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DSpace at VNU: Distribution and Population Densities of Diurnal Primates in the Karst Forests of Phong Nha-Ke Bang National Park, Quang Binh Province, Central Vietnam

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Int J Primatol (2009) 30:301–312 DOI 10.1007/s10764-009-9343-4 Distribution and Population Densities of Diurnal Primates in the Karst Forests of Phong Nha – Ke Bang National Park, Quang Binh Province, Central Vietnam Tanja Haus & Martina Vogt & Bernhard Forster & Ngoc Thanh Vu & Thomas Ziegler Received: August 2008 / Accepted: 18 December 2008 / Published online: February 2009 # Springer Science + Business Media, LLC 2009 Abstract We studied the status and distribution of the diurnal primates in the Phong Nha – Ke Bang National Park (PNKB NP) from April to August 2007 In the past, researchers reported primate species and subspecies for the karst forests of PNKB NP, which constitutes the most important protected area for the endangered Hatinh langur (Trachypithecus hatinhensis) in Vietnam All primate taxa are threatened due to hunting pressure and habitat loss We applied line transect sampling in areas During a total of 117 transect inspections along 12 different transect routes, we confirmed primate taxa and the analysis of population densities resulted in 2143 (±467) Hatinh langurs, 1316 (±871) red-shanked douc langurs (Pygathrix nemaeus), 930 (±489) stump-tailed macaques (Macaca arctoides), 986 (±883) eastern Assamese macaques (M a assamensis), and 18 (±18) southern whitecheeked crested gibbons (Nomascus siki) in the whole PNKB NP, which covers an area of ca 85,000 We could not detect the nocturnal lorises, Bengal slow lorises (Nycticebus bengalensis) and pygmy slow lorises (N pygmaeus), as well as T Haus Zoologisches Forschungsmuseum Alexander Koenig, 53113 Bonn, Germany T Haus AG Zoologischer Garten Köln, 50735 Köln, Germany M Vogt : B Forster Phong Nha – Ke Bang National Park, Son Trach Commune, Bo Trach District, Quang Binh Province, Vietnam N T Vu University of Science, Faculty of Biology, Department of Vertebrate Zoology, Zoological Museum, Vietnam National University, Thanh Xuan, Hanoi, Vietnam T Ziegler (*) AG Zoologischer Garten Köln, 50735 Köln, Germany e-mail: ziegler@koelnerzoo.de 302 T Haus et al rhesus macaques (Macaca mulatta) and northern pig-tail macaques (M leonina) The distribution of the primates predominantly depended on human impact We could not recognize a correlation between habitat constitution and abundance of primates The population density estimates showed a much higher density of the Hatinh langur than previously assumed Thus the importance of the PNKB NP for the conservation of this endangered langur increased significantly Keywords Hatinh langur (Trachypithecus hatinhensis) Phong Nha – Ke Bang National Park Vietnam population densities primate census Introduction Phong Nha – Ke Bang National Park (PNKB NP) is located in the Central Annamite Mountains (170°20′–170°48′N and 1050°46′–1060°24′E) in Quang Binh Province, Vietnam and was declared a UNESCO World Heritage Site in 2003 (Vogt et al 2006; Ziegler et al 2004) Pham Nhat and Nguyen Xuan Dang (2000) documented of the 24 primate taxa known to occur in Vietnam (Nadler and Streicher 2004) for the karst forests of PNKB NP The taxa represent genera and families of both Strepsirrhini and Haplorrhini: Hatinh langurs (Trachypithecus hatinhensis), redshanked douc langurs (Pygathrix nemaeus), stump-tailed macaques (Macaca arctoides), eastern Assamese macaques (M a assamensis; subsequently simply referred to as Assamese macaque, M assamensis), rhesus macaques (M mulatta), northern pig-tail macaques (M leonina), southern white-cheeked crested gibbons (Nomascus siki), and the nocturnal lorises Bengal slow lorises (Nycticebus bengalensis) and pygmy slow lorises (N pygmaeus) Here we follow the taxonomy of Groves (2005) All taxa are listed in the IUCN Red List of Threatened Species and in the Red Data Book of Vietnam (Nguyen Vu Khoi and Shaw 2004; IUCN 2007) They are threatened due to habitat loss and hunting pressure (Nadler et al 2003; Timmins et al 1999; Vogt and Forster 2008; Vu Ngoc Thanh et al 2004) Hatinh langurs and red-shanked douc langurs are endemic to the karst forests of the Truong Son (Annamite Mountains) in Central Vietnam and Laos The distribution of Hatinh langurs is restricted to Vietnam’s Quang Binh and Quang Tri provinces (BirdLife International Vietnam Programme 2005; Nadler et al 2003) Besides the recently declared Bac Huong Hoa Nature Reserve in Quang Tri, the PNKB NP is the