Biological Conservation 182 (2015) 72–86
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Biological Conservation
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An assessment of South China tiger reintroduction potential in Hupingshan and Houhe National Nature Reserves, China ⇑ Yiyuan Qin a,b, Philip J. Nyhus a, , Courtney L. Larson a,g, Charles J.W. Carroll a,g, Jeff Muntifering c, Thomas D. Dahmer d, Lu Jun e, Ronald L. Tilson f a Environmental Studies Program, Colby College, Waterville, ME 04901, USA b Yale School of Forestry and Environmental Studies, New Haven, CT, USA c Department of Conservation, Minnesota Zoo, 13000 Zoo Blvd., Apple Valley, MN 55124, USA d Ecosystems, Ltd., Unit B13, 12/F Block 2, Yautong Ind. City, 17 KoFai Road, Yau Tong, Kowloon, Hong Kong e National Wildlife Research and Development Center, State Forestry Administration, People’s Republic of China f Minnesota Zoo Foundation, 13000 Zoo Blvd., Apple Valley, MN 55124, USA g Graduate Degree Program in Ecology, Colorado State University, Fort Collins, CO 80523, USA article info abstract
Article history: Human-caused biodiversity loss is a global problem, large carnivores are particularly threatened, and the Received 11 June 2014 tiger (Panthera tigris) is among the world’s most endangered large carnivores. The South China tiger Received in revised form 20 October 2014 (Panthera tigris amoyensis) is the most critically endangered tiger subspecies and is considered function- Accepted 28 October 2014 ally extinct in the wild. The government of China has expressed its intent to reintroduce a small popula- Available online 12 December 2014 tion of South China tigers into a portion of their historic range as part of a larger goal to recover wild tiger populations in China. This would be the world’s first major tiger reintroduction program. A free-ranging Keywords: population of 15–20 tigers living in a minimum of 1000 km2 of habitat was identified as a target. We Panthera tigris amoyensis assessed summer and winter habitat suitability of two critical prey species, wild boar (Sus scrofa) and Sika Reintroduction Restoration deer (Cervus nippon), using GIS spatial models to evaluate the potential for tiger reintroduction in one 2 Conservation likely candidate site, the 1100 km Hupingshan–Houhe National Nature Reserve complex in Hunan China and Hubei Provinces, China. Our preliminary analysis estimates that for wild boar, potential summer Habitat and winter habitat availability is 372–714 km2 and 256–690 km2, respectively, whereas for Sika deer, Wild boar Sus scrofa potential summer and winter habitat availability is 443–747 km2 and 257–734 km2, respectively. Our Sika deer Cervus nippon model identifies potential priority areas for release and restoration of prey between 195 and 790 km2 GIS with a carrying capacity of 596–2409 wild boar and 468–1929 Sika deer. Our analysis suggests that Hupingshan–Houhe could support a small population of 2–9 tigers at a density of 1.1–1.2 tigers/ 100 km2 following prey and habitat restorations. Thus, current habitat quality and area would fall short of the target recovery goal. We identify major challenges facing a potential tiger reintroduction project and conclude that restoring the habitat and prey base, addressing concerns of local people, and enhancing coordination across park boundaries are significant challenges to meeting the broader goals of supporting a reintroduced wild tiger population. Tiger range states have committed to doubling the world’s wild tigers by 2022. The results of this study have implications for China’s commitment to this goal and for the future of tiger and other large carnivore reintroduction efforts in Asia and globally. Ó 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http:// creativecommons.org/licenses/by/3.0/).
1. Introduction Marco et al., 2014; Ripple et al., 2014), and the tiger (Panthera tigris) is among the world’s most endangered large carnivores Human-caused biodiversity loss is a global problem that (Tilson and Nyhus, 2010). extends across taxonomic groups and geographic regions (Dirzo The South China tiger (Panthera tigris amoyensis) is a tiger sub- et al., 2014). Large carnivores are particularly threatened (Di species native to China (Nyhus, 2008) that is considered likely extinct in the wild (Tilson et al., 2004). Numbering more than 4000 as recently as the early 1950s, the South China tiger popula- ⇑ Corresponding author at: Environmental Studies Program, Colby College, 5358 tion in China suffered dramatic declines in the past century due to Mayflower Hill, Waterville, ME 04901 USA. Tel.: +1 207 859 5358; fax: +1 207 859 5229. government eradication, habitat loss, unregulated hunting, and E-mail address: [email protected] (P.J. Nyhus). human encroachment into tiger habitat (IUCN, 2011; Tilson et al., http://dx.doi.org/10.1016/j.biocon.2014.10.036 0006-3207/Ó 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/). Y. Qin et al. / Biological Conservation 182 (2015) 72–86 73
2004). It is now the most critically endangered of all tiger subspe- to guide tiger restoration efforts, particularly since historic knowl- cies (IUCN, 2011). edge of tiger habitat use, movement patterns, and diets in this area The government of China, together with the leaders of tiger is limited. Important tiger prey species include forest and grassland range countries, recently declared a goal to double the world’s wild ungulates, ranging from small deer such as barking deer (Muntia- tiger population by 2022 (Global Tiger Summit, 2010; cus muntjak) (20 kg) and wild boar (Sus scrofa) (30–40 kg) to large Wikramanayake et al., 2009). Due to the growing awareness of animals like water buffalo (Bubalus bubalis) (160–400 kg) and sam- the importance of tiger reintroduction as one strategy to support bar (Cervus unicolor) (185–260 kg) (Karanth et al., 2004; Smith and tiger recovery goals (Driscoll et al., 2012; Tilson et al., 2010), Chi- Xie, 2008; Sunquist, 2010). Tiger predation is non-random; tigers nese authorities and international organizations are seeking to select for medium to large-size prey, and only switch to smaller identify one or more existing protected areas of sufficient size prey when critical prey species are non-existent or at extremely within the historical range of South China tigers to support wild low densities (Biswas and Sankar, 2002; Karanth and Sunquist, tiger populations (State Forestry Administration of China, 2010; 1995; Sunquist, 2010, 1981). Tilson et al., 2010). This would be the world’s first large-scale rein- In this study we used spatial Habitat Suitability Index (HSI) troduction of captive tigers back to the wild. models to demonstrate how estimates of prey distribution and Predator reintroductions can enhance conservation by increas- abundance can inform large carnivore restoration. Our specific ing abundance of the target species and other species that share objectives were to identify: (1) the amount of suitable habitat these habitats (Deinet et al., 2013). Notable recent examples of available for tigers and two prey species in the Hupingshan–Houhe reintroductions that led to recovery of extirpated populations National Nature Reserve complex in China, (2) the approximate include wolves in the western United States (Carroll et al., 2006) prey biomass the two reserves could support, and (3) the sizes and Eurasian Lynx in Europe (Deinet et al., 2013). Effective reintro- and configurations of potential core areas that could support initial ductions can have ecosystem-wide benefits by restoring historic release and restoration of both tigers and their prey. species interactions, including trophic cascades (Ripple et al., This effort was part of a larger goal to evaluate the feasibility of 2014). a South China tiger reintroduction program. As field data for wild Since 1994, the Chinese Association of Zoological Gardens South China tiger and prey populations in Hupingshan–Houhe (CAZG) has been managing the remaining captive South China NNR are essentially non-existent, our habitat suitability assess- tigers (Wang et al., 1995). As of October 2011, there were 108 cap- ment was developed using Geographic Information Systems (GIS) tive South China tigers descended from the small founding popula- based on literature reviews, preliminary field work, and expert tion of six individuals captured between 1958 and 1960 (Tilson opinion. Our spatial models provide a preliminary scientific assess- et al., 1997; Traylor-Holzer et al., 2010). However, these remaining ment and reference for habitat evaluation, site selection, and con- South China tigers face significant challenges to remain viable, servation planning for a potential South China tiger reintroduction including relatively low reproduction rates and low genetic varia- in the Hupingshan–Houhe NNR complex. We conclude with a dis- tion (Traylor-Holzer et al., 2010; Yin and Traylor-Holzer, 2011). The cussion of key management issues that address potential ecologi- organization Save China’s Tigers, with the support of the State For- cal, landscape, genetic, and institutional challenges facing a tiger estry Administration of China (SFA), relocated five of these captive reintroduction program. The results of this study have implications tigers to a private captive facility in South Africa to create a founder for other tiger and large carnivore reintroduction efforts in Asia stock for possible future reintroduction of tigers back into the wild and globally. in China (Tilson et al., 2010). As of October 2011, there were 12 liv- ing individuals (four of the original tigers and eight of their off- spring) in South Africa (Yin and Traylor-Holzer, 2011). 