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Bat Conservation in China: Should Protection of Subterranean Habitats Be a Priority?

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Bat Conservation in China: Should Protection of Subterranean Habitats Be a Priority? Bat conservation in China: should protection of subterranean habitats be a priority? J INHONG L UO,TINGLEI J IANG,GUANJUN L U ,LEI W ANG,JING W ANG and J IANG F ENG Abstract Subterranean environments are essential for the Boyles et al., 2011; Kunz et al., 2011). However, populations survival of many bat species and other cave fauna but these of many bat species are declining because of threats places are subject to increasing human disturbance. To such as climate change, habitat loss and degradation, examine the significance of subterranean habitats for the hunting and emerging diseases (Meyer et al., 2010). Of conservation of bats in China we surveyed bat species in these, habitat loss and degradation are the greatest threats 225 underground sites during 2003–2011. Our results show to bats in most regions (Mickleburgh et al., 2002; Racey that 77% of bat species in China, including 30 nationally & Entwistle, 2003; Jones et al., 2009; Kingston, 2010; Meyer Endangered or Vulnerable species and nine endemic et al., 2010). species, roost in caves and other subterranean habitats. Subterranean sites, such as caves and mines, provide The number of species in occupied roosts was 1–15. Almost roosts for many bat species (Kunz, 1982; Hutson et al., 90% of the roosts surveyed contained signs of human 2001), and some of the most important maternity and disturbance, most of which was from recreational activities. hibernating sites (Kunz, 1982; Kunz & Lumsden, 2003; One hundred and twenty-one roosts merit special concern Murray & Kunz, 2005). Such sites are also used as mating because they harbour $ 6 species or . 1,000 individuals, or and aggregation locations for millions of individuals species of special concern (threatened or endemic species). (Kunz, 1982; Hutson et al., 2001). The range and densities Generally, larger roosts support more species and a greater of bats that rely on caves are determined largely by the abundance of bats than smaller roosts but there is no direct distribution, quantity and characteristics of available caves correlation between the presence of species of special (Murray & Kunz, 2005; Struebig et al., 2009). According concern and roost size. Disused tourist caves have to the IUCN Red List of Threatened Species (IUCN, 2010), significantly more bat species than other types of roosts. 449 out of 1,132 extant bat species roost in caves and other Our data demonstrate that roost disturbance by recreational subterranean habitats. activities has pronounced detrimental effects on the number Disturbance of roosts threatens many bat species of bat species and the presence of species of special concern. (Hutson et al., 2001), and declines of cave-dwelling bat We discuss the social, economic and political issues that populations were noted as early as 1952 (Mohr, 1972). could adversely affect bat conservation in caves in China, Activities within or around caves, such as mining, quarry- and we recommend that protection of subterranean habitats ing, guano and bird nest collecting, caving, tourism, and should be a high priority for bat conservation. deliberate or accidental disturbances can all have negative effects on bats (Hutson et al., 2001). In Mexico there have Keywords Bats, China, Chiroptera, conservation priority, been dramatic declines of cave-dwelling bats caused by roost endemism, human disturbance, species richness, tourist disturbance (Hutson et al., 2001) and in the USA roost cave disturbance was the cause of the decline of six threatened bat This paper contains supplementary material that can be species (Elliott, 2000). found online at http://journals.cambridge.org Currently, 121 bat species are known from China (IUCN, 2010). Although only one species (Pteropus lylei) is considered globally threatened, populations of 18 species 79 Introduction are decreasing and the population trends of species are unknown (IUCN, 2010). Sixty-two bat species are con- ats are ecologically important as pollinators, seed sidered nationally threatened (Endangered, Vulnerable or Bdispersers and insect predators (Cleveland et al., 2006; Near Threatened; Wang & Xie, 2004). Betke et al., 2008; Kalka et al., 2008; Lobova et al., 2009; Despite the high proportion of nationally threatened bat species in China and the lack of information on the ecology of these species, little research has focused on bat JINHONG LUO,TINGLEI JIANG,GUANJUN LU,LEI WANG,JING WANG and JIANG conservation in the country (but see Niu et al., 2007). Based FENG (Corresponding author) Jilin Key Laboratory of Animal Resource Conservation and Utilization, Northeast Normal University, 5268 Renmin on our surveys of bats in 225 underground sites during Street, Changchun, 130024, China, and Key Laboratory for Wetland Ecology 2003–2011 and an assessment of related social, economic and Vegetation