NORTH-WESTERN JOURNAL OF ZOOLOGY 15 (2): 179-183 ©NWJZ, Oradea, Romania, 2019 Article No.: e182602 http://biozoojournals.ro/nwjz/index.html

Spatial Distribution Pattern of Sympatric Wintering Birds in the Largest Coastal Nature Reserve in China

Shanshan LI1, Ting LI1, Xiuqing HAO1, Lin ZHU1, Yongqiang ZHAO2, Shicheng LV2, Guang YANG1 and Bingyao CHEN*

1. Jiangsu Key Laboratory for Biodiversity and Biotechnology, College of Life Sciences, Nanjing Normal University, Wenyuan Road NO. 1, Qixia District, Nanjing 210023, China. 2. The National Yancheng Rare Birds Nature Reserve, Yancheng 224333, China. * Corresponding author, B. Chen, E-mail: [email protected]

Received: 11. November 2017 / Accepted: 13. July 2018 / Available online: 18. July 2018 / Printed: December 2019

Abstract. The range pattern of wintering bird communities in the buffer zone of Yancheng Reserve, the largest coastal reserve, China, was investigated using 3S technologies. Differences in bird spatial distributions were also tested for spatial occupation, habitat type preference, and range overlapping ratio. The estimated average range sizes of the 16 bird species with enough sightings were 249.24 (28.17-435.25) km2 of 95% fixed kernel (FK) and 131.03 (15.33-225.25) km2 of minimum convex polygon (MCP). Phoenicurus auroreus and Lanius schach had the largest 95% FK and MCP range, respectively, whereas Larus ridibundus had the smallest 95% FK and MCP range. Most species utilized aquaculture and farmland areas largely, 85.97% of their core range included both habitats. The core range of any paired species overlapped 3.86-41.00 km2, the average overlap ratio was 11.70% (0.58 - 21.91%). The geographic grids analyses showed that 1-3 species, 4-6 species and 7-9 species occupied 111 grids (64.9%), 47 grids (27.5%), and 13 grids (1.75%) individually, implicating low species spatial aggregation. This study suggested that differences in spatial distributions possibly contribute to the coexistence of sympatric species in Yancheng Reserve.

Key words: ecological niche separation, habitat type, range size, spatial distribution, Yancheng Reserve.