2. Methods International tiger experts and the IUCN Cat Specialist Group have proposed a minimum goal for a free-ranging South China 2.1. Study area tiger population by establishing at least three populations, each consisting of 15–20 tigers living in a minimum of 1000 km2 of nat- The Hupingshan–Houhe National Nature Reserve complex con- ural habitat within the historic range of the subspecies sists of two adjacent NNRs located in south-central China (longi- (Breitenmoser et al., 2006). Hupingshan–Houhe National Nature tude 110°20 N – 110°590 N, latitude 29°580 E–30°100 E). Reserve (NNR) complex was identified as the largest and possibly Hupingshan NNR is situated along the northern border of Hunan the most suitable location to support a small population of wild Province adjacent to Houhe NNR in southern Hubei Province tigers (Tilson et al., 2004, 2010). With a total area of 1100 km2 (Fig. 1). Covering nearly 1100 km2, Hupingshan–Houhe is home the reserve complex is larger than 21 other areas identified as to some of China’s most threatened plant and animal species and potential high priority tiger landscapes across Asia (Sanderson occurs in the historic range of the South China tiger (Dahmer et al., 2010). The most recent confirmed records of wild South et al., 2014; Houhe, 2004; Hupingshan, 2004). China tigers in this protected area complex were documented over Hupingshan–Houhe has an annual average temperature of 9.2 ° two decades ago (Koehler, 1991), and protected area staff and vil- C, annual average rainfall of 1900 mm, typically experiences hot lagers also reported visual sightings and anecdotal evidence from and wet summers and cold winters, and supports subtropical ever- the 1970s and the 1980s. green and deciduous mixed forests (Houhe, 2004; Hupingshan, Large carnivores like tigers are often difficult to study in for- 2004). Located in the transition region between the Guizhou Pla- ested environments because of their low population densities, teau and hilly areas in southeastern China, Hupingshan–Houhe is large home ranges, and cryptic behavior. This problem is magnified topographically heterogeneous, including high elevations, deep when the target species is extinct in the wild. Consequently, one ravines, and narrow valleys (Houhe, 2004; Hupingshan, 2004; Li means of addressing this is to examine prey populations. The liter- et al., 2005; Liu and Pang, 2005; Qin et al., 2006). ature documents a strong, positive correlation between tiger abun- The local human population within the protected area complex dance and prey availability (Karanth et al., 2004; Karanth and Stith, was estimated to exceed 30,000 in 2002 (27.3 people/km2); how- 1999; Karanth and Sunquist, 1995; Sunquist, 2010) and highly cor- ever, this estimate is likely unreliable because some residents related activity patterns between tigers and tiger prey (Karanth who emigrated from this area to urban areas are still registered and Sunquist, 2000; Sunquist, 1981). Therefore, an assessment of as living in this area (Houhe, 2004; Hupingshan, 2004). The habitat suitability of tiger prey may serve as a reasonable proxy population is characterized by a low annual per capita income 74 Y. Qin et al. / Biological Conservation 182 (2015) 72–86
Fig. 1. Geographic features of Hupingshan–Houhe National Nature Reserve complex, China. and a high reliance on farming and livestock husbandry. Limited least nine potential prey species may have lived in Hupingshan– industry in the area includes coal and phosphate mining. Tourism Houhe historically, and camera trap studies (Dahmer et al., 2004; is a small but growing economic activity. Key biodiversity threats Tilson et al., 2004) and a 2010 line transect survey (Lou et al., have been identified, including: forest fires, poaching (hunting is 2011) confirmed the presence of at least six prey species (Table 1). not legal), livestock grazing, illegal logging, rapid and unregulated In addition to density, ungulate prey size and biomass are often development from urban sprawl, road construction, mines, and keys to survival and reproduction in wild tiger populations because factories (Dahmer et al., 2014; Houhe, 2004; Hupingshan, 2004). tigers select for large-size prey with a mean weight around 91.5 kg (Karanth and Stith, 1999; Karanth and Sunquist, 1995, 2000; 2.2. Habitat Suitability Index (HSI) Miquelle et al., 1996; Sunquist, 1981). Information on the size, con- servation status, and estimated current density of possible prey Widely used in ecological assessment and conservation plan- species is summarized in Table 1. Chinese serow (Capricornis mil- ning, HSI models incorporate expert opinion and/or ecological needwardsii), wild boar (Sus scrofa), and Sika deer (Cervus nippon) studies to estimate habitat quality using factors, such as land cover are among the relatively large prey species found in Hupingshan and elevation, considered important for the presence or abundance (Table 1). Wild boar and Sika deer were selected as model prey spe- of a target species (Elith and Burgman, 2003; Kliskey et al., 1999; cies based on expert opinion and lack of field data on Chinese Lopez-Lopez et al., 2007; Luan et al., 2011; Store and Kangas, serow (Tilson et al., 2008). Potential suitable habitat for these 2001), especially when species distribution data are lacking two species was modeled in GIS to estimate potential prey densi- (Burgman et al., 2001; Downs et al., 2008; Smith et al., 2007). Vari- ties and thus possible tiger abundance. ables can be scaled to a single standard to create a relative measure of habitat suitability that is comparable across locations (Brooks, 2.2.2. Prey habitat and area requirements 1997; Elith and Burgman, 2003). Each variable in an HSI is repre- 2.2.2.1. Wild boar. Wild boar are widely distributed across Europe, sented using a single suitability index (SI) linked by additive, mul- North Africa, Southeast Asia, Japan, and China, except for dry tiplicative, or logical functions that can best reflect relationships deserts and high plateaus (Leaper et al., 1999; Smith and Xie, among the variables (Burgman et al., 2001). 2008). Wild boar are considered agricultural pests in some areas Since systematic field studies on ungulates in Hupingshan– (Geisser and Reyer, 2004). Habitat use by wild boar is determined Houhe are lacking, we used a comprehensive review of available in part by food availability, vegetation community, cover from pre- literature and expert opinion to create HSI models for two tiger dators, slope, aspect, elevation, distance to water, and weather prey species. The models identify suitable habitat patches and esti- conditions (Baber and Coblentz, 1986; Leaper et al., 1999). mate potential carrying capacity for the two species using variables Wild boar are omnivorous, but plant matter is predominant in deemed significant to their habitat requirements as well as prox- their diet, while crops and high energy food are highly preferred imity to human impacts. Parameters were estimated from research (Herrero et al., 2006; Leaper et al., 1999). Wild boar prefer but on prey populations in other regions, while adjusting for climate, are not restricted to natural woodlands for shelter and food sources topography, and vegetation features of Hupingshan–Houhe. (Leaper et al., 1999; Smith and Xie, 2008). Pinewoods, mixed woodland, scrub, and grasslands provide alternative food 2.2.1. Model prey species selection resources. These habitat types, however, offer suboptimal shelter Forest and grassland ungulates make up the bulk of a tiger’s diet (Leaper et al., 1999; Thurfjell et al., 2009). Forest edges and spar- (Miquelle et al., 1996; Smith and Xie, 2008; Sunquist, 2010). At sely populated areas are also preferred because they provide more Y. Qin et al. / Biological Conservation 182 (2015) 72–86 75
Table 1 Possible prey species historically present in the Hupingshan–Houhe National Nature Reserve Complex. A survey using line transects estimated current density and total number for some species in the Houhe NNR. VU – vulnerable, EN – endangered, LC – least concern.