Restoration of National Environmental Protection, Northeast Normal University, Changchun, China. E-mail [email protected] and political issues, we recommend that protection of Received 15 March 2011. Revision requested 14 June 2011. subterranean habitats should be a high priority for bat Accepted 7 September 2011. First published online 17 July 2013. conservation in China. © 2013 Fauna & Flora International, Oryx, 47(4), 526–531 doi:10.1017/S0030605311001505 Downloaded from https://www.cambridge.org/core. IP address: 170.106.35.229, on 28 Sep 2021 at 08:15:11, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605311001505 Bat conservation in China 527 50°N 70°E 80°E 90°E 100°E 110°E 120°E 130°E 140°E 40°N FIG. 1 China, showing the locations of 30°N potential bat roosts surveyed during 2003–2011. The provinces and municipalities where we surveyed are numbered: 1, Hainan; 2, Yunnan; 3, Guangxi; 4, Guangdong; 5, Guizhou; 6, Hunan; 7, Guangxi; 8, Fujian; 9, 20°N Sichuan; 10, Chongqing; 11, Hubei; 12, Anhui; 13, Zhejiang; 14, Jiangsu; 15, Gusu; 16, Shaanxi; 17, Henan; 18, Shanxi; 19, Shandong; 20, Tianjin; 21, Beijing; 22, Neimenggu; 23, Jilin; 24, Heilongjiang. Methods the year. Using the information gathered we categorized roosts as either visited or seldom visited. Seldom-visited We surveyed bats in 225 subterranean sites in China during roosts were those for which the residents questioned had March–August from 2003 to 2011 (Fig. 1). Information on not seen visitors in the previous 12 months. Within each roost localities was collected from the literature, Internet roost that we could enter we searched for traces of human and local residents. Local people provided information activities (e.g. footprints, food packages, cigarette butts, on numbers of roost entrances, frequency of visits to the scratches, notches and remains of torches). If a roost was roost, identity of visitors, relative number of bats and categorized as seldom visited and we found no obvious safety issues. We entered roosts with torches, in the daytime, traces of human activities it was categorized as undisturbed, when the situation allowed. We recorded locations, with a and otherwise as disturbed. global positioning system, and collected information on the The conservation value of roosts was assessed using freshness of bat faeces, traces of human activities, and roost three criteria (species richness, abundance, and the presence and colony sizes. Colony size was assessed mainly by direct of species of special concern) proposed by Arita (1993, 1996). roost counts except for some inaccessible roosts, for which Species of special concern were those categorized as the colony sizes were estimated by evening emergence Endangered or Vulnerable in China, or species endemic to counts. Methods for estimation of colony size followed China. We regard roosts that harbour $ 6 species or Kunz et al. (2009a). 1,000 individuals as being of special concern. Roost size was measured as the combined inner space Bat species were captured with ground-based mist nets 3 size (in m ) of all chambers and passages of a cave. In most set at entrances during emergence in the evening and cases each chamber and passage was considered a cuboid sometimes in the early morning as bats returned from and its volume determined as total length × mean height × foraging. At least one person monitored the net, and when a width. As the resulting estimates of roost size were not bat entered it was removed with care to avoid any injury precise we identified roosts as large or small based on the to either the bat or the handler (Kunz et al., 2009b). The 3 median (1,000 m ) of the data. Additionally, if a roost was handling of bats conformed to guidelines for animal care too large to be surveyed in 15–30 minutes it was regarded as and use established by the American Society of large. A roost was categorized as inaccessible if its entrances Mammalogists (Gannon & Sikes, 2007). All fieldwork were too small to allow a person to enter. The small abided by the Law of the People’s Republic of China on percentage of roosts for which size could not be determined Protection of Wildlife. were categorized as data deficient. Most species were identified based on their morphologi- Frequency of visitation to a roost was determined by cal characteristics. For species that were ambiguous we interviewing elderly residents, wherever possible farmers carried out DNA-based phylogenetic analysis of one who spent considerable time working outside throughout 3-mm diameter biopsy punch from the wing-membrane © 2013 Fauna & Flora International, Oryx, 47(4), 526–531 Downloaded from https://www.cambridge.org/core. IP address: 170.106.35.229, on 28 Sep 2021 at 08:15:11, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605311001505 528 J. Luo et al. FIG. 2 The number of roosts (see Fig. 1 for locations) in the FIG. 3 The main human activities observed at the sites of the 225 subterranean sites located and surveyed that contained from 225 1 0 .9 bat roosts surveyed (Fig.
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