Implications of Rice Agriculture for Wild in Author(s) :Chris Wood, Yi Qiao, Peng Li, Ping Ding, Baozhong Lu and Yongmei Xi Source: Waterbirds, 33(sp1):30-43. 2010. Published By: The Waterbird Society DOI: 10.1675/063.033.s103 URL: http://www.bioone.org/doi/full/10.1675/063.033.s103

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Implications of Rice Agriculture for Wild Birds in China

CHRIS WOOD1,3, YI QIAO1, PENG LI1, PING DING1, BAOZHONG LU2 AND YONGMEI XI1,*

1College of Life Sciences, Zhejiang University, Zijingang Campus, 338 Yuhangtang Road, Hangzhou 310058, Zhejiang Province, P.R. China

2Shaanxi Hanzhong Crested Ibis National Nature Reserve, Shaanxi Province 723300, P.R. China

3Department of Biology, Faculty of Science, Kyushu University, 6-10-1 Hakozaki, Higashi-ku Fukuoka, 812-8581,

*Corresponding author; E-mail: [email protected]

Abstract.—Data on wild birds in rice fields in China are scarce. The potential significance of Chinese rice fields, which represent about 6% of the world’s area, is considerable but whether this potential is met is largely unknown. In this review, traditional and modern Chinese rice agriculture are compared, including detailing histor- ical changes and their implications for wild birds. Traditional practices, with one crop each year and long periods of fallow flooding, provide greater benefit to biodiversity and such as the Crested Ibis (Nipponia nippon). The method and alternatives, such as rice-, duck-rice and swidden agriculture, are contrasted with modern tech- niques which, through associated water regimes and chemical use, have been implicated in the decline of biodiver- sity and of species such as the Black-faced Spoonbill (Platalea minor). Agrochemical use is particularly pertinent because China is likely to have been the world’s largest pesticide consumer since the mid-1990s, with use greatest in rice (Oryza sativa). However, few studies have measured the direct effects of agro-chemicals on wild birds in Chi- na. The most detailed information on birds in China’s rice fields comes from charismatic species such as the Crest- ed Ibis and Red-crowned Crane (Grus japonensis). Preliminary data from possibly the first systematic survey of a Chinese rural county are presented. More detailed and widespread studies of the implications of rice agriculture to wild birds in China are required. Received 19 August 2008, accepted 16 July 2009. Key words.—agriculture, agrochemical, pesticides, rice fields, . Waterbirds 33 (Special Publication 1): 30-43, 2010

By 2000, rice (Oryza sativa), the world’s nese rice fields constitute approximately 6% most widely cultivated crop, covered 1.55 of the world’s total wetland area. million km2, over 11% of the world’s arable Of the 57 species of endangered birds in land, and over 1% of the Earth’s land surface , 31 (54%) have been found in China’s (Donald 2004). Two rice-producing coun- . Similarly, 50 (30%) of the 166 spe- tries, China and , together produced cies of geese and ducks in the world, and more than half of the global output, and nine of the world’s 15 crane species have since the 1970s China has accounted for been recorded in China’s wetlands (State nearly one-fourth of the total rice-sown area Environmental Protection Administration and more than one-third of total rice pro- 2006). Information regarding bird use of duction in the world (State Environmental rice fields specifically, rather than wetlands Protection Administration 2003a). In 2006, in general, however, remains scarce. None- Chinese rice fields also represented nearly theless, studies from elsewhere in the world 20% of the global land area used for plant- suggest that Chinese ricelands have poten- ing rice (Lu and Li 2006). tial conservation value (Fasola and Ruiz As of 2003, there were 659,400 km2 of 1996; Eadie et al. 2008), and that loss of rice wetland (excluding rivers and ponds) in Chi- habitat and intensification of agricultural na, accounting for 10% of the world’s total practices are of concern. (State Environmental Protection Adminis- tration 2003b). The total included 259,400 RICELANDS IN CHINA km2 of natural wetland (including marsh swamps, natural lakes, tidal beaches and Chinese government statistics revealed a shallow sea areas), 380,000 km2 of rice fields loss of over 25,000 km2 of farmland in 2003 and 20,000 km2 of reservoirs. Overall, Chi- alone. Losses came primarily through con-