Prey speciesa,d Mean weight (kg)a Conservation statusb Density (number) in Houhe NNRc Chinese serow* (Capricornis milneedwardsii) 85–140 VU – Chinese water deer (Hydropotes inermis) 14–17 VU – Forest musk deer* (Moschus berezovskii) 6–9 EN – Long-tailed goral (Naemorhedus caudatus) 32–42 VU 2.1 ± 0.1/km2 (80 ± 4) Reeve’s muntjac (Muntiacus reevesi) 11–16 VU 5.6 ± 0.1/km2 (214 ± 6) Siberian roe (Capreolus pygargus) 20–40 VU – Sika deer (Cervus nippon) 40–150 EN – Tufted deer* (Elaphodus cephalophus) 15–28 VU 5.8 ± 0.2/km2 (222 ± 6) Wild boar* (Sus scrofa) 50–200 LC 7.9 ± 0.3/km2 (302 ± 11)
a Smith and Xie (2008). b Wang and Xie (2004), Smith and Xie (2008). c Line transect method, January–March, 2010 (Lou et al., 2011). d (*) Presence, camera trap study, 2001 (Dahmer et al., 2004). opportunities for food and shelter (Honda, 2009; Thurfjell et al., Ono, 1994). The distribution of Sika deer is also limited by climate, 2009). particularly snow depth, as populations tend to descend to lower Wild boar favor lower elevations and gentle slopes, while in elevations in winter before returning to higher elevations in spring warm, dry regions they avoid south slopes where less grass and (Igota et al., 2004; Smith and Xie, 2008). In a study in Taohongling forbs grow (Baber and Coblentz, 1986; Honda, 2009). In Huping- Nature Reserve, Jiangxi Province, China, Sika deer showed no selec- shan–Houhe, wild boar were found at elevations as high as tion for aspect, but preferred habitat with slopes between 15° and 1400 m (Dahmer et al., 2004). They select areas with snow depth 45° (Liu, 2007). Additionally, Sika deer prefer habitat where water of less than 40–50 cm because snow hinders their movement sources are within 100–400 m (Jiang and Li, 2009). (Honda, 2009) and prefer proximity to water for bathing, resting, The home range of Sika deer ranges from 0.2 to 0.6 km2 in Boso reproduction, and rearing of young (Baber and Coblentz, 1986; Peninsula, Japan, while density ranges from the historical record of Fernandez-Llario, 2004; Leaper et al., 1999; Thurfjell et al., 2009). 3.5–4.5/km2 in southern China to 50/km2 in Northern Japan (Ito, Baber and Coblentz (1986) found in California, USA, that wild boar 2009; Jiang and Li, 2009; Miyashita et al., 2008, 2007; Takada use habitat within 330–370 m to water sources. et al., 2002). A summary of density estimates for Sika deer from The home range of wild boar ranges from 0.7 to 24 km2 for various study sites is listed in Table 2. Home range, density, and females and 1.4–35 km2 for males, while density ranges from 2.6 habitat selection of Sika deer are highly correlated with seasonali- per km2 to 15 per km2. A summary of different density estimates ty. In the summer, the Sika deer home range is generally smaller for wild boar from various relevant study sites is listed in Table 2. and thus deer are more clustered than during the winter (Maeji Additionally, wild boar has been found to migrate from high et al., 1999; Miyashita et al., 2008). (>1000 m) to low (<1000 m) elevation in winter (Andrzejewski and Jezierski 1978; Singer et al., 1981). 2.2.3. Model specifications and data preparation Habitat requirement variables used in our models included: 2.2.2.2. Sika deer. Sika deer are widespread across eastern China land cover (LC), elevation (ELEV), slope (SLP), distance to water and also found in southeastern Siberia, Japan, and Korea (Smith (DW), and distance to forest edge (DFE). Disturbance is represented and Xie, 2008). Habitat selection by Sika deer also depend on veg- by distance to areas of potential human impacts (DD), including etation type, food and water availability, shelter, and snow depth agriculture, roads, and urban centers. Because these HSI variables (Honda, 2009; Jiang and Li, 2009). are synergistic rather than cumulative, they were linked using a Sika deer forage in grass, shrub, shrub-meadow, and broad- multiplicative function (Brown et al., 2000; Burgman et al., 2001; leaved forests and feed on grass, browse, and occasionally on fruit Williams et al., 2008). In summary, the HSI was a geometric mean (Jiang and Li, 2009; Smith and Xie, 2008; Yokoyama, 2009). Sika of the six habitat variables using the following formula: deer will use agricultural fields adjacent to forest edges but avoid = HSI ¼ðDD LC ELEV SLP DW DFEÞ1 6 densely populated urban areas (Honda, 2009; Miyashita et al., 2008). Data were obtained from NASA’s Shuttle Radar Topography In southern China, Sika deer usually live in mountainous habitat Mission (SRTM), Landsat satellite imagery, GIS data obtained from at low elevations (300–800 m), but can range to over 2000 m in Chinese authorities, and data we digitized manually (Table 3). western China (Jiang and Li, 2009; Koda et al., 2008; Koga and ArcGIS 10 (ESRI, Inc.) was used to process and combine thematic
Table 2 Wild boar and Sika deer density estimates from selected locations.
