Introduction

Vietnam has a high diversity of primates; 25 species and subspecies of primates are known to occur there (Fooden 1996; Roos et al. 2007; Van Ngoc Thinh et al. 2010). However, a fast developing economy combined with illegal wildlife trade, habitat degradation and hunting has led to population declines in all species (Lippold and Vu Ngoc Thanh 1998). Currently, five of the world's 25 most endangered primates are found in Vietnam (Mittermeier et al. 2009).

One of these five species, arguably the most endangered in Vietnam (Schrudde et al. 2009), is the golden-headed or Cat Ba langur, Trachypithecus poliocephalus poliocephalus (Trouessart, 1911), which occurs only on Cat Ba Island in northern Vietnam (Schrudde et al. 2009). It belongs to the subfamily of the leaf eating monkeys (Colobinae) and has the smallest distribution of any of the langur species (Nadler et al. 2007). Cat Ba langurs are classified as Critically Endangered on the IUCN Red List (IUCN 2009) as a result of illegal hunting, which has led to small, isolated subpopulations and low population numbers. Poaching has resulted in a serious population decline from an estimated 2,400–2,700 individuals in the 1960's (Nadler and Long 2000) to only 52–54 individuals in 2000 (Stenke 2003). Concerned about the declining numbers, in 2000, Münster Zoo and the Zoological Society for the Conservation of Species and Populations (ZGAP) founded the Cat Ba Langur Conservation Project (CBLCP). The project's implementation of strict protection measures, such as the Langur Guarding Program, and the establishment of a langur sanctuary, has led to an increase in population numbers to 60–70 Cat Ba langurs at present (Schrudde et al. 2009). The remaining individuals at the time of writing are fragmented into six subpopulations of which some are all-female groups while others are isolated on small offshore islands.

Little information is available concerning the ecology and biology of the Cat Ba langur. Research on daily behavior patterns especially can provide crucial data for the conservation management of the Cat Ba langur with respect to population monitoring. The Cat Ba langur shows strict behavioral adaptations to its preferred limestone karst hill habitat. Throughout the year, for example, it sleeps in caves (Nadler and Long 2000). The Cat Ba langur is one of a number of karst-dwelling leaf monkeys that includes another five or six taxa of the T. francoisi group (Groves 2001, 2004; Schrudde et al. 2009) of which the white-headed langur (Trachypithecus p. leucocephalus) in China is its closest relative. Little is known about the ecology and behavior of the T. francoisi group, which makes reference material scarce. Investigating the behavioral adaptation of this species to its habitat could help to understand the species' biology and conservation requirements. Furthermore, data about the vertical ranging behavior of a species can provide important information for conservation and management programs (Clemmons and Buchholz 1997; Caro 1998). This paper describes the daily time allocation to different activities and the vertical ranging behavior of two wild groups of Cat Ba langurs.

Methods

Study area

Fieldwork was conducted on Cat Ba Island in Hai Phong Province, northern Vietnam (20°42′-20°54′N and 106°54′107°09′E). Cat Ba Island (140 km²) is part of the Cat Ba Archipelago which consists of 366 offshore islands (Viet and Lin 2001). The climate is humid, subtropical monsoon, with wet and dry seasons (Nadler and Long 2000). The wet season lasts from May to September and the dry season from November to March. The mean annual rainfall is 1,900 to 2,100 mm, and annual temperatures range from 23°C to 28°C (Viet and Lin 2001). More than half of the main island is covered by the Cat Ba National Park, including the study area. The study site covered an area of about 0.6 km², and is directly connected to human settlements and frequently used boat routes in the west. The area consists largely of vertical limestone cliffs, up to 300 m above sea level, with the slopes mostly covered with dense bushy vegetation (Nadler and Long 2000). Moist tropical limestone forest is found at the lower elevations.

Table 1.

Age and sex composition of the two free-ranging study groups of Cat Ba langurs, Trachypithecus p. poliocephalus.

Figure 1.

Trachypithecus p. poliocephalus adults, juveniles and infant of group GR10 at the study site. At the time the photograph was taken GR10 comprised six adults, two juveniles and two infants. The pelage gradually changes from all orange in infants to black with golden-yellow heads in adults. Photo by Johanna Rode, 2009.

Figure 2.

