Plate Ⅰ.
Crested Ibis (Nipponia nippon). (a) Crested Ibis in flight; (b) Young Crested Ibis (photos by Zhinong Xi).
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Csaba MOSKÁT, Fugo TAKASU, A. Roman MUÑOZ, Hiroshi NAKAMURA, Miklós BÁN, Zoltán BARTA. 2012: Cuckoo parasitism on two closely-related Acrocephalus warblers in distant areas: a case of parallel coevolution?. Avian Research, 3(4): 320-329. DOI: 10.5122/cbirds.2012.0038
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Common Cuckoos (Cuculus canorus) parasitize nests of small passerines. The Cuckoo chicks cause the death of their nest-mates when evicting eggs or nestlings from the nests; consequently, hosts suffer from a high loss of reproduction. Host adaptations against parasitism, e.g., by egg discrimination behavior, and cuckoo counter-adaptations to hosts, e.g., by mimetic eggs, are often regarded as a result of the arms race between the two interacting species. In Hungary Great Reed Warblers (Acrocephalus arundinaceus) are the main hosts of cuckoos, suffering from heavy parasitism (ca. 40-65%). The Oriental Reed Warbler (A. orientalis), formerly a subspecies of the Great Reed Warbler (A. a. orientalis), is also a highly parasitized host in Japan (25-40%). We compared main characteristics of Cuckoo parasitism in these two distant areas from the Western and Eastern Palearctic by comparing cuckoo egg mimicry. We measured color characteristics of host and parasitic eggs by spectrophotometer. Visual modeling revealed lower chromatic distances between Cuckoo and host eggs in Hungary than in Japan, but high variation both in host and Cuckoo eggs may cause matching problems in Hungary. Achromatic (brightness) difference between host and Cuckoo eggs were lower in Japan than in Hungary, and it proved to be the most important factor affecting egg rejection. Hosts rejected Cuckoo eggs at similar frequencies (37% and 35% in Hungary and Japan, respectively). Host adaptation, i.e., egg rejection behavior, seems to be preceding Cuckoo counter-adaptations to hosts in Japan. We suggest that the Cuckoo-Great/Oriental Reed Warbler relationships developed in alternative ways in Japan and Hungary, and they represent different stages of their arms race.
The Crested Ibis (Nipponia nippon, Plates Ⅰ and Ⅱ) (Ciconiiformes: Threskiornithidae) is a medium-sized wading bird, ranging in length from 57.5 to 84.0 cm, with a longish neck and legs, a red featherless face with a crested white head. Its most distinctive morphological character is the long, slender and decurved bill, perfectly adapted for probing in water and mud, or even in cracks on dry ground. The non-breeding adult is white, with orange cinnamon tones in the tail and flight-feathers. The long bill is black with a red tip. Its red legs do not extend beyond the tail in flight (Hoyo et al., 1992).
The Crested Ibis is categorized as Endangered (EN) in the IUCN Red List (BirdLife International, 2001) and is listed in Appendix Ⅰ of CITES. It is also ranked as a first class national key protected animal in China (Zheng and Wang, 1998; Ding, 2004).
The Crested Ibis was widespread and locally common in North-East Asia until the late nineteenth century, when it was breeding in far eastern Russia, Japan and mainland China and was a presumed non-breeding visitor to the Korea Peninsula and Taiwan Island (Fig. 1). The population of the Crested Ibis rapidly declined in the late nineteenth and early twentieth centuries, related to deforestation of pine woodlands as nesting habitat, human persuit, especially over-hunting, drying out of wetland and the abuse of chemical fertilizers and pesticides in paddy fields during the 1950's. This species was even evaluated as extinct in the wild (EW) when the last five wild birds in Japan were caught into captivity in 1981.
In China, the last specimen was collected in Gansu Province in 1964, after which there were no records for a long time (Ding, 2004). In May 1981, after three years of a nation-wide survey, a tiny wild population of seven birds (two pairs and three fledglings) was re-discovered in Yangxian, Shaanxi Province in central China and renewed hope for this species (Liu, 1981).
After the rediscovery of the wild population, the Chinese government and authorities have made great efforts for the conservation of the Crested Ibis and its habitats. The Shaanxi Crested Ibis Nature Reserve was established in 1990 and this magnificent bird has since been the focus of intensive conservation efforts. The seven original birds are the source of all present Crested Ibis populations, both in the wild and in captivity. Now there is only one wild population remaining in the world, located in Yangxian and nearby counties in Shaanxi Province and has been gradually recovering to more than 600 birds in 2007 (Fig. 2) (Zhang and Ding, 2008). One reintroduced population of about 20 birds has been established in Ningshan County, Shaanxi Province since 2007.
Six fledglings were taken from the wild to initiate a captive population in Beijing Zoo before 1986, where the first successful breeding was achieved in 1989 (Li, 1991). Another captive rearing and breeding program began at the Shaanxi Crested Ibis Breeding Centre in 1990 with the rescue of sick or injured chicks and the collection of some of the eggs deserted by parental birds in the wild (Xi et al., 2002). There are now five captive populations with a total of about 600 birds in the Beijing Zoo, Yangxian and Zhouzhi counties of Shaanxi Province, the Dongzhai Nature Reserve of Henan Province and in Deqing County of Zhejiang Province.
