study area

Yancheng Biosphere Reserve is located on the east coast of China (32°34′–34°28′ N, 119°48′–120°56′ E). It was established in 1983, and accepted as an international biosphere reserve in 1992. The reserve stretches 584 km along the coast near Yancheng City and encompasses an area of 453 000 ha (Ma et al. 2000), within which the core zone, comprising mainly natural coastal wetland habitats, extends over 17 400 ha, and the buffer covers 38 900 ha. The latter includes natural and artificial wetlands (such as saltworks) with little human disturbance, providing habitats for red-crowned cranes and other resident and migratory waterbirds (Fig. 1). Major habitats within the reserve include grass and sedge marshes, common reed Phragmites australis wetlands, grasslands dominated by cogon grass Imperata cylindrica, tree plantations and agroecosystems planted with wheat, paddy rice and cotton. The sedimentation of sand and silt from the Yangtze River results in the continual extension of the intertidal area in the centre and south of the reserve, while erosion causes the loss of intertidal habitats in the north. The coastline in the north has, however, been stable since dykes were built there in the 1980s. Land in the core zone is owned by the reserve authorities while land in the buffer and transition zones is under the control of the local governments. Approximately 2 million people now live in the transition zone of the reserve.

Two separate populations of red-crowned crane occur in north-east Asia, the non-migratory Japanese population (approximately 900 birds) and the migratory mainland population (1750 birds) (Wetlands International 2006). The migratory population mainly winters in the Demilitarized Zone of Korea and on the east coast of China (BirdLife International 2001), with Yancheng Biosphere Reserve forming the primary wintering area between October and March (Ma et al. 2000).

Prior to 1995, the scale of land exploitation was relatively small within the reserve. However, in that year the local government approved a series of plans to exploit intertidal land (Wan et al. 2000). Consequently, coastal wetlands outside the core zone have come under intense pressure from development (Ma et al. 2000; Wan et al. 2000). Developments have also controversially been promoted in the core zone (China's National Committee on Man and Biosphere 2000), in part to provide income for the reserve. Four types of development have been promoted: aquacultural ponds for fish; planted reedbeds for thatch and paper-making materials; clamworm (Perinereis sp.) and mollusc fields for the collection of clamworms, snails and shellfish for food. The reserve authorities have not participated directly in the development projects in the core zone, but rent the land to contractors. Agreements have been signed between the reserve authorities and the contractors for each project in the core zone, stipulating the area of development, land-use type and management (Xue & Willoughby 2001). In this way, it was intended that all such projects should not only provide suitable habitats for cranes and other waterbirds, but also bring economic benefits to the reserve and local communities (Wan et al. 2000).

It should also be noted that since the early 1990s, maize has occasionally been fed from December to February to red-crowned cranes in the core zone during some harsh winters. In 1995, 1996 and 1998, cranes were fed with approximately 25 kg of maize each morning, giving a total throughout the winter of approximately 1000 kg. Unfortunately, detailed records of artificial food provision are unavailable.

development projects in the reserve and its core

Data on the extent of development within the transition, buffer and core zones of the reserve from 1982 to 2003 were obtained from local statistical yearbooks (Yancheng statistical yearbook 1990, 1992, 1993, 1995, 1996, 1999–2004; Jiangsu Provincial Annals 1995; Jiangsu Statistical Yearbook 1995), documentation of the reserve and from satellite images.

Land-use types in the reserve were identified using satellite images from 1984, 1992 and 2000 (Landsat TM). The ortho-corrected ETM panchromatic images were geo-rectified and converted to a UTM coordination using road intersections and other prominent visible features on the image. Average error (RMS) of less than 0·5 m was achieved for all images, and the pixel size was kept at 30 × 30 m. We adopted a combination of unsupervised and supervised classification based on expert knowledge. More than 20 training locations were collected in the field for different land-use types. The data on land-use in 1995 came from the land-use map (1:10 000), and were interpreted using the satellite images. The area of each type of land use was calculated using Arcview GIS version 3·2.

