) to finish their migration (Table 1).

Figure 2 shows a quick migration pattern with few rests for eastern cranes, a similarly quick migration with a complex pattern of local movements among wintering sites by two eastern migrants, and a laddered migration pattern including long rest periods in western cranes.

Movements between wintering sites

Two satellite tracked cranes (ID 3622, 3623) from Lake Khanka in 1994 showed a complex pattern of movement within their wintering grounds on the Korean Peninsula (Fig. 3). The cranes moved among Cholwon, Anbyon and Kumya, and showed similar patterns of site choices and timing, with ID 3623 consistently changing sites 1 day later than 3622. The reason for this is unknown, as no relationship between the two was noted at capture. They were possibly responding to conditions such as weather on the wintering grounds, which affected cranes broadly.

After arriving at Cholwon on 18 November, the cranes stayed 3-4 days before moving to Anbyon, where they stayed 6 days. Then they moved to the Ryonghung River mouth in Kumya, staying for 6 days. They then returned to Anbyon and continued to move between there and Kumya, spending between 3 and 8 days at each site. One crane returned to Cholwon for 8 days before its PTT quit functioning.

The wintering sites of Cholwon, Kumya and Anbyon are within 125 km of each other, and their proximity apparently allows cranes to make these local movements. However, a total of eight cranes had PTTs which continued signalling for 10 days or more after the migration period was over, including those of the western route or those tracked in 1993, but no other cranes showed any tendency to travel between sites.

Wintering ground daily movements

The daily movements on wintering grounds of the eastern route showed a clear pattern only at Cholwon. The site can be divided into two sections (Fig. 4): the DMZ and the CCZ. The DMZ is off-limits to regular human activities, while the CCZ is a buffer zone which is used only for agriculture and military installations. In addition to this, there is a difference in habitat types. The DMZ is an area of low hills and meadows with natural vegetation, and streams which are ice-free due to the presence of hot springs. The CCZ is a developed area of irrigated agricultural fields.

Six cranes were located at the Cholwon site, and the four which did not commute provided enough data to show daily movement patterns by comparison of day and night locations. Two cranes (ID 20265, 20267) used the CCZ during the day (14 of 15 locations; 93.3%) as a foraging site, but roosted in the DMZ at night (25 of 25 locations; 100%) (Fig. 4). A third crane (ID 20266) used the CCZ as both its primary feeding site (four of six locations; 66.7%) and roost (10 of 12 locations; 83.3%). The fourth crane (ID 20263) used the DMZ for both its primary foraging site (six of seven locations; 85.7%) and roost (seven of nine locations; 77.8%).

Pae and Won (1994) noted that the CCZ is used as a foraging site by wintering red-crowned cranes because of a low disturbance rate, and an abundance of grain remaining in the fields after harvest. They also reported that cranes can roost on frozen reservoirs in the CCZ, as well as in ice-free streams in the DMZ, although they did not report on movement patterns of individuals. Their observations are coincident with our results, although it is not known why one crane would remain only in the DMZ.

Almost no location data was received from outside the DMZ and the CCZ. This is probably due to disturbance levels outside the controlled zones, and not to a difference in habitat (Fig. 4). It appears that in both North Korea and South Korea agriculture is present outside of those zones, but it is likely that disturbance in those areas leads the cranes to prefer the DMZ and CCZ. Adjacent to the north border of the DMZ, North Korea does not maintain a zone similar to the CCZ, and thus the cranes may find too much disturbance in those areas.

Important sites and their conservation

Along both migration routes a total of 25 rest sites were used. Fourteen were used by one or two cranes for only 1 or 2 days (overnight roosts), and four were used by only one crane each for durations between 3-5 days. The remaining seven rest sites were visited by a high percentage of tracked cranes, and/or for durations up to 25 days.

The latter seven sites plus the wintering sites are considered to be important sites for migrating cranes due to the number of visiting cranes or the duration of stay. The names, latitudes and longitudes of these sites, and their habitat types, are shown in Table 2.

These sites can be considered internationally important habitats for the migrating cranes. The cranes rest their wings and take energy there before leaving for the next site. If these sites are lost, the cranes may not be able to complete their migration. Some of the sites, such as Shuang Tai He Kou National Nature Reserve of Panjin Marsh and Yangcheng National Nature Reserve are designated as protected areas. Even some protected sites are reportedly inadequate to conserve the cranes' habitat, and proposals have been made to expand both Lake Khanka Nature Reserve and Khasanskiy Nature Park (Tumen River) in order to protect important crane habitats (Gluschenko & Shibaev 1996; Litvinenko & Shibaev 1996).

