- Email: [email protected]
Habitat evaluation and population viability analysis of the last population of cao vit gibbon (Nomascus nasutus): Implications for conservation
Biological Conservation 161 (2013) 39–47
Contents lists available at SciVerse ScienceDirect
Biological Conservation journal homepage: www.elsevier.com/locate/biocon
Habitat evaluation and population viability analysis of the last population of cao vit gibbon (Nomascus nasutus): Implications for conservation Peng-Fei Fan a,1, Guo-Peng Ren b,1, Wei Wang c, Matthew B. Scott a, Chang-Yong Ma a, Han-Lan Fei a, Lin Wang b, Wen Xiao a,⇑, Jian-Guo Zhu b,⇑ a
Institute of Eastern-Himalaya Biodiversity Research, Dali University, Dali, Yunnan 671003, China Ecology, Conservation, and Environment Center (ECEC), Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650223, China c State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences (CRAES), Chaoyang, Beijing 100012, China b
a r t i c l e
i n f o
Article history: Received 9 December 2012 Received in revised form 16 February 2013 Accepted 25 February 2013
Keywords: Cao vit gibbon (Nomascus nasutus) Habitat quality Potential habitats Habitat carrying capacity Conservation suggestions
a b s t r a c t The cao vit gibbon (Nomascus nasutus) is among the most endangered primates in the world. The only surviving population lives in a karst forest patch along the China–Vietnam border. In this study, we used high-resolution satellite images to evaluate the habitat quality of the gibbon in the area immediately surrounding the last population and predict the potential gibbon habitat. We then used Vortex to simulate population responses to changes in the habitat’s carrying capacity. Our results showed the gibbon population is approaching the carrying capacity of their current habitat, and carrying capacity has a significant impact on population changes. Two potential habitats were located in a forest connected to the current habitat by a narrow forest corridor, situated above an underground river. Based on the results, we recommend: (1) prohibiting agriculture and grazing activities within the current gibbon habitat; (2) expanding the Cao Vit Gibbon Conservation Area in order to protect potential cao vit habitats in Vietnam; (3) protecting forest corridor that connect the current cao vit habitat to potential habitats; and (4) rehabilitating the forests currently depauperate of important food species in order to support the expansion of both the gibbon population and the range. This research both provides important insight into sustaining the current gibbon population as well as suggestions for both Vietnamese and Chinese local governments planning habitat restoration at the study site. Ó 2013 Elsevier Ltd. All rights reserved.
1. Introduction The cao vit, or eastern black crested gibbon (Nomascus nasutus) is a Critically Endangered species (IUCN, 2012) with only one known population. Historically, the species was widespread east of the Red River (Hong He) in both southern China and northern Vietnam (Geissmann et al., 2003). By the 1960s the cao vit gibbon was considered extinct (Tan, 1985; Geissmann et al., 2003), but was rediscovered along Vietnam’s nothern border in 2002 (La et al., 2002) and in China in 2006 (Chan et al., 2008). In 2007, a trans-boundary census of the population recorded 18 groups and approximately 110 individuals in the area (Le et al., 2008), making ⇑ Corresponding authors. Addresses: Institute of Eastern-Himalaya Biodiversity Research, Dali University, 2 Hongsheng Road, Dali, Yunnan 671003, China (W. Xiao), Ecology, Conservation, and Environment Center (ECEC), Kunming Institute of Zoology, Chinese Academy of Sciences, 32 Jiaochang Donglu, Kunming, Yunnan 650223, China. Tel. +86 871 65190776 (J.-G. Zhu). E-mail addresses: [email protected] (W. Xiao), [email protected] (J.-G. Zhu). 1 These authors contributed equally to this research. 0006-3207/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biocon.2013.02.014
it the second smallest population of any ape species worldwide after the Hainan gibbon (Zhou et al., 2005). Consequently, the cao vit gibbon has been listed as one of the World’s 25 Most Endangered Primates (Long and Nadler, 2009). To protect the remaining population and its karst forest habitat, the Cao Vit Gibbon Conservation Area in Vietnam and Bangliang Gibbon Nature Reserve in China were established in 2007 and 2009, respectively. Previous interviews with local people indicated that the cao vit gibbon habitat has degraded over time as a result of timber extraction, fuel-wood collection, the making of charcoal, selective logging, and agriculture encroachment (Fan et al., 2011a). While the establishment of the conservation areas has reduced forest degradation, local inhabitants from both countries still plant corn in some of the valleys and some Chinese villagers continue to graze goats inside the Bangliang Nature Reserve. The mean canopy height over the site is 10.5 m, which is the lowest forest canopy height ever reported for gibbon habitat (Fan et al., 2011a). To survive in the degraded karst forest, cao vit gibbons consume nearly half of the tree and liana species recorded (81 of the 159 species) at the site (Fan et al., 2011a). Like all other
40
P.-F. Fan et al. / Biological Conservation 161 (2013) 39–47
gibbons, cao vit gibbons eat fruit when it is available, and shift to a leaf-dominant diet when fruit becomes less available (Fan et al., 2012). They also rest more and sleep huddled together when the temperature cools (Fan et al., 2012). To find sufficient food, cao vit gibbons occupy home ranges (130 ha, Fan et al., 2010) larger than those of other species in south tropical rain forests (on average 40 ha, Bartlett, 2007), but comparable with or smaller than the Nomascus gibbons in the north (N. hainanus: 300–500 ha, Liu et al., 1989; N. concolor: 151 ha, Fan and Jiang, 2008; N. leucogenys: ca. 540 ha, Hu et al., 1990). Based on the estimated ca. 2000 ha of suitable habitat available (Le et al., 2008), the cao vit gibbon population is likely close to its carrying capacity. Remote Sensing (RS) and Geographic Information Systems (GIS) techniques have been widely used to evaluate habitat quality (Hansen et al., 2001; Xiao et al., 2003; Zhang et al., 2010), predict potential habitat (Wang et al., 2008; Zhang et al., 2010), and plan conservation strategies (Maiorano et al., 2006; Zhang et al., 2010). In this study, we aim to: (1) evaluate current habitat quality using RS and GIS techniques; (2) predict potential habitat in surrounding areas and identify some ecological corridors for dispersal; and (3) use a Vortex model to simulate the sensitivity of population dynamics to changes of habitat carrying capacity.
2. Methods 2.1. Study area Gibbons are strict canopy dwellers and cannot disperse beyond rivers, roads and other breaks in the forest canopy. We accordingly focused on the areas immediately surrounding the current cao vit gibbon habitat (22°49–590 N, 106°220 –350 E). Several rivers and paved roads bisect the total research area, which can be divided into five different zones (Fig. 1). Gibbons currently only live in Zone I; however, local people reported knowing of gibbons inhabiting Zone IV before 2000 (Le et al., 2008). Zones I and IV are separated by a river, but the forests are relatively contiguous because some 900 m of the river is underground. 2.2. Forest cover mapping 2.2.1. Classification scheme and ground-truth data collection Land cover in the study area was classified as Forest, Scrub, Shrubland and Developed areas (Table 1). Between July 15 and August 5 2010, 412 land cover polygons in China were classified and delineated on satellite images with the aid of relief maps and a Glo-
Fig. 1. Study area along the China–Vietnam border. The five zones outlines in this study are divided by rivers and roads.
41
P.-F. Fan et al. / Biological Conservation 161 (2013) 39–47 Table 1 Land cover classification scheme. Land cover type
Description
1. Forest 2. Scrub
Some trees >10 m height with a canopy cover P50% Near continuous canopy of tall shrubs and dwarfed/young trees, tree canopy cover comprises <50% Mosaic of shrubs and grasses, trees few or absent Areas of farmland, town, villages, open water and other nonforested land
3. Shrubland 4. Developed
bal Position System (GPS) receiver (Garmin eTrex). Using the same method, 28 land cover polygons were delineated in Vietnam from June 15 to 26 in 2011. Half of these polygons were randomly chosen as validation data, and the remainders as training data for classification. 2.2.2. Remote sensing data Two scenes of Advanced Land Observation Satellite (ALOS) images, one from Panchromatic Remote-sensing Instrument for Stereo Mapping (PRISM, 1 band, resolution = 2.5 m) and the other from Advanced Visible and Near Infrared Radiometer (AVNIR-2, 4 bands, resolution = 10 m), both acquired on November 23, 2009, were used to map forest cover over the study area. After referencing with Google Earth, the ALOS PRISM image was properly geocorrected. We subsequently geo-corrected the AVNIR-2 image band by band to the ALOS PRISM. Afterward, we used a pixel-based fusion method to derive a pan-sharpened image (4 bands, resolution = 2.5 m) from the ALOS AVNIR-2 and PRISM images. UTM coordinates system (Projection: Universal Transverse Mercator, Spheroid: WGS84, Datum: WGS84, Zone: 48N) was used in this study. The remote sensing data processes were conducted using Erdas Imagine (Leica Geosystems Geospatial Imaging, LLC, Norcross, Georgia, US) and R Statistics software. 2.2.3. Land cover mapping Based on the ALOS images and the training data from the field, we produced a preliminary land cover map using the Random Forest classification algorithm (Breiman, 2001). The classification process was implemented using the RandomForest package (Liaw and Wiener, 2002) and Raster package (Hijmans and van Etten, 2011) in R Statistics software (2.1.0, http://www.r-project.org/). Then we aggregated 144 pixels in the preliminary land cover map to one pixel in order to derive a land cover map at 30 m resolution, as 2.5 m resolution was too fine for a land cover map. The accuracy of the 30 m resolution land cover map was evaluated (producer’s accuracy) using validation data obtained from field surveys. 2.2.4. Habitat quality evaluation On the basis of the 2.5 m resolution preliminary land cover map, we calculated the forest pixel percentage as tree cover percentage (%tree) at 30 m resolution. Then, we performed a focal analysis using a 5 by 5 Gaussian filter on the %tree to produce a habitat quality index (hi) able to evaluate the quality of gibbon habitat. The Gaussian filter, defined by Eq. (1), places the heaviest weight on the focal pixel (the pixel having the highest Gaussian value), with the weighting of neighboring pixels varying proportionately with distance from the focal pixel. The hi can be used to evaluate habitat quality for two reasons. First, gibbons only inhabit forests and avoid all other land cover types; second, the possibility of site suitability for gibbons depends not only on the forest cover percent, but also on the cover of the adjacent area, both of which are taken into account in the hi.