Density (per km2) Location References Wild boar 2.6 Pench National Park, India Biswas and Sankar (2002), Sunquist (2010) 4.4 Bardia National Park, Nepal Sunquist (2010) 4.4–6.1 Sumatra, Indonesia O’Brien et al. (2003) 7.9 Houhe NNR, China Lou et al. (2011) 15.0 South Carolina, USA Saunders and McLeod (1999) Sika deer 0.5–0.7 Korea McCullough (2009) 3.5–4.5 Ningguo, China Jiang and Li (2009) 8.6 Lazovsky reserve, Russia Voloshina and Myslenkov (2009) 27.6 Taiwan Pei (2009) 50.0 Kinkazan Island, Japan Ito (2009), McCullough (2009) 76 Y. Qin et al. / Biological Conservation 182 (2015) 72–86 layers. All layers were projected into Universal Transverse Merca- divide the forest, shrub/scrub, grassland, and barren/minimal veg- tor zone 49 N using the WGS84 datum, and all raster layers were etation classes into either agriculture or shrub/grass classes. resampled to a cell size of 28.5 28.5 m2, the native size of the All parameters were constructed on a scale from 0 to 10. Defini- Landsat satellite imagery. tions of SI ranges were adapted from other HSI studies and stan- Where the original SRTM elevation data included significant dardized (Brown et al., 2000; Burgman et al., 2001)(Table 4). SI data gaps, we carried out our own interpolation by kriging, using value estimations used in this study linked habitat suitability to digitized contour lines obtained from China’s State Forestry population abundance as well as fecundity and survival. A high Administration, and GPS elevation points. We derived slope from SI value indicates high relative abundance or density and possibly the original Digital Elevation Model (DEM) for all intact areas high fecundities and survivorships (Burgman et al., 2001). and used the modified SRTM elevation layer for the large interpo- To account for uncertainties in habitat requirement parameter- lated areas. We created a Normalized Difference Vegetation Index izations in the model, we created three scenarios (high – H, mid – (NDVI) using imagery from the Landsat Enhanced Thematic M, and low – L) of suitability indices of habitat requirement for Mapper (ETM+) sensor to assess photosynthetic activity (United each species (Burgman et al., 2001). We created one scenario for States Geological Survey, 2008). distance to disturbance (DD). Since habitat selection of both spe- The land cover data layers were obtained from MacDonald cies varies seasonally, particularly with elevation change, summer Dettwiler and Associates (MDA) federal (MDA Federal, 2008) and (S) and winter (W) scenarios were also constructed with different are based on a 2000 Landsat ETM + image. Land cover classes elevation parameterizations to accommodate such potential varia- located in the study area include deciduous forest, evergreen for- tions. Six HSI scenarios in total were created for each species: three est, shrub/scrub, grassland, barren/minimal vegetation, urban/ each for summer and winter. built-up, agriculture (general), agriculture (rice/paddy), wetland, Categorical values were assigned for variables LC, ELEV, and SLP. and water. However, based on comparison to ground truthing A summary of suitability indices is presented for wild boar (Table 5) GPS field data points from the Hupingshan–Houhe study area in and for Sika deer (Table 6). We used continuous linear functions 2007, some areas originally classified as natural vegetation (e.g., rather than categorical values to convert DW, DFE, and DD into shrub/scrub, grassland, and barren/minimal vegetation) are actu- suitability index values for both species. For DW, we expect that ally agricultural areas. Additionally, this classification scheme distances closer than 400 m are optimal, with suitability declining failed to identify agricultural areas alongside rivers and roads. at greater distances (Fig. 2). Functions used to convert DFE to SI val- To resolve these overestimations of potential habitat, we used ues were based on species requirements for foraging and shelter as NDVI values to differentiate natural vegetation from agriculture. well as daily movement distance. Negative values for DFE repre- We gathered ground control points in the field using GPS in 2007 sent areas within the forest and positive values represent areas and compared the relative reflectance patterns of known agricul- outside the forest. We expect that suitability for prey species tural areas from those with natural vegetation. The mean NDVI would be high to optimal in areas inside the forest and at the forest value of the agriculture points (0.102 ± 0.113) was significantly dif- edge, and would decline steeply just outside the forest (<200 m), at ferent than that of the natural vegetation points (0.423 ± 0.083) which point suitability would continue to decline gradually (Fig. 3). (Mann–Whitney U-test, n = 52, p < .001). We then derived a thresh- We assumed a positive correlation between DD and suitability old value of 0.275 to divide the shrub/scrub, grassland, and barren/ until 1000 m or greater, at which point habitat is optimal (Fig. 4). minimal vegetation land cover classes into new agriculture or Distances were obtained using euclidean distance. Agriculture, shrub/grassland classes, while keeping the original forest, urban/ grassland/shrub, forest, and urban center land cover classes were developed, wetland, water, and agriculture land cover classes extracted from the land cover data. Inside and outside distances intact. We also created 100 m buffers along both sides of all roads to forest edges – borders between forest and shrub/grassland and and rivers, within which we used the above NDVI thresholds to agriculture – were derived by first generalizing each category from
Table 3 Sources for spatial data used in the habitat suitability analysis for wild boar and Sika deer in Hupingshan–Houhe.
Model input Source Elevation NASA Shuttle Radar Topography Mission (SRTM) Digital Elevation Model Version 3 (2006); elevation contour lines for interpolation from Chinese Academy of Forestry, provided by State Forestry Administration of China (2008) Slope Derived from elevation Land cover MDA Federal EarthSat GeoCover LC 2000 Normalized Difference Vegetation Landsat Enhanced Thematic Mapper (2002, 2008) Index (NDVI) Roads Combination of GPS data from Nyhus (2008) and digitized data from maps provided by State Forestry Administration of China (2008) Water Digitized from maps provided by State Forestry Administration of China (2008) Reserve boundaries Digitized from Hunan Hupingshan National Nature Reserve Management Plan from the Administration of Hunan Hupingshan National Nature Reserve (2004)
Table 4 Definitions of suitability index values used in the habitat suitability analysis for wild boar and Sika deer in Hupingshan–Houhe National Nature Reserve complex.
Suitability index Description of habitat use 0–2 Not suitable: little or no occurrence in field studies; mortality may occur; active avoidance in field studies 2.01–4 Least suitable: rare occurrence or very low density in field studies 4.01–6 Moderately suitable: low occurrence or density in field studies 6.01–8 Highly suitable: average occurrence or density in field studies 8.01–10 Most suitable: high density or relative abundance in field studies; high growth potential; active preference in field studies Y. Qin et al. / Biological Conservation 182 (2015) 72–86 77
Table 5 Suitability index values, assumptions, and relevant references for habitat type, slope, and elevation requirement for wild boar (Sus scrofa) in Hupingshan–Houhe National Nature Reserve complex.
Variable Suitability index Assumption References High Medium Low Habitat type Forests are optimal habitat, providing food and shelter; Baber and Coblentz (1986), Leaper et al. (1999), Fernandez Forest 10 10 10 agriculture lands and shrub/grassland provide alternative food et al. (2006), Herrero et al. (2006), Smith and Xie (2008), Agriculture 8 6 4 sources, but shelter is suboptimal Honda (2009), Thurfjell et al. (2009) Shrub/ 88 6 grassland Urban 00 0 built-up Slope (°) Gentle slopes are preferred for the ease of movement Geisser and Reyer (2004), Honda (2009) 0–15 10 10 10 15–30 8 8 8 30–45 6 4 2 >45 0 0 0 Summer Lower elevations are preferred; presence was recorded in areas Baber and Coblentz (1986), Leaper et al. (1999), Dahmer elevation above 1400 m; vegetation structure shifts around 1800 m; et al. (2004), Honda (2009) (m) winter migration to low (<1000 m) elevation ranges occurs as <1500 10 10 10 snow depth restricts movement 1500– 86 4 1800 >1800 6 4 2 Winter elevation (m) <1000 10 10 10 1000–1800 8 6 4 >1800 6 4 2
Table 6 Suitability index values, assumptions, and relevant references for habitat type, slope, and elevation requirement for Sika deer (Cervus nippon) in Hupingshan–Houhe National Nature Reserve complex.
