Blackwell Science, LtdOxford, UK ERE Ecological Research 0912-38142002 Ecological Society of Japan 175September 2002 515 Habitat evaluation for crested ibis X. Li et al. 10.1046/j.0912-3814.2002.00515.x Original Article565573BEES SGML

Ecological Research (2002) 17, 565–573

Habitat evaluation for crested ibis: A GIS-based approach

XINHAI LI,1* DIANMO LI,1 YIMING LI,1 ZHIJUN MA2 AND TIANQING ZHAI3 1Institute of Zoology, Chinese Academy of Sciences, 19 Zhongguancun Lu, Beijing 100080, , 2Institute of Biodiversity Science, Fudan University, Shanghai 200433, China and 3The Conservation and Observation Station of Crested Ibis, 723300, China

We evaluated habitat quality for crested ibis (Nipponia nippon) using a geographic information system (GIS). First, we digitized the topography map, vegetation map, river map, road map and villages/ towns map by ArcInfo, and gave each map layer a suitability index based on our perceptions of the needs of crested ibis. Second, we overlayed these maps to obtain an integrated map of habitat quality. Finally, we compared the calculated habitat quality with the actual distribution of crested ibis. We found that the birds were almost always located at the site of high quality (habitat suitability index [HSI] > 0.6), which indicated that the factors we selected were important for crested ibis. We also found that crested ibis were never located at some sites of high quality, thus, we assume that other factors not considered in this study limit the distribution of crested ibis. Regression analysis indicated that crested ibis preferred lower elevation habitats and tolerated higher levels of human disturbance in recent years than previously reported. These results reflected a 20-year protection program for this species.

Key words: geographic information system; habitat quality; habitat suitability index; Nipponia nippon.

INTRODUCTION erences and use. Shi et al. (1991a) reviewed the extinction process of crested ibis at many of its The crested ibis (Nipponia nippon) became one of original habitats and discussed how habitat loss the most endangered birds in the world in the late played a role in its decline. Zhai and Lu (1991) 20th century. Its population size has fluctuated at described the current distribution and abundance a very low level since its rediscovery in 1981 (Li of crested ibis at different habitats in different & Li 1998), but recently increased to 155 individ- stages of its annual life cycle. Wang et al. (1985), uals (including 31 pairs) in the summer of 2001 Wang (1993) and Shi et al. (1991b) evaluated sev- (T. Zhai, pers. comm., 2001). Among the reasons eral features of the landscape that were important for declining numbers of ibis, habitat destruction for crested ibis. Shi et al. (1991c) and Wang et al. is the most important (Lu 1989; Shi et al. 1991a; (1994, 1995) examined the relationship between Cao & Lu 1994). After rediscovering crested ibis population dynamics and habitat quality. Li et al. in remote mountains in Yang County, (1998) discussed key factors for the survival of province, China in 1981 (Liu 1981), researchers crested ibis and evaluated the carrying capacity of have completed several studies on its habitat pref- its current habitat. Ma et al. (2000) analyzed nest site alternation and its influence on population dynamics. Li et al. (2001) weighted the birds’ pref- erences for different habitat factors. However, no reserchers have evaluated habitat quality by *Author to whom correspondence should be considering numerous habitat features simulta- addressed. Email: [email protected] neously. We used a geographic information system Received 27 September 2001. (GIS) to record detailed information on the habitat Accepted 25 February 2002. of crested ibis and we used these data to assess