only protected area within the distribution range of Hatinh langurs in Vietnam (Nguyen Manh Ha 2006; Timmins et al 1999) There have been several recent surveys to determine the biodiversity of the PNKB NP including studies focused on primates (Dinh Hai Duong 2005; Le Khac Quyet et al 2002; Le Xuan Canh et al 1997; Nguyen Quang Vinh 2002; Timmins et al 1999) Results of these investigations showed that the density of most primate species and subspecies seems to be relatively low However, these data did not provide estimates of the population densities To protect endangered species and to observe important changes of population structure and size in time, data collected by standardized census methods are necessary To date there have been approximations of only 520–750 Hatinh langurs occurring in that area (Le Xuan Canh et al 1997; Diurnal Primates in Phong Nha – Ke Bang National Park 303 Pham Nhat et al 1996) Thus it was essential to investigate for the first time the population densities of the primates in the PNKB NP Methods Study Site PNKB NP is in the western part of Central Vietnam 500 km south of Hanoi and borders on Laos (Fig 1) It includes ca 85,000 of karst forests, providing habitat for many endemic species of both flora and fauna (Herrmann and Pagel 2000; Timmins et al 1999; Ziegler et al 2006, 2007) The area is characterized by steep limestone hills, which are covered by dense forests The evergreen primary forest, which has remained almost unaffected, accounts for ca 88% of the area (Cao Xuan Chinh 2005) Large portions of the National Park are 500–1000 m above sea level (Herrmann and Pagel 2000) Census Method and Data Collection We conducted line transect sampling in different areas in the PNKB NP from April to August in 2007: Cha Noi in the north, Hung Lau and Hang E in the east, and Ban Doong in the southeast of the National Park (Fig 1) We did not include the difficult-to-access southwest part of the National Park because of time limits Except for Hang E, the survey areas are composed predominately of unaffected primary forests The Hang E area is situated near villages in the border zone and is delimited by roads that cross the National Park (Fig 1) The survey area is characterized by a flat lowland valley surrounded by steep limestone cliffs and hills The valley is Fig Location of the survey areas in the Phong Nha – Ke Bang National Park in Central Vietnam 304 T Haus et al covered by dense secondary forest, whereas the surrounding higher elevations are covered by primary forest In each of the survey areas we defined different line transects (Hung Lau: HL1–3, Hang E: HE4–6, Cha Noi: CN7–9, Ban Doong: BD10–12), which ran nearly parallel at ca 500 m from each other or from the base-camp in different directions (Peres 1999) In Hang E, we could not maintain the minimum distance throughout the transect lines because of terrain topography According to Ross and Reeve (2003) it is less important if objects are detected twice in different transect walks of the same transect or in walks of different transects, provided that detections are independently; then they should be treated as separate independent encounters for analyses Because of dense vegetation and the prevalence of steep and cliffy terrain, we predominantly used preexisting trails as transects We marked parts of transects, and transects not following trails, by snapping off branches In addition, we tracked all transects via a GPS (Garmin GPS 60) with an external antenna (Gilsson Technologies, High Gain GPS Antenna, MCX) Because of the assumed low density of primates, ideally we should have surveyed each transect 10 times during study periods from April to June and July to August 2007, but we surveyed the transects BD10 and BD11 only and times respectively, due to weather conditions The length of transects varied between 1.74 km and 5.03 km; depending on terrain and distance we were able to walk in a 4-h interval We walked very slowly and as quietly as possible, stopping often to avoid obstacles and uneven ground to meet the assumptions that all primates are detected directly on and above the transect line and not move before in response to the observers (Buckland et al 2001; Ross and Reeve 2003) We walked each transect twice a day, between 0600 h and 1000 h and 1400 h and 1800 h during the greatest periods of diurnal primate activity (Peres 1999) The duration of a single transect walk varied depending on time allocated to detection events and data collection We kept a midday period of ca h to avoid influencing observations on the afternoon walk In the event of rainfall we