Variable Suitability index Assumption References High Medium Low Habitat type Forests and shrub/grass lands are both optimal habitat for Borkowski and Furubayashi (1998), Maeji et al. (1999), Koda Forest 10 10 10 food and foraging; agricultural fields provide high amounts et al. (2008), Miyashita et al. (2008), Smith and Xie (2008), Agriculture 8 6 4 of plan material Honda (2009), Jiang and Li (2009), Pei (2009), Yokoyama Shrub/ 10 10 10 (2009) grassland Urban 00 0 built-up Slope (°) Gentler slope preferred, especially between 15° and 45° Maeji et al. (1999), Liu (2007), Honda (2009), Jiang and Li 0–15 10 10 10 (2009) 15–30 10 10 10 30–45 8 6 4 >45 0 0 0 Summer Usually found in mountainous habitat at relatively low Koga and Ono (1994), Maeji et al. (1999), Igota et al. (2004), elevation elevation of 300–800 m; winter migration to lower Koda et al. (2008), Smith and Xie (2008), Jiang and Li (2009), (m) elevation occurs as snow depth restricts movement Takatsuki (2009) <1000 10 10 10 1000–1800 8 6 4 >1800 6 4 2 Winter elevation (m) <800 10 10 10 800–1500 8 6 4 >1500 6 4 2
land cover data and then combining reclassifications of the Euclid- (HSIPrey). Six scenarios of HSIPrey were created using corresponding ean distances. Finally, HSI results were reclassified into five catego- HSIWB and HSISD scenarios. To simplify the analysis we assumed ries, ranging from 0–2 (not suitable) to 8.01–10 (most suitable) in complete niche differentiation and no density dependent mortality accordance with the SI definitions (Table 4). feedbacks between these two species. Both these assumptions may lead to an overestimation of suitable habitat and potential prey 2.2.4. Potential priority release sites and restoration areas density. To identify core areas for possible prey release and restoration Studies have shown that the relative importance of prey in the in Hupingshan–Houhe we combined HSI values for both wild boar tiger diet is correlated with prey biomass density and prey size
(HSIWB) and Sika deer (HSISD) to estimate total prey suitability (Table 7)(Biswas and Sankar, 2002; Miquelle et al., 1996; O’Brien 78 Y. Qin et al. / Biological Conservation 182 (2015) 72–86
12 12
a b 10 b-H 10 c-H 8 b-M 8 c-M 6 b-L 6 a c-L
Suitability Index 4
Suitability Index 4
2 2
0 0
100 200 300 400 500 600 700 800 900 0 1000 1100 1200 1300 1400 1500 1600 1700 1800 1900 2000 2500 3000 Distance to water (m) DW - High DW - Mid DW - Low Distance to disturbance (m)
Fig. 2. Functions used to convert distance to water (DW) to suitability index values Fig. 4. Functions used to convert distance to disturbance (DD) to suitability index for wild boar and Sika deer, based on the species habitat requirement and daily values for wild boar and Sika deer. Different sections of the functions were given by 2 movement distance. Three scenarios of parameterization (high – H, mid – M, and (SI = suitability index, d = DD) (a) SI =10 d (d < 1000) and (b) SI =10(d > 1000) low – L) were created to account for uncertainty in the model. Different sections (Thurfjell et al., 2009). of the functions were given by (SI = suitability index, d = DW) (a) SI =1 (d < 400); (b-H) SI = 10.5–1.25 10 3 d (400 < d < 2000); (b-M) SI = 11–2.5 10 3 d 3 1=2 (400 < d < 2000); (b-L) SI = 11.5–3.75 10 d (400 < d < 2000); (c-H) SI =8 HSIPrey ¼ðHSIWB HSISDÞ (d > 2000); (c-M) SI =6 (d > 2000); (c-L) SI =4 (d > 2000) (Agetsuma et al., 2003; Baber and Coblentz, 1986; Jiang and Li, 2009; Leaper et al., 1999; Thurfjell et al., We identified potential priority areas by selecting habitat 2009). patches with HSI values greater than 6 and larger than 1 km2 in size. We identified contiguous patches larger than 20 km2 as potential priority release sites and smaller patches as priority res- 12 toration areas.
a-H 10 2.2.5. Carrying capacity estimation b-M HSI models typically assume a direct linear relationship with a-M 8 carrying capacity, reflected in population density or biomass per b-L unit area (Rand and Newman, 1998). To estimate the carrying a-L capacity of wild boar and Sika deer in Hupingshan–Houhe, we first 6 c extrapolated the number of animals (n) each square pixel (812.25 m2) can potentially support based on its HSI value. For
Suitability Index 4 each pixel (i, j): g ¼ 0:1 HSI d 2 ij d e where d is the average species density estimate (converted to ani- 0 mals per pixel area), i and j reference a specific pixel. Because HSI 0 400 800 200 600 models were constructed based on a 0–10 scale, a coefficient of -800 -400 -600 -200 1000 1600 2000 1200 1400 1800 -2000 -1800 -1000 -1600 -1400 -1200 0.1 was applied to rescale the HSI to 0–1. Carrying capacity was cal- Distance to Forest Edge (m) culated by summing the density values of each pixel in Huping- DFE - High DFE - Mid DFE - Low shan–Houhe: X Fig. 3. Functions used to convert distance to forest edge (DFE) to suitability index K ¼ nij values for wild boar and Sika deer, based on the species habitat requirement and daily movement distance. Three scenarios of parameterization (high – H, mid – M, From the literature (Table 2), we calculated the mean densities and low – L) were created to account for uncertainty in the model. Negative values for wild boar and Sika deer after excluding the two highest density for DFE represent areas within the forest and positive values represent areas outside the forest. Different sections of the functions were given by (SI = suitability index, estimates to reduce the risk of over-estimating potential prey den- 2 d = DFE) (a-H) SI =10(d < 0); (a-M) SI =8(d < 500); (a-L) SI =6(d < 100); (b-M) sity. We used density estimates (d) of 4.6 wild boar per km and 3.6 SI =10+4 10 4d ( 500 < d < 0); (b-L) SI =10+4 10 3 d ( 100 < d < 0); (c) Sika deer per km2. We estimated carrying capacity for both species 3 3 SI = 10–4 10 d (0 < d < 200); (d) SI = 2.25–1.25 10 d (200 < d < 1800); and for the entire Hupingshan–Houhe NNR complex as well as poten- (e) SI =0(d > 1800) (Fernandez et al., 2006; Geisser and Reyer, 2004; Leaper et al., 1999; Thurfjell et al., 2009; Yamada et al., 2003). tial priority areas.