566 X. Li et al. habitat quality. Our study provides an important METHODS base for determining potential habitats of crested ibis and provides information on how to rehabili- Selection of key habitat features tate other habitats to support large populations of Habitat use by crested ibis has been documented ibis, including potential areas for the reintroduc- from 19 years of monitoring (Wang et al. 1985; Li tion of captive ibis into the wild. et al. 1998). The crested ibis is a mid-sized wading Crested ibis live in Basin and on the bird that roosts in tall trees, and feeds in shallow southern slopes of Mountain in central water. In addition to being found at different alti- China (33°08–35′ N, 107°17–44′ E), mainly in tudes in different seasons, these birds are timid Yang County, Shaanxi Province (Fig. 1). The and are, therefore, easily disturbed by humans. We crested ibis’ habitat consists of breeding, post- analyzed nest site selection of this species using breeding and intermediary prebreeding regions. logistic regression, and the results indicated that From February to June, crested ibis breed in forest vegetation, elevation, wetland and human distur- patches in remote, high (680–1300 m) mountains bance have larger selection coefficients than six within Yang County. After reproduction, crested other factors (density of trees, average height of ibis congregate and fly to the postbreeding region, trees, slope [where the nest tree was located] direc- south of the breeding region. Low hills (450– tion, slope gradient, nest orientation in the tree 840 m) and plains are the main landscape features and coverage above the nest) (Li et al. 2001). of these areas. In the postbreeding season, ibis Consequently, we selected vegetation, elevation, occasionally fly to neighboring counties. In wetland and human disturbance as key habitat November, flocks of crested ibis divide into small features to evaluate for habitat quality. groups and fly to a separate area/habitat between the breeding and postbreeding regions to spend the winter. GIS analysis Vegetation type, topography, rivers, reservoirs, roads, villages and towns were digitized from 1996 to 1998 using ArcInfo (PC Version 3.4.2) on the basis of topography maps (1:100 000) (China National Mapping Bureau 1990) purchased from China National Mapping Bureau, and vegetation maps from the Department of Forestry, Yang County in 1995. The GIS database was modified by ground investigation from 1997 to 2000. Dig- Shaanxi Province itized maps were edited to four different ‘coverage’ layers in ArcInfo (Workstation Version 7.0): the Yang County vegetation layer contained 12 different vegetation types, the topographic layer included contours ranging from 200 m to 2600 m by 200 m inter- vals, the river and reservoir layer contained 1756 main and branch rivers and 72 lakes or reservoirs, and the human disturbance layer included a 482 km highway, 20 km railway and 47 villages N and towns. The map covers the whole Yang County, which includes most crested ibis’ activity ranges. Within each layer, different habitats were assigned different suitability values based on the Fig. 1. The location of crested ibis’ habitat, Yang opinion of six experts (Y. Zhang & B. Lu, Crested County, Shaanxi Province, China. Ibis Conservation Station; Y. Cao & X. Lu, Shaanxi