Information about the contracts and supervision of the development projects in the core zone were obtained from interviews with the reserve managers in 2000–2001. At the same time, one-on-one interviews were conducted with contractors and a sample of hired labourers (two to four people) from the local communities for each development project, from whom information on the inputs and outputs of each development project was obtained using a standard questionnaire (see Supplementary Material Appendix S1). Field surveys were conducted in December 2000, and January and August 2001 to confirm the actual management associated with each development project in the core zone. We also investigated the income of local people from the artificial wetlands in the core, buffer and transition zones by interviewing a sample of approximately 10 people within each zone.

red-crowned cranes and their habitat associations

Red-crowned cranes and their habitat associations were investigated in the whole reserve each winter from 1982 to 2003. Since cranes frequently move habitats when they first arrive on the wintering grounds (Ma et al. 2000), the surveys were conducted in December or January when the distribution of cranes was relatively stable. Two or three groups of surveyors conducted fieldwork simultaneously in different parts of the reserve. This allowed the number, distribution and habitat associations of red-crowned cranes to be surveyed over a period of about 3 days each winter. Each group recorded the cranes along fixed routes approximately 5 km apart. As the crane is such a large bird, observers could easily record the cranes with ×60 spotting scopes. The search effort in each zone was the same each year. Prior to 1996, the distribution of cranes was marked on a 1:10 000 map and thereafter recorded using GPS. The low mobility of the cranes minimized the possibility of double counting individuals, but surveyors also compared records of location, movement and flock size to further reduce the chance of double counting.

waterbird communities before and after the construction of waterfowl lake

A 240-ha aquacultural lake was constructed on the supralittoral tidal zone in the core zone in March 1994 (Wan et al. 2000), and was the first development project in this part of the reserve. The species and number of waterbirds were investigated in the same region at 1- to 2-week intervals between December 1992 and February 1993 (before construction of the lake) and again between December 1996 and February 1997 (after construction). The flatness of the landscape meant that a pavilion (about 6 m high) near the lake site could be used to record waterbirds accurately using a spotting scope. In order to obtain the best visibility, waterbird counts were conducted in the afternoon about 2 h before sunset. The diurnal activities of cranes were also recorded simultaneously, along with human activities and their effects on waterbirds.

data analysis

The percentage of land that had been developed in each zone from 1982 to 2003 was calculated, together with the proportion of different land-use types in each zone; regression analysis was used to analyze the rate of change. One-way anova was used to compare the mean net income of local people (per person per year) from the artificial wetlands established in the three zones.

The numbers and densities of cranes in the core, buffer and transition zones were calculated for each of the annual winter surveys together with a 3-year running mean. These figures were then considered alongside the changes in total crane numbers in the reserve, land-use types and management patterns in each of the three functional zones, and whether or not the cranes were observed in natural or artificial habitats (aquacultural ponds, saltworks and managed reedbeds). Linear regression was used to relate the proportion of crane numbers in each zone out of the total crane numbers in the reserve to the changes of total crane numbers and percentage of developed land in the reserve. We used these two predictor variables based on a priori hypotheses that they would be the most important in determining the proportion of cranes in each zone. Models were run separately for each zone, and were evaluated using Akaike's second-order information criterion (AIC_c), Adjusted R², and Akaike weights (StatSoft Inc. 2001); the models with the lowest AIC_c, and the highest adjusted R² and Akaike weights were selected.

The degree of aggregation of the cranes in the reserve was quantified by calculating the ratio of the variance to the mean (Blackman 1942) for the number of birds counted in 5 × 5 km² areas across the reserve. This ratio describes the degree of clumping, with values > 1 indicating an increasing degree of aggregation, values < 1 a relatively even distribution, and a value = 1 a random distribution. In order to take account of the effects of changing crane numbers between years on the index, we used a modified coefficient of dispersion (CD): CD = (V/) × 100/N_C, where , X is the number of cranes in each plot, is the mean number of cranes in each plot, N_C is the total number of cranes in the entire reserve, N_P is the total number of plots.

The mean number of each bird species recorded in the waterfowl lake over the winter was used as the measure of abundance. A two-tailed t-test was used to compare the difference in species richness and the total number of waterbirds, and the density of cranes in the area before and after construction of the waterfowl lake.

We used a significance level (α) of 0·05 for all statistical tests and reported the results as mean ± SD. Data were examined for normality and homogeneity assumptions with Kolmogorov–Smirnov and Levene's tests, respectively, and were logarithmically transformed (base 10) if needed. The proportion values were arcsin square-root-transformed to avoid skewed data. STATISTICA version 6·0 (Statsoft Inc. 2001) was used to analyze the data.

development projects in the reserve and its core zone

In 1982, none of the core, 15% of the buffer and 34% of the transition zone had been developed. Over the next 11 years the core zone remained undeveloped, while the buffer and transition zones experienced annual habitat losses of 1·5% and 0·6%, respectively (Fig. 2). Following introduction of the development plan in 1995, annual development rates in all three zones rose steeply, averaging 4·2%, 5·1%, and 4·5% per annum in the core, buffer, and transition zones respectively. By 2003, developments affected 42% of the core zone and approximately twice that percentage in the buffer (83%) and transition (85%) zones, where very little natural wetland remained. Overall, the percentage of natural wetlands in the entire reserve decreased from 69% in 1982 to 16% in 2003, an average decline of 11 800 ha per year (linear regression, r = 0·92, P < 0·001).