30 BIRDS IN CHINA’S RICE FIELDS 31 version to other uses under the banner of hold-based farming instigated a major ecological conservation (State Environmen- change in the nature of China’s grain pro- tal Protection Administration 2003b). Most duction. This shift brought China in line of this land (>21,000 km2) was converted to with the rest of the world where, despite ur- forest, with other areas converted to grass- banization and industrialization, more than land or lakes. During the same period, a pol- half of the world’s people still live as subsis- icy to offset losses resulted in gains of about tence or small scale farmers (Donald 2004). 3,100 km2 of farmland. Despite the potential In China, following this policy change, for conservation benefits from these chang- resource use decisions have been largely es, there was a clear net loss of flooded rice transferred to individual households. How field habitat. By 2006, the rate of habitat con- households have responded, and how poli- version had slowed but net losses continued cies can be shaped to encourage sustainable (State Environmental Protection Adminis- resource use, remain key questions (Heerink tration 2006). et al. 2006). Tax cuts, income subsidy and Conversion to rice is often considered a price changes all influence farmers’ choices major cause of the loss of natural wetlands about methods of rice production, and the (Donald 2004). In China, 2003 statistics sug- transfer of land and resources to alternative gest that significant areas of wetlands may uses. In turn, these factors impact the quality have been claimed for conversion to agricul- and quantity of rice land available as bird tural fields (State Environmental Protection habitat. Specific policies have included at- Administration 2006), but specific informa- tempts since 1994 to shift production from tion on the exact nature of these transforma- other crops to grain; maintaining domestic tions is lacking. In particular, there are limit- fertilizer prices below world market prices; ed data on the nature of the pre-existing wet- abolishing agricultural taxes; and direct in- lands or other areas that have been convert- come subsidies to farmers with grain crops, ed to rice, the nature and relative amounts of including rice (Lin and Zhang 1998; Heer- different forms of rice agriculture that are ink et al. 2006). In Jiangxi Province, one of used on converted land, and the impacts on China’s main grain producing areas, such use of these areas by birds and other species. measures produced rapid increases in rice Agricultural intensification is occurring prices coupled with much lower increases in in China. Conversion of wetlands to modern fertilizer prices, causing increased fertilizer agricultural fields results in habitat simplifi- use and conversion of land from other crops cation to favor the rice crop, creating a far to rice. In more prosperous provinces, these from optimal situation for many species and policy changes have caused larger areas with ecosystem functions. In China, as elsewhere, two rice crops per year, at the expense of the intensive modern farming contrasts directly more ecologically beneficial single-crop sys- with the traditional agricultural systems that tem (NBS 2004; Heerink et al. 2006). nevertheless persist in some areas. Overall, the major changes brought by Historically, rice production in China in- modern rice production, include more irri- volved one crop per year followed by a long gation, artificial soil enrichment, increased fallow period when fields were flooded, pro- chemical use, and multiple cropping cycles, viding ideal feeding habitat, particularly for usually resulting in decreased feeding and wading birds. Native vegetation recovered breeding opportunities for birds as fields are during such fallow periods, particularly in no longer left fallow and the periods when field margins, and birds were able to breed native vegetation can recover are drastically in overgrown areas. Many birds benefited reduced (Fanslow 2006). from this system, including the Crested Ibis While large numbers of birds can be (Nipponia nippon). Modernization and inten- found in modern rice fields, species are not sification, however, began to change this nearly as abundant as in undisturbed wet- model, particularly in the 1970s when a poli- lands. Some species do occupy an ecological cy shift from collective farming to house- niche that is realized in the modern rice sys- 32 WATERBIRDS