0
1 B B2 B The 5 by 5 Gaussian filter ¼ B B3 B @2
1
2 3 2 1 C 3 4 3 2C C 4 5 4 3C C=65 C 3 4 3 2A 1 2 3 2 1
ð1Þ
We then used the hi to evaluate the quality of the gibbon habitat by arbitrarily dividing the study area into the following four types: (a) (b) (c) (d)
high-quality habitat: hi P 80; moderate-quality habitat: 60 6 hi < 80; low-quality habitat: 40 6 hi < 60; non-habitat (not suitable for gibbon): hi < 40.
We tested whether the hi is an accurate measure of habitat quality by using the field data from the extant gibbon population habitat sites, as described in the next section. The trans-boundary survey conducted by Fauna & Flora International (FFI) in September 2007 identified 18 groups using direct observation and listening to gibbon calls on hill tops – a widely used method in gibbon surveys developed in 1987 by Brockelman and Ali, 1987 (Johnson et al., 2005; Buckley et al., 2006; Phoonjampa and Brockelman, 2008; Fan et al., 2011b; Le et al., 2008). FFI directly observed 17 of the 18 gibbon populations and recorded their group compositions (Le et al., 2008). All group locations obtained from direct observations and calls were marked on a topography map (1:50,000), which was used to estimate the centre of each group’s home range (Le et al., 2008). Referencing Appendix 4 in the study done by Le et al. (2008), two of the 17 locations were re-located according to our subsequent long-term field observations. We drawn 8 concentric rings in 200 m intervals around the 17 gibbon locations to cover the range of the current gibbon (Fig. 2). Rings were labelled ring 1–8, from the innermost ring outwards. If the hi is a good index for the habitat quality evaluation, the inner rings should be expected to have a higher hi than the outer rings. We conducted wilcoxon-tests between hi values for all combination of paired rings, and used the Bonferroni method in R 2.1.0 to adjust the p-values.
2.3. Potential habitat prediction To predict potential habitat for the cao vit gibbon, we made three assumptions according to previous research and our knowledge: Assumption 1: Potential habitat should be in close proximity to high-quality habitat patches larger than 100 ha, because the home range size of all Nomascus gibbons (who occupy home ranges of equal or greater size to the cao vit gibbon) in northern areas is larger than 100 ha (Liu et al., 1989; Hu et al., 1990; Fan and Jiang, 2008; Fan et al., 2010). Assumption 2: Gibbons mostly inhabit high-quality habitat, and can move between any two high-quality habitat patches if the distance between them is less than 100 m and the two patches are connected by at least moderate-quality habitat patches. Assumption 3: Gibbons do not live in low-quality habitat or nonhabitat. Based on these assumptions, we used the following steps to predict potential gibbon habitat: Step 1: Select high-quality habitat patches larger than 100 ha as the core habitat. Step 2: Select high-quality habitat patches connected to the core habitat by at most 100 m of moderate-quality habitat as additional patches of core habitat.
42
P.-F. Fan et al. / Biological Conservation 161 (2013) 39–47
Fig. 2. Concentric buffer rings around gibbon group locations to evaluate habitat quality (rings were labeled as ring 1 to ring 8 from inner to outer).
Step 3: Repeat step 2 until no more patches can be added to the core habitat. Step 4: Select moderate-quality habitat connected to high-quality habitat as the marginal habitat. Step 5: Select both the core and marginal habitats as potential habitats for cao vit gibbons.
2.4. Population dynamics and viability analysis (PVA) We used Vortex 9.99 (http://www.vortex9.org/vortex.html) to simulate the population dynamics of the cao vit gibbon over the next 200 years (ca. 6–7 generations) assuming different habitat carrying capacities. Vortex was developed by Lacy (1993) and has been widely used to analyze population viability, including gibbon population viability (Seal, 1994; Fan and Jiang, 2007). Beginning in December 2007, we monitored three Chinese cao vit gibbon groups for at least 7 days each month, recording the data required to model population dynamics (Fan et al., 2010; unpublished data). Over those 5 years, we recorded nine births. The inter-birth interval of the five females who gave birth twice was 34 months. One older female did not give birth during the 5 years. On average, 30% of the adult females (SD = 18.2%) reproduced each year. Mortality of gibbons from age 0 to 1 was 20% (2 deaths out of 10 infants). Mortality of gibbons from age 3–4 was 20% (2 deaths of small juveniles out of 10). Mortality of gibbons at other ages was 0. We assumed that mortality was the same between sexes. Because of the gibbons’ longevity, it was difficult to determine the age at which females and males have their first offspring, as well as the maximum age of reproduction. Brockelman et al. (1998) provide the only known information on wild gibbons, and report that female Hylobates lar has their first offspring at around
10 years of age, and males at around 12 years. In the absence of other data, we used these parameters in our model. We also assumed that the maximum age of reproduction for gibbons is 30 years old (Seal, 1994). The lethal equivalent, a measure of the severity of inbreeding, was set at 3.14; in studying 40 captive vertebrate populations, Ralls et al. (1988) found 3.14 lethal equivalents to be the median value. The average home range size of these three groups was 130 ha (Fan et al., 2010), which 99.8 ha (G1) and 114.2 ha (G4) was used exclusively by a single group (Fei et al., 2012). The average exclusive territory range is 107 ha for G1 and G4. Cao vit gibbons may potentially live in smaller home ranges in well-protected forests, but such data is not available at present. We calculated the carrying capacity by dividing the total habitat area by the average exclusive territory range for one group, and then multiplied by the average group size (6.0, Fan et al., 2010). We assumed no catastrophes, harvest/hunting, supplementation and genetic management in the model. All parameters are summarized in the online Appendix 1.
3. Results 3.1. Forest cover map and accuracies A land cover map of the whole study area was produced on the basis of the ALOS images (Fig. 3). Mapping accuracies of both Forest and Developed areas were satisfied (>0.85), although the accuracies for the Scrub and Shrubland areas were low (Table 2). The lower accuracies for the transitional land cover types between forests and developed areas were due to the confusion of the two land cover types. To correct for this, we combined Scrub and Shrubland
43
P.-F. Fan et al. / Biological Conservation 161 (2013) 39–47
Fig. 3. Classification results of forest map over the study area.
Table 2 Producer’s accuracies of the land cover classification map over study area based on 2009 satellite imageries. Land cover type
Forest Scrub Shrubland Developed Producer’s accuracy
Table 3 The area and patch number of forest at three tier levels in each zone. Zone
Validation data (n = 2353) Forest
Scrub
Shrubland
Developed
875 111 20 0 0.87
22 70 27 0 0.59
16 301 485 61 0.56
0 15 11 339 0.93
into one category in the following analyses. As gibbons do not use either scrub or shrubland, pooling the categories was not expected to influence the results. In total, forests comprised 6600.3 ha of the whole 22,700 ha study area, 93% of which (6144.9 ha) was in Zones I and IV (Table 3, Fig. 3). There were only five forest patches larger than 100 ha with the total area of 5170.2 ha in Zones I and IV (Table 3).
I IV III V II Total
Area of forest patches (patch number) 1.0–9.9 ha
10.0–99.9 ha
>100.0 ha
Total
196.4 (78) 416.8 (173) 166.3 (55) 85.4 (29) 4.7 (2) 914.5 (337)
11.7 (1) 304.8 (13) 178.2 (8) 20.8 (2) 0 515.6 (24)
2835.1 (1) 2335.1 (4) 0 0 0 5170.2 (5)
3043.2 (80) 3101.7 (190) 344.6 (63) 106.2 (31) 4.7 (2) 6600.3 (366)
being close to 600 m (calculated from home range size 130 ha) suggests that more than 90% of a groups home range is high-quality forest and that the hi index is a reasonable assessment of habitat quality for the cao vit gibbon. There are still 3951.1 ha of high-quality habitat and 1409.6 ha of moderate-quality habitat within Zones I and IV (Fig. 4, Table 4). Only four patches of high-quality habitat are both larger than 100 ha and located in Zones I and IV (Table 4).