Surveys in 2000 indicated that approximately 2·5 × 10⁵ ha of intertidal marshes had been developed outside the core zone. About half of the developed area comprised artificial wetlands (e.g. aquacultural ponds, saltworks, reedbeds, zoobenthos fields), while the remaining area was dryland, including some residential and industrial areas in the transition zone (Fig. 3). In contrast, all of the developed area in the core comprised artificial wetlands. Although there were extensive artificial wetlands outside the core zone, there was much more human disturbance in these zones; the average population densities in the core, buffer and transition zones were 7·6, 120 and 570 persons per 100 ha respectively. Farmland dominated the transition zone by the year 2000, while aquacultural ponds and zoobenthos fields dominated the buffer zone. Only the core zone contained a significant proportion of intertidal habitats (Fig. 3).

As a consequence of the restrictions on development activities, the production values from activities within the core (1900–17 300 US$ per ha, depending on land-use patterns) were lower than those elsewhere in the reserve (2280–37 600 US$ per ha). However, the net income that could be obtained from development projects across the three zones was relatively similar (Table 1), because of the lower rent charged for land in the core zone (from one-tenth to half of what was charged outside, depending on the development activities).

number, distribution and habitat associations of red-crowned crane

Red-crowned crane increased from fewer than 400 in the early 1980s to a peak of 1128 individuals in 1999, an annual increase of 6·5%, before starting a decline that at the last count (2003) was 612 individuals (Fig. 4a,b). The core zone has supported an increasing proportion of the population (Fig. 4c,d) over the last two decades. The transition zone has, in contrast, supported a smaller percentage of the crane population such that it now supports only about 10% of the population (57 birds, 9% of total in 2003) in comparison with approximately 50% at the start of the study (177 birds, 49% of total in 1982). At the same time, crane density has shown a similar trend. With the redistribution of cranes, the density in the core zone reached a peak of 3·7 ± 0·5 individuals per km² from 1998 to 2001, a much higher density than that in both the buffer (0·5 ± 0·1 individuals per km²) and transition zones (0·02 ± 0·01 individuals per km²).

The coefficient of dispersion indicates that the cranes have consistently exhibited an aggregated distribution (CD > 1) in the reserve, but that the degree of aggregation has increased through time and especially since the mid-1990s when development began in the core zone (Fig. 5). Although crane numbers were relatively low in the early 1980s, the cranes occurred across most of the reserve. In the subsequent 20 years, the cranes aggregated and contracted initially into the centre and south of the reserve followed by further aggregation and contraction into the core zone (Fig. 6) where they used all of the different types of artificial wetland along with the natural wetlands. Hence, by 2001, 75% of the cranes recorded were in the core zone, which represents 4% of the total reserve area.

Regression analysis indicates that the proportion of cranes in the core zone relative to the total number of cranes in the reserve (C) was positively correlated with the proportion of developed land (D) (arcsin C^0·5 = 0·36 + 0·51 arcsin D^0·5, R² = 0·35, n = 22, P = 0·004), while the proportion of cranes in the buffer zone (B) increased with total crane numbers in the reserve (T) (arcsin B^0·5 = −0·77 + 0·45 log T, R² = 0·23, n = 22, P = 0·02). Both total crane numbers (T) and the proportion of developed land (D) were significant predictors of the change in proportion of crane numbers in the transition zone (TR) (arcsin TR^0·5 = 2·16 − 0·48 log T − 0·41 arcsin D^0·5, R² = 0·72, n = 22, P < 0·001) (Table 2, Fig. 7), the proportion of cranes declining with both.

In the 1980s, the major habitats used by cranes were natural wetlands (Fig. 8), including intertidal areas dominated by the plants Suaeda salsa and Aeluropus littoralis, where the cranes fed on snails, crabs, and other macro-invertebrates. The number of cranes using artificial wetlands (saltworks, aquacultural ponds and reedbeds) has increased since the mid 1990s. The first appearance of cranes on farmland (wheat and fallow paddy fields) was recorded in 1995. In recent years, farmland has become the major habitat of the cranes; surveys in 1999, 2000 and 2001 indicated that 37%, 38%, and 29% of cranes, respectively, foraged for food and especially grain in deserted paddies. Less than 30% of the cranes are now recorded in natural habitats.

waterbird community before and after the construction of waterfowl lake

Before construction of the waterfowl lake, a total of 16 waterbird species were recorded in the winter of 1992 in the area where the waterfowl lake was constructed in 1994. After construction, in the winter of 1996, 39 species were recorded, including all of the species observed before construction together with red-crowned crane and eight other threatened species (see Supplementary Material Appendix S2).