tem, and some do extremely well. Thus, the widespread use, prior to its ban in many modern rice fields may provide excellent countries, of the pesticide DDT. The use of feeding habitat for certain species including this organochlorine pesticide for three de- many seasonal migrants, but for resident spe- cades led to it being labeled as “the most cies breeding opportunities are limited and widespread and pernicious of all global pol- restricted to field margins; almost no birds lutants” (Cox 1991: 2). DDT killed many actually breed in modern rice fields birds through outright toxicity, resulted in (Fanslow 2006). the thinning of eggshells, and has been im- plicated as a primary cause of the decline for AGROCHEMICAL USE numerous endangered species (e.g. Safford and Jones 1997; Elphick et al. 2007). For ex- The impact of agrochemical use on birds ample, DDT may have played a role in the can be highly significant (Parsons et al. decline of the endangered Black-faced 2010). In China, pesticide production in- Spoonbill (Platalea minor) in China. A demo- creased from about 1,000 t in 1950 to a high graphic analysis showed that the scale of of 537,000 t in 1980 (Huang et al. 2003). population reduction and the timing and More than three-quarters of all pesticides pattern of recovery correspond clearly with produced in China in the 1980s were insecti- the use and subsequent ban of DDT (Yeung cides. Fungicides accounted for approxi- et al. 2006). Though no such study has yet mately 10%, and herbicides 6-7%. Since the been carried out for the Crested Ibis, it is no- mid-1980s, methamidophos, dimthypo, and table that they often feed with spoonbills in parathionmethyl have been gradually replac- rice fields and also suffered a major decline ing dichlorodiphenyltrichloroethane (DDT), in China over a similar period. Similar situa- benzene hexachloride (BHC), dichlorvos tions have been found for charismatic spe- and dimethoate as the dominant insecticides. cies in other countries (e.g. Poole 1989; Herbicide production increased more than Newton and Wyllie 1992), suggesting the four-fold between 1985 and 1996, a factor possibility of much broader and more wide- linked to rising labor costs. Following the spread impacts. high of 1980 there was a seven-year decline in pesticide use, but use doubled again be- Beyond DDT tween 1987 and 1995. By 1996, the total pes- ticide supply reached 339,600 t (Huang et al. After the 1972 DDT ban, agrochemical 2003). use has not ceased to be of concern. Other Overall, China is likely to have been the organochlorine insecticides are still being largest pesticide consumer in the world since used and are known to have detrimental ef- the mid-1990s, with rice having the greatest fects on avian species (Cox 1991; Parsons et use and the greatest increase in use of all al. 2010). Notable studies in China include crops (Huang et al. 2003). Average applica- the use of waterbirds as potential bioindica- tion rates amounted to 27.7 kg/ha (12-14 kg tors of such chemical impacts. of active ingredients), similar to that in Ja- Dong et al. (2004) studied organochlo- pan (14.3 kg of active ingredients) and the rine compounds in the of Black- Republic of Korea (10.70 kg), but much crowned Night (Nycticorax nyctico- higher than other Asian countries (Barker rax), Little Egrets (Egretta garzetta), Eastern and Herdt 1985). Such use has been consid- Cattle Egrets (Bubulcus coromandus) and Chi- ered to be excessive and unnecessary (Hua- nese Pond Herons (Ardeola bacchus) from Tai ng et al. 2003). Lake on the border between Jiangsu and Zhejiang Provinces. This location was ex- Impacts of DDT pected to be subject to serious pesticide and heavy metal pollution from both agriculture Perhaps the best known and most serious and industry, with most agricultural inputs example of agrochemical impact on birds is thought to come from rice fields. The DDT BIRDS IN CHINA’S RICE FIELDS 33 derivative, DDE, was found at a higher level land region of Jiangsu Province. In that area, in these eggs than in many other studies the loss of natural wetlands and the conse- worldwide, including those from Italy (Faso- quent increasing use of farmland and rice la et al. 1998), Romania (Aurigi et al. 2000) fields by cranes has led to the implication of and most studies from the USA (Frank et al. agrochemicals in multiple cases of poison- 2001; Rattner et al. 2000, 2001); even higher ing. The paper suggests an average of nearly values have been found in some USA studies ten cases a year since the early 1990s, but (Custer and Custer 1995; Hothem et al. provides no further details. In the same area, 1995). The DDE burdens in Tai Lake, howev- Wang (1995) points to deliberate poisoning er, were much lower than those thought to of cranes by duck hunters. have significant adverse effects on reproduc- tive success in adult Black-crowned Night TRADITIONAL AGRICULTURAL PRACTICES Herons (8 μg/g wet weight; Henny et al. 1984; Ohlendorf and Marois 1990). Never- In China, as elsewhere, many areas of theless, DDE concentrations in over half the natural wetlands have been replaced by rice Black-crowned Night eggs sampled, production resulting in waterbird popula- 14% of Little Egret eggs, and 12% of Chi- tions becoming increasingly dependent on nese eggs were above the criti- rice agriculture for their survival (Donald cal threshold level of 1 μg/g (wet weight) es- 2004). Traditional rice agriculture takes sev- tablished by Connell et al. (2003), indicating eral forms and is usually considered to sup- that chick survival could be adversely affect- port more biodiversity than modern inten- ed (Dong et al. 2004). Cyclodiene pesticides, sive systems, although little data exists. Tradi- compounds which include the most toxic or- tionally-farmed paddies contain a variety of ganochlorine insecticides especially in terms aquatic species, including many plants, fish, of acute poisoning, are not used as frequent- mollusks and that in many cases ly in China as in Europe and the USA. Bur- are harvested in conjunction with rice. dens of hexachlorocyclohexane (HCH) at Tai Lake were generally higher, and those of Rice-Fish Systems cyclodienes generally lower, than those found elsewhere (Dong et al. 2004). A key alternative to intensive rice agricul- Zhang et al. (2006) compared Little Egret ture is the traditional rice-fish farming mod- samples from the relatively unpolluted biodi- el, in which the presence of fish and other versity hotspot of Poyang Lake in Jiangxi aquatic fauna in flooded fields helps to con- Province, which provides habitat for half a trol rice pests and decreases the need for million migratory birds, with samples from pesticide use. Such organisms also aid in nu- Tai Lake and the Pearl River Delta (an area trient cycling, decreasing the need for fertil- covering nine prefectures including Guan- izer application and producing a more sus- dong, and Maccau), each of tainable system conducive to the recovery of which are hotspots of pollution in central soil fertility and the prevention of soil degra- China. Eggs, body feathers from chicks, prey dation (Halwart and Gupta 2004). In some regurgitated by chicks and sediments at the places, the aquatic fern Azolla is added to the areas most used by foraging egrets were col- agricultural mix (Lu and Li 2006). This float- lected and analyzed. Contrary to expecta- ing pteridophyte has symbiotic nitrogen-fix- tions, for each of these areas the concentra- ing cyanobacteria, and can be turned into tions of the various elements examined were the paddy soils as green manure or harvested below the threshold at which survival or re- as feed for pig, chickens, ducks or fish. production effects on the birds are consid- Integrated rice-fish production systems ered likely (Zhang et al. 2006). have been used in China for 1700 years, and Zuo et al. (2004) also mention a more di- have been listed by the United Nations Food rect case of poisoning for the Red-crowned and Agriculture Organization and the Unit- Crane (Grus japonensis) in the Yancheng wet- ed Nations Educational, Scientific and Cul- 34 WATERBIRDS