3. Results et al., 2003; Sunquist, 2010). Population densities and mean weights of wild boar and Sika deer indicate a theoretically compa- For each prey species, six different HSI scenarios showed a rable biomass density of the two species, and thus similar potential range of suitable habitats in Hupingshan–Houhe (Figs. 5 and 6). significance in tiger prey selection. Based on the above estimation, For wild boar, mean HSI values ranged from 5.00 to 5.99 for the
HSIPrey was calculated using the following formula to identify sites summer range, and 4.70 to 5.91 for the winter range (Table 8). that meet the needs of both prey species: Our model identified potential habitat (HSI > 6) for the summer Y. Qin et al. / Biological Conservation 182 (2015) 72–86 79
Table 7 Ungulate species biomass density and relative biomass in tiger diet in India, Russian far east, and Indonesia.
Prey (mean weight, Biomass density Relative biomass in tiger diet References kg) (kg/km2) (%) Pench NP, India Wild boar (38) 98.4 7.7 Biswas and Sankar (2002), Sunquist (2010) Sambar (212) 1291.1 29.3 Chital (55) 4441.3 39.6 Muntjac (20) – 2.6 Sikhote-Alin, Russia Wild boar (125) – 24–29.5 Miquelle et al. (1996), Smith and Xie (2008), Takayoshi and Kousaku (2009), Sika deer (45) – 0.5 Sunquist (2010) Red deer (180) – 63.9 Roe deer (30) – 0.9–6.3 Sumatra, Indonesia Wild boar (38) 190.8 –a O’Brien et al. (2003), Smith and Xie (2008), Sunquist (2010) Sambar (212) 206.3 –a Muntjac (20) 67.7 –
a Tiger abundance is found to be significantly correlated with that of the wild boar (p < 0.05) and Sambar (p < 0.1).
Fig. 5. Summer and winter range Habitat Suitability Index (HSI) models of low to high habitat requirement estimations for wild boar in Hupingshan–Houhe National Nature Reserve complex (HSI: 0–2, not suitable; 2.01–4, least suitable; 4.01–6, moderately suitable; 6.01–8, highly suitable; 8.01–10, most suitable). 80 Y. Qin et al. / Biological Conservation 182 (2015) 72–86
Fig. 6. Summer and winter range Habitat Suitability Index (HSI) models of low to high habitat requirement estimations for Sika deer in Hupingshan–Houhe National Nature Reserve complex (HSI: 0–2, not suitable; 2.01–4, least suitable; 4.01–6, moderately suitable; 6.01–8, highly suitable; 8.01–10, most suitable).
Table 8 Mean (standard deviation) and range of Habitat Suitability Index for wild boar and Sika deer in Hupingshan–Houhe National Nature Reserve complex under different scenarios.
High Mid Low Summer Winter Summer Winter Summer Winter Wild boar Mean 5.99 5.91 5.63 5.44 5.00 4.70 (SD) (2.63) (2.59) (2.46) (2.37) (2.23) (2.09) Range 0–10 0–9.8 0–9.9 0–9.5 0–9.7 0–9.0 Sika deer Mean 6.13 6.04 5.69 5.55 5.11 4.91 (SD) (2.68) (2.63) (2.46) (2.40) (2.22) (2.12) Range 0–9.9 0–9.9 0–9.5 0–9.5 0–9.0 0–9.0
range with total sizes varying from 372 to 714 km2 (35–66% of where the total areas ranged from 443 to 747 km2 (41–69%). Suit- total area in the reserve complex), while for the winter range, able winter range for Sika deer also decreased relative to summer the extent of suitable habitat (HSI > 6) ranged from 256 to range. The extent of suitable winter habitats (HSI > 6) ranged from 696 km2 (24–65% of total area) (Fig. 7A). 257 to 734 km2 (24–68%). The percentages of habitat of different For Sika deer, mean HSI values ranged from 5.11 to 6.13 for the qualities are summarized by the five HSI categories in Fig. 7B. summer range, and 4.91 to 6.04 for the winter range (Table 8). Our We identified a range of potential priority areas (HSI > 6, model identified potential habitat (HSI > 6) for the summer range, area > 1 km2)(Fig. 8). The extent of total potential priority area Y. Qin et al. / Biological Conservation 182 (2015) 72–86 81
One of the constraining factors is the complex topography in HS Hupingshan–Houhe, where about 20% of the NNR is above 1500 m and 38% of the area has a slope steeper than 30°. Addition- HW ally, the presence of farmland, towns, and roads in the NNR frag- ments and limits suitable habitat. To meet the needs of tigers MS with large home ranges, major habitat restoration and expansion efforts, such as enhancement of corridors among habitat patches and reforestation of degraded area, would be needed in Huping- MW shan–Houhe. HSI Scenario Tiger territory size is correlated with prey abundance. Increas- LS ing prey density is associated with decreasing tigress territory size up to a prey biomass of 2000 kg/km2, at which point female terri- tory size levels off (Karanth et al., 2004; Smirnov and Miquelle, LW 1999; Sunquist, 2010, 1981). In the Russian Far East, tiger popula- tion densities are low (0.3–0.7 per 100 km2) due to the relatively 0 - 2 2.01 - 4 4.01 - 6 6.01 - 8 8.01 - 10 short growing season and low primary production to support prey (A) species (Karanth et al., 2004). In comparison, in India and Nepal, tiger population densities can exceed 10 tigers per 100 km2 (Karanth et al., 2004; Sunquist, 1981). HS Recent field surveys in Hupingshan–Houhe have reported low wild boar abundance (Dahmer et al., 2004; Lou et al., 2011; HW Tilson et al., 2004). A recent survey of Sika deer found no evidence of this endangered species in the wild in Hunan or Hubei provinces (Jiang and Li, 2009). This deteriorated prey base is a result of illegal MS harvesting, habitat conversion, and logging (Houhe, 2004; Hupingshan, 2004). Low prey biomass can lead to suppressed tiger MW reproduction and survivorship, and hence low tiger population HSIScenario densities (Karanth and Stith, 1999). It has been reported that tigers living on a diet mainly consisting of small prey like barking deer LS (Muntiacus muntjak) may be unable to raise young (Sunquist et al., 1999). The recovery of an assemblage of sufficient large LW ungulate prey species is thus particularly important for tiger conservation. 0 - 2 2.01 - 4 4.01 - 6 6.01 - 8 8.01 - 10 In concurrence with field studies in other regions where tiger (B) and prey densities have been studied, one ad hoc method for esti- mating tiger populations is to assume that an ‘‘average tiger” Fig. 7. Percent of habitat in each Habitat Suitability Index (HSI) category, based on requires 50 ungulate prey animals annually, assuming these are different HSI scenarios for (A) wild boar and (B) Sika deer in Hupingshan–Houhe ungulate prey such as deer and wild boar (Karanth and Nichols, National Nature Reserve complex (scenario: high – H, mid – M, low – L, summer – S, 2010). Using an ecological model that predicts that each year tigers and winter –W). crop about 10% of the available prey population, approximately 500 medium-sized prey animals (i.e., wild boar and deer) are needed to support one tiger (Karanth and Nichols, 2010; Karanth ranged from 195 km2 (18%) (LW) to 709 km2 (66%) (HS) and the et al., 2004). Although the ultimate prey carrying capacity would extent of potential priority release sites ranged from 93 km2 (9%) depend on the nature of the actual species assemblage, considering (LW) to 610 km2 (57%) (HS) (Table 9). wild boar and Sika deer as potential critical prey species for rein- Carrying capacity of prey species in