Habitat evaluation for crested ibis 567

Department of Forestry; Y. Liu & Y. Tan, Institute cell was assigned a habitat suitability index (HSI) of Zoology, Chinese Academy of Sciences) on this value according to the following rules. species (Tables 1,2). After overlaying the four lay- ers with different weights, we obtained the average Vegetation value of the suitability index for each layer, which is the integrated suitability of the complicated Vegetation types differ in habitat suitability in landscape for crested ibis. different seasons (Fig. 2). Rice paddies are the For ease of calculation, we transformed vector major feeding sites of crested ibis during the late images to raster images by using the grid module prebreeding and breeding season. During the post- of ArcInfo. Each raster layer contains 13 192 cells breeding season, however, rice paddies are not suit- measuring 500 m2. In each layer, every individual able for feeding because the rice grows too dense and high. Near the end of the postbreeding season and at the beginning of the prebreeding season, Table 1 The suitability of different vegetation types cropland is usually rotated to rape, which is sel- to crested ibis dom used by crested ibis. Masson pine forests and oak or birch forests are often selected for roosting Vegetation type Seasons HSI and these forests are considered to be highly suit- Masson pine forest 1 able habitats for ibis. Fuel forest and economic Oak or birch forest 1 forest are designed for the farmers’ daily use, they Conifer-broadleaf forest 0.75 are frequently disturbed by humans; wasteland is Cypress forest 0.5 unused mine or idle crop field with rare vegetation Chinese pine forest 0.5 cover. Such areas are seldom visited by crested ibis Cropland Breeding season 1 and were assigned low suitability (Table 1). Postbreeding season 0.25 Prebreeding season 0.5 Wasteland 0.1 Altitude Fuel forest 0.25 Crested ibis move annually between their breeding Shrubland 0.1 and postbreeding regions. The breeding region is Sand 0.1 centered on the middle slope of Qinling Mountain Economic forest 0.25 Fir forest 0.25 at approximately 1000 m a.s.l. The postbreeding region is near the bottom of at (HSI), habitat suitability index. an altitude of 500 m. We believe that crested ibis prefer different altitudes in different seasons. Based on the experience and knowledge of experts, Table 2 The suitability of different altitudes to we assigned a suitability value to the different crested ibis altitudes in the different seasons (Table 2) (Fig. 3). HSI Altitude Breeding Postbreeding Prebreeding Rivers, reservoirs, roads and towns (m) season season season Rivers, reservoirs and their adjacent habitats are 200–400 0.25 0.5 0.15 foraging sites for crested ibis. Thus, areas within 400–600 0.5 1 0.5 250 m of water bodies were assigned a suitability 600–800 0.75 1 1 of 1.0, areas within the next 250 m from rivers 800–1000 1 0.75 1 were assigned 0.75, whereas all other areas had a 1000–1200 1 0.5 1 suitability of 0.5. Conversely, roads and towns, 1200–1400 0.75 0.25 0.75 including nearby areas, are not suitable for crested 1400–1600 0.25 0.15 0.25 ibis because of human disturbance. Areas within 1600– 1800 0.25 0.15 0.15 500 m of roads and 1000 m of towns were assigned 1800–2800 0.15 0.15 0.15 a suitability of 0, areas within the next 500 m from (HSI), habitat suitability index. roads and 1000 m from towns had a suitability of

568 X. Li et al.

Breeding Postbreeding season season

Prebreeding season

Suitability index 0.1 0.25 0.5 0.75 0 10 20 km 1

Fig. 2. The suitability of different vegetation types for crested ibis in Yang County, Shaanxi Province, China.

0.25, with all remaining areas having a suitability Yang County, China. The HSI value of each grid of 0.5 (Fig. 4). was normalized at the range of 0–1 (Fig. 5).

Integrated habitat suitability of Yang County Field investigation for crested ibis The Crested Ibis Conservation Station (CICS) has We have studied nest site preferences of the crested monitored crested ibis since its rediscovery in ibis using logistic regressions and the results indi- 1981. All nest sites were recorded by CICS. From cated that the selection coefficients of height of 1998 to 2000, we located 35 nests that were cur- nest trees, human disturbance, wetland accessibil- rently being used by the crested ibis or that had ity and elevation are 2.91, −2.58, 2.12 and −1.97, been used in Yang County since 1981, and seven respectively (Li et al. 2001). Thus, we weighted sites that were used by the crested ibis as roost sites the vegetation, human disturbance, wetland and at night in the wintering season. The latitude and elevation layers by the four selection coefficients, longitude of all the sites were recorded using glo- separately. Combining the four layers, we derived bal positioning system (GPS) and were imported the overall suitability of habitat for crested ibis in into the GIS database.

Habitat evaluation for crested ibis 569

Breeding Postbreeding season season

Prebreeding season

Suitability index 0.15 0.25 0.5 0.75 010 20 km 1

Fig. 3. The suitability of different altitudes for crested ibis in Yang County, Shaanxi Province, China.

