The size of the captive RC population was determined on the basis of the average annual growth rate, the mortality rate and the reproductive success rate. These three parameters were used to build a model to examine whether a growing captive population is eroding the wild RCs in China. Our results show that the number of new-born cranes, bred in captivity, was insufficient to account for the increasing captive population with a gap of 10‒27 birds per year and a total of 244 for the entire 14 year periods from 1999 to 2013. Thus, we accept the hypothesis that part of the captive RC population in zoos and nature reserves came from the wild, through taking eggs and capturing juveniles/adults. In the context of a self-sustaining captive population, our results provide a new perspective on the continuing decline of the RC population in the wild in China.

The erosion effect received little attention in previous studies of captive RCs which generally focused on genetic variation (Zou et al. 2007), blood biochemical indices (Zeng and Xu 2012), behavioral ecology (Cao and Wu 2013) and population surveys (Tian et al. 2006; Zhou et al. 2012). Regarding the enormous size of their captive population, zoos and nature reserves maintain that they caught RCs and took eggs from the wild at the very beginning of the establishment of a captive population, while all captive RCs are currently produced through captive breeding (Wang et al. 2011a). However, this statement is untenable. We found the N _s is greater than one in each of the 14 year periods from 1999 to 2013, which suggests that a supplementary number of cranes are needed to support this growing captive population. Moreover, the import of RCs from abroad is almost impossible because it is listed as an Appendix I species by CITES. Thus, we conclude that part of the captive RC population can only come from the wild. It should be noted that zoos and nature reserves with large captive RC populations generally are adjacent to wild crane areas, which facilitates the transition of RCs from the wild to become captive birds. Of course, it is permissible to pick up eggs and capture juveniles/adults from the wild for ex situ conservation purpose. The establishment of captive population through capturing wild birds is a successful case for the recovery of wild Crested Ibis (Nipponia nippon) population (Ding and Li 2005). We hold that the emphasis in similar cases is the rational number of captured wild birds. Currently, the population size of captive RCs was nearly three times as high as that in the wild. Under this circumstance, it is obviously unreasonable and illegal to fill the gap of the growing captive RC population through capturing birds from the wild, and releasing the captive birds to the wild would be the right way, just like the case of the Crested Ibis.

This study found that a total of 244 cranes were needed to supplement the captive population during the 1999‒2013 period, an average of 17.4 per year period. However, we believe the real number to be higher because the total number of captive RCs in 2013 was underestimated and the annual reproductive success rate in the zoos overestimated. Based on the population survey of zoos by Zhou et al. (2014a) and that of nature reserves in this study, we found a total of 1520 captive RCs in China. This is the most extensive survey to date, providing the largest estimate of the size of the captive population. However, these data are still incomplete, for the size of captive RC population in wildlife or crane farms is unclear. Hence we are sure that the total number of captive RCs in China is greater than 1520. This underestimate of the total number of captive RCs would lead to an equal underestimate of the average annual growth rate and thus, an underestimate of the erosion effect. We calculated the average annual reproductive success rate in zoos based on the rate in nature reserves. Compared with the number of captive cranes in zoos, the birds in nature reserves have larger populations and a better living environment, such as a more natural habitat with less human disturbance, which helps to increase their mating chances and improve their rate of reproductive success in captivity. Because of this and the fact that only about half of the cranes are involved in breeding programs in zoos, we conclude that the average annual reproductive success rate in zoos is probably overestimated. Zhou et al. (2012) found that only 80 birds from 12 captive crane species were new-born in 2011, with an annual reproductive success rate of about 4.4%, much less than our estimate of 9.17%, providing indirect evidence of an overestimation of the annual reproductive success rate of captive cranes which, in turn, leads to an underestimate of the erosion effect. In our opinion, the estimate of N _s in this study is very conservative and the erosion effect substantially underestimated. All the same, about 0.4‒1.0% of wild RCs in the world, i.e. about 2800 birds (Su and Zou 2012) are annually lost because of the erosion effect. Considering only the western subpopulation of the RC in the wild, about 560 birds (Zhou et al. 2014b) wintering primarily at Yancheng, 1.8‒4.8% of wild cranes were lost per year, which represents a great loss for this endangered species and is sufficient to push it to the edge of extinction. We suggest that it is necessary to enhance efforts to determine the size and reproductive success rate of RC populations in zoos, as well as the mortality rate of these captive cranes in China and to conduct a more accurate assessment of the erosion effect on the growing population of RCs in captivity.