would pause the survey until the rain stopped, due to bad visibility and the distracting noise caused by the rain Two observers recorded the data, and both surveyed each transect route 4–6 times A team consisting of ≤3 people accompanied the observers, a National Park staff member, rangers, and local guides We recorded date, start and ending time, transect identity, weather conditions, personnel, and human activities of each transect walk and species identity, group size, group structure, cue, activity, substrate, sighting height in the tree, vegetation features, and GPS coordinates (Garmin GPS 60 with external Antenna and Garmin GPS 12) at every detection event To analyze the population density we measured the perpendicular distance or the radial distance and the angle relative to the transect line to each first sighted individual via a range finder (Bushnell, Yardage Pro Legend) and an angle board (Buckland et al 2001) Transect Measuring and Vegetation Description To compare the primate densities between the different transects and survey areas, we measured the surface area of each transect; for this purpose, we measured the perpendicular visibility range to both sides of the transect line at every 20 m on average by a range finder Thereby several sections originated, the surface area of Diurnal Primates in Phong Nha – Ke Bang National Park 305 which we calculated from the length and the mean of the lateral visibility ranges at the beginning and the end of the section The sum of all surface areas resulted in the total area of each transect The basic vegetation structure was described by parameters determined for each section of transect We measured the height of canopy via a range finder and determined canopy cover by measuring the percentage of open sky We estimated the density of understorey by percentage of ground covered with vegetation and the growth of liana on a scale from to (1: few, 2: medium, 3: plenty) Data Analyses The applied distance sampling method assumes that only a proportion of primates will be seen and that the detection probability decreases with increasing distance from the line We used DISTANCE (Version 5.0, Thomas et al 2006) to fit a set of detection probability models to the observed perpendicular distances, and selected the best model showing the smallest value of Akaike’s Information Criterion In this manner, DISTANCE estimates the proportion of primates missed by the survey and computes the population density in the survey area (Thomas et al 2002) In multispecies surveys of animals similar in size and aural cues, the data of all taxa can be pooled to estimate a common detection function increasing sample size and statistical power (Buckland et al 2001) Based on poststratifying (Thomas et al 2006), we obtained the mean group size and population density estimates of each taxon We conducted Mann-Whitney U and regression tests —linear correlation (r) or Spearman rank correlation (rs)— on a level of significance with α=0.05, using PAST (Hammer et al 2001) The encounters along transects were partially clustered To analyze the relation between vegetation structure and primate abundance, we divided each transect into equal parts to obtain more small-scale vegetation descriptions and to specify potential influence of the vegetation structure Results During survey phases we conducted 117 transect inspections covering an area of 2410.47 on a length of 358.15 km There is no significant difference in the number of encounters across the observers (N1 =47, N2 =49, p=0.317), and the number of sightings is independent of the number of team members (N=121, rs =0.028, p=0.757) Further, the number of observations not differ significantly across the morning and afternoon transects (Nam =68, Npm =53, p=0.845) We recorded 72 observations of diurnal taxa Sighting events and observed group sizes of each taxon were relatively low (Table I) We detected no correlation between group size and perpendicular distance (N=43, r=−0.239, p=0.122) Hatinh langurs were present in each of the survey areas, and we encountered significantly more Hatinh langurs than stump-tailed macaques (N=12, p=0.018), Assamese macaques (N=12, p=0.038), and white-cheeked crested gibbons (N=12, p=0.001) 306 T Haus et al Table I Number of observed groups (n), mean group size (M), and range (R) in comparison with results of previous studies Current study Results of previous studies n M R M R Source Trachypithecus hatinhensis 27 3.54 1–10 Pygathrix nemaeus Macaca a assamensis 13 12 6.25 5.11 1–11 1–12 2–18 1–11 6–24 1–20 10–50 Pham Nhat et al 1996a Haus et al., unpubl