3.2. Habitat quality 3.3. Potential habitat Gibbon habitat quality was evaluated using the hi index. Our results showed that habitat quality decreased significantly as distance from the nearest gibbon location buffer ring increased (p < 0.001), except habitat quality within the first two rings (p = 0.641) and last two rings (p = 0.152) did not vary significantly. According to our definition of high-quality habitat (hi P 80), more than 97% of the first ring is high-quality habitat, and more than 95%, 90%, 74%, 50% of the successive four rings are high-quality habitat, respectively. The home range radius of a single group
The total potential habitat area contains 3401.6 ha of high-quality habitat (Table 5) and 1125.1 ha of moderate-quality habitat. We divided them into three conservation priority areas using relatively compacted high-quality habitats as boundaries (Fig. 5, online Appendix 2). The first conservation priority area is the only area currently inhabited by gibbons, comprising a total 2216.7 ha (79.9%) of high-quality habitat. The second priority area is connected by a narrow strip (width = 900 m) of forest to the first pri-
44
P.-F. Fan et al. / Biological Conservation 161 (2013) 39–47
Fig. 4. Habitat quality over the five zones in the study area.
Table 4 Area and patch number of different habitat quality within Zone I & IV. Quality level
High Moderate Low
Area (patch number)
Total
1.0–9.9 ha
10.0–99.9 ha
>100.0 ha
274.9 (82) 1074.7 (435) 1094.9 (471)
605.9 (17) 334.9 (22) 121.8 (10)
3080.3 (4) 0 0
3951.1 (102) 1409.6 (457) 1216.7 (481)
Table 5 Area and patch number of high-quality habitat within each conservation priority areas. Priority area
1st 2nd 3rd Total
Area (patch number)
Total
1.0–9.9 ha
10.0–99.9 ha
>100.0 ha
8.1 (3) 3.5 (2) 21.8 (7) 33.5 (12)
31.8 (2) 87.5 (3) 170.8 (4) 290.0 (9)
2176.8 (1) 590.6 (1) 310.7 (2) 3078.1 (4)
2216.7 (6) 681.6 (6) 503.4 (13) 3401.6 (25)
ority area, and the forest is above an underground river. The second and third conservation priority areas are separated by a village and the surrounding farmland. The percentage of high-quality habitat within the second and third priority areas was 57.8% and 41.8%, respectively. Areas of high-quality habitat and the types of land cover are summarized in Tables 5 and 6. 3.4. Population viability analysis Excluding patches smaller than 100 ha, the high-quality forest in the first priority area was 2176.8 ha (Table 5), which can provide
sufficient habitat for 20 groups (or 120 individuals). The first priority area (2775.3 ha, Table 6) could support 26 groups or 156 individuals if the area was rehabilitated to support gibbons. Furthermore, if gibbons could disperse to the second priority area, and all the first and second priority areas were rehabilitated in order to support gibbons, then the area could support 37 groups or 222 individuals. If gibbons could further disperse to the third priority area, then the area could possibly support 48 groups or 288 individuals. Without catastrophes and hunting, habitat capacity has a significant impact on population growth. In each of these situations, this population could reach carrying capacity within 40 years (Fig. 6). 4. Discussion Although the cao vit gibbons from the study site live in a low karst forest (Fan et al., 2011a), gibbons are canopy dwellers and tend to avoid lower forest stratum (Gittins, 1983; Cannon and Leighton, 1994; Hasan et al., 2007; Fan et al., 2009; Fan et al., 2013). During the 2096 h spent observing the behavior of three cao vit gibbon groups (Fan et al., 2013), we observed only one case in which a juvenile male walked on a stone for few seconds. To date, no study has reported the ability of gibbons to disperse across rivers or roads, suggesting that the current population of cao vit gibbon cannot naturally disperse out of the study area. In a broader sense, we noted that for canopy dwellers, like the gibbon, forest canopy cover could be used as a proxy to evaluate habitat quality. Our results, based on the assumption that canopy dwellers depend on the canopy cover of not only their habitat but also that of adjacent areas, showed that the habitat quality index (hi) is useful for studying the habitat of cao vit gibbon, and could potentially be applied to other canopy dwellers.
P.-F. Fan et al. / Biological Conservation 161 (2013) 39–47
45
Fig. 5. Three suggested priority conservation areas for the cao vit gibbon.
Table 6 Area (ha) and patch number of different land cover types within each conservation priority areas. Priority area
1st 2nd 3rd Total
Area (patch number)
Total
Forest
Scrub/Shrubland
Developed
2469.7 (15) 900.6 (21) 796.1 (29) 4166.4 (65)
274.3 220.3 268.2 726.9
31.3 (119) 58.3 (125) 138.6 (253) 228.2 (497)
(540) (372) (509) (1421)
2775.3 1179.2 1202.9 5157.4
As the last refuge of the cao vit gibbon, the Zone I habitat is integral to conservation efforts. However, human disturbances on both sides of the border continue to frustrate government efforts at conserving gibbon habitat (Fan et al., 2011a), and subsequently raising the carrying capacity beyond 20 groups. The total area of Zone I is 3043.2 ha (Table 3), and the total potential gibbon habitat is 2775.3 ha in the first priority area (Table 6), 2176.8 ha of which are high-quality patches larger than or equal to 100 ha (Table 5). This area has a carrying capacity of approximately 20 groups. In the 2007 trans-boundary census, 18 groups were recorded (Le et al., 2008), indicating the current population is nearing the 20group carrying capacity of the current habitat. This hypothesis is further supported through direct observation; no new group has formed since observation in China after 2009, despite observing 5 floating females and upwards of 6 floating males in the area over a 4-year span. If the entire area of the first priority area were upgraded to a high-quality habitat, then the carrying capacity would increase to 26 groups. PVA demonstrated that this population will likely reach carrying capacity in 15 years. Moreover, transforming all the first priority area into high-quality habitat is the most
feasible and effective way to conserve and grow the cao vit gibbon population. We identified two potential habitats (the 2nd and 3rd priority areas) in Zone IV. Only a narrow forest corridor (900 m in length) above an underground river connects the current habitat in the 1st conservation area and the 2nd priority area. If this corridor were destroyed, the gibbons could not disperse naturally (Fig. 5). Compared with the 1st priority area, the 2nd and 3rd priority areas may not be able to support gibbon populations at present because the percentage of high-quality forests are lower, forests are more fragmented, and there are more farmlands (Tables 5 and 6, Fig. 2). Unfortunately, we were unable to set plant plots in the 2nd and 3rd priority areas this time to conduct a detailed comparison of the forest quality (forest structure and plant diversity) with the current gibbon habitat (1st priority area), as they are primarily located in Vietnam. Likewise, the presence of villages and farmlands in or near the potential gibbon habitats disconnected the 2nd and 3rd priority areas and threaten the possibility of establishing them as future cao vit habitat. Zones II, III and V are separated from Zones I and IV by roads and rivers. These zones were generally more degraded than Zones I and IV with no forest patches larger than 100 ha recorded (Table 3). Consequently, we concluded that Zones II, III and V should have a lower priority for future gibbon conservation. PVA shows that the current population could reach carrying capacity within 40 years in any situations barring catastrophes and hunting. Since the population was rediscovered in 2002, hunting has not been reported in either China or Vietnam. Forest fires are thought to be a serious threat in some gibbon habitat (Cheyne, 2007), but none have been recorded in our study site for more than
46
P.-F. Fan et al. / Biological Conservation 161 (2013) 39–47
Fig. 6. Population dynamics of the cao vit gibbon under four situations with the carrying capacity (K) set at 126 (current habitat capacity), 156 (all area could be used in priority forest 1), 222 (all area could be used in priority forest 1 and 2), and 288 (all area could be used in priority forest 1, 2 and 3) individuals.
30 years (data not published, personal communication from our field guides). Because gibbons occupy home ranges used almost exclusively by the resident group (Bartlett, 2007), the breeding of females is thought to be independent of group densities. However, mortality rates of adults and sub-adults were higher in populations close to carrying capacity (Brockelman et al., 1998). In this research, we did not consider the effects of population density on gibbon mortality rates. While we acknowledge the limitations of the parameters of the model, PVAs provide us with some crucial information, namely that habitat carrying capacity is the most important factor limiting gibbon population expansion. In summary, the last remaining population of cao vit gibbon is nearing its carrying capacity in the current remaining forest patch (Zone 1). There are two potential areas for the gibbon’s future dispersal in the adjacent Zone IV. Currently, the Vietnamese government has not protected these two potential habitats. However, high-quality habitat within these two potential areas is more fragmented than the current gibbon habitat in Zone I. Forest protection and active forest restoration using important food tree plantings to increase habitat quality and connectivity should be the most critical part of the ongoing conservation management strategy, as has already been suggested (Fan et al., 2011a). Specific conservation recommendations: 1. Agriculture and grazing should be prohibited within the three conservation priority areas, particularly within the 1st conservation priority area (the only current habitat of cao vit gibbon). 2. Given that natural regeneration of karst forest takes long time, seedlings from local tree species that nourish the gibbon should be planted inside and around the three priority areas to promote habitat restoration, with efforts concentrated on the north part of the first priority area and the area between the 2nd and 3rd potential habitats (Fig 5, online Appendix 2). 3. Two potential habitats are located in Zone IV, mostly in Vietnam. We suggest the Vietnamese government expand the Cao Vit Gibbon Conservation Area to encompass these regions, and relocate the villages inside and close to the two potential habitats. 4. The narrow corridor connecting current gibbon habitat with suggested potential habitats should be protected to enable the potential natural dispersion of the gibbon in the future (Fig 5).