tural Organization as a Globally Important insignificant (Wang and Lei 2000; Yang and Ingenious Agricultural Heritage System. The Lu 2001; Lu and Li 2006). A complete ac- total area of rice-fish farming in China is the counting of the economic and environmen- highest in the world, having peaked at about tal value of the two systems is, however, need- 15,000 km2 in 2000. Of 200,000 km2 of rice ed. agriculture in China, nearly 70,000 km2 are considered suitable for rice-fish farming Other Traditional Systems (Zhang et al. 2001; Lu and Li 2006). The structural changes required for such The small rural villages of Daka and Ba- a system are thought to benefit bird life. The ka, in Xishuang-banna, southwest China horizontal field structure is changed into a have been heralded as providing important ridge-ditch pattern, and the application of examples of swidden agriculture (Guo et al. fertilizer and pesticides is reduced. The 2002; Fu et al. 2005; Padoch et al. 2007). Swid- number of species in fields with these condi- den, with its cyclical agricultural system tions is greater than in most other rice sys- whereby fields are abandoned and left to re- tems. Organisms benefiting from this system cover for a period, allows the regeneration of include weedy plants, plankton, various habitat in fields and field margins that is like- types of bacteria, aquatic , water mice, ly to benefit birdlife more than would con- water snakes and potentially birds (Lu et al. tinuous cropping. Again, impacts to birdlife 2001). Natural enemies of rice pests, such as are not known, but a change from swidden spiders and parasitic wasps, also increase to other agricultural systems has been associ- considerably (Lu and Li 2006). To date, such ated with a loss of biodiversity (Padoch et al. studies have made some attempt to examine 2007). fish biodiversity and other aquatic species, Tending ducks in rice paddies is another but detailed studies of the effects on birds traditional practice in some southern prov- are not available. inces of China (Li et al. 2009; Muzaffar et al. Research in Fujian Province, southeast 2010). Young ducks are placed in the fields China (Chen 1990) and Qingtian County, at the rice tilling stage, and kept there day Zhejiang Province, eastern China (Lu and Li and night for about two months. Before the 2006) have found high yields of fish and rice, rice matures, ducks are removed from the and the need for only small amounts of pes- fields and sold at market. While in the fields, ticide and fertilizer. In some cases, no pesti- ducks eat insects and weeds, thus reducing cide application was required because natu- the need for insecticides and herbicides. ral enemies of rice pests were abundant, thus The economic value of duck-rice systems is making biocontrol of rice diseases and pests estimated as 30% greater than that from rice feasible. Instead of depleting soil nutrients, monoculture (Wen et al. 1992), providing a nitrogen-fixation increased the amount of strong incentive to use this method. Again organic matter, total nitrogen, and total no detailed studies of the effects on wild bird phosphorus in the soil, and reduced meth- species have been conducted and indeed ane emissions when compared with most one Japanese farmer’s report suggests that rice farming systems (Chen 1990; Wen et al. the presence of ducks seems to deter herons, 1992; Lu and Li 2006). How birds respond in egrets and other “fish predators” from enter- these areas, however, has not been docu- ing his paddy fields (Furuno 2001). mented. The presence of fallow fields and longer Due to agricultural intensification the ar- flooding periods are common aspects of tra- ea of rice-fish habitat in China is declining by ditional farming methods. One preliminary about 300 km2 annually (Lu and Li 2006). study of three rice field areas in Pakistan and Several studies have demonstrated that rice- two in China (Tai and Poyang), found that fish systems either produce more rice than herons and egrets used fields as their main does rice monoculture, or that they produce foraging habitat at the two sites that had more fish where the rise in rice production is been flooded for over 20 d, but used fields BIRDS IN CHINA’S RICE FIELDS 35 much less at the three sites that had been The survival of the last few birds in a re- flooded for less than 10 d (M. Fasola, unpub- mote area of the Hanzhong Basin in Shaanxi lished data). This result suggests that the du- Province, central China, has been linked to ration of flooding matters to waterbirds (see the more traditional and less intensive agri- also Elphick et al. 2010); further study of this cultural practices used there. The basin is issue is to be encouraged. characterized by broad rice fields and areas of drier farmland, combined with a complex network of small handmade reservoirs and FOCAL SPECIES rivers. Seasonally flooded grasslands and di- verse forests help provide a good mix of Crested Ibis feeding, nesting and roosting habitats. On the rediscovery of the ibis in this region, con- Perhaps the best candidate for a species servation teams moved in, decreasing pesti- to promote sustainable rice-agriculture in cide use in rice fields in breeding areas, pro- east Asia is the Crested Ibis. This bird was viding food supplements in regular feeding once abundant throughout Japan, China, areas and protecting key trees for nesting Korea and , but by 1981 only 13 indi- (Lu 1989). Little by little, the population be- viduals were known to remain (seven in the gan to increase. In the last decade, the wild in China, six in captivity in Japan). A breeding, nesting, feeding and roosting ar- quarter of a century later, the original cap- eas have been enlarged and expanded be- tive population had died out, but the wild yond the initial nature reserve boundaries, population had risen to approximately 600 and approximately 600 birds are now regu- individuals, with a similar number in captivi- larly seen across a 100 km spread of eight ty, and the ibis has thus become one of Chi- counties of the Hanzhong region. na’s major conservation success stories. The As with the decline, population recov- ibis was once abundant in rice fields and may ery has been closely related to rice farming, serve, in both its historic decline and subse- with local residents using fewer pesticides quent partial recovery in rural central China, and fertilizers than in the past and almost as an indicator of environmental change. never poaching Crested Ibises. In addition, Typical habitat has been described as a farmers have reverted to the production of mix of forest, wetland and rice paddies (Liu a single rice crop and now keep some pad- 1981; Wang et al. 1985; Li et al. 2006). Histor- dies filled with water year-round to con- ically, most of China provided ideal ibis hab- serve aquatic for foraging ibises (Li itat. Wetlands were full of Asian Pond Loach et al. 2002). Earlier suggestions that ibises (Misgurnus anguillicaudatus), which together are prone to human disturbance have not with worms and insects comprised the main been confirmed. Since ibises primarily feed prey for the ibis. Shrimps and crabs were also in rice fields, their occurrence is often available in streams and rivers. Fallow rice greatest in areas where people live and fields provided ideal winter feeding farm (Ma et al. 2000) and nest-sites are usu- grounds, and a further source of loach, ally located near paddy fields (Yu et al. worms and insects. By the 1930s, the species 2006). In general it seems that Crested Ibis- was still abundant in 14 provinces, including es select sites with moderate human activity and Island, but agricultural at the landscape level (i.e. rice paddies), intensification reduced the area of fallow but low activity at the nest site level. In re- fields in subsequent decades. Probable caus- cent years, however, some Crested Ibises es of the population decline include logging have even selected nest trees within farm- of mature trees used for nesting, draining of ers’ yards (Li et al. 2002). Away from nest- rice paddies in winter, widespread use of fer- ing sites, Crested Ibises are sometimes at- tilizers and other agrochemicals, hunting, tracted by farming activities; for instance, reduction of food supply, and industrial pol- they will follow plowing cows to feed on ex- lution (Shi et al. 1991 in Yu et al. 2006). posed worms (Li et al. 2006). 36 WATERBIRDS

