Migration by the Japanese Wood Pigeon ( janthina) across the islands of East Asia: Direct tracking by satellite telemetry

By Soon Kyoo Choi, Yung Chul Park, Jong Chul Park, Gi Chang Bing, Woo Yuel Kim*

Abstract The Japanese Wood Pigeon, Columba janthina, is an endemic that lives only on the East Asia Pacific islands. The population of this species on Ulleung Island, South varies in size with season, but the cause for this was unknown. We hypothesized that Japanese Wood Pigeons migrate seasonally between breeding and non-breeding sites and accordingly studied their movement from June 28, 2017 to April 20, 2018 using GPS transmitters. We report the first evidence of seasonal migration of Japanese Wood Pigeons to non-breeding sites (Okinoshima and Nishinoshima Islands in ), 278 km from the breeding site (Ulleung Island). This migration route was on the East Asian-Australasian flyway and constitutes the longest flight ever recorded for Japanese Wood Pigeons. Our finding has significant implications for understanding previously disputed aspects of the ecology of Japanese Wood Pigeons, including geographical isolation, hybridization, population retention, and patterns of movement.

*Corresponding Author E-mail: [email protected]

Pacific Science, vol. 73, no. 2 December 5, 2018 (Early view) Introduction

Globally, 81% of the endangered species in the order Columbiformes inhabit island environments (Walker 2007). Japanese Wood Pigeons, Columba janthina, are endemic to the

East Asia-Pacific islands, and only occupy the islands of Japan and southern Korea (Seki &

Takano 2005, Brazil 2009). Because of the restricted range and small population size of the Japanese Wood Pigeon, it is an internationally protected species, categorized as Near

Threatened (NT) by the International Union for Conservation of Nature (IUCN 2017). Several studies have determined that Japanese Wood Pigeons eat seeds and of evergreen broad- leaved trees in subtropical and temperate regions (Won 1981, Oh et al 1994, Takano et al 1995,

Ando et al. 2017). Other studies on this species include observational location reports (Takano

2004) and genetic studies comparing subspecies (Seki et al. 2007).

Habitat networks and long-distance flying ability are closely associated with how populations are structured and can affect the chances of survival of a given species, including

Japanese Wood Pigeons, inhabiting a limited space (Seki et al. 2007). of Japanese

Wood Pigeons are distributed across the Eastern Asian island region of the Pacific. The sizes of

Japanese Wood Pigeon populations vary greatly according to the season; thus, the possibility of long distance movement has been suggested (Park 2002, Ando et al. 2015, Ando et al. 2016).

However, no previous studies have focused on the movement of Japanese Wood Pigeons.

Furthermore, Japanese Wood Pigeons are not observed on Ulleung island in winter, and the wintering areas during the non-breeding season are as yet unknown (Park 2002).

We aimed to determine the causes of seasonal variation in population sizes of Japanese

Wood Pigeons on Ulleung Island, South Korea. This study was conducted to confirm the hypothesis that the capacity for long-distance movement and migration are important components of the life history of Japanese Wood Pigeons.

2 Methods

Study site

Ulleung Island (geographical coordinates are 130° 47′ 37″–130° 56′ 20″ longitude East, and 37°

27′ 2″–37° 33′ 01″ latitude North) is an East Asia-Pacific island located between Japan and

Korea. It covers a total land area of approximately 7256 ha (Fig. 1). Ulleung Island is located approximately 130 km from the east coast of the Korean peninsula. Because of its warm and humid maritime climate, it has a greater distribution of subtropical plants such as Machilus thunbergii than inland areas at the same latitude. Its annual average temperature is 12.3 °C, and its annual average snowfall is 233 cm, with heavy snowfall occurring during the winter months

(Korea Meteorological Administration 2016).

Attaching global positioning system (GPS) transmitters to Japanese Wood Pigeons

A preliminary survey was performed on Ulleung Island in April 2017, to identify the habitats frequently visited by Japanese Wood Pigeons during foraging. Individual pigeons were captured near a forest at 37° 30′ 49″ N, 130° 48′ 13″ E at an altitude of 45 m. We captured pigeons on

June 27, 2017 using a mist-net and a bow net, after obtaining approval from the Ministry of

Environment and the Cultural Heritage Administration of the Korean Government. We selected individuals suitable for attaching GPS transmitters (WT-300, GPS-Mobile phone-based

Telemetry built in Solar System, KoEco, Korea, 27 g) by measuring their weight (mean = 454 g,

SD = 75, range = 350 – 557 g, n = 14). The GPS transmitters weighed less than 7% of the body weight of the pigeons (Taylor et al. 2017) and were attached to two individuals. We assigned ID numbers to the individuals with transmitters and released them at the location where they were captured within 20 min of capture. Subsequently, we monitored the incoming signals for five

3 days at the site to assess signal reception from the trackers and the mobility of the tracked individuals.