Acknowledgements This study was supported by the Conservation Leadership Programme, Association of American Zoo and Aquarium, the National
Natural Science Foundation of China (#30900169, 31272327), and Fauna and Flora International (FFI). Idea Wild provided equipment for this research. All research methods adhered to the appropriate Chinese legal requirements. We would like to thank the staffs of Bangliang Nature Reserve in China, Cao Vit Gibbon Conservation Area in Vietnam, and FFI Vietnam for their much needed support during our field work. We are also grateful to Dr. Li Li, Mr. Paul Insu-Cao and the two anonymous reviewers for their helpful comments. Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.biocon.2013.02.014. These data include Google maps of the most important areas described in this article. References Bartlett, T.Q., 2007. The hylobatidae, small apes of Asia. In: Campbell, C.J., Fuentes, A., Mackinnon, K.C., Panger, M., Bearder, S.K. (Eds.), Primates in Perspective. Oxford University Press, New York, pp. 274–289. Buckley, C., Nekaris, K.A.I., Husson, S.J., 2006. Survey of Hylobates agilis albibarbis in a logged peat-swamp forest: Sabangau catchment, Central Kalimantan. Primates 47, 327–335. Breiman, L., 2001. Random forests. Mach. Learn. 45, 5–32. Brockelman, W.Y., Ali, R., 1987. Methods of Surveying and Sampling Forest Primate Populations. Primates Conservation in the Tropical Rain Forest. Alans R. Liss, Inc. Brockelman, W.Y., Reichard, U., Treesucon, U., Raemaekers, J.J., 1998. Dispersal, pair formation and social structure in gibbons (Hylobates lar). Behav. Ecol. Sociobiol. 42, 329–339. Cannon, C.H., Leighton, M., 1994. Comparative locomotor ecology of gibbons and macaques: selection of canopy elements for crossing gaps. Am. J. Phys. Anthropol. 93, 504–524. Chan, B.P.L., Tan, X.F., Tan, W.J., 2008. Rediscovery of the critically endangered eastern black-crested gibbon Nomascus nasutus (Hylobatidae) in China, with preliminary notes on population size, ecology and conservation status. Asian Primates J. 1, 17–25. Cheyne, S.M., 2007. Effects of meteorology, astronomical variables, location and human disturbance on the singing apes: Hylobates albibarbis. Am. J. Primatol. 70, 386–392. Fan, P.F., Jiang, X.L., 2007. Population viability analysis for black crested gibbon (Nomascus concolor jingdongensis) in Dazhaizi at Mt. Wuliang, Yunnan, China. Acta Ecol. Sin. 27, 620–626. Fan, P.F., Jiang, X.L., 2008. Sleeping sites, sleeping trees and sleep-related behavior of black crested gibbons (Nomascus concolor jingdongensis) at Mt. Wuliang, Yunnan, China. Am. J. Primatol. 70 (2), 153–160. Fan, P.F., Jiang, X.L., Tian, C.C., 2009. The critically endangered black crested gibbon Nomascus concolor on Wuliang Mountain, Yunnan: the function of different forest types for the gibbon’s conservation. Oryx 43, 203–208. Fan, P.F., Fei, H.L., Xiang, Z.F., Zhang, W., Ma, C.Y., Huang, T., 2010. Social structure and group dynamics of the cao vit gibbon (Nomascus nasutus) in Bangliang, Jingxi, China. Folia Primatol. 81, 245–253. Fan, P.F., Fei, H.L., Scott, M.B., Zhang, W., Ma, C.Y., 2011a. Habitat and food choice of the critically endangered cao vit gibbon (Nomascus nasutus) in China: implications for conservation. Biol. Conserv. 144, 2247–2254.
P.-F. Fan et al. / Biological Conservation 161 (2013) 39–47 Fan, P.F., Xiao, W., Huo, S., Ai, H.S., Wang, T.C., Lin, R.T., 2011b. Distribution and conservation status of the vulnerable eastern hoolock gibbon Hoolock leuconedys in China. Oryx 45, 129–134. Fan, P.F., Fei, H.L., Ma, C.Y., 2012. Behavioral responses of cao vit gibbon (Nomascus nasutus) to variations in food abundance and temperature in Bangliang, Jingxi, China. Am. J. Primatol. 74, 632–641. Fan, P.F., Scott, M.B., Fei, H.L., Ma, C.Y., 2013. Locomotion behavior of cao vit gibbon (Nomascus nasutus) living in karst forest in Bangliang Nature Reserve, Guangxi, China. Integr. Zool.. http://dx.doi.org/10.1111/j.1749-4877.2012.00300.x. Fei, H.L., Scott, M.B., Zhang, W., Ma, C.Y., Xiang, Z.F., Fan, P.F., 2012. Sleeping tree selection of cao vit gibbon (Nomascus nasutus) living in degraded karst forest in Bangliang, Jingxi, China. Am. J. Primatol. 74, 998–1005. Geissmann, T., La, T.Q., Trinh, D.H., Vu, D.T., Dang, N.C., Pham, D.T., 2003. Rarest ape rediscovered in Vietnam. Asian Primates 8, 8–10. Gittins, S.P., 1983. Use of the forest canopy by the agile gibbon. Folia Primatol. 40, 134–144. Hansen, M.J., Franklin, S.E., Woudsma, C.G., Peterson, M., 2001. Caribou habitat mapping and fragmentation analysis using Landsat MSS, TM, and GIS data in the North Columbia Mountains, British Columbia, Canada. Remote Sens. Environ. 77, 50–65. Hasan, M.K., Feeroz, M.M., Islam, M.A., Kabir, M.M., Begum, S., 2007. Substrate use by the western hoolock gibbon (Hoolock hoolock) in a semi-evergreen forest of Bangladesh. Zoo’s Print 22, 2702–2705. Hijmans, R.J. van Etten, J. 2011. Raster: Geographic Analysis and Modeling with Raster Data.. Hu, Y., Xu, H.W., Yang, D.H., 1990. Feeding ecology of the white-cheek gibbon (Hylobates concolor leucogenys). Acta Ecol. Sin. 10 (2), 155–159. IUCN. 2012. IUCN Red List of Threatened Species. Version 2012.2. (downloaded 17.11.12). Johnson, A., Singh, S., Duangdala, M., Hedemark, M., 2005. The western black crested gibbon Nomascus concolor in Laos: new records and conservation status. Oryx 39 (3), 311–317. La, Q.T., Trinh, D.H., Long, B., Geissmann, T. 2002. Status review of black crested gibbons (Nomascus concolor and Nomascus sp. cf. nasutus) in Vietnam. In: Caring for Primates, Abstracts of the XIXth Congress of the International Primatological Society, 4–9th August, 2002, Beijing, China. pp. 131–132. Lacy, R.C., 1993. Vortex: a computer simulation model for population viability analysis. Wildlife Res. 20, 45–65. Le, T.D., Fan, P.F., Yan, L., Le, H.O., Josh, K. 2008. The Global Cao vit gibbon (Nomascus nasutus) Population. Fauna & Flora International, Vietnam Programme and China Programme, Hanoi.
47
Liaw, A., Wiener, M. 2002. Classification and Regression by randomForest. R News. vol. 2. pp. 18–22. Liu, Z.H., Zhang, Y., Jiang, H., Southwick, C., 1989. Population structure of Hylobates concolor in Bawangling Nature Reserve, Hainan, China. Am. J. Primatol. 19, 247– 254. Long, Y.C., Nadler, T., 2009. Eastern black crested gibbon Nomascus nasutus (Kunkel d’Herculais, 1884) China, Vietnam. In: Mittermeier, R.A., Wallis, J., Rylands, A.B., Ganzhorn, J.U., Oates, J.F., Williamson, E.A., Palacios, E., Heymann, E.W., Kierulff, M.C.M., Long, Y.C., Supriatna, J., Roos, C., Walker, S., Cortés-Ortiz, L., Schwitzer, C. (Eds.). Primates in Peril: The World’s 25 Most Endangered Primates 2008–2010. IUCN/SSC Primate Specialist Group (PSG), International Primatological Society (IPS), and Conservation International (CI), Arlington, VA. pp. 60–61. Maiorano, L., Falcucci, A., Boitani, L., 2006. Gap analysis of terrestrial vertebrates in Italy: priorities for conservation planning in a human dominated landscape. Biol. Conserv. 133, 455–473. Phoonjampa, R., Brockelman, W.Y., 2008. Survey of pileated gibbon Hylobates pileatus in Thailand: populations threatened by hunting and habitat degradation. Oryx 42 (4), 600–606. Ralls, K., Ballou, J.D., Templeton, A.R., 1988. Estimates of lethal equivalence and cost of inbreeding in mammals. Conserv. Biol. 2, 185–193. Seal, U. 1994. Thai gibbon life history and vortex analysis. In: Tunhikorn, S., Brockelman, W., Tilson, R., Nimmanheminda, U., Ratanakorn, P., Cook, R., Teare, A., Castle, K., Seal, U. (Eds.). Population and Habitat Viability Analysis Report for Thai Gibbons: Hylobates lar and H. pileatus. IUCN/SSC Conservation Breeding Specialist Group: Apple Valley, MN. pp. 23–36. Tan, B., 1985. The status of primates in China. Primates Conser. 5, 63–81. Wang, W., Ren, G.P., He, Y.H., Zhu, J.G., 2008. Habitat degradation and conservation status assessment of gallinaceous birds in the Trans-Himalayas. J. Wildlife Manage. 72, 1335–1341. Xiao, W., Ding, W., Cui, L.W., Zhou, R.L., Zhao, Q.K., 2003. Habitat degradation of Rhinopithecus bieti in Yunnan, China. Int. J. Primatol. 24, 389–398. Zhang, M.X., Fellowes, J.R., Jiang, X.L., Wang, W., Chan, B.P.L., Ren, G.P., Zhu, J.G., 2010. Degradation of tropical forest in Hainan, China, 1991–2008: conservation implications for Hainan gibbon (Nomascus hainanus). Biol. Conserv. 143, 1397– 1404. Zhou, J., Wei, F.W., Li, M., Zhang, J.F., Wang, D., Pan, R.L., 2005. Hainan black-crested gibbon is headed for extinction. Int. J. Primatol. 26, 453–465.