datab Lippold and Vu Ngoc Thanh 2008c Haus et al., unpubl datab Fooden 1971d Macaca arctoides Nomascus siki 5.89 2–11 7.30 5.09 14.25 7.14 – – – Phong Nha – Ke Bang (PNKB) and adjacent areas Recorded during point transect sampling in the PNKB National Park in 2007 c Son Tra Nature Reserve, Da Nang, Vietnam d Western Thailand a b We recognized differences in species distribution and abundance across the survey areas and transects The fewest primate species (2 species) occurred in Hang E and the most (5 species) in Hung Lau (Fig 2a) We observed most Hatinh langurs in Hang E, where in addition only Macaca was present Red-shanked douc langurs were the second most frequent species, which were most common in Hung Lau (Fig 2) We observed Assamese macaques most often in Ban Doong, whereas we recorded all sightings on the same transect (BD12, Fig 2) We observed a single white-cheeked Fig Distribution and density of recorded primate groups throughout the survey areas (a) and transects (b) from April to August in 2007 Diurnal Primates in Phong Nha – Ke Bang National Park 307 crested gibbon only once in Hung Lau on HL1 (Fig 2) For all species combined, the highest primate densities were on BD12 in Ban Doong and on HL1 in Hung Lau, and the lowest on HL2 and HL3 in Hung Lau (Fig 2b) Population density estimates received from DISTANCE (Table II) showed highest density with lowest standard deviation (SD) for Hatinh langurs If we analyzed the population density with a higher mean group size of 5.09 individuals, derived from point transect sampling in the PNKB NP in 2007 (Haus et al., unpubl data), the population density of Hatinh langurs increased by 44% (Table II) We estimated the lowest density with highest SD for southern white-cheeked crested gibbons In addition to the single encounter of the southern white-cheeked crested gibbon in Hung Lau, we heard several song bouts early as well as late in the morning and during midday on different days Between 0512 h and 0649 h we noticed both solos of a single male and duet song bouts One time we heard pairs simultaneously from different directions During the midday breaks on HL1 we heard duet song bouts as well as a male solo song bout; the latest song bout was produced at 1320 h Even though we did not record any gibbon in Ban Doong during survey time, male and female individuals sang between 0454 h and 0530 h on d We noticed duet song bouts of pairs simultaneously from different directions as well as a solo song bout of a single male The analyses of the vegetation parameters of the transects show no correlation between canopy cover (N=34, rs =0.184, p=0.298), height of canopy (N=34, rs =−0.045, p=0.799), density of understorey (N=34, rs =−0.064, p=0.719) and growth of liana (N=34, rs =0.12, p=0.5), and primate abundance, neither for all species pooled, nor for any single species During the transect surveys we met 42 groups of people, who passed through the PNKB NP for logging activities Most people came from villages of the border area The primate abundance correlates significantly negatively with the number of loggers encountered on transects (N=111, rs =−0.336, p=0.001; Fig 3), as does the number of camp sites and recorded primates (N=12, r=−0.688, p=0.013; Fig 4) Table II Number of observed groups (n) and population density estimates of the primates in the Phong Nha–Ke Bang National Park (PNKB NP) in 2007 n Trachypithecus hatinhensis Trachypithecus hatinhensisb Pygathrix nemaeus Macaca a assamensis Macaca arctoides Nomascus siki a 27 27 13 12 Population densities DISTANCE Groups/100 Individuals/100 Individuals in the PNKB NPa 0.495±0.108 0.495±0.108 0.248±0.157 0.227±0.193 0.186±0.094 0.021±0.021 1.754±0.500 2.520±0.550 1.548±1.024 1.160±1.093 1.094±0.575 0.021±0.021 1491±425 2143±467 1316±871 986±883 930±489 18±18 Area of the PNKB NP: 85,000 Densities using an average group size of 5.09 (derived from point transect sampling in the PNKB NP in 2007; Haus et al., unpubl data) b 308 T Haus et al Fig Relation of abundance of primates and loggers on transects Discussion Distribution Except for Hang E, we observed similar numbers of taxa and primate densities in all survey areas Hang E is in the border zone and is delimited by the roads crossing the National Park Hunting pressure and habitat disturbance become more apparent in such restricted areas Roads often constitute an impassable barrier for many species and obstruct migration of primate groups (Nadler et al 2003) Owing to the lack of exchange possibilities with other groups of adjacent areas, already disturbed populations can hardly regenerate