Biological Conservation 234 (2019) 180–187 Contents lists available at ScienceDirect Biological Conservation journal homepage: www.elsevier.com/locate/biocon The next widespread bamboo flowering poses a massive risk to the giant panda T ⁎ Zhaoxue Tiana, Xuehua Liua, , Zhiyong Fanb, Jianguo Liuc, Stuart L. Pimmd, Lanmei Liua, Claude Garciae,f, Melissa Songerg, Xiaoming Shaoh, Andrew Skidmorei,j, Tiejun Wangi, Yuke Zhanga, Youde Changb, Xuelin Jink, Minghao Gongl, Lingguo Zhoum, Xiangbo Hen, Gaodi Dangn, Yun Zhuo, Qiong Caio a State Key Joint Laboratory of Environmental Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing 100084, China b WWF-Beijing Office, 22 Baiwangzhuang Street, Xicheng District, Beijing 100035, China c Center for Systems Integration and Sustainability, Department of Fisheries and Wildlife, Michigan State University, East Lansing M148823-5243, USA d Nicholas School of the Environment, Duke University, Box 90328, Durham, NC 27708, USA e ForDev Group, Department of Environmental Systems Science, Swiss Federal Institute of Technology (ETH), CH-8092, Zurich, Switzerland f Research Unit Forests and Societies, Centre International de Recherche Agronomique pour le Développement (CIRAD), F-34392 Montpellier, France g Conservation Ecology Center, Smithsonian Conservation Biology Institute, Front Royal, Virginia 22630, USA h Beijing Key Laboratory of Biodiversity and Organic Farming, College of Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China i Faculty of Geo-Information Science and Earth Observation (ITC), University of Twente, 7500 AE Enschede, The Netherlands j Macquarie University, NSW 2109, Australia k Shaanxi Institute of Zoology, Chinese Academy of Sciences, 88 Xingqing Street, Xi'an 710032, China l Institute of Wetland Research, Chinese Academy of Forestry, Summer Palace, Beijing 100091, China m Wildlife Protection Station, Department of Shaanxi Forest Administration, 233 Xiguanzheng Street, Xi'an 710082, China n Foping Nature Reserve, Foping County, Shaanxi 723400, China o Guanyinshan Nature Reserve, Foping County, Shaanxi 723400, China ARTICLE INFO ABSTRACT Keywords: The IUCN Red List has downgraded several species from “endangered” to “vulnerable” that still have largely Scenario analysis unknown extinction risks. We consider one of those downgraded species, the giant panda, a bamboo specialist. Massive bamboo flowering Massive bamboo flowering could be a natural disaster for giant pandas. Using scenario analysis, we explored Risk pattern possible impacts of the next bamboo flowering in the Qinling and Minshan Mountains that are home to most Giant panda giant pandas. Our results showed that the Qinling Mountains could experience large-scale bamboo flowering Qinling Mountains leading to a high risk of widespread food shortages for the giant pandas by 2020. The Minshan Mountains could Minshan Mountains similarly experience a large-scale bamboo flowering with a high risk for giant pandas between 2020 and 2030 without suitable alternative habitat in the surrounding areas. These scenarios highlight thus-far unforeseen dangers of conserving giant pandas in a fragmented habitat. We recommend advance measures to protect giant panda from severe population crashes when flowering happens. This study also suggests the need to anticipate and manage long-term risks to other downgraded species. 1. Introduction Administration, 2015). The number of wild giant pandas has increased by 17% since the Third National Giant Panda Survey (the third survey) Giant pandas (Ailuropoda melanoleuca), the globe's most beloved conducted in 1999–2003 (China's State Forestry Administration, 2006). conservation icon as well as the symbol of the World Wide Fund for This increase led to the downgrading of the giant panda from “en- Nature (WWF), are only found in China's Sichuan, Shaanxi and Gansu dangered” to “vulnerable” on the International Union for Conservation provinces. According to the Fourth National Giant Panda Survey (the of Nature (IUCN) Red List in 2016. Indeed, some threats such as logging fourth survey) conducted by the Chinese government in 2011–2014, stopped in late 1999 (Xu et al., 2017) and much more of the species there were 1864 giant pandas in the wild (China's State Forestry range is now protected. However, what risks giant pandas will ⁎ Correspondence author. E-mail address: [email protected] (X. Liu). https://doi.org/10.1016/j.biocon.2019.03.030 Received 18 December 2018; Received in revised form 12 March 2019; Accepted 19 March 2019 0006-3207/ © 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/). Z. Tian, et al. Biological Conservation 234 (2019) 180–187 Fig. 1. Study area in China. The Qinling Mountains with 23 nature