potential priority areas in troduced tigers, our analysis suggest that the potential priority Hupingshan–Houhe was estimated to range ( 25%, +25%) from areas could possibly support 2–9 tigers at a density of 1.1–1.2 2 2 596 (447, 745) (LW) to 2409 (1807, 3011) (HS) for wild boar and tigers per 100 km up to 1.5 tigers per 100 km assuming a 25% from 468 (351, 585) (LW) to 1929 (1447, 2411) (HS) for Sika deer increase in prey abundance. The most optimistic of our carrying (Table 10). For the entire Hupingshan–Houhe area, carrying capac- capacity estimates for wild boar and Sika deer alone would thus ity for wild boar was estimated to range from 2321 (LW) and 2960 fall short of meeting the minimum goal of supporting 15–20 tigers (HS) (Fig. 9A). Estimates of carrying capacity for Sika deer ranged (Fig. 8). Prey population density could be higher if additional spe- from 1895 (LW) to 2370 (HS) (Fig. 9B). cies are available, such as Chinese serow, or if prey species densi- ties were artificially enhanced through supplementation of stock from breeding facilities and with the provision of additional forage 4. Discussion (Tilson et al., 2008). As a result, our estimates of potential tiger abundance are likely conservative. Our analysis identified potential priority areas, ranging from Carrying capacities for wild boar and Sika deer could be con- 195 km2 (18%) (LW) to 709 km2 (66%) (HS), and current potential strained by the fragmented habitat, potential interspecific compe- priority release sites for wild boar and Sika deer from 93 km2 tition, and low quality habitat patches. Another constraint to the (9%) (LW) to 610 km2 (57%) (HS) (Table 9). Although Huping- prey species is the limited extent of suitable lowland in Huping- shan–Houhe is relatively large compared to other protected areas shan–Houhe, as demonstrated in our models in which the area of in south-central China (MacKinnon et al., 1996), the limited extent suitable habitat decreased considerably for the winter scenarios of connected suitable habitat could be a major challenge in meet- for wild boar and Sika deer. ing the tiger reintroduction goals proposed by international tiger The limited extent of suitable habitat and the current low prey experts and the IUCN Cat Specialist Group. density are likely some of the most daunting challenges, but habi- 82 Y. Qin et al. / Biological Conservation 182 (2015) 72–86
Fig. 8. Potential priority areas for prey release and restoration in Hupingshan–Houhe National Nature Reserve complex (HSI: 0–2, not suitable; 2.01–4, least suitable; 4.01–6, moderately suitable; 6.01–8, highly suitable; 8.01–10, most suitable).
Table 9 including reducing illegal harvesting of timber and wildlife, could Size (km2) of potential priority area for prey release and restoration in Hupingshan– have significant positive impacts on the biological diversity in Houhe National Nature Reserve complex under different scenarios. Hupingshan–Houhe and regional biodiversity conservation goals. High Mid Low Summer Winter Summer Winter Summer Winter 4.1. Model limitations and potential improvements Release 610 591 493 447 176 93 Restoration 99 102 120 114 139 102 Uncertainties and errors are inevitable in habitat suitability Total 709 693 613 561 315 195 assessment models. Although HSI models are relatively transpar- ent, some commonly recognized uncertainties and errors in these models include temporal variability, spatial variability, and sys- tat and prey base restoration in Hupingshan–Houhe would also tematic and random measurement errors (Barry and Elith, 2006; likely provide extended benefits to the conservation of biodiversity Burgman et al., 2001; Storch, 2002). in the area. Hupingshan–Houhe is among the most biologically Our prey models were constructed using information sourced diverse forest ecosystems in China, home to at least ten globally from published literature and expert knowledge. Although suitabil- threatened plant and animal species, and is significant as one of ity index values were defined in the study, there is variability in the the last large ecosystems within the historic range of the South information on species habitat preferences. Given the different China tiger (Houhe, 2004; Hupingshan, 2004; Xie et al., 2004). As vegetation types, climates, topographies, and other environmental a result, even if reintroduced tiger populations remained small, factors of the various study locations, uncertainties in setting limits the act of further supporting wildlife protection in these areas, and developing functions for suitability index estimations are Y. Qin et al. / Biological Conservation 182 (2015) 72–86 83
Table 10 Carrying capacity ( 25%, +25%) of wild boar and Sika deer in the potential priority area for prey release and restoration in Hupingshan–Houhe National Nature Reserve complex under different scenarios. Density estimates of 4.6 wild boar per km2 and 3.6 Sika deer per km2 were used.
High Mid Low Summer Winter Summer Winter Summer Winter Wild boar Release 2087 2001 1615 1428 616 289 25% 1565 1501 1211 1071 462 217 +25% 2609 2501 2019 1785 770 361 Restoration 322 330 380 355 369 307 25% 242 248 285 266 277 230 +25% 403 413 475 444 461 384 Total 2409 2331 1995 1783 985 596 25% 1807 1748 1496 1337 739 447 +25% 3011 2914 2494 2229 1231 745 Sika deer Release 1670 1601 1270 1135 478 223 25% 1253 1201 953 851 359 167 +25% 2088 2001 1588 1419 598 279 Restoration 259 266 302 283 290 245 25% 194 200 227 212 218 184 +25% 324 333 378 354 363 306 Total 1929 1867 1572 1418 768 468 25% 1447 1400 1179 1064 576 351 +25% 2411 2334 1965 1773 960 585
inevitable. Limited availability of field data is another constraint. 3500 Some data, including snow depth, that may contribute to better predictions of species movement and habitat selection were not 3000 available for modeling. Improved data on the number and charac- teristics of people living within the reserves would also help better 2500 model potential human–wildlife conflict for management. 2000 We recognize that HSI models include variables that may be correlated and the strength of the correlation varies (Burgman 1500 et al., 2001), but without additional information, we assumed inde- pendence of variables used in our model. Errors in remote sensing
Carrying Capacity 1000 and GIS technologies are also common. For example, misclassifi- cation can cause errors when classifying vegetation cover from 500 satellite data (Shao and Wu, 2008). Finally, our HSI models did 0 not include species population dynamics, i.e., interspecific interac- H, S H, W M, S M, W L, S L, W tions and density-dependent effects such as social behaviors, Scenario which could potentially influence species distribution, movements and ultimately carrying capacity. 2.01 – 4 4.01 – 6 6.01 – 8 8.01 – 10 To improve the reliability of the model, a study of species distri- (A) bution and movement is well warranted. Field surveys will help improve and verify variable parameterization, selection, and assignment of relative importance as well as structure of the equa- 2500 tion that combines SI values into the HSI model.