Nevertheless we noticed a distribution peak of Hatinh langurs in Hang E The wide valley is surrounded by steep limestone cliffs, which offer the species many potential sleeping sites The single encounter of Macaca during transect surveys in Hang E was a specimen seen near the campsite in the morning Most probably it was an Assamese macaque, because we recorded a male specimen that was unmistakably referred to this species in the immediate Fig Relation of abundance of primates and camp sites on transects Diurnal Primates in Phong Nha – Ke Bang National Park 309 vicinity of the campsite in the evening Macaques seem much more likely to cross roads than the colobines or gibbons White-cheeked crested gibbons occurred in only of the survey areas and seem to be restricted to certain regions of the National Park The species usually inhabits elevations 30–100 m above sea level (Geissmann et al 2000), but we observed it ≤600 m above sea level in Hung Lau and also in elevations 176–398 m above sea level in Ban Doong, where we heard song bouts The karst forests of the PNKB NP, predominantly >100 m above sea level, are a suboptimal habitat for the taxon (Herrmann and Pagel 2000) The restricted distribution could also be due to the specialized diet, making the species dependent on the availability of widespread ripe fruits (Geissmann 2003) In previous studies, researchers documented northern pig-tail macaques and rhesus macaques for the PNKB NP, but we did not recognize the species during the mo There are different data about the distribution of northern pig-tail macaques in Vietnam According to Fooden (1996), the distribution stretches from 14°41′N southward (southernmost part of PNKB NP: 17°48′N) and there exists only disputed information about an occurrence farther to the north Nevertheless Le Xuan Canh et al (1997) and Timmins et al (1999) recorded the species in the PNKB NP in the past During more recent studies, northern pig-tail macaques were not recorded (Dinh Hai Duong 2005; Le Khac Quyet et al 2002; Nguyen Quang Vinh 2002) Information of records of rhesus macaques also varies from study to study; Pham Nhat et al (1996), Le Xuan Canh et al (1997), and Dinh Hai Duong (2005) found rhesus macaques, whereas Timmins et al (1999), Le Khac Quyet et al (2002), and Nguyen Quang Vinh (2002) failed to record the species In Nepal, within the distribution range of western Assamese macaques (Macaca assamensis pelops), mulatta and pelops occur parapatrically due to the similar niche utilization (Wada 2005) Hence status and distribution of northern pig-tail and rhesus macaques in the PNKB NP are still unclear and should be emphasized in further studies Because we conducted surveys only in daytime, we did not see any of the nocturnal lorises There is only minor evidence of the lorises, due to their cryptic behaviour at day and low numbers of night surveys conducted in the PNKB NP Most data are based on interviews with local hunters (Le Xuan Canh et al 1997) Vogt and Ziegler observed pygmy slow loris in the PNKB NP during a night survey on June 14, 2005 To determine their status and distribution in the PNKB NP, we recommend night surveys focused on lorises in the near future We found no correlation between vegetation parameters and primate abundance But at large, the vegetation structures of the transects did not differ greatly from each other A more detailed habitat description and phenology would be necessary to determine primate distribution depending on habitat structure Population Sizes In dense habitats, group sizes are easily underestimated because not all individuals are detected due to bad visibility conditions and the fact that group members may be dispersed over a large area This can influence the estimation of population densities Mean group sizes in our study were relatively low compared to results of previous surveys in the area We often observed a single male Hatinh langur (in 10 of 27 310 T Haus et al cases) sitting and scanning in the top of a tree The possibility remains that other group members were undetected in the dense vegetation beneath, but because they were not observed this is simply a hypothetical supposition Therefore the population density estimate of the Hatinh langur based on our reliable mean group size of 5.09 results in a population estimate of 2143 (± 467) individuals for PNKB NP This is a more reasonable estimate than that offered by Pham Nhat et al (1996), who suggested that ca 520–670 individuals were in the PNKB area or Le Xuan Canh et al (1997), who estimated ≤750 individuals Thus the density of Hatinh langurs is much