However, most sites are not protected and face serious threats from economic development. In the Tumen River estuary, the Rajin-Sonbong Free Economic Trade Area has been proposed in North Korea (Chong & Morishita 1996), and the Tumen River Economic Development Area (TREDA) is a four country project sponsored by the United Nations Development Program. In Panjin Marsh, China, excessive reed harvesting and oil development are having an impact on wildlife, while all along the Bohai Bay agricultural development and attendant habitat reclamation are considered to be a threat to coastal marshes, including south-east of Tangshan and the Yellow River mouth (Scott 1989).

Particularly important for the migrating cranes on the Korean Peninsula are the DMZ and CCZ in Cholwon area. The DMZ and CCZ areas were also frequently used by white-naped cranes, Grus vipio Pallas, as rest sites (Higuchi et al. 1992, 1994, 1996). These areas do not presently have any wildlife protection status, and development projects for infrastructure are presently being conducted, with industrial projects in the planning stages.

We must conserve these important sites as a network, not separately. The conservation of these areas must be approached from an international perspective because the migration routes themselves cross several national boundaries. Satellite tracking data should be useful to promote international cooperation for conservation of migrating cranes and their habitat.

 ACKNOWLEDGEMENTS Go to: GO up down

We sincerely thank scientists of the nature reserve staff in Khingansky Nature Reserve and Lake Khanka Nature Reserve for field assistance, and J. Chong, C. H. Halvorson, G. Archibald, J. Harris, F. Kaliher and S. Chan for valuable information on cranes and wetlands, and E. Morishita for preparing the manuscript. This research was supported by the Yomiuri Newspaper Company, the NEC and NTT Corporations of Japan.

 
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Footnotes

Email: higuchi@uf.a.u-tokyo.ac.jp

Present address: Department of Electrical and Computer Engineering, Kumamoto University, Kurokami 2-39-1, Kumamoto-shi, Kumamoto 860-0862, Japan.


Ecological Research
Volume 13 Issue 3 Page 273  - October 1998
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Authors:
Hiroyoshi Higuchi
Yuri Shibaev
Jason Minton
Kiyoaki Ozaki
Sergey Surmach
Go Fujita
Kunikazu Momose
Yuria Momose
Mutsuyuki Ueta
Vladimir Andronov
Nagahisa Mita
Yutaka Kanai
conservation
Grus japonensis
migration route
red-crowned crane
satellite tracking


1Laboratory of Wildlife Biology, The University of Tokyo, Yayoi 1-1-1, Bunkyo-ku, Tokyo 113-8657, Japan 2Institute of Biology and Soil Sciences, Russian Academy of Sciences, Vladivostock 690022, Russia 3Wild Bird Society of Japan, WING, 2-35-2 Minamidaira, Hino-shi, Tokyo 191-0041, Japan 4Yamashina Institute for Ornithology, Konoyama, Abiko-shi, Chiba 270-1145, Japan 5Wakatake-cho 10-2, Kushiro-shi, Hokkaido 085-0036, Japan 6Khingansky Nature Reserve, Arkhara, Amursk Region, Russia 7NTT Wireless Systems Laboratories, Take 1-2356, Yokosuka-shi, Kanagawa 238-0313, Japan



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Table 1 Individual tracking data for nine adult red-crowned cranes of unknown sex, satellite-tracked...




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Table 2 Important migration rest sites of red-crowned cranes satellite-tracked in north-east Asia




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Fig. 1.  Migration routes of red-crowned cranes satellite tracked from Lake Khanka to the Korean Penins...



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Fig. 2.  Migration patterns of satellite-tracked red-crowned cranes, represented as distance traveled o...




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Fig. 3.  Satellite location data from two migrant red-crowned cranes, illustrating the locations of thr...




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Fig. 4.  Satellite image of the Cholwon wintering site, with diurnal (yellow, 9:00-15:00) and nocturnal ...



To cite this article
Higuchi, Hiroyoshi, Shibaev, Yuri, Minton, Jason, Ozaki, Kiyoaki, Surmach, Sergey, Fujita, Go, Momose, Kunikazu, Momose, Yuria, Ueta, Mutsuyuki, Andronov, Vladimir, Mita, Nagahisa & Kanai, Yutaka (1998)
Satellite tracking of the migration of the red-crowned crane Grus japonensis.
Ecological Research  13 (3), 273-282.
doi: 10.1046/
j.1440-1703.1998.00271.x