Considering that habitat preferences might in the breeding season, 86.9% area in the post- change during the period from 1981 to 1999, we breeding season and 74.0% area in the prebreed- calculated the HSI of nest sites in each year, as well ing season, respectively (Table 3). as the elevation of the nest sites. In addition to The distribution of crested ibis (Fig. 5) revealed considering the distance effect of roads and vil- that they were found almost exclusively in areas lages, we designed a set of degrees of human dis- where the habitat suitability was >0.6 (Fig. 6). If turbance range from 0 to 6 for each nest and crested ibis only occur in areas where habitat suit- summarized the mean human disturbance ability is >0.6, then the area of suitable habitat is (degrees) for each year. 859.5 km2 during the breeding season in Yang County. Given that each crested ibis pair occupies a territory of 3 km2 (Zhai & Lu 1991), the carrying RESULTS capacity of Yang County is approximately 286.5 pairs. Suitable habitat for crested ibis appears to be The distribution patterns of crested ibis in dif- severely fragmented (Fig. 5). Patches with a suit- ferent seasons are quite distinct (Fig. 5). During ability value measuring <0.6 occupied 73.9% area the breeding season, each pair occupies and

570 X. Li et al.

(a) (b)

Suitability index 0 0.25 0.5 0.75 010 20 km 1

Fig. 4. The suitability of (a) different wetlands and (b) human disturbance for crested ibis in Yang County, Shaanxi Province, China.

Breeding Postbreeding season season

Prebreeding season

Suitability index 0-0.25

010 20 km 0.25-0.5 0.5-0.75 Crested ibis 0.75-1

Fig. 5. The calculated integrated suitability of the habitat for crested ibis and its actual distribution in 1999 in Yang County, Shaanxi Province, China.

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2 Table 3 The area (km ) of patches of different habitat 6 (a) suitability for crested ibis in Yang County 5 Breeding Postbreeding Prebreeding HSI season season season 4

0.0–0.2 395.25 623.25 565.50 3 0.2–0.4 1181.25 1387.50 1134.75

0.4–0.6 861.75 854.25 738.75 2 0.6–0.8 680.25 363.75 678.75 Human disturbance

0.8–1.0 179.25 69.75 180.00 1

(HSI), habitat suitability index. 0 N = 1 1 1 2 2 3 4 3 3 3 3 4 3 6 5 7 10 9 18 1981 1984 1987 1990 1993 1996 1999

1400 (b) defends its territory, and this produces a relatively even distribution pattern. However, at other times 1200 non-breeding individuals will flock to relatively lower elevation habitats. In the postbreeding sea- 1000 son, crested ibis congregate in a few flocks and move from the mountain region to the Hanzhong

Elevation (m) 800 Basin (the lowest region in southwest Yang County). In the prebreeding season the large flocks divide into several smaller groups and return to 600 the mountain area. 400 In recent years, there is evidence to suggest that N = 1 1 1 2 2 3 4 3 3 3 3 4 3 6 7 7 11 10 18 many crested ibis select lower elevation habitats as 1981 1984 1987 1990 1993 1996 1999 1.0 nest sites and, thus, tolerate higher levels of (c) human disturbance (Fig. 6). Our observations indicated that crested ibis paid less attention to 0.9 human activities in these years. From 1990 to 0.8 1999, the number of breeding pairs increased from

4 to 18. Most of the new pairs nested in the down- 0.7 stream area (700–900 m a.s.l., where human den- sity is relative higher), whereas the older pairs 0.6 nested in the upstream area (1000–1200 m a.s.l.). Habitat suitability index (HSI) We used SAS/STAT (SAS 1996) for all HSI statis- 0.5 tical analyses at the nest sites: mean = 0.747, 0.4 SD = 0.089, P(HSI < 0.6) < 0.05. N = 1 1 1 2 2 3 4 3 3 3 3 4 3 6 7 7 11 10 18 1981 1984 1987 1990 1993 1996 1999

Year DISCUSSION Fig. 6. Boxplots show (a) disturbance degrees, (b) altitudes of nest sites and (c) habitat suitability index We used the artificially assigned HSI to evaluate of crested ibis from 1981 to 1999 in Yang County, habitat quality for crested ibis. This is a fast, con- Shaanxi Province, China. venient method for estimating habitat availability with spatial explicitness in a heterogeneous land- scape. However, it is not very objective or accurate. from 1981 to present, although such changes have The HSI values were estimated on the basis of occurred. We used the habitat selection coeffi- experts’ long-term experiences, irrespective of any cients calculated from nest site data to weight the changes to the habitat preferences of this species four key habitat features over a 1-year life cycle,