Contents lists available at SciVerse ScienceDirect
Biological Conservation journal homepage: www.elsevier.com/locate/biocon
Habitat evaluation and population viability analysis of the last population of cao vit gibbon (Nomascus nasutus): Implications for conservation Peng-Fei Fan a,1, Guo-Peng Ren b,1, Wei Wang c, Matthew B. Scott a, Chang-Yong Ma a, Han-Lan Fei a, Lin Wang b, Wen Xiao a,⇑, Jian-Guo Zhu b,⇑ a
Institute of Eastern-Himalaya Biodiversity Research, Dali University, Dali, Yunnan 671003, China Ecology, Conservation, and Environment Center (ECEC), Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan 650223, China c State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences (CRAES), Chaoyang, Beijing 100012, China b
a r t i c l e
i n f o
Article history: Received 9 December 2012 Received in revised form 16 February 2013 Accepted 25 February 2013
Keywords: Cao vit gibbon (Nomascus nasutus) Habitat quality Potential habitats Habitat carrying capacity Conservation suggestions
a b s t r a c t The cao vit gibbon (Nomascus nasutus) is among the most endangered primates in the world. The only surviving population lives in a karst forest patch along the China–Vietnam border. In this study, we used high-resolution satellite images to evaluate the habitat quality of the gibbon in the area immediately surrounding the last population and predict the potential gibbon habitat. We then used Vortex to simulate population responses to changes in the habitat’s carrying capacity. Our results showed the gibbon population is approaching the carrying capacity of their current habitat, and carrying capacity has a significant impact on population changes. Two potential habitats were located in a forest connected to the current habitat by a narrow forest corridor, situated above an underground river. Based on the results, we recommend: (1) prohibiting agriculture and grazing activities within the current gibbon habitat; (2) expanding the Cao Vit Gibbon Conservation Area in order to protect potential cao vit habitats in Vietnam; (3) protecting forest corridor that connect the current cao vit habitat to potential habitats; and (4) rehabilitating the forests currently depauperate of important food species in order to support the expansion of both the gibbon population and the range. This research both provides important insight into sustaining the current gibbon population as well as suggestions for both Vietnamese and Chinese local governments planning habitat restoration at the study site. Ó 2013 Elsevier Ltd. All rights reserved.
1. Introduction The cao vit, or eastern black crested gibbon (Nomascus nasutus) is a Critically Endangered species (IUCN, 2012) with only one known population. Historically, the species was widespread east of the Red River (Hong He) in both southern China and northern Vietnam (Geissmann et al., 2003). By the 1960s the cao vit gibbon was considered extinct (Tan, 1985; Geissmann et al., 2003), but was rediscovered along Vietnam’s nothern border in 2002 (La et al., 2002) and in China in 2006 (Chan et al., 2008). In 2007, a trans-boundary census of the population recorded 18 groups and approximately 110 individuals in the area (Le et al., 2008), making ⇑ Corresponding authors. Addresses: Institute of Eastern-Himalaya Biodiversity Research, Dali University, 2 Hongsheng Road, Dali, Yunnan 671003, China (W. Xiao), Ecology, Conservation, and Environment Center (ECEC), Kunming Institute of Zoology, Chinese Academy of Sciences, 32 Jiaochang Donglu, Kunming, Yunnan 650223, China. Tel. +86 871 65190776 (J.-G. Zhu). E-mail addresses: [email protected] (W. Xiao), [email protected] (J.-G. Zhu). 1 These authors contributed equally to this research. 0006-3207/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biocon.2013.02.014
it the second smallest population of any ape species worldwide after the Hainan gibbon (Zhou et al., 2005). Consequently, the cao vit gibbon has been listed as one of the World’s 25 Most Endangered Primates (Long and Nadler, 2009). To protect the remaining population and its karst forest habitat, the Cao Vit Gibbon Conservation Area in Vietnam and Bangliang Gibbon Nature Reserve in China were established in 2007 and 2009, respectively. Previous interviews with local people indicated that the cao vit gibbon habitat has degraded over time as a result of timber extraction, fuel-wood collection, the making of charcoal, selective logging, and agriculture encroachment (Fan et al., 2011a). While the establishment of the conservation areas has reduced forest degradation, local inhabitants from both countries still plant corn in some of the valleys and some Chinese villagers continue to graze goats inside the Bangliang Nature Reserve. The mean canopy height over the site is 10.5 m, which is the lowest forest canopy height ever reported for gibbon habitat (Fan et al., 2011a). To survive in the degraded karst forest, cao vit gibbons consume nearly half of the tree and liana species recorded (81 of the 159 species) at the site (Fan et al., 2011a). Like all other
40
P.-F. Fan et al. / Biological Conservation 161 (2013) 39–47
gibbons, cao vit gibbons eat fruit when it is available, and shift to a leaf-dominant diet when fruit becomes less available (Fan et al., 2012). They also rest more and sleep huddled together when the temperature cools (Fan et al., 2012). To find sufficient food, cao vit gibbons occupy home ranges (130 ha, Fan et al., 2010) larger than those of other species in south tropical rain forests (on average 40 ha, Bartlett, 2007), but comparable with or smaller than the Nomascus gibbons in the north (N. hainanus: 300–500 ha, Liu et al., 1989; N. concolor: 151 ha, Fan and Jiang, 2008; N. leucogenys: ca. 540 ha, Hu et al., 1990). Based on the estimated ca. 2000 ha of suitable habitat available (Le et al., 2008), the cao vit gibbon population is likely close to its carrying capacity. Remote Sensing (RS) and Geographic Information Systems (GIS) techniques have been widely used to evaluate habitat quality (Hansen et al., 2001; Xiao et al., 2003; Zhang et al., 2010), predict potential habitat (Wang et al., 2008; Zhang et al., 2010), and plan conservation strategies (Maiorano et al., 2006; Zhang et al., 2010). In this study, we aim to: (1) evaluate current habitat quality using RS and GIS techniques; (2) predict potential habitat in surrounding areas and identify some ecological corridors for dispersal; and (3) use a Vortex model to simulate the sensitivity of population dynamics to changes of habitat carrying capacity.
2. Methods 2.1. Study area Gibbons are strict canopy dwellers and cannot disperse beyond rivers, roads and other breaks in the forest canopy. We accordingly focused on the areas immediately surrounding the current cao vit gibbon habitat (22°49–590 N, 106°220 –350 E). Several rivers and paved roads bisect the total research area, which can be divided into five different zones (Fig. 1). Gibbons currently only live in Zone I; however, local people reported knowing of gibbons inhabiting Zone IV before 2000 (Le et al., 2008). Zones I and IV are separated by a river, but the forests are relatively contiguous because some 900 m of the river is underground. 2.2. Forest cover mapping 2.2.1. Classification scheme and ground-truth data collection Land cover in the study area was classified as Forest, Scrub, Shrubland and Developed areas (Table 1). Between July 15 and August 5 2010, 412 land cover polygons in China were classified and delineated on satellite images with the aid of relief maps and a Glo-
Fig. 1. Study area along the China–Vietnam border. The five zones outlines in this study are divided by rivers and roads.
41
P.-F. Fan et al. / Biological Conservation 161 (2013) 39–47 Table 1 Land cover classification scheme. Land cover type
Description
1. Forest 2. Scrub
Some trees >10 m height with a canopy cover P50% Near continuous canopy of tall shrubs and dwarfed/young trees, tree canopy cover comprises <50% Mosaic of shrubs and grasses, trees few or absent Areas of farmland, town, villages, open water and other nonforested land
3. Shrubland 4. Developed
bal Position System (GPS) receiver (Garmin eTrex). Using the same method, 28 land cover polygons were delineated in Vietnam from June 15 to 26 in 2011. Half of these polygons were randomly chosen as validation data, and the remainders as training data for classification. 2.2.2. Remote sensing data Two scenes of Advanced Land Observation Satellite (ALOS) images, one from Panchromatic Remote-sensing Instrument for Stereo Mapping (PRISM, 1 band, resolution = 2.5 m) and the other from Advanced Visible and Near Infrared Radiometer (AVNIR-2, 4 bands, resolution = 10 m), both acquired on November 23, 2009, were used to map forest cover over the study area. After referencing with Google Earth, the ALOS PRISM image was properly geocorrected. We subsequently geo-corrected the AVNIR-2 image band by band to the ALOS PRISM. Afterward, we used a pixel-based fusion method to derive a pan-sharpened image (4 bands, resolution = 2.5 m) from the ALOS AVNIR-2 and PRISM images. UTM coordinates system (Projection: Universal Transverse Mercator, Spheroid: WGS84, Datum: WGS84, Zone: 48N) was used in this study. The remote sensing data processes were conducted using Erdas Imagine (Leica Geosystems Geospatial Imaging, LLC, Norcross, Georgia, US) and R Statistics software. 2.2.3. Land cover mapping Based on the ALOS images and the training data from the field, we produced a preliminary land cover map using the Random Forest classification algorithm (Breiman, 2001). The classification process was implemented using the RandomForest package (Liaw and Wiener, 2002) and Raster package (Hijmans and van Etten, 2011) in R Statistics software (2.1.0, http://www.r-project.org/). Then we aggregated 144 pixels in the preliminary land cover map to one pixel in order to derive a land cover map at 30 m resolution, as 2.5 m resolution was too fine for a land cover map. The accuracy of the 30 m resolution land cover map was evaluated (producer’s accuracy) using validation data obtained from field surveys. 2.2.4. Habitat quality evaluation On the basis of the 2.5 m resolution preliminary land cover map, we calculated the forest pixel percentage as tree cover percentage (%tree) at 30 m resolution. Then, we performed a focal analysis using a 5 by 5 Gaussian filter on the %tree to produce a habitat quality index (hi) able to evaluate the quality of gibbon habitat. The Gaussian filter, defined by Eq. (1), places the heaviest weight on the focal pixel (the pixel having the highest Gaussian value), with the weighting of neighboring pixels varying proportionately with distance from the focal pixel. The hi can be used to evaluate habitat quality for two reasons. First, gibbons only inhabit forests and avoid all other land cover types; second, the possibility of site suitability for gibbons depends not only on the forest cover percent, but also on the cover of the adjacent area, both of which are taken into account in the hi.