The community composition and spatial distribution of munity, and mudflats. It is an ideal survey site for studying the sympatric birds are commonly influenced by both biotic and range patterns and coexistence strategy of sympatric birds. A total of abiotic environmental conditions (Li et al. 2014, Martínez– 18 transects ranging from 2.0 to 12.0 km (188.8 km) was designed and surveyed during 15th to 30th of December 2010 when the winter Felipe et al. 2015, Carrara et al. 2015). Facing competition for migratory birds arrived. resources, sympatric species commonly separate in the selec- The survey was initiated by trained researchers from 0730 to tion of ecological niche and produce a set of adaptation 0830 hr and lasted until 1300 to 1600 hr, depending on the length of strategies (Koladiya et al. 2012, Phillimore & Owens 2008). the selected survey line. Walking speed in the transect lines was un- For instance, birds with different body sizes (Clegg & Owens der control of 2–3 km / hr. In the field, we only counted birds within 2002), beaks (Hill and Lein 1989), and claws select different about 200 m from the transect, the actual effective strip distance was foraging tree species, foraging position, height (Lee et al. no more than 100 m (Wang et al. 2019). When birds were sighted, the 2005), foraging pattern (Bates et al. 2014) and resources (Gar- species name, number of individuals, habitat type, and latitude and longitude coordinates of sightings using GPS were recorded. To cia & Arroyo 2005). Some species form a geographical distri- avoid double-counts, we did not record the birds flying forward. bution of allopatric speciation on different gradients and ex- When multispecies were found in same flock, we then photographed pand niche breadth to reduce overlap and sustain the eco- and counted different birds separately. Birds were photographed as logical needs of species (Zhou & Fang 2000). many as possible by using a Canon EOS-1Ds Mark II or III digital Yancheng Rare Birds National Nature Reserve camera with a 100–400 mm zoom lens and 1.4× tele-converter for fur- (Yancheng Reserve) is the largest coastal nature reserve in ther identification. China covering 2472.6 km2 areas, supporting 394 species that Range Size. The range sizes of birds during the study period were estimated using minimum convex polygon (MCP) and fixed belong to 52 families of 19 orders (Wang and Lv 2008), and it kernel (FK) methods. In the present paper, 95% FK and MCP repre- is also an important wintering habitat for millions of migra- sents the general distribution scale, 50% FK reflects the core area of tory birds (Wang et al. 2011). Abundant information on the animal activity (McGrady et al. 2002, McLeod et al. 2002). diversity, distribution, and habitat selection of the birds is The home range size of each species was generated based on po- available (Liu et al. 2010, Liu et al. 2013, Jiang et al. 2010, sition records of all sightings of species by using animal movement Wang et al. 2015, Li et al. 2016), nevertheless the pattern un- analysis extension (Hooge and Eichenlaub 1997) in Arc View 3.3. FK derlying their co-existence has been rarely investigated. method used a smoothing factor, which was calculated using a cross- In this study, we examined the distribution patterns of validation procedure for the least squares (Seaman et al. 1999, Pattis- hall and Cundall 2008). sympatric wintering birds, calculated the home range of dif- Habitat Preference and Overlap Ratio. The habitat types of land- ferent species of birds in the northern buffer zone of scape were judged under the support of remote sensing (RS), GPS Yancheng Reserve, and tested whether different bird species and GIS technologies. Satellite image analysis and adjustment were occupy different spatial ecological niches. based on Landsat satellite RS images (in 2000), and GPS-fixed point data was collected. The 2008 Landsat TM images covering the north Study Area and Survey Design. Yancheng nature reserve was di- buffer zone of the Yancheng Reserve were selected according to 1:5 vided into three functional zones: core zone, buffer zone and ex- million topographic map of the image geometric correction, with in- perimental zone. The buffer zone is delimited on the periphery of the terpretation accuracy higher than 90%. Various class interpretation core area where any anthropogenic activities were prohibited, the marks were established using land use maps, comprehensive data on scientific research activities were allowed. The northern buffer zone the coastal zone, and field survey data in tidal land resources. In Ar- of Yancheng nature reserve covers 224.9 km2 and comprises a variety cGIS 9.3, information on spatial landscape type was extracted by of habitats, such as cultivated fields, aquaculture, reed-grass com- visual interpretation. The area was divided into five types of habi- 180 S. Li et al. tats: aquaculture area, farmland, plantation, residential area, and 47.31 km2 between 3.15 and 91.92 km2. river, with areas of 115.3, 89.1, 20.5, 2.0, and 7.7 km2, respectively. Phoenicurus auroreus and Lanius schach in Passeriformes The habitat preference of 16 species with sufficient site location has the largest 95% FK and MCP ranges, respectively, never- data were tested. The range of birds in five types of habitats was theless Larus ridibundus of Lariformes has the smallest 95% separately calculated and compared among different species. The 50% FK range could represent the habitat preference of FK and MCP range. birds and thus, it was used as test parameter. Range overlap of paired bird species in the same orders is calculated by overlap ratio Habitat Preference (Cederlund and Sand 1994): On average, 85.97% (72.01%–100%) of the core range (50% r = 2 , /  MMM bac  FK) of the 16 species of birds was concentrated in the aqua-

where, Ma and Mb are the 50% FK range size of the two-detected culture areas and farmlands (Table 2, Fig. 1, Fig. 2). The high species, and Mc is the overlapping area between them. proportions of the core range of seven species, namely, 74.02% Mergus merganser, 66.59% Grus japonensis, 64.76% La- Range Size rus vegae, 63.39% Emberiza rustica, 62.50% Phasianus colchicus, Among the 50 species recorded in the buffer zone of 61.77% Lanius schach and 57.56% Ardea cinerea, were distrib- Yancheng Reserve (Li et al. 2016), the range size of 16 species uted in aquatic culture ponds. The main core range of three was measured based on an average of 24 sightings (from 9 to species, namely, 60.30% Grus grus, 70.22% Egretta garzetta 59). The estimated range size of 95% FK was 28.17-435.25 and 100% Larus ridibundus, was in farmlands. km2, with an average of 249.24 km2 (Table 1). The mean MCP Residential, woodland, and riverside areas were the sec- range size was 131.03 km2, ranging from 15.33 km2 to 225.25 ondary habitats with lower contribution of core ranges km2. The birds occupied the mean core range (50% FK) of (13.97%, 0%–27.99%). Six species avoided the residential

Table 1. The range sizes of 16 bird species coexisting in north buffer zone of Yancheng Reserve, China.