572 X. Li et al. based on a hypothesis that the four features used than 2 km from a village. There are large areas of affect ibis habitat preference in a stable way over the breeding range of this species that are not the different periods of its life cycle. occupied by either humans or ibis. In fact, the rice On the basis of habitat evaluation, we believe paddies are the only wetland areas in the moun- that the overall habitat quality of Yang County is tains that attract crested ibis. In recent years, sev- not ideal for crested ibis because the HSI values eral pairs of crested ibis selected nest trees that of the four habitat features are all high only in a were within farmers’ yards. These individuals few grids. However, compared to neighboring tended to ignore the activities of the farmers, but counties, Yang County is the most suitable area. were still vigilant with respect to strangers. Although we did not collect habitat data from The habitat preferences of the crested ibis neighboring counties as part of this study, it is change over its life cycle. During the breeding clear that wetlands are scarce in , season individuals forage and roost within their but the vegetation condition is better and human territories, feeding nestlings until they have density is lower. Conversely, wetlands are plentiful fledged. However, during the postbreeding season in , but human density is high. crested ibis forage in a large flock by the Hanjiang In general, crested ibis typically live in wetland River or in the nearby wetlands, up to 20 km from habitats because they are wading birds (Zheng the roost site. We used the roost sites (in the 1973). However, in Yang County this species lives postbreeding and prebreeding seasons) to indicate mainly in mountainous regions during the breed- habitat use (Fig. 5) because the roost sites are more ing season, particularly during the 1980s when stable than the foraging sites (i.e. some crested ibis the species was rediscovered. Wetlands are rare in flew outside Yang County for food). mountain regions except for a few areas with rice Many factors affect wildlife habitat selection paddies near villages; however, in these cases it is and no single theory is suitable for every animal the rice paddy that provides most of the food for (Rosenzweig 1985). Crested ibis live in a patchy the ibis not the wetland. It is not known why the habitat and move between patches to gain the crested ibis left the wetlands for the remote moun- most food for the least energetic cost. Meanwhile, tains. Over the 20th century the crested ibis has human disturbance, competition and the risk of been severely affected by human disturbance, predation negate the benefits of foraging in what including hunting and habitat contamination, as might otherwise be a suitable habitat. We selected well as various other disturbances resulting from what we determined to be the most relevant fac- human activities. Population numbers declined tors to evaluate habitat for crested ibis. Wetlands rapidly in East Asia until only two pairs existed in are the most important food source for this bird, the remote mountains of Yang County. Because the vegetation types determine roosting site quality, density of humans is very high in wetland areas, roads and towns restrict habitat suitability because we believe that this is the cause of the shift in of human disturbance, and different altitudes sat- habitat utilization by crested ibis. isfy different seasonal preferences throughout its The crested ibis is moving back to its original life cycle. Because the habitats that crested ibis habitat gradually (Fig. 6). After 20 years of conser- select are highly correlated with the calculated vation efforts, local residents have begun to protect suitability index, the four factors we considered this endangered species. They are using fewer pes- appear to be important in determining the distri- ticides and fertilizers than in the past and almost bution of crested ibis. We also found that some never poach the crested ibis. In addition, farmers areas with a high suitability index were never vis- keep some rice paddies filled with water all year ited by crested ibis, therefore, some other factors round to conserve the aquatic animals for crested must limit their distribution. In cponclusion, ibis, although this means that they can only plant overall habitat quality (Fig. 5) provides an impor- rice once a year. tant base for determining potential habitats of Through habitat evaluation, we find that crested crested ibis and provides information on how to ibis do not live very far from humans. Thus, it is rehabilitate other habitats to support large popu- not possible to say that crested ibis are sensitive to lations of ibis, including potential areas for the human disturbance because they never nest more reintroduction of captive ibis into the wild.

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