All waterbird species showed an increase in abundance, except for the black-crowned night heron Nycticorax nycticorax. Before construction, the waterbird species and abundance recorded per survey were 10·9 ± 1·7 and 1297 ± 265, respectively; these values increased respectively to 27·3 ± 3·2 (two-tailed t-test, t = 12·7, d.f. = 14, P < 0·001) and 46 950 ± 13 390 (two-tailed t-test, t = 9·6, d.f. = 14, P < 0·001) after construction. The waterfowl lake also became a major roosting site for the cranes. The density of cranes roosting in the area increased from 0·3 ± 0·1 individuals per ha before construction to 1·4 ± 0·7 per ha afterwards (two-tailed t-test, t = 4·6, d.f. = 14, P < 0·001), with the largest recorded number in the lake being 546.

red-crowned crane and land development

The number of wintering cranes in Yancheng Biosphere Reserve more than doubled from 1982 to 1999. This might be due to displacement of birds from other areas in China, where there has been a loss or degradation of wetlands (China Forestry Bureau et al. 2000). However, crane numbers have declined significantly (~50%) in recent years, which is a worrying trend.

Despite the increased number of cranes in Yancheng Biosphere Reserve, the transition zone supports a lower number and proportion of birds now than in the 1980s. This can be largely attributed to development activities and the loss of suitable wetland habitats. In the buffer zone, the changing proportions of crane numbers have been largely driven by the changes in the total number of birds visiting the reserve, while the extent of development has also impacted on the proportions of crane numbers in the core. It is unclear whether the positive correlation between the proportion of cranes in the core and development in the reserve relates to birds being driven out of the transition zone or other wintering grounds due to loss of habitats there, or to the birds being attracted into the core due to suitable development activities providing habitats in it. In addition, occasional artificial feeding might have also attracted the cranes into the core zone, resulting in artificially high crane numbers.

Although developments have occurred in the core zone since 1995, the density of cranes is still 10 times higher there than in the buffer, and 100 times higher than in the transition zone. All of the development projects in the core zone, and most in the buffer zone, have involved constructed artificial wetlands which retain some characteristics of natural wetlands, while much of the development in the transition zone has involved land reclamation, drainage and conversion to farming, woodland, and even industrial zones, which are unsuitable for cranes. Since the reserve has land ownership of the core zone, the wetland characteristics there have been developed and maintained to provide a range of natural and artificial habitats for the cranes. However, without land ownership outside the core zone, it is hard for the reserve to influence the decisions made by local government. With the changes from a planned to a market economy over the past two decades, land ownership in the buffer and transition zones has become very complicated with state, collective and private rights of use (Li et al. 2004). The emphasis on economic development has clearly resulted in substantial wetland loss and degradation outside the core zone with a substantial loss of cranes from the transition zone.

With so many changes occurring simultaneously, it is often difficult to disentangle the effects of various drivers on crane distribution and feeding. The decline in the area of natural wetlands and the increase in managed wetlands have seen an increase in the use of managed wetlands by the birds. It is not clear to what extent this reflects the loss of natural wetlands or the attractiveness of the artificial wetlands in terms of foraging. The recent use of farmland by cranes for feeding and the significant decline of crane numbers (~50%) over the last few years may indicate that there is now a lack of sufficient wetland habitats in the reserve to support the cranes. The increase in the number of waterbirds as a result of the creation of the artificial lake in the core may also have increased intra- and inter-species competition for resources.

The role of supplemental feeding in concentrating cranes within the core remains unclear. There are clear conservation benefits in the provision of additional food (Newton 1998) and a number of winter feeding programmes have benefited cranes temporarily, including the non-migratory red-crowned crane population in Hokkaido, Japan (Jones 2004). However, artificial feeding in Izumi has led to a massive concentration of hooded cranes in a small area, with significant conflicts with local farmers and major threats from disease outbreak. Furthermore, it is hard to disperse the flocks to other sites once cranes have become dependent on and accustomed to artificial feeding (BirdLife International 2001). Supplemental feeding of the cranes may also inadvertently be domesticating the birds or reducing their wariness of people. This is an important consideration for an endangered species. With about one-quarter of the total world population in the core zone of Yancheng Biosphere Reserve, the population is clearly much more at risk than when it was dispersed over a larger area.