reserves (A) and the Minshan Mountains with 22 nature reserves (B). encounter after the delisting remain unclear. semelparous — they flower and then die, doing so infrequently but Human activities like farming, deforestation, or other development, synchronously over large areas. Researchers have long explored the have driven the giant panda out of the lowland areas where it once features of bamboo flowering and have established a series of theories lived (Pan et al., 2014; Wei et al., 2015; Yang et al., 2017). It now lives including cyclicity of flowering periods, dynamic of bamboo nutrition, only in six mountains, i.e. the Minshan, Qionglai, Liangshan, Daxian- and responsiveness to drought (Ding, 2006; Peng et al., 2013). The gling, Xiaoxiangling Mountains, and the southern slope of the Qinling giant panda has evolved behavioral, physiological, morphological, and Mountains. The giant panda habitat is becoming more fragmented and genetic adaptations that enable them to survive on a bamboo diet (Nie their populations becoming more isolated (Li et al., 2015; Xu et al., et al., 2015). Bamboo recovery after episodic bamboo flowering events 2017), with the smaller ones having high risk of local extinction (Shen is a natural process but takes several years before it provides sufficient et al., 2015). Despite comprehensive conservation efforts over the last nutrition for giant pandas (Jeffrey, 1984). During field surveys, 13 dead few decades, threats to the giant panda remain. For example, human giant pandas were found during the large-scale bamboo flowering event activities degraded the Wolong Nature Reserve (Liu et al., 2001). The in Wanglang Nature Reserve in 1975 (Kang and Li, 2016). Between the Daxiangling Mountains have been fragmented by exploitation of forest, 1970s and 1980s, there were two large-scale Fargesia bamboo flowering mining, traffic, and agriculture (Xu, 2006). Grazing has degraded events in the Minshan and Qionglai Mountains in Sichuan province. Wanglang Nature Reserve (Li et al., 2017) and giant pandas were Remains of 138 giant pandas were found in the following years (Hu, trapped in snares poachers set for musk deer (Schaller, 1987). Besides 1986 ). In Wolong Nature Reserve, 40–50% of the giant pandas may land-use change and fragmentation, climate change will also likely af- have died, and other individuals may have emigrated as the con- fect giant pandas through habitat degradation and a predicted sub- sequence of flowering during 1983–1985 (O'Brien and Knight, 1987). stantial reduction of three dominant bamboo species in the Qinling Suitable giant panda habitat must contain at least two bamboo species Mountains during the 21st century (Tuanmu et al., 2013). As with other that allows giant pandas to migrate to another suitable patch if one ecosystems, direct human activities and climate change are the two bamboo species flowers (Schaller et al., 2012). Although dispersal has factors that can limit the recovery of the giant panda population and been the strategy evolved in response to widespread, simultaneous die- constrain its future (Malhi et al., 2014). We ask: do features of the offs of bamboo, highly fragmented panda habitat and substantial bar- panda's ecology predispose it to be vulnerable to natural changes given riers, including new roads, likely make their dispersal much more dif- its current circumstances? A study on bamboo is essential. ficult. Giant pandas rely on bamboo for 99% of their diet. Bamboos are The IUCN Red List has downgraded the risk for giant pandas after 181 Z. Tian, et al. Biological Conservation 234 (2019) 180–187 wild numbers improved over the last few decades. However, long-term them, the first three largest distributions are Fargesia denudata risks for this species remain largely unquantified. In this study, we show (2510 km2, accounting for 35% of the total areas), Fargesia nitida the importance of quantifying risks after downgrading. Our objective is (1697 km2, accounting for 24% of the total areas) and Fargesia rufa to propose spatially-explicit risk scenarios that will help managers (1055 km2, accounting for 14% of the total areas). The nine other identify the forces driving the system changes and the possible vul- bamboo species occupy the remaining 27% of the area. nerabilities, and develop better management strategies in anticipation. 2.3.2. Spatial flowering pattern 2. Materials and methods Using questionnaires, we surveyed 45 giant panda nature reserves in the Qinling and Minshan Mountains in 2014, since the data of the 2.1. Study area fourth survey were not available. The questionnaires were given to the experienced staffs in the nature reserves, who worked in the mountains In this