0
1 B B2 B The 5 by 5 Gaussian filter ¼ B B3 B @2
1
2 3 2 1 C 3 4 3 2C C 4 5 4 3C C=65 C 3 4 3 2A 1 2 3 2 1
ð1Þ
We then used the hi to evaluate the quality of the gibbon habitat by arbitrarily dividing the study area into the following four types: (a) (b) (c) (d)
high-quality habitat: hi P 80; moderate-quality habitat: 60 6 hi < 80; low-quality habitat: 40 6 hi < 60; non-habitat (not suitable for gibbon): hi < 40.
We tested whether the hi is an accurate measure of habitat quality by using the field data from the extant gibbon population habitat sites, as described in the next section. The trans-boundary survey conducted by Fauna & Flora International (FFI) in September 2007 identified 18 groups using direct observation and listening to gibbon calls on hill tops – a widely used method in gibbon surveys developed in 1987 by Brockelman and Ali, 1987 (Johnson et al., 2005; Buckley et al., 2006; Phoonjampa and Brockelman, 2008; Fan et al., 2011b; Le et al., 2008). FFI directly observed 17 of the 18 gibbon populations and recorded their group compositions (Le et al., 2008). All group locations obtained from direct observations and calls were marked on a topography map (1:50,000), which was used to estimate the centre of each group’s home range (Le et al., 2008). Referencing Appendix 4 in the study done by Le et al. (2008), two of the 17 locations were re-located according to our subsequent long-term field observations. We drawn 8 concentric rings in 200 m intervals around the 17 gibbon locations to cover the range of the current gibbon (Fig. 2). Rings were labelled ring 1–8, from the innermost ring outwards. If the hi is a good index for the habitat quality evaluation, the inner rings should be expected to have a higher hi than the outer rings. We conducted wilcoxon-tests between hi values for all combination of paired rings, and used the Bonferroni method in R 2.1.0 to adjust the p-values.
2.3. Potential habitat prediction To predict potential habitat for the cao vit gibbon, we made three assumptions according to previous research and our knowledge: Assumption 1: Potential habitat should be in close proximity to high-quality habitat patches larger than 100 ha, because the home range size of all Nomascus gibbons (who occupy home ranges of equal or greater size to the cao vit gibbon) in northern areas is larger than 100 ha (Liu et al., 1989; Hu et al., 1990; Fan and Jiang, 2008; Fan et al., 2010). Assumption 2: Gibbons mostly inhabit high-quality habitat, and can move between any two high-quality habitat patches if the distance between them is less than 100 m and the two patches are connected by at least moderate-quality habitat patches. Assumption 3: Gibbons do not live in low-quality habitat or nonhabitat. Based on these assumptions, we used the following steps to predict potential gibbon habitat: Step 1: Select high-quality habitat patches larger than 100 ha as the core habitat. Step 2: Select high-quality habitat patches connected to the core habitat by at most 100 m of moderate-quality habitat as additional patches of core habitat.
42
P.-F. Fan et al. / Biological Conservation 161 (2013) 39–47
Fig. 2. Concentric buffer rings around gibbon group locations to evaluate habitat quality (rings were labeled as ring 1 to ring 8 from inner to outer).
Step 3: Repeat step 2 until no more patches can be added to the core habitat. Step 4: Select moderate-quality habitat connected to high-quality habitat as the marginal habitat. Step 5: Select both the core and marginal habitats as potential habitats for cao vit gibbons.
2.4. Population dynamics and viability analysis (PVA) We used Vortex 9.99 (http://www.vortex9.org/vortex.html) to simulate the population dynamics of the cao vit gibbon over the next 200 years (ca. 6–7 generations) assuming different habitat carrying capacities. Vortex was developed by Lacy (1993) and has been widely used to analyze population viability, including gibbon population viability (Seal, 1994; Fan and Jiang, 2007). Beginning in December 2007, we monitored three Chinese cao vit gibbon groups for at least 7 days each month, recording the data required to model population dynamics (Fan et al., 2010; unpublished data). Over those 5 years, we recorded nine births. The inter-birth interval of the five females who gave birth twice was 34 months. One older female did not give birth during the 5 years. On average, 30% of the adult females (SD = 18.2%) reproduced each year. Mortality of gibbons from age 0 to 1 was 20% (2 deaths out of 10 infants). Mortality of gibbons from age 3–4 was 20% (2 deaths of small juveniles out of 10). Mortality of gibbons at other ages was 0. We assumed that mortality was the same between sexes. Because of the gibbons’ longevity, it was difficult to determine the age at which females and males have their first offspring, as well as the maximum age of reproduction. Brockelman et al. (1998) provide the only known information on wild gibbons, and report that female Hylobates lar has their first offspring at around
10 years of age, and males at around 12 years. In the absence of other data, we used these parameters in our model. We also assumed that the maximum age of reproduction for gibbons is 30 years old (Seal, 1994). The lethal equivalent, a measure of the severity of inbreeding, was set at 3.14; in studying 40 captive vertebrate populations, Ralls et al. (1988) found 3.14 lethal equivalents to be the median value. The average home range size of these three groups was 130 ha (Fan et al., 2010), which 99.8 ha (G1) and 114.2 ha (G4) was used exclusively by a single group (Fei et al., 2012). The average exclusive territory range is 107 ha for G1 and G4. Cao vit gibbons may potentially live in smaller home ranges in well-protected forests, but such data is not available at present. We calculated the carrying capacity by dividing the total habitat area by the average exclusive territory range for one group, and then multiplied by the average group size (6.0, Fan et al., 2010). We assumed no catastrophes, harvest/hunting, supplementation and genetic management in the model. All parameters are summarized in the online Appendix 1.
3. Results 3.1. Forest cover map and accuracies A land cover map of the whole study area was produced on the basis of the ALOS images (Fig. 3). Mapping accuracies of both Forest and Developed areas were satisfied (>0.85), although the accuracies for the Scrub and Shrubland areas were low (Table 2). The lower accuracies for the transitional land cover types between forests and developed areas were due to the confusion of the two land cover types. To correct for this, we combined Scrub and Shrubland
43
P.-F. Fan et al. / Biological Conservation 161 (2013) 39–47
Fig. 3. Classification results of forest map over the study area.
Table 2 Producer’s accuracies of the land cover classification map over study area based on 2009 satellite imageries. Land cover type
Forest Scrub Shrubland Developed Producer’s accuracy
Table 3 The area and patch number of forest at three tier levels in each zone. Zone
Validation data (n = 2353) Forest
Scrub
Shrubland
Developed
875 111 20 0 0.87
22 70 27 0 0.59
16 301 485 61 0.56
0 15 11 339 0.93
into one category in the following analyses. As gibbons do not use either scrub or shrubland, pooling the categories was not expected to influence the results. In total, forests comprised 6600.3 ha of the whole 22,700 ha study area, 93% of which (6144.9 ha) was in Zones I and IV (Table 3, Fig. 3). There were only five forest patches larger than 100 ha with the total area of 5170.2 ha in Zones I and IV (Table 3).
I IV III V II Total
Area of forest patches (patch number) 1.0–9.9 ha
10.0–99.9 ha
>100.0 ha
Total
196.4 (78) 416.8 (173) 166.3 (55) 85.4 (29) 4.7 (2) 914.5 (337)
11.7 (1) 304.8 (13) 178.2 (8) 20.8 (2) 0 515.6 (24)
2835.1 (1) 2335.1 (4) 0 0 0 5170.2 (5)
3043.2 (80) 3101.7 (190) 344.6 (63) 106.2 (31) 4.7 (2) 6600.3 (366)
being close to 600 m (calculated from home range size 130 ha) suggests that more than 90% of a groups home range is high-quality forest and that the hi index is a reasonable assessment of habitat quality for the cao vit gibbon. There are still 3951.1 ha of high-quality habitat and 1409.6 ha of moderate-quality habitat within Zones I and IV (Fig. 4, Table 4). Only four patches of high-quality habitat are both larger than 100 ha and located in Zones I and IV (Table 4).