waterbird communities and development activities

The value of artificial wetlands for conservation is a source of much debate (Elphick & Oring 1998; Malakoff 1998). In Yancheng Biosphere Reserve, the creation of the waterfowl lake has had a beneficial impact on waterbird diversity. The increase in the number of species and their abundance after construction of the lake most probably results from an increase in the quantity and diversity of food resources, the openness of the water surface providing protection (Froneman et al. 2001; Masero 2003), and differences in water depth allowing different foraging opportunities (Colwell & Taft 2000). It appears that the increased disturbance associated with the management of the lake does not negatively affect bird populations as disturbance may only temporarily affect the birds and does not prevent the exploitation of resources in the longer term (Gill, Sutherland & Watkinson 1996).

However, the considerable increase of waterbird species and numbers in a limited area may have increased both intra- and inter-specific competition. Moreover, while artificial lakes and other artificial wetlands can provide habitats for wintering waterbirds including red-crowned cranes, this should wherever possible not be at the expense of natural wetland ecosystems (Kaiser 2001). In Yancheng, the natural wetlands dominated by Suaeda salsa and Aeluropus littoralis are important nest sites for Saunders’ gull Larus saundersi, listed as vulnerable in IUCN's Red Data Book (BirdLife International 2001; Jiang, Chu & Hou 2002), Chinese water deer Hydropotes inermis depend on the natural saltmarsh wetlands year-round and the open mudflats are particularly important stopover habitats for migratory shorebirds (Ma et al. 2000). This implies that consideration needs to be given to a diverse array of wetland-dependent species for an integrated assessment of wetland quality in the reserve as a whole (Balcombe et al. 2005, Lougheed, Parker & Stevenson 2007). Unfortunately, there is a paucity of information on the effects of natural wetland loss on the majority of taxa in the reserve.

implications for the management of the reserve

The loss of natural wetlands, the collapse of the range of the cranes into the core of the reserve and the increased reliance of cranes on artificial wetlands all point to a loss of ecosystem integrity within Yancheng Biosphere Reserve. Increasingly, the reserve is taking on the characteristics of a highly managed wetland that will rely more and more on intensive management to maintain species diversity (Ausden & Treweek 1995; Smart et al. 2006). Yancheng Biosphere Reserve is not alone in this respect (China's National Committee on Man and Biosphere 2000). There is a need to halt the loss of natural wetlands and simultaneously restore natural wetlands in other zones to provide more available habitats for waterbirds, prioritizing ecosystem conservation and management (Grumbine 1994; Gray 2000). Otherwise, the transition zone will become completely dysfunctional from a conservation viewpoint. It is also essential to develop an evidence base for the impact of various development activities on the wetland ecosystem and biodiversity. This is currently lacking and would allow some of the more sympathetic methods of managing artificial wetlands that have been deployed in the core and buffer zones to be encouraged elsewhere in the transition zone and in the newly formed wetlands in the southern part of the reserve.

Zonation of the reserve and the lack of an overall ecosystem perspective for reserve management as a whole has led to a fragmented consideration of conservation and development, and contributed to the over-exploitation of the reserve. This highlights the issue of governance in the management of Biosphere Reserves (Heinen 1996; UNESCO 1996; Schneider & Burnett 2000) and the need for the reserve authorities, local government and communities to work more closely together to achieve the objectives of the Biosphere Reserve. With land ownership, local governments together with the local communities have placed too great an emphasis on development in the buffer and transition zones. The rapid development of the core has also obviously resulted in substantial part from a conflict of interest; the reserve authorities are supposed to protect the land but also need, and have the rights, to develop these same lands for the economic benefits of the reserve and its staff (China's National Committee on Man and Biosphere 2000). Clearly, if this conflict of interest is to be removed, the reserve needs adequate financing so that the core can be restored to its natural condition.

With 2 million people living in the transition zone and the loss of natural wetlands from the core zone, our study has highlighted the tensions and trade-offs in the management approaches of the reserve authorities and local governments. Given the rapid economic development in China over the last two decades and the evident pressure on biosphere reserves, we would argue that it is now time to re-examine the governance of Biosphere Reserves in China to better conserve ecosystem structure and functioning. We also argue, given the substantial changes in the transition zone, that it is now appropriate to reconsider zonation within the reserve, perhaps redefining and narrowing the transition zone (Li et al. 2004). This reduction should be coupled with an expansion of the core zone, taking advantage of the expanding intertidal area in the south of the reserve.