Kor. J. Orni. Vol. 21, No. 2 : 1-11, 2014

A Study on Breeding Ecology of Oystercatcher (Haematopus ostralegus) at Yubu Island

Sang-Duck Lee1･Sun-Gyeum Kim2･Sun-Ho No3･Heui-Young Kang1･Chung-Yeol Baek4･ Sam-Rae Cho3* 1Daejeon Metropolitan City Maninsan Green Learning Institute, Daejeon 300-250, Korea 2Korea Environmental Research, Anyang 431-804, Korea 3Department of Biology, Kongju National University, Kongju 314-701, Korea 4National Wetlands Center, National Institute of Environmental Research, Changnyeong 635-833, Korea

A survey of the breeding ecology of Oystercatcher (Haematopus ostralegus) inhabiting in the Youbu Island was conducted from February to August 2006. The maximum number of Oystercatcher was 2,500 in February and the minimum 150 in July. The nests had outer diameter of 191.7±6.14 mm, inner diameter of 127.3±3.90 mm, depth of 34.2±16.2 mm, and had far from high tide of 617.2±302.0 cm. The laying of eggs starts at the early April with average incubation of 29 days. The total number of eggs laid was 168, and the clutch size was 2.47±0.89. The eggs had a major axis of 57.51±0.06 mm, minor axis of 39.15±0.34 mm, and the weight was 44.30±0.26 g. The hatching success rate among 168 eggs was 78.6% (132 eggs), and the fledgling success rate was 9.8% (13 eggs). During the period of study, there were disturbance factors on 105 occasions and it was accounted for 54.3% by other , 14.3% by fishermen, 10.5% by fish boat and 20.9% by other causes.

key words: Oystercatcher, Breeding Ecology, Yubu Island, Disturbance Factors

Introduction

The oystercatcher is a which falls in , Haematopodidae, it is known that twelve species in one inhabit around the world, and one species of Haematopus ostralegus lives in Korea (Lee et al. 2014). The Haematopus ostralegus breeds its cubs in Europe, the Kamchatka Peninsula, and the northern part of East Asia, and stays over the coldest season in Africa, Middle East, South Asia, and the southern part of China (Seo and Park 2013). Goss-Custard et al. (1995) reported that about 214,000 to 291,000 pairs (876,500 individuals) breed their cubs in Europe, but it has been little known about the individuals and breeding pairs that breed their cubs in Korea. With the start of the fact that two eggs were observed in a small island of an estuary of Yeongsan River in 1917, one pair was found at Daesong Island in Gangwha Island in June 1971, while 18 individuals

* Corresponding author: Sam-Rae Cho, E-mail: [email protected] Received June 27, 2014, Revised September 17, 2014, Accepted October 17, 2014

1 2 Sang-Duck Lee･Sun-Gyeum Kim･Sun-Ho No･Heui-Young Kang･Chung-Youl Baek･Sam-Rae Cho Kor. J. Orni. Vol. 21. and two eggs under the brooding stage on a rock were found in the same place in 1972 and 1973, respectively. Through these cases, it was confirmed that a small number of the birds have bred their cubs continuously in the islands of the West Coast of Korea (Won 1975). Afterwards, according to a simultaneous census of winter birds by the Ministry of Environment, at least 4 individuals were found at the whole area of Yubu Island, a target area of the subject survey in 2007, and the maximum of 3,145 individuals were found at the same place in 2008 (MOE 2004-2012). In the meantime, the results of a study on surveying ecological resources in Seocheon Coastal Wetland Protected Area conducted in 2013 reported that at least 41 individuals to the maximum of 7,190 ones were found there (Seocheon 2013). In addition, it is also known that only a few individuals have survived to the last and bred their cubs so far. Yubu Island has been regarded as the birds' greatest wintering and breeding place in Northeast Asia, but their main habitats have been recently threatened due to a variety of development and reclamation projects, which may cause the reduction of the number of those individuals in the long term. Thus, this study attempted to understand the Oystercatchers' breeding ecology by investigating their nests, number of eggs laid for one breeding season, hatching rates, and fledging rates, and to provide basic materials to conserve their population in a reasonable and deliberate way.