In the recovering wild population, winter crop rice, where fields are left fallow and feeding sites include paddy fields, river flooded over winter, the maintenance of shoals, and reservoirs, with paddy fields be- other alternative traditional rice methods ing the main feeding sites for adults and riv- such as rice-fish and duck-rice systems and er shoals for juveniles (Ma et al. 2001). Rice the setting aside of natural wetland areas, paddies are also the major feeding sites of may also be effective measures to counter Crested Ibises during the late pre-breeding food shortages. and breeding season. Post-breeding, howev- As the Chinese government has begun er, rice paddies were unsuitable because the promoting the strategy of “harmonizing peo- rice was too dense and tall, a pattern seen ple and nature”, with a particular focus on with other waterbird species elsewhere (Pier- sustainable agriculture, there is a renewed luissi 2010). Near the end of the post-breed- focus on reintroducing the ibis into areas of ing season and at the beginning of the pre- its former range. Areas of the Demilitarized breeding season, cropland was usually rotat- Zone in Korea and other potential sites in Ja- ed to Oilseed Rape (Brassica napus), which pan and China are all under consideration. was also seldom used by ibises. China has already translocated ibises to one Seasonal movements of ibises seem to be new area and breeding has been confirmed related to the availability of rice field habitat, there. Both Korea and Japan have also main- particularly in the absence of other wetland tained a strong desire to reestablish wild habitats. In the early period of recovery in populations (Fujioka et al. 2010). In Septem- the early 1980s, ibises tended to retreat to ber 2008, ten wild ibises were released on Sa- mountainous regions in the breeding sea- do Island, Japan, becoming the first ibis to fly son. In such regions, rice paddies are the free in Japan since 1981. They immediately only wetland areas that attract ibises and it is began to feed in rice fields and now four clear that they provide the majority of their have flown over to mainland Japan, four re- food (Li et al. 2002). main on Sado Island, one is confirmed dead Food shortages have been reported sug- and the location of one is currently un- gesting that ibises are failing to find suffi- known. Simultaneously, China and Korea cient food throughout their range. During have instigated efforts for a Korean captive the 20 years since restoration began, hun- breeding effort. dreds of kg of loach have been purchased every spring and put into rice fields as sup- Other Focal Birds plemental food to help breeding ibises raise their chicks. In winters, deliberate re-flood- The Yancheng Nature Reserve in Jiangsu ing of the dried rice fields is attempted to province is China’s largest coastal wetland maintain a suitable feeding environment. reserve. About 3 million birds of 200 species, Nevertheless the expanding population still 29 of which are on the IUCN Red List of has to face food shortages, a problem often Threatened Species, migrate through the associated with pesticide and chemical use site annually. Much of the reserve’s natural and further exacerbated by the dramatic habitat, which originally consisted of inter- decrease of invertebrates in rice fields dur- tidal mudflats, creeks, salt marshes and reed ing dryer years (Xi et al. 1997; Y. Xi, person- beds, has been enclosed by sea dykes and al observation). Dissections of birds found converted to other uses. Agriculture or dead in the wild have shown that 80% had aquaculture has replaced large areas of the very little food in their stomachs, and starva- original wetlands and agricultural, urban tion and malnutrition could indeed be a and industrial development continues. Pol- significant cause of chick mortality (Zhang lution from local and upstream sources has et al. 2000). This issue highlights the con- caused declining water quality and flow and tinuing need to decrease pesticide and oth- altered sedimentation patterns. Measures to er chemical use that would limit feeding op- address many of these issues are underway tions for ibises. Areas set aside for single- (ADB Project 2007). BIRDS IN CHINA’S RICE FIELDS 37