Data collection

Each transmitter transmitted GPS tracking data (error range < 40 m) in the form of wireless satellite signals. The transmitters had an embedded solar battery and were configured to maximize the number of satellites from which the signal was received. The locations were recorded in the integrated server for 24 h/day at 4-h intervals via a mobile communication system, Wideband Code Division Multiple Access (WCDMA). Location information was retrieved from the website (WILDTRACKER, http://www.wi-tracker.com).

Data analysis

We analyzed the movement data of one of two captured individuals, a male pigeon, identified as

#1704, with a body weight of 535 g. Unfortunately, the transmitter for the other individual, #

1703, did not receive data after Oct 2, 2017. Data were analyzed based on 524 valid data points of the 642 total data points obtained between June 28, 2017 and April 20, 2018. The GPS points were analyzed using the Movement Tool in the computer program QGIS 2.10.1. Given the 4-h interval transmission used in this study, the “distance flown” refers to the straight-line distance covered by the individual over 4 h; tracking data were analyzed to yield the distance flown per hour. The resulting dataset was used for movement and migration analyses after dividing the entire duration of the GPS tracking data into periods that showed clear changes in movement patterns (Table 1) and long-distance movement between regions, respectively.

4 Results

Evidence of Migration

Pigeon #1704 migrated to Japan in September 2017, spent the winter season in Japan and returned to Ulleung Island in April 2018. An increase in the frequency of movement within

Ulleung Island was observed in early September, which is when usually start their fall migration in Korea (Fig. 2). On September 20, 2017, pigeon #1704 repeatedly moved long distances over Ulleung Island, and GPS coordinates were recorded once on the northwest and east of Ulleung Island, respectively. Finally, it migrated to Okinoshima Island in Japan, which is

278 km away from Ulleung Island.

Following its arrival at Okinoshima Island, pigeon #1704 showed restricted movement patterns from September 21 to September 23, and then flew 28.6 km southward to Nishinoshima

Island on September 24 (Fig. 2). It remained on Nishinoshima Island for 18 days, and then returned to Okinoshima Island, where it remained for 185 days. In the wintering area, pigeon

#1704 spent considerable time in three locations within a radius of 500 m. Then, on April 14,

2018, before returning to the breeding grounds of Ulleung Island in April, it moved to

Nishinoshima Island, which is 31 km southwest of Okinoshima Island, the main wintering area.

Two days later, the pigeon returned to Ulleung Island, the breeding site, on April 16, 2018, completing the migratory route and behavior. The maximum flight distance for pigeon #1704 was 278.43 km, and the longest distance flown in terms of coordinates was recorded during pigeon #1704’s migration to Japan, moving from 37° 28′ N, 130° 51′ E to 36° 12′ N to 133° 17′

E, spanning one degree of latitude (1° N) and three degrees of longitude (3° E). This migration path is the first to be identified for this species.

Movements

5 On Ulleung Island, Analysis of major activity times by hour shows indicated varying patterns of active hours, but, the pigeon was mostly active at night—from 20:00–24:00 on Ulleung Island, and 08:00–12:00 and 20:00–00:00 in Japan (Table 2).

Pigeon #1704 moved over the entirety of Ulleung Island for several days before migration.

However, when it migrated to the breeding site in spring, it tended to move in a direct pattern. In addition, the Japanese Wood Pigeon displayed a homing instinct, returning to the place where the transmitter was attached when it arrived at the breeding site.

Discussion

This study provides the first evidence of seasonal migration of Japanese Wood Pigeons, which are endemic to the East Asia-Pacific islands, to non-breeding sites (Okinoshima, Nishinoshima

Islands) 278 km from the breeding site (Ulleung Island). This migration route was on the East

Asian-Australasian flyway. The pigeon moved actively throughout the period considered to be the autumn migration period of birds—late August to September (Michev et al. 2011, La Sorte et al. 2015)—and on September 20, 2017, the tracked pigeon (#1704) migrated to a non-breeding site, returning to the breeding site on April 16, 2018. Migratory birds live in two habitats, and both breeding and non-breeding sites are important for birds (Morton & Stutchbury 2005). The data recorded on the seasonal migration is the longest flying distance recorded for a Japanese

Wood Pigeon—although the coordinates were recorded at a 4-h interval, there is no landing place in the route, and the distance was therefore assumed to be covered without a pause.

