Breeding range shift of the red-crowned crane (Grus japonensis) under climate change

land cover, and biotic factors such as competition and predation restrict the red-crowned crane to fill all its climatic niche space. At large spatial scale, the climate is the most important factor shaping the breeding range of the red-crowned crane. Among 19 bioclimatic variables, the temperature seasonality (Bio4) and precipitation seasonality (Bio15) are the top two vari- ables in determining the breeding range of the red-crowned crane. It suggests that the climate change, which results in spatial shift of seasonality of temperature and precipitation, would cause the shift of the breeding range. There are many threats on the red-crowned crane in the breeding range, and affect the extent of breeding range. The population has been severely declined because of habitat modifi- cation, pollution and poaching [4,11,48]. Although the population was slightly increased after implementing the conservation policy made for this endangered species, and building pro- tected area for it, such as Zhalong National Natural Reserve and Yancheng Biosphere Reserve, the population size is still very low, estimated at 2,750 [3,49]. Therefore it is under severe extinction risk from environmental change, especially the unprecedented climate change. Cli- mate change would cause poleward shift of breeding range of the red-crowned crane. Some studies have already shown that some bird species extend their ranges northwards under cli- mate change [23]. Climate change also affected the phenology of the red-crowned crane,

which affected the adaptation capacity of this species [50,51]. Climate change also has indirect effects on the red-crowned crane, for example, one study showed that climate change altered the animal-plant interactions and thereby affected bird and plant communities [52]. The effects of climate change on the red-crowned crane and its breeding range, therefore, should be taken into consideration when making preservation policy for this endangered species. The predicted shift of the breeding range of the red-crowned crane under changing climate from our bioclimatic niche models suggests that China would lose a proportion of the breeding range, Russia would gain some breeding range area. This effect might be overestimated, because the red-crowned crane has adaptation potential to climate change. Our model also neglected other abiotic and biotic factors affecting the breeding range of the red-crowned crane and the prediction accuracy of range shift in the face of climate change. This impact means that the role of conserving this endangered species would be changed, because the pro- portion of the breeding area in China, Russia and Mongolia would be changed. The area of breeding range in China would be shrunk as climate changes. The effectiveness of the pro- tected area in China, therefore, would be jeopardized in the future. The increasing area of the breeding range in Russia and Mongolia means these two countries would take more responsi- bility to conserve this endangered species. However, the conservation policy in each country is

different and does not necessarily consider the effects of climate change on the breeding range of this species. The international collaboration among the three countries would increase the conservation effectiveness of this species under climate change. Some studies showed that international collaboration can benefit the birds in Europe [53]. Supporting information S1 Fig. Predicted breeding range of the continental population of the red-crowned crane at 2030s, 2050s, 2070s and 2080s. Blue polygons are the current actual breeding area, green polygons are the predicted potential breeding area under current climate condition, and orange areas are the predicted potential breeding area climate change. Scenario is RCP4.5, intermediate emission scenario. (DOC) S2 Fig. Predicted breeding range of the continental population of the red-crowned crane at 2030s, 2050s, 2070s and 2080s. Blue polygons are the current actual breeding area, green PLOS ONE Breeding range shift of the red-crowned crane (Grus japonensis) under climate change PLOS ONE | https://doi.org/10.1371/journal.pone.0229984 March 12, 2020 13 / 16