In this area, rice fields provide feeding and egrets than previously estimated for habitat for many migrant birds, such as China. Specifically large numbers of Little cranes and storks. Many of the Red-crowned Egrets, Intermediate Egrets (Egretta inter- Cranes that breed in China migrate along media), Eastern Great Egrets (Ardea modes- the coast of the Bo and Yellow Seas to winter- ta), Eastern Cattle Egrets, Chinese Pond ing grounds in Jiangsu using coastal salt Herons and Black-crowned Night Herons, marshes, rivers, freshwater marshes, rice were observed. paddies and cultivated fields (Swengel 2006). Rice fields in particular offer a mosaic ZHEJIANG PROVINCE SURVEY of habitats with irrigation channels, ditches and levees harboring a diverse and rich fau- The paucity of systematic knowledge na and flora. Every year, about 1,000 Red- about Chinese birdlife in general, and par- crowned Cranes, representing 60% of the ticularly about the birds of rural environ- world total, along with Common (Grus grus) ments, is a major limitation of the current re- and White-naped Cranes (Grus vipio) mi- view. Most existing knowledge comes from a grate from the north of China and Russia few key reserves, hotspot areas or charismat- and winter along the Yancheng coast. Over ic species. In 2006-2007, however, we com- the last ten years, however, Red-crowned pleted what we believe to be the first system- Cranes have lost nearly 60% of their natural atic bird survey of an entire county in China. habitat. As a result, an increasing reliance on The survey took place in Lin’an County, Zhe- farmlands and artificial fishponds for food jiang Province, which is a major agricultural and water, particularly in fallow winter areas, region of eastern China, and focused on the has been observed (Zuo et al. 2004). presence and absence of species. Detailed Li et al. (2002) studied the feeding habits habitat data were not collected, and only a of Little Egrets, Black-crowned Night Her- minority of records were specifically linked ons, Chinese Pond Herons and Eastern Cat- to rice fields. Nonetheless, many records tle Egrets around Taihu Lake, Jiangsu Prov- were from agricultural areas, in which rice ince. The egrets sought prey mainly in fish fields were common. ponds and lakes, and less in rice fields. Only Lin’an County lies to the west of Hang- Chinese Pond Herons were recorded to feed zhou, the capital of Zhejiang Province in rice fields and even this species used rice (Fig. 1) and is roughly 30 km from north to fields only 6% of the time. These investiga- tions, however, were done in early June when field irrigation had only just began and may, therefore, underestimate use, which increas- es in fields that have been flooded for longer periods (M. Fasola, unpublished data). Ori- ental Storks (Ciconia boyciana) breeding in Anhui Province have also been reported to feed mainly in paddy fields and ponds (Hou et al. 2007). A census of the heronries in several ar- eas of eastern China (Fasola et al. 2004), concluded that herons were extremely abundant where rivers, fishponds, rice paddies and other water bodies provide foraging habitat. The censuses in these ar- eas, which are representative of much of central and southeast China, with rice Figure 1. Study area surveyed in Lin’an County, Zhejiang Province. Solid lines represent transects surveyed; dashed fields are a dominant land cover, suggested lines those that could not be accessed. Major towns (cir- much higher numbers of breeding herons cles), rivers, and the capital Lin’an City are shown. 38 WATERBIRDS