Study area and Methods

1. The study area and term The subject research area is an inhabited island located at the whole area of Yubu Island in Songrim-ri, Janghang-eup, Seocheon-gun, Chungcheongnam-do, South Korea, which consists of five islands in the north, east and west 120 to 1,450 m away from it (Fig. 1). The mud flat in Korea accounts for 2.4% of the nation's total land area, 83% (1,980 km2) of which is distributed in the West Coast. Wide and gentle mud

Fig. 1. The map of survey site. December 2014 A Study on Breeding Ecology of Oystercatcher (Haematopus ostralegus) at Yubu Island 3 flats are formed in the West Coast because its mean depth is comparatively shallow (about 55 m) and makes a big tidal basin of 3 to 9 m, along with its active sedimentation (Lee et al. 2004). Especially, the whole area (15.3 km2) of Seo-myeon, Biin-myeon and Jongcheon-myeon including the subject research area, Yubu Island, have been designated and managed as the Seocheon Coastal Wetland Protected Area (Article 8 of the Wetland Conservation Act, Ministry of Land, Transport and Maritime Affairs). This research was conducted for one year from February 2006 to January 2007, two times per week from April to June in the period of propagation, and one time (07:00-17:00) per week in the other periods.

2. Measurements of the Nests The measurements of the nests internal and external diameters and depth were made using a vernier calipers (mitutpyo, unit: 0.5 mm), and the distances between nests and the coastline were measured using a range finder (Nikon, Laser 800).

3. Measurements of the Eggs The weights of the eggs were measured using a spring scale (unit 0.1 g), while the major and minor axes were measured using a vernier calipers.

4. Hatching and Fledging Rates The research about the hatching rates, fledging rates, and breeding success rates were made for 68 nests in total, which were confirmed that they succeeded in breeding. In addition, the hatching rates, fledging rates, and breeding success rates were calculated using the following expressions: - Hatching success (%) = No. of hatching / No. of egg × 100 - Fledging success (%) = No. of fledging / No. of hatching × 100 - Breeding success (%) = No. of fledging / No. of egg × 100

5. Growth of Baby Birds The weight changes during the process of growth were measured using a spring scale, while the growth changes in their whole lengths, distances between their shinbones and toes, bills, tails and wings were measured using a vernier calipers. In addition to this, other subjects which required to be captured during the research period were recorded using a portable video camera (Hitachi video camera/recorder VM-E58A ×24 zoom).

6. Research of Diet A 1m × 1m quadrat was installed in the mud flat and rocks appeared around the Yubu Island, and their potential diet was investigated there. The species whose taxonomic belongings or names were difficult to define, were collected and then defined referring to Marine Invertebrates in Korea Coasts (Academy Book 2006). The food sizes were measured using a vernier calipers. The lengths and diameters were measured for 4 Sang-Duck Lee･Sun-Gyeum Kim･Sun-Ho No･Heui-Young Kang･Chung-Youl Baek･Sam-Rae Cho Kor. J. Orni. Vol. 21. arthropods and , while heights were measured for mollusks.

7. Intervening Factors The intervening factor refers to the case in where approximately more than 70% of the whole oystercatchers circle around the island during the rest time or food gathering activities at the same time as they are soaring and making warning sounds for more than 3 minutes. The intervening factors are largely divided into fish boats, fishermen, birds, and others.

Results and Discussion

1. Life History The whole area of Yubu Island is a wintering and breeding place of oystercatchers, and so wintering individuals formed some groups in winter and the other wintering groups, except the individuals which breed their cubs in this area from March, moved to the north. Considering the change of individuals of the oystercatchers during the research period, it was confirmed that they reached the maximum number of individuals (2,500 ones) in February, and afterwards, decreased gradually up to the minimum number (150 ones) in July when their breeding season is supposed to end up (Fig. 2). The oystercatchers started to build their nests for the first time on March 4, and it took 21 days (11 to 35 days) on average to the newly to build the nests, repair and then finish them up. Their spawning was made for the first time on April 2, and it took 29 days (22 to 35 days) on average to incubate their eggs. Their first hatching was made on April 30, while the last hatching was made on June 20, with the number of eggs laid reaching 2.47±0.89. Parent birds incubate their baby birds for 3 to 4 days after hatching, and the baby birds left their nests and hid in nearby woods or dents on rocks as two days passed by.

Fig. 2. Variation of Oystercatcher number form February 2006 to August 2006 in Yubu Island. December 2014 A Study on Breeding Ecology of Oystercatcher (Haematopus ostralegus) at Yubu Island 5

Fig. 3. Breeding chronology of the Oystercatcher.

The last fledging was made on July 9, and the fledging period was 30 days on average, which is the same as 30 days which Lee (1988) suggested and shorter than 33 days of their average fledging period (Cramp and Simmons 1983). It is considered that this is because they had sufficient foods at the mud flat around the Yubu Island (Table 5).