3.2. Habitat quality 3.3. Potential habitat Gibbon habitat quality was evaluated using the hi index. Our results showed that habitat quality decreased significantly as distance from the nearest gibbon location buffer ring increased (p < 0.001), except habitat quality within the first two rings (p = 0.641) and last two rings (p = 0.152) did not vary significantly. According to our definition of high-quality habitat (hi P 80), more than 97% of the first ring is high-quality habitat, and more than 95%, 90%, 74%, 50% of the successive four rings are high-quality habitat, respectively. The home range radius of a single group
The total potential habitat area contains 3401.6 ha of high-quality habitat (Table 5) and 1125.1 ha of moderate-quality habitat. We divided them into three conservation priority areas using relatively compacted high-quality habitats as boundaries (Fig. 5, online Appendix 2). The first conservation priority area is the only area currently inhabited by gibbons, comprising a total 2216.7 ha (79.9%) of high-quality habitat. The second priority area is connected by a narrow strip (width = 900 m) of forest to the first pri-
44
P.-F. Fan et al. / Biological Conservation 161 (2013) 39–47
Fig. 4. Habitat quality over the five zones in the study area.
Table 4 Area and patch number of different habitat quality within Zone I & IV. Quality level
High Moderate Low
Area (patch number)
Total
1.0–9.9 ha
10.0–99.9 ha
>100.0 ha
274.9 (82) 1074.7 (435) 1094.9 (471)
605.9 (17) 334.9 (22) 121.8 (10)
3080.3 (4) 0 0
3951.1 (102) 1409.6 (457) 1216.7 (481)
Table 5 Area and patch number of high-quality habitat within each conservation priority areas. Priority area
1st 2nd 3rd Total
Area (patch number)
Total
1.0–9.9 ha
10.0–99.9 ha
>100.0 ha
8.1 (3) 3.5 (2) 21.8 (7) 33.5 (12)
31.8 (2) 87.5 (3) 170.8 (4) 290.0 (9)
2176.8 (1) 590.6 (1) 310.7 (2) 3078.1 (4)
2216.7 (6) 681.6 (6) 503.4 (13) 3401.6 (25)
ority area, and the forest is above an underground river. The second and third conservation priority areas are separated by a village and the surrounding farmland. The percentage of high-quality habitat within the second and third priority areas was 57.8% and 41.8%, respectively. Areas of high-quality habitat and the types of land cover are summarized in Tables 5 and 6. 3.4. Population viability analysis Excluding patches smaller than 100 ha, the high-quality forest in the first priority area was 2176.8 ha (Table 5), which can provide
sufficient habitat for 20 groups (or 120 individuals). The first priority area (2775.3 ha, Table 6) could support 26 groups or 156 individuals if the area was rehabilitated to support gibbons. Furthermore, if gibbons could disperse to the second priority area, and all the first and second priority areas were rehabilitated in order to support gibbons, then the area could support 37 groups or 222 individuals. If gibbons could further disperse to the third priority area, then the area could possibly support 48 groups or 288 individuals. Without catastrophes and hunting, habitat capacity has a significant impact on population growth. In each of these situations, this population could reach carrying capacity within 40 years (Fig. 6). 4. Discussion Although the cao vit gibbons from the study site live in a low karst forest (Fan et al., 2011a), gibbons are canopy dwellers and tend to avoid lower forest stratum (Gittins, 1983; Cannon and Leighton, 1994; Hasan et al., 2007; Fan et al., 2009; Fan et al., 2013). During the 2096 h spent observing the behavior of three cao vit gibbon groups (Fan et al., 2013), we observed only one case in which a juvenile male walked on a stone for few seconds. To date, no study has reported the ability of gibbons to disperse across rivers or roads, suggesting that the current population of cao vit gibbon cannot naturally disperse out of the study area. In a broader sense, we noted that for canopy dwellers, like the gibbon, forest canopy cover could be used as a proxy to evaluate habitat quality. Our results, based on the assumption that canopy dwellers depend on the canopy cover of not only their habitat but also that of adjacent areas, showed that the habitat quality index (hi) is useful for studying the habitat of cao vit gibbon, and could potentially be applied to other canopy dwellers.
P.-F. Fan et al. / Biological Conservation 161 (2013) 39–47
45
Fig. 5. Three suggested priority conservation areas for the cao vit gibbon.
Table 6 Area (ha) and patch number of different land cover types within each conservation priority areas. Priority area
1st 2nd 3rd Total
Area (patch number)
Total
Forest
Scrub/Shrubland
Developed
2469.7 (15) 900.6 (21) 796.1 (29) 4166.4 (65)
274.3 220.3 268.2 726.9
31.3 (119) 58.3 (125) 138.6 (253) 228.2 (497)
(540) (372) (509) (1421)
2775.3 1179.2 1202.9 5157.4
As the last refuge of the cao vit gibbon, the Zone I habitat is integral to conservation efforts. However, human disturbances on both sides of the border continue to frustrate government efforts at conserving gibbon habitat (Fan et al., 2011a), and subsequently raising the carrying capacity beyond 20 groups. The total area of Zone I is 3043.2 ha (Table 3), and the total potential gibbon habitat is 2775.3 ha in the first priority area (Table 6), 2176.8 ha of which are high-quality patches larger than or equal to 100 ha (Table 5). This area has a carrying capacity of approximately 20 groups. In the 2007 trans-boundary census, 18 groups were recorded (Le et al., 2008), indicating the current population is nearing the 20group carrying capacity of the current habitat. This hypothesis is further supported through direct observation; no new group has formed since observation in China after 2009, despite observing 5 floating females and upwards of 6 floating males in the area over a 4-year span. If the entire area of the first priority area were upgraded to a high-quality habitat, then the carrying capacity would increase to 26 groups. PVA demonstrated that this population will likely reach carrying capacity in 15 years. Moreover, transforming all the first priority area into high-quality habitat is the most
feasible and effective way to conserve and grow the cao vit gibbon population. We identified two potential habitats (the 2nd and 3rd priority areas) in Zone IV. Only a narrow forest corridor (900 m in length) above an underground river connects the current habitat in the 1st conservation area and the 2nd priority area. If this corridor were destroyed, the gibbons could not disperse naturally (Fig. 5). Compared with the 1st priority area, the 2nd and 3rd priority areas may not be able to support gibbon populations at present because the percentage of high-quality forests are lower, forests are more fragmented, and there are more farmlands (Tables 5 and 6, Fig. 2). Unfortunately, we were unable to set plant plots in the 2nd and 3rd priority areas this time to conduct a detailed comparison of the forest quality (forest structure and plant diversity) with the current gibbon habitat (1st priority area), as they are primarily located in Vietnam. Likewise, the presence of villages and farmlands in or near the potential gibbon habitats disconnected the 2nd and 3rd priority areas and threaten the possibility of establishing them as future cao vit habitat. Zones II, III and V are separated from Zones I and IV by roads and rivers. These zones were generally more degraded than Zones I and IV with no forest patches larger than 100 ha recorded (Table 3). Consequently, we concluded that Zones II, III and V should have a lower priority for future gibbon conservation. PVA shows that the current population could reach carrying capacity within 40 years in any situations barring catastrophes and hunting. Since the population was rediscovered in 2002, hunting has not been reported in either China or Vietnam. Forest fires are thought to be a serious threat in some gibbon habitat (Cheyne, 2007), but none have been recorded in our study site for more than
46
P.-F. Fan et al. / Biological Conservation 161 (2013) 39–47
Fig. 6. Population dynamics of the cao vit gibbon under four situations with the carrying capacity (K) set at 126 (current habitat capacity), 156 (all area could be used in priority forest 1), 222 (all area could be used in priority forest 1 and 2), and 288 (all area could be used in priority forest 1, 2 and 3) individuals.
30 years (data not published, personal communication from our field guides). Because gibbons occupy home ranges used almost exclusively by the resident group (Bartlett, 2007), the breeding of females is thought to be independent of group densities. However, mortality rates of adults and sub-adults were higher in populations close to carrying capacity (Brockelman et al., 1998). In this research, we did not consider the effects of population density on gibbon mortality rates. While we acknowledge the limitations of the parameters of the model, PVAs provide us with some crucial information, namely that habitat carrying capacity is the most important factor limiting gibbon population expansion. In summary, the last remaining population of cao vit gibbon is nearing its carrying capacity in the current remaining forest patch (Zone 1). There are two potential areas for the gibbon’s future dispersal in the adjacent Zone IV. Currently, the Vietnamese government has not protected these two potential habitats. However, high-quality habitat within these two potential areas is more fragmented than the current gibbon habitat in Zone I. Forest protection and active forest restoration using important food tree plantings to increase habitat quality and connectivity should be the most critical part of the ongoing conservation management strategy, as has already been suggested (Fan et al., 2011a). Specific conservation recommendations: 1. Agriculture and grazing should be prohibited within the three conservation priority areas, particularly within the 1st conservation priority area (the only current habitat of cao vit gibbon). 2. Given that natural regeneration of karst forest takes long time, seedlings from local tree species that nourish the gibbon should be planted inside and around the three priority areas to promote habitat restoration, with efforts concentrated on the north part of the first priority area and the area between the 2nd and 3rd potential habitats (Fig 5, online Appendix 2). 3. Two potential habitats are located in Zone IV, mostly in Vietnam. We suggest the Vietnamese government expand the Cao Vit Gibbon Conservation Area to encompass these regions, and relocate the villages inside and close to the two potential habitats. 4. The narrow corridor connecting current gibbon habitat with suggested potential habitats should be protected to enable the potential natural dispersion of the gibbon in the future (Fig 5).