south and almost 100 km wide (29°56’N to the transect route. Species abundances were 30°23’N, 119°52’E to 118°51’E). Elevation recorded for each transect, together with da- ranges from 1,787 m on Qing Liang Moun- ta on altitude, weather, brief information on tain to 9 m and tends to be higher to the habitat and any sources of disturbance. For northwest (>1000 m, on average in the west- this paper, transects were categorized as ern region), and slope towards the south- “High Rice” when at least 50% of records list- east (50 m, on average in the eastern re- ed “rice” in the habitat description; “Some gion). The county has an area of 3,127 km2, Rice”, when less rice was present; “High Ag- over 70% of which is forested. Of the 191 riculture” when agricultural terms were list- km2 of cultivated land, 169 km2 contains ir- ed for at least 50% of records; “Some Agri- rigated fields most of which are predomi- culture” when less agricultural was present; nantly rice, with some fields that include and “No Agriculture” when there was no ref- rice as part of a wider mosaic agricultural erence to rice or agriculture (Fig. 2). Avian mix. Lin’an has a subtropical monsoon cli- species richness was calculated for each mate with high rainfall in spring, hot and transect. wet summers, cool autumns and dry, cold Overall, nearly 18,000 birds of at least winters. 170 species were observed. At least 98 spe- Surveys were conducted by scientists cies were noted in the October survey, 154 from Zhejiang University, together with rep- in the May survey and 52 in the August sur- resentatives from the Hong Kong Bird vey. Species richness was generally lower in Watching Society and other zoological insti- High Rice than in the other habitat catego- tutions, predominantly from the USA. One ries (Table 1), but varied considerably hundred and six 3-km east/west transects among transects both within and among were evenly-spaced across the county, with a habitat types (Fig. 2). A total of 59 species 4-km gap between transects in all directions were associated with rice habitats, al- (Fig. 1). Seven additional transects were though few were directly linked with High placed in urban areas and three in areas of Rice areas (Table 2). Of those species asso- particular interest (e.g. around lake margins ciated with High Rice, only Black-crowned or across low lying floodlands). Twelve Night Heron was noted to have a high like- transects were not covered because they lay lihood of rice dependency. The others— in inaccessible or restricted areas, leaving a Greater Spotted Eagle (Aquila clanga), un- total of 104 transects. identified sp., House Swift (Apus For each transect, the starting point was located using a GPS unit (Garmin ETrex), and a 3-km trail was slowly walked in the ap- proximate direction, along an available route, until the end point was reached, again determined by GPS. Where no suitable route continued in the direction of the end point, the transect was terminated prematurely. Each survey group covered one transect in the early morning and one in the late after- noon. Data were gathered from 2-8 October 2006 for autumn migrants and early-arriving winter visitors, from 7-13 May 2007 to coin- Figure 2. Lin’an County, Zhejiang Province, showing ar- eas of rice agriculture (medium gray background; solid cide with late spring, when most summer vis- lines indicate “High Rice”, dashed lines “Some Rice”), itors had arrived and breeding begun, and other agriculture (white background; solid lines indicate from 29 August-1 September 2007 to fill in “High Agriculture”, dashed lines “Some Agriculture”), and “No Agriculture” (black). Areas not covered are previously unsurveyed transects. white with no lines. Circles show locations of surveyed The primary data were all bird species transects, with circle size proportional to the number of seen or heard within approximately 100 m of bird species detected. BIRDS IN CHINA’S RICE FIELDS 39

Table 1. Number of bird species found in each habitat category and season during surveys in Lin’an County, Zhe- jiang Province. See text for habitat definitions.

High Rice Some Rice High Agriculture Some Agriculture No Agriculture

All Seasons 5 54 109 71 108 2-8 Oct 2006 5 36 22 42 46 7-13 May 2007 2 39 57 60 66 29 Aug-1 Sept 2007 1 12 47 2 6