higher than previously assumed Timmins et al (1999) recorded only group of red-shanked douc langurs during a 4-mo study Based on results of previous studies, they assumed the population of the species had undergone a more significant decline than most other primate species Consistent with our results, red-shanked douc langurs were more often observed in recent surveys (Dinh Hai Duong 2005; Nguyen Quang Vinh 2002), and appear to be the second most frequent primate species in the PNKB NP today In contrast to those of Timmins et al (1999), our results show that Assamese and stump-tailed macaques are less common than Hatinh and douc langurs within the study area This may be due to the methods used by the different authors, or the populations of the langur species may have increased within the past few years and the macaque populations may have declined Stump-tailed macaques often forage on the ground, making them easier to trap than the other primate species Consequently it is the most frequently confiscated species in the Rescue Centre of the PNKB NP, often showing limb injuries caused by snare traps The population estimate of southern white-cheeked crested gibbons is based on only observation, and therefore likely reflects a low density in the PNKB NP Solo songs of crested gibbons appear to be produced only by nonmated males (Geissmann et al 2000) Thus we confirmed ≥10 individuals in Hung Lau and Ban Doong based on vocalisations In addition, we observed individuals at km 33.12 (Ho Chi Minh Road) in the PNKB NP in 2007 Ruppel (2007) tape-recorded song bouts of the gibbons along 40–52 km at the Ho Chi Minh Road and recorded ≥30 individuals Consequently there are ≥43 individuals in only a part of the PNKB NP The population densities are most likely underestimated because of low mean group sizes and human impact on primate density along transects Nevertheless there are more Hatinh langurs than assumed before, which reinforce the importance of the PNKB NP for the conservation and long-term survival of this endangered species To our knowledge, this was the first systematic survey to determine primate densities in Vietnam Further research on population densities is preferable in the near future to determine priority primate conservation areas in Vietnam and to effect appropriate conservation measures Acknowledgments We thank the People's Committee of Quang Binh, the Phong Nha – Ke Bang National Park directorate and Science Research Centre, and the Centre for Natural Resources and Environmental Studies, Hanoi, for their cooperation and issuance of the necessary permits For financial support we thank the Cologne Zoo and the Frankfurt Zoological Society We also thank the Phong Nha – Ke Bang National Park directorate for providing literature Special thanks go to Nguyen Hoang Dung, assistant of the Cologne Zoo Nature Conservation Project Vietnam/Frankfurt Zoological Society, for translation, supporting cooperation with local people, and for his constant helpful advice We also thank all staffs of the Phong Nha – Ke Bang National Park joining our surveys for their field assistance and Diurnal Primates in Phong Nha – Ke Bang National Park 311 cooperation Professor Dr Herbert H Covert, University of Colorado kindly commented on a previous version of the manuscript, and we thank him for his careful revision and helpful suggestions Last but not least, T Haus thanks Professor Dr Wolfgang Böhme of the Zoologisches Forschungsmuseum Alexander Koenig, Bonn, for supervising her diploma thesis at Bonn University References BirdLife International Vietnam Programme (2005) The rare Hatinh langur discovered in Quang Tri province for the first time News Release Available from Accessed January 24, 2008 Buckland, S T., Anderson, D R., Burnham, K P., Laake, J L., Borchers, D L., & Thomas, L (2001) Introduction to distance sampling Estimating abundance of biological populations New York: Oxford University Press Cao Xuan Chinh (2005) Conservation and development of the heritage values of Phong Nha–Ke Bang National Park, current situation and solution In Training Workshop 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Number of observed groups (n) and population density estimates of the primates in the Phong Nha–Ke Bang National Park (PNKB NP) in 2007 n Trachypithecus hatinhensis Trachypithecus hatinhensisb Pygathrix... species in the immediate Fig Relation of abundance of primates and camp sites on transects Diurnal Primates in Phong Nha – Ke Bang National Park 309 vicinity of the campsite in the evening Macaques

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