The annual activity of the Crested Ibis can be divided into a breeding season (February to June), a wandering season (July to October) and a wintering season (November to January) (Wang and Shi, 2000). The breeding areas are located in middle and lower mountains with wintering paddy fields, nesting on tall trees, close to villages. The position of the nest sites is closely related to the availability of feeding grounds and many nests are built close to human settlements, often less than 100 m and sometimes the nest tree is only a few meters from a human settlement. The trunks of nest trees (and adjacent trees) are covered with plastic cloth or razor blades to prevent snakes from climbing up and nets are placed under the nests to catch any chicks that fall out (Ding and Li, 2005).
The mating system is monogamous. Male and female birds both contribute to nesting, hatching and feeding chicks. Pairs will use the same nesting territory if not disturbed. In the past they were observed to re-use old nests but most pairs now build new nests every year (Shi et al., 2001).
The wild population no longer migrates, only making short flights to feed in paddy fields below 700 m during the winter and moving to higher elevations (up to 1200 m) to nest in the spring. During the wandering season, the birds move about 25 km (15−45 km) from their breeding areas to planes along the Hanjiang River. They move back to their breeding areas during the wintering season. During the non-breeding season, the ibises gather in flocks for feeding and roosting.
Breeding starts in late February to early March, with laying from mid March to early April. Nests are flimsy stick platforms, lined with small twigs, leaves and hay, built on branches of trees (Pinus massoniana, Quercus variabilis, chestnut or poplar), at heights of 4−22 m. Usually there are 3−4 eggs per nest, the incubation period is about 28 days; chicks have gray down, white below and become fledglings after 40−45 days. The young birds are sexually mature in 2−3 years. Captive birds in Japan have lived to become 37 years old.
The size of the home range averages 100.8 ± 49.8 ha (according to MCP method) and 175.6 ± 91.3 ha (according to 90% Kernel method); the breeding home range of different pairs overlaps about 24.5 ± 27.3% and some pairs can overlap up to 46.8−64.3% (Liu et al., 2003).
The success of fledglings from the wild population was only 11% in the early 1980s, but with effective conservation measures taken since then, it increased to 53% in the late 1990s (Shi and Cao, 2001). Because a high proportion of the wild population consists of young birds that have not yet started to breed (Lu et al., 2000), it is predicted that the wild population of the Crested Ibis will continue to increase and that they will expand their breeding range. The distribution area has been increased from less than 100 km2 to more than 3000 km2 at present. The discovery of a nesting pair in Xixiang County of Shannxi Province in 1999 provides evidence for such an expansion (Ding et al., 1999). Figure 3 shows the dispersal of breeding sites from 20 nests in 1999 to 102 nests in 2007 (Zhang and Ding, 2008).
Birds forage during the daytime in small flocks, probe into mud or shallow water with their bill, or pick up prey from the ground. The diet consists of freshwater fish (loaches and eels), amphibians (frogs, newts and salamanders), crustaceans, freshwater mollusks and insects, especially grasshoppers, crickets and adults and larvae of aquatic beetles.
In winter, the main feeding habitats are paddy fields, riverbanks and reservoirs, mainly close to human settlements. Birds seem able to tolerate human activities in these areas (Ma et al., 2001). The areas where they currently breed are at 470–1300 m elevation (Ma et al., 2001), but elders in Yangxian reported that, prior to the 1940s, they were usually found at lower elevations in areas with slow-flowing rivers. In recent years, they have tended to move into new nesting sites at lower elevations in this area (Zhai et al., 2001), presumably indicating that this relict population had become confined to suboptimal upland areas but is now expanding back into more typical lowland habitats.
The use of fertilizer and pesticides usually causes pollution in feeding areas and threatens food diversity and richness of the Crested Ibis, especially in the chick hatching period. Research has indicated that food shortage is a major factor affecting the chick survival rate (Ding, 2004). Food supplementation in paddy fields is an effective measure during the breeding season.
Since there is only one wild population in the world, found in a very limited area, the Crested Ibis cannot avoid being threatened. If wildlife diseases (such as New Castle disease and bird flu), climate disasters (such as heavy snow and extreme drought during breeding season) and outbreaks of pollution in feeding areas, the wild population of the Crested Ibis will be faced with a serious threat to its survival. It is urgently required to conduct a reintroduction program to establish a second and third wild population in other areas (Ding and Li, 2005).
At present, with the development of captive breeding populations, there are enough captive birds reserved for release into the wild. In 2004, the State Forestry Administration (SFA) organized a survey for reintroduction sites in China (Ding and Li, 2005). GIS techniques were used to detect potential suitable breeding sites for the Crested Ibis (Liu et al., 2006). Since then, four captive populations have been established for wild training in Huayang, Ningshan, Dongzhai and Deqing. Where could potential reintroduction places be found?
In October 2004, a small captive population was transferred to Huayang, a higher elevation area in Yangxian, for wild training. Up to 2006, 23 birds were released. Now the released birds have joined the local wild population and eight of them bred successfully in seven nests in 2010.
In May 2007, 26 birds were released in Ningshan County, Shaanxi Province. It was the first reintroduction attempt of the Crested Ibis. With 16 more birds released later, there are more than 20 birds surviving in Ningshan and five pairs of them bred with six fledglings surviving in 2009 (XY Chang, unpublished data).
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