nipalensis), Lanceolated Warbler (Locustel- CONCLUSIONS la lanceolata) and Common Reed (Emberiza schoeniclus)—all range over a va- Data on bird use of rice fields in China riety of habitats. is scarce and the need for more intensive The data summarized here clearly pro- and widespread studies cannot be overstat- vide only a foundation for more detailed ed. The potential significance of Chinese study. This survey was not designed to study rice fields, which represent about 6% of use of rice fields and detailed habitat infor- the world’s wetland area, is considerable mation was not systematically collected. Rice but whether this potential is met is un- was frequently part of the agricultural mix known. The contrast between traditional and often the dominant crop around and modern rice agriculture is particularly transects (C. Wood, personal observation). important. Traditional practice, with one Many areas identified as High Agriculture crop each year and long periods of fallow may have contained substantial amounts of flooding, may be of considerable benefit to rice. Likewise, the activity or location of birds biodiversity generally and to species of with respect to rice fields was not directly high conservation interest (e.g. Crested sampled. Ibis). In contrast, modern intensive farm- There are notable absences from the ing, with double-cropping, associated wa- list of species associated with rice and the ter regimes and greater chemical use, are list must be considered preliminary. Brown implicated in the decline of biodiversity Bush-hens (Amaurornis akool) and White- and of certain species (e.g. Black-faced breasted Waterhens (Amaurornis phoenicu- Spoonbill). Where traditional and alterna- rus) are typical of wet agricultural areas in tive techniques such as rice-fish agriculture southern China, as are a range of ardeids, have continued to be used, species such as including Chinese Pond Heron, Little the Crested Ibis and Red-crowned Crane Egret and Eastern Cattle Egret. Also, Eur- have apparently benefited. We hope that asian Tree Sparrow (Passer montanus) and this paper becomes a springboard for Scaly-breasted Mannikin (Lonchura punctu- more studies of birds and biodiversity in lata) were not listed in this category, nor rice fields in China and, more generally, are Yellow (Ixobrychus sinensis), Cinnamon that it will promote the further integration (Ixobrychus cinnamomeus) or Black Bittern of Chinese agricultural development and (Dupetor flavicollis), which are typically governmental policy with biodiversity con- found in rice fields in this region. Clearly, servation. further work, focusing specifically on hab- itat use and with the addition of winter sur- ACKNOWLEDGMENTS veys, is necessary. During the winter The work was supported by funding from Toyota months, rice fields elsewhere in China are Foundation to Xi (D07-N-144). We thank the editors for used by a range of species, including ar- comments; M. Kilburn of the Hong Kong Bird Watch- deids, ducks, larks, pipits, wagtails and ing Society for extremely valuable support in both the Lin’an survey and manuscript preparation; Professor buntings, and may also provide winter for- Yahara of Kyushu University for logistical and practical aging for starlings and mynas. support; and all the Lin’an survey volunteers. 40 WATERBIRDS icates that a species was detected on transect in than half the records on a transect. than half the records Chinese Bamboo PartridgeBlack-crowned Night HeronChinese Pond HeronEastern Cattle EgretEastern Great EgretLittle Egret X Chinese SparrowhawkGreater Spotted EagleWhite-breasted WaterhenCommon Snipe DoveOriental Turtle X Spotted DoveAsian Barred Owlet X House Swift X Oriental Dollarbird X Common Kingfisher X Brown Shrike X Long-tailed ShrikeBlack Drongo X Red-billed Blue Magpie X Great TitCollared FinchbillLight-vented X X X Red-rumped SwallowManchurian Bush WarblerBrownish-flanked Bush Warbler X Rufous-faced Warbler X Black-throated BushtitDusky Warbler X Arctic Warbler X X X X X X X X X X X X X X X Bambusicola thoracicus Nycticorax nycticorax bacchus Ardeola Bubulcus coromandus modesta Egretta garzettaEgretta Accipiter soloensis Aquila clanga phoenicurusAmaurornis Gallinago gallinago orientalis Streptopelia chinensis Streptopelia Glaucidium cuculoides Apus nipalensis orientalis Alcedo atthis Lanius cristatus Lanius schach Dicrurus macrocercus erythrorhynchaUrocissa Parus major Spizixos semitorques Pycnonotus sinensis daurica Cecropis Cettia canturians Cettia fortipes albogularis Abroscopus Aegithalos concinnus Phylloscopus fuscatus Phylloscopus borealis Alcedinidae Dicruridae Corvidae Paridae Pycnonotidae Hirundinidae Cettidae Aegithalidae Phylloscopidae Table 2. Birds detected on transects containing rice habitats during surveys High Rice ind Birds Zhejiang Province. 2. in Lin’an County, Table associated with rice; Some Rice indicates that rice was present, were but associated with less which at least half the records OrderGALLIFORMESPELECANIFORMESFALCONIFORMES Ardeidae Phasianidae GRUIFORMES FamilyCHARADRIIFORMESCOLUMBIFORMES STRIGIFORMES Scolopacidae APODIFORMES Rallidae Columbidae LatinPASSERIFORMES Strigidae Apodidae Laniidae English High Rice Some Rice BIRDS IN CHINA’S RICE FIELDS 41 igh Rice indicates that a species was detected on ted with less than half the records on a transect. ted with less than half the records Lanceolated WarblerPlain PriniaGrey-sided Scimitar BabblerRufous-capped BabblerChinese HwameiVinous-throated ParrotbillJapanese White-eyeCrested Myna X Red-billed StarlingCommon BlackbirdOriental Magpie Robin RedstartPlumbeous Water White-crowned ForktailSiberian StonechatBrown Dipper X Russet Sparrow SparrowEurasian Tree X White-rumped Munia X Scaly-breasted Munia X Grey WagtailWhite Wagtail X PipitRichard’s X Olive-backed PipitGrey-capped Greenfinch X X X Meadow Bunting X X Little Bunting X BuntingYellow-breasted Chestnut BuntingCommon Reed Bunting X X X X X X X X X X X X X X X X Locustella lanceolata Prinia inornata Pomatorhinus swinhoei Stachyris ruficeps canorus Paradoxornis webbianus japonicus Zosterops cristatellus Acridotheres Spodiopsar sericeus merula mandarinus Turdus Copsychus saularis Rhyacornis fuliginosa Enicurus leschenaulti Saxicola maurus Cinclus pallasii Passer rutilans Passer montanus Lonchura striata Lonchura punctulata Motacilla cinerea Motacilla alba Anthus richardi Anthus hodgsoni sinica Carduelis Emberiza cioides Emberiza pusilla Emberiza aureola Emberiza rutila Emberiza schoeniclus Megaluridae Cisticolidae Timaliidae Zosteropidae Sturnidae Turdidae Muscicapidae Cinclidae Passeridae Estrildidae Motacillidae Fringillidae Emberizidae Table 2. (Continued) Birds detected on transects containing rice habitats during surveys H 2. (Continued) Birds Zhejiang Province. in Lin’an County, Table associated with rice; Some Rice indicates that rice was present, were but associa a transect in which at least half the records Order Family Latin English High Rice Some Rice 42 WATERBIRDS

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