2. Locations and Structures of Nests The nests found during the research period were 68 in total, and the ones whose trails were not left were not considered as normal ones. Regarding the places at which those 68 nests were located, 18 ones were found most in west, while 3 ones were found least in northwest, with no nests being found in northeast (Fig. 4). These results show a similar distribution to the results where most of the nests are intensively distributed in west, which were surveyed in Napjak Island by Lee (1998). Even though the location of a nest is generally affected by wind directions and the sun, this research area was not affected by them at all because it is small in size. Considering the geographical characteristics of the island, the northeast

Fig. 4. Location of nest in survey area (n=68). 6 Sang-Duck Lee･Sun-Gyeum Kim･Sun-Ho No･Heui-Young Kang･Chung-Youl Baek･Sam-Rae Cho Kor. J. Orni. Vol. 21. direction with no nests consisted of rock regions whose northeast side was not comparatively smooth with more than 30% bank angles. The locations of the nests were plane topographies whose rocks were smooth with the bank angles of about 30°, or flat areas. In addition, the nests were built on grasslands, sand and rocks. 22 ones were found most on rocks, while five ones were found on sand, with no difference in each side (Fig. 5). However, it is judged that they selected open places where they could secure a clear view in choosing the locations of their nests, instead of preferring a certain area. The nests built on rocks poorly had soft soil beneath them, and small pebbles less than 1cm in diameter, dry grass and boughs were poorly laid on them (Fig. 6). However, for the nests built on sand, dry grass is presumed to act as a place to lay their eggs, considering the research results that they lay eggs with no pebbles and grass on them. The depth of the nests were 34.2±16.2 mm on average, 191.7±6.14 mm in major axis, 127.3±3.90 mm in minor axis (Table 2), and the least distance between the nests and the sea due to a tidal basin was

Fig. 5. Number of nests in the survey area (n=68).

Fig. 6. Cross-sectional diagram of nests. December 2014 A Study on Breeding Ecology of Oystercatcher (Haematopus ostralegus) at Yubu Island 7

Table 1. Distance from nest to high tide line (n=68). Site Mean±SDa (cm) Distance range (cm) Site 1 (n=14) 477.4±263.2 126~1,029 Site 2 (n=11) 668.7±200.3 372~1,048 Site 3 (n=23) 503.3±290.6 215~1,526 Site 4 (n=18) 829.7±298.8 217~1,025 Site 5 (n=2) 710.5±21.9 685~726 Mean±SDa 617.2±302.0 126~1,526 a Standard deviation

Table 2. Nest size of Oystercatcher (n=68). Outer diameter (mm) Inner diameter (mm) Depth (mm) Mean±SDa 191.7±6.14 127.3±3.90 34.2±16.2 (Distance range) (181~205) (111~142) (24~43) a Standard deviation

617.2±302.0 cm on average, and the difference of distances were 126 to 1,526 cm (Table 1). It seems that the places at which the nests were located are not related with the distances between the grass and them. It is thought that the reason that they are near the eyecatchers, having their nests near the surface of the sea, may be in order to easily react to their natural enemies or discouragements, also to be able to eat their prey within a shorter distance in mud flats or on rocks.

3. Characteristics of Eggs According to Won (1975), it was reported that the eggs had big rough dark brown patterns and scattered coal-colored spots based on light brown color, which was similar to the results of this study. The numbers of eggs laid were usually 1 to 5, which was somewhat different from 2 to 5 (Bent 1927) and 2 to 3 (Lee 1998). It has been known that this difference was due to the female's immaturity, ageing, and physical abnormalities, or richness of foods in their breeding place (Price et al. 1988). It was confirmed that 168 eggs in total were found in 68 nests. The results show that the average sizes of the eggs were 37.82 to 42.04 mm (39.15±0.34) in minor axis, 45.22 to 60.49 mm (57.51±0.06) in major axis, and 44.30±0.26 (41.3～46.9)g in weight (Table 3). Compared to Won (1975)'s major axis 56 to 59.3 mm and minor axis 36.4 to 46.6 mm, and Lee (1998)'s major axis 56.2 to 59.8 mm and minor axis 37.0 to 38.2 mm, there was a little difference among their major axes, but no difference among the minor ones. In the meantime, the results were within the Bent (1927)'s average major axis of 57 mm, minor axis 40, and weight of 46 g.

Table 3. Structure of egg (n=168). Major axis (mm) Minor axis (mm) Weight (g) Mean±SDa 57.51±0.06 39.15±0.34 44.30±0.26 (Distance range) (45.22~60.49) (37.82~42.04) (41.3~46.9) a Standard deviation 8 Sang-Duck Lee･Sun-Gyeum Kim･Sun-Ho No･Heui-Young Kang･Chung-Youl Baek･Sam-Rae Cho Kor. J. Orni. Vol. 21.