Data were collected over 208 days in Japan and 90 days on Ulleung Island. We believe that fewer data points were recorded in Japan because the transmitter, which was solar-powered, was not charged because the Japanese Wood Pigeon may have spent more time in darker areas under

6 the trees. Based on this, one could infer that Japanese Wood Pigeons spend more time in darker forests at the non-breeding site or wintering site than at the breeding site.

However, the distance covered, as indicated by the number of coordinates, suggested twice as much activity in Japan. This observation is interpreted as being indicative of a wider range of activities to secure food, which is more scarce (Klatt & Paszkowski 2005). Pigeons that inhabit islands and that mainly feed on fruits exhibit narrower movement ranges in areas with abundant food resources (Powlesland et al. 2011). Securing food in the winter is an important aspect of survival and reproduction (Studds & Marra 2005). On Ulleung Island, a considerable amount of snowfall occurs during the winter, which buries the food items used by Japanese Wood Pigeons.

As such, this species is not observed on Ulleung Island during the winter (Park 2002). Thus, the purpose of the seasonal migration of Japanese Wood Pigeons might be to enable them to forage for food items during the winter (Ando et al. 2017).

A recent study identified the hybridization of two subspecies of Japanese Wood Pigeons,

C. j. janthina and C. j. nitens (Ando et al. 2015). These subspecies occupy different habitats, and plant genes from islands 150 km away have been identified in the feces of C. j. nitens, raising the possibility of long-distance movement (Ando et al. 2017). A previous study also suggested that stable gene flow between dispersed island habitats and subspecies differentiation is the result of migration by Japanese Wood Pigeons (Seki et al. 2007), but there is no direct evidence to support this hypothesis. The results of our satellite telemetry study provide an explanation for the stable maintenance and seasonal fluctuation of Japanese Wood Pigeon populations in Korea and Japan.

Furthermore, our results suggest that ensuring the genetic stability of Japanese Wood Pigeons may require the conservation of geographically independent habitats. Based on the above results, we believe the seasonal migration case documented here is not unique and is likely part of the life history of Japanese Wood Pigeons.

7 Here, we identify the causes of the seasonal changes in the population of Japanese Wood

Pigeons on Ulleung Island, South Korea. Our results provide the first evidence to suggest that migration is an important behavioral characteristic for Japanese Wood Pigeons. However, further investigation is required to fully understand the movement ecology of Japanese Wood Pigeons.

We hope that future studies will be conducted between the breeding site and non-breeding sites of Japanese Wood Pigeons, and that studies will focus on habitat conservation and protection of this species.

Acknowledgments

This study was conducted as part of the 4th National Natural Environment Research Project. We thank the Ministry of Environment and Cultural Heritage Administration of Korea for approving the study, and for the technical advice provided by KOECO (WT-300).

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11 Table 1. Movements recorded by an attached global positioning system (GPS) transmitter for a male Japanese Wood Pigeon captured on Ulleung Island.

Number of Distance Duration Area Date range GPS points flown (m) (days) (n) 49,218 28 Jun–31 Aug 65 262 Ulleung Island, Korea 152,560 1 Sep–20 Sep 20 99 Okinoshima Island, 231,698 21 Sep–23 Sep 3 15 Japan Nishinoshima Island, 38,164 23 Sep–10 Oct 18 34 Japan Okinoshima Island, 41,452 11 Oct–25 Mar 166 51

Japan 1,862 26 Mar–13 Apr 19 39 Nishinoshima Island, 21,204 14 Apr–15 Apr 2 3 Japan Ulleung Island, Korea 253,845 16 Apr–20 Apr 5 21 Total 790,003 28 Jun–2 Oct 298 524 GPS tracking data of Japanese Wood Pigeon in each period was separated into breeding and non- breeding seasons on Ulleung Island and the period of time during which the rate of the main movement changed in Japan.

12 Table 2. Mean movement distance segregated by time period (unit: km)

#1704 (mean ± SE) Time (hours) Japan (Okinoshima and Korea (Ulleung Island) Nishinoshima Islands) 0–4 0.65 ± 0.001 0.03 ± 0.001 4–8 0.28 ± 0.001 0.31 ± 0.02 8–12 0.29 ± 0.02 9.34 ± 0.001 12–16 0.28 ± 0.03 0.99 ± 0.02 16–20 0.22 ± 0.03 0.15 ± 0.01 20–0 0.74 ± 0.01 2.51 ± 0.01

Fig. 1. Location of Ulleung Island, where two global positioning system (GPS) trackers were attached to two Japanese Wood Pigeons.

13 Fig. 2. Migration route of a Japanese Wood Pigeon (#1704), measured using an attached global positioning system (GPS) transmitter. Dates shown as year – month – day.

14