Order Species 50%FK 95%FK MCP (km2) (km2) (km2) Passeriformes Lanius schach 50.93 376.68 225.25 Phoenicurus auroreus 82.36 435.25 183.52 Pica pica 70.59 338.16 212.74 Passer montanus 43.09 271.51 187.70 Motacilla alba 42.63 208.76 100.70 Emberiza rustica 50.67 245.50 111.39 Emberiza pallasi 91.92 357.51 151.01 Gruiformes Grus japonensis 25.39 196.76 101.75 Grus grus 45.71 185.70 77.72 Ciconniformes Egretta garzetta 55.99 289.81 181.30 Ardea cinerea 35.37 167.46 96.59 Lariformes Larus ridibundus 3.15 28.17 15.33 Larus vegae 53.42 241.62 131.60 Podicipediformes Tachybaptus ruficollis 10.69 199.17 189.39 Anseriformes Mergus merganser 21.17 91.82 35.35 Galliformes Phasianus colchicus 42.84 226.86 99.47

Table 2. The contribution of core home range (50% Fixed Kernel) of birds to five types of habitats

Order Species Aquaculture area Farmland Plantation Residential area River Passeriformes Lanius schach 30.83 11.74 1.74 3.42 2.19 Phoenicurus auroreus 37.05 23.20 0.37 17.73 4.00 Pica pica 27.59 22.73 2.36 11.15 2.90 Passer montanus 22.70 17.74 0.26 1.20 0.43 Motacilla alba 26.93 10.04 0.25 3.42 1.84 Emberiza rustica 18.81 22.00 0.12 7.39 2.35 Emberiza pallasi 33.83 35.79 4.35 12.10 5.85 Gruiformes Grus japonensis 14.99 4.19 0 3.33 0 Grus grus 15.02 27.56 0.46 2.15 0.52 Ciconiiformes Egretta garzetta 2.20 20.73 0 6.23 0.37 Ardea cinerea 18.34 9.88 0 3.44 0.20 Lariformes Larus ridibundus 0 3.15 0 0 0 Larus vegae 33.00 12.75 0.13 4.24 0.84 Podicipediformes Tachybaptus ruficollis 5.91 4.78 0 0 0 Anseriformes Mergus merganser 15.67 4.47 0 0.22 0.81 Galliformes Phasianus colchicus 26.19 13.29 0.09 1.77 0.57 Distribution pattern of Yancheng Reserve wintering birds 181

Figure 1. The 50% fixed kernel home range overlap of different species in 4 orders of Passeriformes (top left), Ciconiiformes (top right), Lariformes (bottom left) and Gruiformes (bottom right) in north buffer zone of Yancheng Reserve, China.

Figure 2. Percent of five habitat types of 16 bird species’ occupation in Yancheng Reserve, China during winter 2010.

area. Grus japonensis and Grus grus in the Gruiformes had a low overlap ratio of 2.66%, with an area of 5.56 km2. The overlap Home Range Overlap Ratio ratio between Larus ridibundus and Larus vegae in the Lari- The 50% FK core range overlap area size and ratios among formes was 0. the seven different species in Passeriformes are listed in Ta- ble 3. In 21 paired species, the core range of two given spe- This study provided evidence that different bird species cies overlapped at 3.86-41.00 km2, which generated an aver- have different habitat type preference, spatial separation, age overlap ratio of 11.70%, ranging from 0.58% to 21.91%. and low-range overlap ratio, all these possibly contributed to Egretta garzetta and Ardea cinerea in the Ciconiiformes the coexistence of sympatric birds. had the highest overlap ratio of 35.06%, with an area of 26.05 In this paper, the negative correlation between home km2 mainly in the aquaculture area and farmlands (Fig. 2). range size and body size of the species was observed. In

182 S. Li et al.

Table 3. Home range overlap area (upper right matrix, km2) and ratio (lower left matrix, percent) in the core home range (50% FK) of different species in Passeriformes in study area.

L.s. P.a. P.p. P.m. E. r.. E. p. M.a. Lanius schach - 20.08 29.68 20.52 17.73 33.63 19.71 Phoenicurus auroreus 9.61% - 24.13 9.36 31 35.47 20.83 Pica pica 24.51% 10.02% - 13.38 12.12 41 11.53 Passer montanus 19.18% 2.47% 5.88% - 12.08 16.31 10.95 Emberiza rustica 12.18% 23.03% 4.11% 6.69% - 22.22 6.83 Emberiza pallasi 24.15% 16.61% 25.91% 6.72% 10.60% - 8.87 Motacilla alba 17.89% 12.35% 4.42% 6.53% 2.16% 2.01% -

Yancheng Reserve, large birds in Lariformes and Anserifor- Education Institutions, and Jiangsu Province Wildlife Conservation mes had a small range (Table 1). In comparison, small birds Station (commissioned projects). We thank the National Yancheng in Passeriformes occupied the largest FK and MCP distribu- Rare Birds Nature Reserve for their coordination with the local affairs. We also appreciate Chen Yuan for his assistance in the field tion range. Body size influences the absolute energy re- survey. All applicable ethical guidelines for bird observation in quirement of each species (Garcia & Arroyo 2005) and food research have been followed with approval from Animal Research partitioning (Shelley et al. 2004). 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