4. Hatching Rates and Fledging Rates It was reported that 168 eggs were laid at 68 nests in five research areas around the Yubu Island, and the average number of the eggs laid was 2.47±0.89. Among these, the number of the eggs that succeeded in hatching was 132, and the number of the individuals that succeeded in fledging was just 13 (9.8%) (Table 4). This shows the results which are lower than the breeding success rate (20.5%) that Lee (1998) suggested. According to Yoon (2004), it is thought that considering the ecological characteristics of this species, that they forage for food in restricted areas for a limited time according to a tidal basin, they experience serious conspecies and interspecies competition, and especially, their breeding success rates are slightly low because they are vulnerable in food competition due to the predation by black-tailed gulls.

Table 4. Breeding success rate of Oystercatcher (n=168). Clutch size Mean±SDa Hatching success Fledging success (n=68) (%) (%) 2.47±0.89 78.6 9.8 a Standard deviation

5. Diet Wintering individuals of oystercatchers move to and fro according to the flow of seawater due to a tidal basin and foraged for prey, while breeding individuals took in food around each breeding place. The results confirmed that they took in arthropods, mollusks, annelids, etc. It was also confirmed that the average sizes of 7 species of arthropods were 3.63±4.75 cm in each length and 2.50±1.09 cm in each axis; those of 14 species of mollusks 4.13±2.99 cm in each height and 6.39±3.21 cm in each axis; and those of 2 species of annelids 16.88±2.32 cm in each length and 0.70±0.11 cm in each axis (Table 5). Especially, oystercatchers mainly ate Macrophthalmus japonicus, Uca arcuata, Philyra pisum, Upogebia major, etc. among arthropods; Crasssotrea echinata, Mactra veneriformis, Meretrix lusoria, Solen strictus, etc. among mollusks; and Periserrula leucophryna, Perinereis vancaurica tetradentata, etc. among annelids. According to the previous studies, it has been reported that oystercatchers mainly eat arthropods, including crabs, , insects, small fish and seaweeds at shorelines and mud flats (Won 1975), and Manila clams, blue , lugworms, , etc. in Siwha Area (Yoon 2004). Considering the food distribution in each site, mollusks account for high rates of 78.6% and 57.1% respectively in Site 1 and Site 2, while arthropods account for high rates of 41.7% and 51.1% respectively in Site 3 and Site 4. In Site 4, arthropods, mollusks and annelids showed similar distributions in the rate (Fig. 7). According to Yoon (2004), it has been reported that oystercatchers mainly took in Tapes philippinarum, Mytilus edulis, Crassostrea gigas, lugwarms, etc. In addition, their feeding behaviors may vary according to the kind of their prey. Lugwarms immediately feed the prey after catching it, but Tapes philippinarum waits for a certain period of time after catching the prey, and then eats it when their shells open. It has been also reported that Crassostrea gigas opens the prey's shells using its sharp mouth like a chisel and then eats it. December 2014 A Study on Breeding Ecology of Oystercatcher (Haematopus ostralegus) at Yubu Island 9

Fig. 7. Percentage of food materials in survey area.

Table 5. Biomass of food materials in survey area (1 m×1 m). Mean±SDa (cm) Species Height Length Diameter Arthropoda Macrophthalmus japonicus - 2.43±1.82 3.82±2.56 Uca arcuata - 1.83±1.05 3.08±2.41 Cleistostoma dilatatum - 2.17±1.62 2.85±1.95 Philyra pisum - 2.02±1.32 1.97±1.25 Oratosquilla oratoria - 14.36±5.78 1.75±1.03 Upogebia major - 1.57±0.74 0.68±0.58 Callianassa japonica - 1.03±0.68 3.36±2.14 Meretrix lusoria 6.43±3.67 - 8.77±5.32 Cyclina sinensis 2.14±1.24 - 2.47±1.09 Dosinorbis japonicus 5.36±3.26 - 5.79±3.57 Ruditapes philippinarum 2.82±1.62 - 3.78±2.61 Mactra veneriformis 3.04±2.04 - 4.73±2.85 Crasssotrea echinata 2.80±1.98 - 2.57±1.56 Sinonovacula constricta 2.78±1.52 - 9.61±4.78 Solen strictus 1.53±1.23 - 11.27±6.24 Solecurtus divaricatus 2.94±1.47 - 6.63±3.54 Rapana venosa 13.46±8.54 - 10.35±8.47 Ceratostoma roriflum 2.59±2.05 - 3.85±2.04 Reishia clavigera 3.07±2.61 - 1.92±3.20 Lunatia gilva 4.61±2.46 - 8.58±4.51 Glossaulax didyma 4.23±2.03 - 9.24±7.53 Annelida Periserrula leucophryna - 18.52±7.25 0.62±0.57 Perinereis vancaurica tetradentata - 15.24±6.54 0.78±0.23 Others Echinodermata, Cnidaria, -10.38±8.32- Protocordata etc. a Standard deviation 10 Sang-Duck Lee･Sun-Gyeum Kim･Sun-Ho No･Heui-Young Kang･Chung-Youl Baek･Sam-Rae Cho Kor. J. Orni. Vol. 21.