Floating village adjacent to the study site and the home ranges of GR6 and GR10. Human settlements close to the Cat Ba langur's habitat still pose a threat. Photo by Isabell Schneider, 2009.

Results

Time budget

One or more individuals were out of sight for the majority of observations (55% of the time). The Cat Ba langurs spent on average 66% of their time resting. Considerably less time was spent moving (11%) and foraging (15%), and in social behavior, which accounted for 8% of their daily activities.

Figure 3.

Comparison of time budgets (mean ± SE) between age classes for GR6 and GR10 combined (Adults: out of sight 53%; Juveniles: out of sight 66%; Infants: out of sight 65%).

The time budgets of adult and juvenile langurs were similar (Fig. 3), but infants spent one-third (33%) of their daily activities in social behavior, which included playing. Adult Cat Ba langurs, on the other hand, spent the least time of all age classes in social behavior (6%) and the most time resting (69%).

Vertical ranging pattern

The langurs spent more than half of their time in the top section of the hills (58%). The middle section was used for 29.5% of the time and the lowest part of the hill for 10.3%. They only spent 2.2% of the time in the valley. Generally, the langurs moved from one elevation to another 1.5 times per hour. The langurs spent more time resting on the hill slopes and cliffs, and especially near the top, than elsewhere. The time spent in social behavior decreased as they descended, and social behavior was not observed at all in the valley. Foraging activity increased considerably in the lower elevations and was predominant in the valleys (Fig. 5).

Figure 4.

Daily activity pattern of adult langurs of groups GR6 and GR10 for six time intervals between 06:00 and 18:00. Percentages of ‘Out of sight’ and ‘Time seen’ of the langurs are given for each interval.

Discussion

In this study the langurs were often difficult to see when in the dense vegetation which, as pointed out by Plowman (2006), can lead to underestimation of the frequency of certain behaviors. The fact that we observed the langurs only from some distance away might likewise have led to the frequency of some behaviors being underestimated and others overestimated. Resting and foraging were at times difficult to distinguish and small movements of the hands were difficult to see with the result that foraging as a behavior category may have been underestimated.

Figure 5.

Behaviors displayed in different elevations (GR6 and GR10 combined) and the number of hours that the langurs were recorded in each.

Figure 6.

Limestone karst hills on Cat Ba Island are the prime habitat for Trachypithecus p. poliocephalus. The densely vegetated lower slopes of the hills offer abundant food for the Cat Ba langurs. Photo by Pieter Levelink, 2010.

The results of this study show similarities as well as differences in the behavior patterns and spatial distribution of Cat Ba langurs compared to other species of the Trachypithecus francoisi group of karst langurs. The time budget of the folivorous colobines is largely influenced by their diet. They spend the majority of their time resting and considerably less time feeding and moving (Clutton-Brock 1977; Stanford 1991; Fleagle 1999), and this is evidently the pattern for the two Cat Ba langur groups that we have studied. Infants and juveniles spent considerably more time than the adults in social behavior—grooming and playing. The same is true for the white-headed langur (Li and Rogers 2004), and is associated with their physical and behavioral development and socialization (Poirier et al. 1978).

The langurs spent much of their day resting, especially in the morning hours and around mid-day up to 14:00 (more than 70% of each 2-hour period). Other langurs such as Francois' langur (Zhou et al. 2007), the Yunnan snub-nosed monkey (Rhinopithecus bieti) (Ding and Zhao 2004) and the white-headed langur (Huang et al. 2003) are similar in this respect. The two groups spent less time resting in the afternoon (50% to 55% of the two 2-hour periods from 14:00 to 18:00) and more time foraging. Duc et al. (2009) found that, while eating similar amounts of leaves through the day, the black-shanked doue langurs (Pygathrix nigripes) they studied ate more fruits (energy-rich) in the morning. They argued that this was to compensate for an energy deficit that they accumulate during the night (as suggested Clutton-Brock 1977; Oates 1987). Perhaps for this reason, the Cat Ba langurs spent a little more time foraging early in the morning (about 15% of the time from 06:00 to 08:00) but less than 10% of their time foraging for the rest of the morning and early afternoon up to 14:00. Lacking fruit for this purpose the langurs may be expected to rest more in order to save energy (Ding and Zhao 2004). Considerably more time was spent foraging in the afternoon (around 30%). Morning and afternoon foraging periods and similar patterns of moving have also been found for the white-headed langur (Huang et al. 2003), Francois' langur (Yang et al. 2007), the Yunnan snub-nosed monkey (Ding and Zhao 2004), and the Nilgiri langur (Semnopithecus johnii) (Sunderraj 1998). The preponderance of social activities around noon shown by the Cat Ba langurs has not been mentioned for other langur species.