The reproductive success rate of captive RCs was nearly twice as high in nature reserves as in zoos. We suggest that the captive population in nature reserves is both capable to maintain itself and to produce extra birds, which actually violates the original intention of nature reserves. In contrast, the captive RCs in zoos have a low reproductive success rate and thus have difficulty maintaining sustained growth. More specifically, we can say the illegal removal of cranes from the wild by zoos and nature reserves has a clear erosion effect on the RC population in the wild. In addition, we speculate that some of the captive RCs in zoos came from nature reserves through trade, but the number of these extra birds cannot completely meet the needs of zoos. The number of supplementary RCs coming to zoos are probably from the wild, but the zoos are isolated from the wild RC population. So the question arises as to how the zoos obtain wild RCs. In contrast to the zoos, nature reserves can more easily obtain wild RCs because they function as breeding, stopover and wintering sites. In fact, we have found and heard that some nature reserves caught cranes in the wild, turned them to be the “captive” population and then sold or rented them to other captive-feeding establishments (such as urban zoos, wildlife parks, wetland parks and crane farms) for profitable ends. The famous illegal wildlife trading case, i.e., the “bird king” Wu Liu Case, provides some direct evidence for this erosion path (Lu et al. 2015). As well, some facilities, such as the Shenyang Forest Zoological Garden and Zhalong National Nature Reserve, hold more than 100 captive RCs. Why these facilities need such a large captive population of cranes is a question worth pondering.

Previous studies of RCs in the wild generally focused on the negative effects of habitat loss or degeneration (Ma et al. 2000; Jiang et al. 2012), climate change (Wu et al. 2012; Peng et al. 2014), the effect of human disturbance on behavioral ecology (Wang et al. 2011b; Ge et al. 2011; Li et al. 2013), fire (Kong et al. 2007) and pollution from heavy metals (Luo et al. 2013, 2014). Direct human disturbances also play a non-negligible role in the decline of populations in the wild (Harris and Mirande 2013). For example, Zhou et al. (2014b) found that approximately 2.1% of the RC population in the wild is lost each year due to poisoning, poaching, becoming entangled in fish nets and flying into power lines. In this study, we first quantified the erosion effect of a growing captive population on RCs in the wild in China, which elucidated the source of captive cranes and provide a new perspective on the continued decline of the RC population in the wild.

Regarding the conservation of our wild cranes, we first suggest controlling the size of the captive-feeding population in zoos and nature reserves, especially in zoos, to reduce the need for supplementary birds. Secondly, it is necessary to enhance the supervision of captive feeding in nature reserves. For example, the impacts of taking eggs from the wild should be assessed. It is possible that free-ranging captive RCs would mix with cranes from the wild which poses a health risk to both (Feare 2007; Boyce et al. 2009). More importantly, nature reserves should focus on the protection of natural habitats and wild populations, rather than hold large captive populations. In third place, we recommend that the management of the captive RC population in zoos, especially in small zoos, be further strengthened. Due to the small population, the limited number of potential mates, the living conditions and their inability to prevent diseases, it is difficult for the RCs to be healthy and breed under stable conditions in small zoos. The resulting high mortality rate and low breeding success in zoos would probably lead to an increased demand for supplementary birds, which would exacerbate the erosion of the RC population in the wild. Finally, we should strictly enforce the newly revised Law of Wildlife Protection of the People’s Republic of China, which clearly stipulates that hunting national key protected animals is illegal and will be fined or investigated for criminal responsibility.