6. Intervening Factors The intervening factors observed within the breeding areas consisted of the four factors such as fish boats, fishermen, birds and others (105 times in total), and among these, birds as seagulls and longbills acted as the greatest intervening factor, followed by fishermen (15 times; 14.3%), fish boats (11 times; 10.5%), and others (22 times; 20.9%) (Fig. 8). Considering the intervening factors by each month, birds had the greatest effect on them in February (64.3%). In addition, fishermen and fish boats appeared 16.7% in August, and other factors did 33.3% in July (Fig 9). It appeared that among the intervening factors, birds had the greatest effect on them; this was because their nests are located at the exposed spots such as rocks or sand and thus its predator, seagulls, interfered with most of them. It was also because they had to make a serious competition for prey with seagulls and longbills which shared the food collecting areas with them. According to Yoon (2004), it was reported that oystercatchers make a little competition within the same species, but experience a serious competition for prey with other species which shares the food gathering places with them. In addition, they had a very limited feeding and drinking area, even though the mud

Fig. 8. Factors of disturbance in survey area.

Fig. 9. Percentage of disturbance factors in survey area during each month. December 2014 A Study on Breeding Ecology of Oystercatcher (Haematopus ostralegus) at Yubu Island 11 flat spread widely for them due to a tidal basin. Especially, when they breed their cubs in islands, the reduction of their feed resources may have a direct connection with the reduction of their population because they forage for food within 500 m from their habitats. Thus, it is considered that the fundamental method for conserving and protecting their population is to reject senseless collection of the main diet of bird lifet and to minimize the possible damage of the mud flat.

References

Academy Book. 2006. Marine Invertebrates in Korea Coasts, Korea. Bent A.C. 1927. Life histories of North American shorebirds. Dover Publications. Newyork. Cramp and Simmons. 1983. Handbook of the birds Europe, Middle East and North Africa; the birds of the Western Palearctic, Vol. Ⅲ. to Gulls, Oxford University Press, Oxford. Goss-Custaed J. D., R. T. Clarke, K. B. Briggs, B. J. Ens, K. M. Exo and C. Smit. 1995. Population Consequences of winter habitat loss in a migratatory shorebird : Ⅰ. Estimating model parameters. Journal of Applied Ecology 32:317-333. Lee S.D. 1998. The study on breeding ecology of Oy stercatcher (Haematop us ostralegus) at Napjak Island in the west sea, Korea. Ph.M.thesis. Dissertation, Kongju National University, Korea. Lee S.W, G.J. Jong and H.S. Lee. 2004. Tidal Flat Aspects of Yellow Sea Area and Conservation for Migratory Birds. Korean Journal of Ecology and Environment 17: 295-303. Lee W.S., T.H. Lee and J.Y. Park. 2014. A Field Guide to the Birds of Korea, LG Evergreen Foundation, Seoul. pp. 210-211. Ministry of Environment (MOE). 2012. Winter bird census simultaneous (2004-2012), National Institute of Environmental Research, National Institute of Environmental Research (NIER). Seo J.H. and J.G. Park. 2008. A Photographic Guide to the Birds of Korea. Shingu Publishing, Korea. pp. 116-117. Secheon. 2013. Research of wetland in Seocheon mud flat, Secheon. 34pp Won P.O. 1975. Natural Monument of Korea. Samhwa Printing, Seoul. pp. 105-109. Won P.O. 1981. Illustrated Flora & Fauna of Korea Vol. 25. Minister of Education. pp. 436-438. Yoon M.B. 2004. The Diversity of Reproductive and Foraging on Breeding Season of (Haematopus ostralegus). Korean Journal of Environment and Ecology 27: 383-390. (In Korean with English title and abstract).