2000 4.2. Additional considerations and implications
1500 Regardless of the underpinning limitations and uncertainties in the model, suitable areas identified by our HSI models correspond 1000 well with the occurrence of prey species from the 2001 camera trap study, except for the records near major roads (Dahmer
Carrying Capacity et al., 2004, 2014). Our study is not intended to provide a fine- 500 grained analysis, but to evaluate the general suitability of the area as the first attempt to analyze the potential for prey and tiger res- 0 toration efforts in Hupingshan–Houhe. Our methods have implica- H, S H, W M, S M, W L, S L, W tions for other regions under considerations for tiger recovery Scenario efforts where field data are limited. 2.01 – 4 4.01 – 6 6.01 – 8 8.01 – 10 According to the IUCN/SSC reintroduction guidelines, recovery of prey populations at proposed release site(s) should be addressed (B) before any reintroduction could be considered (IUCN/SSC, 1998). Given that tigers are capable of thriving in environments ranging Fig. 9. Carrying capacity estimate of (A) wild boar and (B) Sika deer in Hupingshan– from the temperate forests of the Russian far east to the jungles Houhe National Nature Reserve complex based on different Habitat Suitability Index scenarios. Density estimates of 4.6 wild boar per km2 and 3.6 Sika deer per of Sumatra, Miquelle et al. (1996) have argued that tigers have km2 were used (scenario: high – H, mid – M, low – L, summer – S, and winter –W). few ecological constraints that relate to specific habitat require- 84 Y. Qin et al. / Biological Conservation 182 (2015) 72–86 ments except for the direct influence from the abundance and Our analysis of potential prey and tiger suitability within the composition of prey species. In addition, tigers have also shown 1100 km2 Hupingshan–Houhe NNR complex suggests that the hab- considerable plasticity in predation behavior and relatively quick itat currently available is fragmented and dominated by upland recovery records given favorable conditions (Sunquist et al., forests, steep slopes, agricultural lands, and substantial human 1999). Restoration of prey species could be enhanced from existing populations. At best, this area currently would support only a small wild boar and deer farms in Hunan and Hubei Provinces (Tilson population of 2–9 tigers and would require intensive management et al., 2008). to sustain tigers and prey and to mitigate human–wildlife conflict. Our HSI analysis and prey carrying capacity model estimates A larger tiger population would likely be possible only if more area suggest that the size and habitat quality of Hupingshan–Houhe and in particular more lowland habitat—now largely dominated by are not ideal compared to high priority tiger conservation land- people and agriculture—was available to support a more robust scapes elsewhere in Asia (Sanderson et al., 2006). However, there prey base. At present, it is likely that too many people live within is adequate habitat that could support a small, highly managed the reserve complex to justify a free-ranging population of tigers. population of tigers if prey species were restored to their full At the same time, the area likely represents the largest remain- potential and sufficient lowland areas were made available. Land ing protected area complex within the historic range of South external and adjacent to the two reserves is dominated by people China tigers, and tigers were recorded in the area within the past and agriculture, limiting opportunities for reserve expansion or four decades. Our analysis identifies potential priority restoration any meaningful corridors to other protected areas. A more nuanced areas that would support modest tiger reintroduction and recovery discussion that evaluates additional benefits for both broader bio- goals, assuming appropriate attention to the needs and safety of diversity values and socio-political aspects that might result from local communities as per IUCN reintroduction guidelines (IUCN/ the project’s implementation is thus well warranted. SSC, 1998). Conservation and restoration of former tiger habitat Reintroduction of large carnivores is enormously controversial would meet other biodiversity conservation objectives associated and carries a high risk of failure when the concerns of local people with the high biodiversity value currently represented within are not addressed (Breitenmoser et al., 2001; Jiménez, 2009). For these reserves (Muntifering et al., 2010) and could help catalyze any reintroduction of tigers, a comprehensive assessment of the conservation education and awareness programs and scientific attitudes and needs of local people near possible release sites research that further supports national and global biodiversity would be necessary to ensure protection of villagers and their live- conservation objectives. stock, and a reintroduced population of tigers (IUCN/SSC, 1998). A If free-ranging tigers are ever to return to south-central China, strategy for meaningful local participation and for mitigating con- long-range planning is needed to identify areas that can in the flicts between local people and reintroduced tigers would need to future become sufficiently large, connected, and protected to main- be established. This is especially critical when reintroducing a spe- tain an adequate prey base and to address the needs of local people cies which may prey upon livestock or even people. Given the to sustain a viable population of large carnivores. Large landscape number of people in the area and limited suitable habitat, creating conservation efforts in Europe and North America have shown this barriers such as fences would likely be necessary. Additional con- is possible over time, and China could become a conservation lea- flict prevention and mitigation efforts, such as modifying livestock der in developing this vision in Asia. husbandry practices and establishing effective compensation pro- grams, are used in other areas with high potential for tiger-human Acknowledgements conflict (Nyhus and Tilson, 2010). Organizational issues can exert a significant influence on spe- This research was made possible with support of and through a cies recovery (Breitenmoser et al., 2001; Jiménez, 2009; Reading Memorandum of Understanding between the South China Tiger et al., 1997). Although Hupingshan and Houhe NNRs are spatially Advisory Office and the National Wildlife Research and Develop- contiguous, they adjoin along the Hunan–Hubei provincial bound- ment Center, National Academy of Forestry, State Forestry Admin- ary and have separate, independent management structures: each istration (SFA) of the People’s Republic of China. Numerous reserve has its own park office, directors, staff, and management individuals and organizations supported earlier discussions or field plan. Coordination among authorities across park and provincial work, including: Wang Wei, Director of Forestry, SFA; Wang boundaries is imperative to develop coherent management goals Weisheng, Director, and Ruan Xiangdong, Deputy Director, Wildlife and objectives for habitat restoration and expansion, prey base Management Divisions, SFA; SFA staff and collaborators in Hubei recovery, management of human–wildlife conflict, and ultimately and Hunan Provinces, including Gui Xiaojie, Director of the Nature the survival of free-ranging tiger populations. Conservation Division, Forestry Department of Hunan Province; Finally, the population of captive South China tigers available Wang Guoping, Director, Hunan Forestry Department; the park for reintroduction is small and genetic diversity is a concern directors at Hupingshan and Houhe National Nature Reserves (Traylor-Holzer et al., 2010). At a minimum, intensive genetic and their staff, particularly Tian Shurong; and other collaborators and meta-population management in collaboration with the including Hu Defu and Wang Bin. We thank Tara Harris, Depart- Chinese Association of Zoological Gardens would be needed, and ment of Conservation, Minnesota Zoo, and Kevin Potts for their hybridization with other tiger subspecies might need to be consid- ideas and input. We appreciate the financial and logistical support ered for long-term viability (Qin, 2012). of the Minnesota Zoo Foundation, Colby College, Andrew W. Mel- lon Foundation, the Gary and JoAnn Fink Foundation, Columbus Zoo, Woodland Park Zoo, Ecosystems Ltd., Round River Conserva- 5. Conclusions tion Studies, International Business and Cooperation Agency of the Netherlands, and Gisbert Nollen of International Consultancy The global tiger conservation community and tiger range states Europe. We appreciate support for digitizing and other GIS work have committed to doubling the world’s wild tiger population by by: Rob Mehlich, Jr., Brendan Carrol, Carolyn Hunt, Caitlin Dufraine, 2022. Reintroduction of captive tigers into the wild may be one Greg LaShoto, Katie Renwick, and Noah Teachey. We are particu- important step towards achieving this goal. The Government of larly indebted to co-author and South China Tiger Advisory Office China and international researchers have identified Hupingshan Founder and Director Dr. Ronald Tilson, who passed away unex- and Houhe National Nature Reserves as one potential release site. pectedly before this study was published. Y. Qin et al. / Biological Conservation 182 (2015) 72–86 85
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