Figure 7.

View from one of the fixed observation points showing the preferred limestone karst hill habitat of the Cat Ba langurs on Cat Ba Island. Photo by Johanna Rode, 2009.

Time budgets are in most cases influenced by seasonal changes in temperature. Stanford (1991) observed that from summer to winter, capped langurs (T. pileatus) increased their time resting from 26% to 41%, and decreased feeding time from 41% to 27%. Huang et al. (2003) also found that midday resting periods of the white-headed langur were related to season; their study group spent less time resting in winter (57%) than in Spring (79%) or Summer and Autumn (84%). We studied the Cat Ba langurs in the early summer when the rainy season begins. This would suggest that the time spent resting by Cat Ba langurs would be less in the winter periods and even more in the summer months. This seasonal variation in time budget could influence the probability of observing the langurs, and thus the efficiency of the monitoring program. Long-term research on time budgets of the Cat Ba langurs is required for that reason.

The results of this study show that the Cat Ba langurs spent most of their time on the highest reaches of the cliffs and hills. This contrasts with the study of Li and Rogers (2005) on the white-headed langurs, which were found to use the lower slopes most of the time (60%). Li and Rogers (2005) suggested that this resulted from a preference for the less fragmented and less disturbed habitats found in the denser vegetation of the lower slopes and valleys in the Fusui Precious Animal Reserve where they lived. Like Fusui, the vegetation in the study area on Cat Ba Island was taller and less fragmented on the lower slopes of the hills but the langurs still used the upper slopes more often. This may indicate that the vertical ranging of the langurs was not directly influenced by the vegetation but by hunting. Cat Ba langurs do not have natural predators but have experienced severe hunting in the past (Nadler and Long 2000; Schrudde et al. 2009) and are still threatened by the presence of humans close by. Likewise, white-headed langurs were reluctant to go to the ground when humans were near (Li and Rogers 2005).

The Cat Ba langurs called a lot when on the upper slopes, perhaps to maintain contact, perhaps to alert group members of predators, convey behavioral states, attract mating partners or in territory defense (Eschmann et al. 2008).

With respect to their vertical ranging behavior, the langurs tended to rest when on the upper slopes of the hills. Tarsiers and baboons do the same (Fleagle 1999), possibly to avoid predation when they are inactive. The same reasoning would apply for the social behavior which decreased on the lower slopes the hills, as the vigilance levels in primates are usually lower during grooming (Cords 1995). The Cat Ba langurs spent more time foraging on the lower slopes of the hills. The same was found for white-headed langurs, which carried out their maintenance activities such as feeding in the lower and middle slopes (Li and Rogers 2005) as a result of high food diversity (Huang et al. 2008). However, one must be careful with these conclusions as the sample size differed for each elevation level, and was especially small for the valley.

Overall, studies on closely related species such as the white-headed langur and Francois' langur suggest that vertical ranging patterns and their activity budgets are strongly dependent on food availability, food diversity and probably human presence. This study has discovered similar dependencies for the Cat Ba langurs. Their vertical ranging pattern is likely adapted to the abundant food in the lower parts of the hills as well as to possible threats from humans. However, since food availability/diversity and human presence have not been measured quantitatively in this study we propose further research in this direction to find possible limiting factors in the distribution of Cat Ba langurs across the island.

In our study, the langurs were most often seen between 06:00 and 10:00, while observations in the afternoon were limited to the period between 14:00 and 16:00. The fact that the langurs were seen less in the late afternoon could be explained by their return to the sleeping caves, which generally faced the open water and were obscured from our observation posts. When censusing the population it is essential to detect all individuals of a group, and we found that most individuals were usually seen between 08:00 and 12:00 in the morning, when ‘out of sight’ rates were smallest for both study groups. The crucial time for monitoring would be from 08:00–10:00, while the optimal hours for detecting all individuals of a group would be until 12:00. Keeping in mind that there is a potential seasonal effect on the time budget, which could alter the probabilities of observing the langurs and getting good counts, the most favorable hours for monitoring could be different in the summer and winter periods.