Acknowledgements This study was supported by the Conservation Leadership Programme, Association of American Zoo and Aquarium, the National
Natural Science Foundation of China (#30900169, 31272327), and Fauna and Flora International (FFI). Idea Wild provided equipment for this research. All research methods adhered to the appropriate Chinese legal requirements. We would like to thank the staffs of Bangliang Nature Reserve in China, Cao Vit Gibbon Conservation Area in Vietnam, and FFI Vietnam for their much needed support during our field work. We are also grateful to Dr. Li Li, Mr. Paul Insu-Cao and the two anonymous reviewers for their helpful comments. Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.biocon.2013.02.014. These data include Google maps of the most important areas described in this article. References Bartlett, T.Q., 2007. The hylobatidae, small apes of Asia. In: Campbell, C.J., Fuentes, A., Mackinnon, K.C., Panger, M., Bearder, S.K. (Eds.), Primates in Perspective. Oxford University Press, New York, pp. 274–289. Buckley, C., Nekaris, K.A.I., Husson, S.J., 2006. Survey of Hylobates agilis albibarbis in a logged peat-swamp forest: Sabangau catchment, Central Kalimantan. Primates 47, 327–335. Breiman, L., 2001. Random forests. Mach. Learn. 45, 5–32. Brockelman, W.Y., Ali, R., 1987. Methods of Surveying and Sampling Forest Primate Populations. Primates Conservation in the Tropical Rain Forest. Alans R. Liss, Inc. Brockelman, W.Y., Reichard, U., Treesucon, U., Raemaekers, J.J., 1998. Dispersal, pair formation and social structure in gibbons (Hylobates lar). Behav. Ecol. Sociobiol. 42, 329–339. Cannon, C.H., Leighton, M., 1994. Comparative locomotor ecology of gibbons and macaques: selection of canopy elements for crossing gaps. Am. J. Phys. Anthropol. 93, 504–524. Chan, B.P.L., Tan, X.F., Tan, W.J., 2008. Rediscovery of the critically endangered eastern black-crested gibbon Nomascus nasutus (Hylobatidae) in China, with preliminary notes on population size, ecology and conservation status. Asian Primates J. 1, 17–25. Cheyne, S.M., 2007. Effects of meteorology, astronomical variables, location and human disturbance on the singing apes: Hylobates albibarbis. Am. J. Primatol. 70, 386–392. Fan, P.F., Jiang, X.L., 2007. Population viability analysis for black crested gibbon (Nomascus concolor jingdongensis) in Dazhaizi at Mt. Wuliang, Yunnan, China. Acta Ecol. Sin. 27, 620–626. Fan, P.F., Jiang, X.L., 2008. Sleeping sites, sleeping trees and sleep-related behavior of black crested gibbons (Nomascus concolor jingdongensis) at Mt. Wuliang, Yunnan, China. Am. J. Primatol. 70 (2), 153–160. Fan, P.F., Jiang, X.L., Tian, C.C., 2009. The critically endangered black crested gibbon Nomascus concolor on Wuliang Mountain, Yunnan: the function of different forest types for the gibbon’s conservation. Oryx 43, 203–208. Fan, P.F., Fei, H.L., Xiang, Z.F., Zhang, W., Ma, C.Y., Huang, T., 2010. Social structure and group dynamics of the cao vit gibbon (Nomascus nasutus) in Bangliang, Jingxi, China. Folia Primatol. 81, 245–253. Fan, P.F., Fei, H.L., Scott, M.B., Zhang, W., Ma, C.Y., 2011a. Habitat and food choice of the critically endangered cao vit gibbon (Nomascus nasutus) in China: implications for conservation. Biol. Conserv. 144, 2247–2254.
P.-F. Fan et al. / Biological Conservation 161 (2013) 39–47 Fan, P.F., Xiao, W., Huo, S., Ai, H.S., Wang, T.C., Lin, R.T., 2011b. Distribution and conservation status of the vulnerable eastern hoolock gibbon Hoolock leuconedys in China. Oryx 45, 129–134. Fan, P.F., Fei, H.L., Ma, C.Y., 2012. Behavioral responses of cao vit gibbon (Nomascus nasutus) to variations in food abundance and temperature in Bangliang, Jingxi, China. Am. J. Primatol. 74, 632–641. Fan, P.F., Scott, M.B., Fei, H.L., Ma, C.Y., 2013. Locomotion behavior of cao vit gibbon (Nomascus nasutus) living in karst forest in Bangliang Nature Reserve, Guangxi, China. Integr. Zool.. http://dx.doi.org/10.1111/j.1749-4877.2012.00300.x. Fei, H.L., Scott, M.B., Zhang, W., Ma, C.Y., Xiang, Z.F., Fan, P.F., 2012. Sleeping tree selection of cao vit gibbon (Nomascus nasutus) living in degraded karst forest in Bangliang, Jingxi, China. Am. J. Primatol. 74, 998–1005. Geissmann, T., La, T.Q., Trinh, D.H., Vu, D.T., Dang, N.C., Pham, D.T., 2003. Rarest ape rediscovered in Vietnam. Asian Primates 8, 8–10. Gittins, S.P., 1983. Use of the forest canopy by the agile gibbon. Folia Primatol. 40, 134–144. Hansen, M.J., Franklin, S.E., Woudsma, C.G., Peterson, M., 2001. Caribou habitat mapping and fragmentation analysis using Landsat MSS, TM, and GIS data in the North Columbia Mountains, British Columbia, Canada. Remote Sens. Environ. 77, 50–65. Hasan, M.K., Feeroz, M.M., Islam, M.A., Kabir, M.M., Begum, S., 2007. Substrate use by the western hoolock gibbon (Hoolock hoolock) in a semi-evergreen forest of Bangladesh. Zoo’s Print 22, 2702–2705. Hijmans, R.J. van Etten, J. 2011. Raster: Geographic Analysis and Modeling with Raster Data.
47
Liaw, A., Wiener, M. 2002. Classification and Regression by randomForest. R News. vol. 2. pp. 18–22. Liu, Z.H., Zhang, Y., Jiang, H., Southwick, C., 1989. Population structure of Hylobates concolor in Bawangling Nature Reserve, Hainan, China. Am. J. Primatol. 19, 247– 254. Long, Y.C., Nadler, T., 2009. Eastern black crested gibbon Nomascus nasutus (Kunkel d’Herculais, 1884) China, Vietnam. In: Mittermeier, R.A., Wallis, J., Rylands, A.B., Ganzhorn, J.U., Oates, J.F., Williamson, E.A., Palacios, E., Heymann, E.W., Kierulff, M.C.M., Long, Y.C., Supriatna, J., Roos, C., Walker, S., Cortés-Ortiz, L., Schwitzer, C. (Eds.). Primates in Peril: The World’s 25 Most Endangered Primates 2008–2010. IUCN/SSC Primate Specialist Group (PSG), International Primatological Society (IPS), and Conservation International (CI), Arlington, VA. pp. 60–61. Maiorano, L., Falcucci, A., Boitani, L., 2006. Gap analysis of terrestrial vertebrates in Italy: priorities for conservation planning in a human dominated landscape. Biol. Conserv. 133, 455–473. Phoonjampa, R., Brockelman, W.Y., 2008. Survey of pileated gibbon Hylobates pileatus in Thailand: populations threatened by hunting and habitat degradation. Oryx 42 (4), 600–606. Ralls, K., Ballou, J.D., Templeton, A.R., 1988. Estimates of lethal equivalence and cost of inbreeding in mammals. Conserv. Biol. 2, 185–193. Seal, U. 1994. Thai gibbon life history and vortex analysis. In: Tunhikorn, S., Brockelman, W., Tilson, R., Nimmanheminda, U., Ratanakorn, P., Cook, R., Teare, A., Castle, K., Seal, U. (Eds.). Population and Habitat Viability Analysis Report for Thai Gibbons: Hylobates lar and H. pileatus. IUCN/SSC Conservation Breeding Specialist Group: Apple Valley, MN. pp. 23–36. Tan, B., 1985. The status of primates in China. Primates Conser. 5, 63–81. Wang, W., Ren, G.P., He, Y.H., Zhu, J.G., 2008. Habitat degradation and conservation status assessment of gallinaceous birds in the Trans-Himalayas. J. Wildlife Manage. 72, 1335–1341. Xiao, W., Ding, W., Cui, L.W., Zhou, R.L., Zhao, Q.K., 2003. Habitat degradation of Rhinopithecus bieti in Yunnan, China. Int. J. Primatol. 24, 389–398. Zhang, M.X., Fellowes, J.R., Jiang, X.L., Wang, W., Chan, B.P.L., Ren, G.P., Zhu, J.G., 2010. Degradation of tropical forest in Hainan, China, 1991–2008: conservation implications for Hainan gibbon (Nomascus hainanus). Biol. Conserv. 143, 1397– 1404. Zhou, J., Wei, F.W., Li, M., Zhang, J.F., Wang, D., Pan, R.L., 2005. Hainan black-crested gibbon is headed for extinction. Int. J. Primatol. 26, 453–465.