Introduction

Neotropical forests are areas of high biodiversity (Mittermeier et al. 2002) but are threatened due to human activities such as logging, hunting, and deforestation (Chapman and Peres 2001). There, primates represent a major group of vertebrates that play a fundamental role in forest regeneration (Heymann 1993). In the Guianas, the biogeography and conservation status of the primates are still poorly known, although the eastern part of this region has been better documented in recent years (Sussman and Phillips-Conroy 1995; Lehman 2000; Boinski 2002). The main goal of this research was to survey primate populations in the northeastern-most part of the state of Bolívar, Venezuelan Guayana, in the western Guiana Shield (Fig. 1).

Figure 1.

Location of sites surveyed in northeastern Venezuelan Guayana (see Table 1).

Table 1.

Sites surveyed in northeastern Venezuelan Guayana.

In a previous review, Bodini and Pérez-Hernández (1987) suggested that red howler monkeys (Alouatta seniculus), white-faced sakis (Pithecia pithecia), and wedge-capped capuchin monkeys (Cebus olivaceus) were present in this region. Ten years later, Linares (1998) reported the existence of golden-handed tamarins (Saguinus midas) and black spider monkeys (Ateles paniscus) there, although the evidence for the occurrence of these two primates remains unclear. That for S. midas is restricted to a general map and the name of Bochinche (Bolívar state) as the locality. Similarly, Kinzey et al. (1988) reported the possible presence of the night monkey, Aotus, in Venezuelan Guayana, but there has been no additional field research to confirm this. Kinzey et al. (1988) observed Alouatta seniculus, Cebus olivaceus, and Pithecia pithecia during their surveys in the Lago Guri–El Callao area (Venezuelan Guayana) (Fig. 1B), and local people reported what may be the night monkey Aotus and an Ateles-like monkey, but not tamarins.

The region I surveyed, located between that visited by Kinzey et al. (1988) and the Venezuelan–Guyanese border, represented a gap in our knowledge of the primate populations of the Guianas (Fig. 1). A survey of the Sierra de Imataca was of considerable importance due to increasing cattle ranching, agriculture, logging, and illegal mining that will result in significant forest loss and fragmentation over the coming years. My particular goals were to: a) determine the presence or otherwise of Saguinus midas, Ateles paniscus, Aotus and other primates; b) collect data on group size and the habitats occupied by primate species in the survey area; and c) interview local people to update our knowledge of the geographic distribution of Guayanan primates and document the human activities that may threaten them.

Methods

The reconnaissance sites were located mostly in the forested region of the Río Cuyuní basin. From north to south this area includes Río Grande, Altiplanicie de Nuria (Imataca), Tumeremo, Bochinche (Imataca), Anacoco–San Martín de Turumbán (Río Cuyuní), and El Dorado–La Fé-San Isidro; all in the northeastern part of the state of Bolívar, Venezuela, near the border with Guyana (Table 1, Fig. 1). The survey covered the Venezuelan drainage of the Río Cuyuní, one of the main tributaries of the Essequibo River in Guyana (Venezuela, Instituto de Ingeniería 1992). The vegetation there is mostly tropical evergreen humid forest with continuous canopies at heights of 20 – 40 m (Velasco and Aguilera 1987; Huber and Alarcón 1988). The climate is sub-humid/macrothermic and humid-perhumid/macrothermic, both >24°C (Velasco and Aguilera 1987). The region is in the Guiana Shield of Precambrian- age bedrock, with igneous and metamorphic rocks outcrops and limited, minor alluvial cover near the main drainage (Salazar and Briceño 1987). Altitudes range from 120 m a.s.l. in Anacoco and San Martín de Turumbán to 500 m a.s.l. in Altiplanicie de Nuria (Imataca) (Fig. 1).

The forests have been impacted by cattle ranching, agricultural expansion, so-called “selective” logging, and goldmining. The major sawmills there have logged between 1% and 20% of the commercial trees in their concessions (Bevilacqua et al. 2002). Given “current management [these] practices result in inadequate revenue capture and potentially high environmental costs” (Bevilacqua et al. 2002, pp.50–51). Illegal mining is also causing severe forest degradation besides health problems for the local communities (Bevilacqua et al. 2002). These abandoned mining “pods” are core locations for the propagation of malaria (Jorge Moreno pers. comm. 2003; Urbani pers. obs. 2003).

The survey was carried out from 30 June to 21 July 2003. A total of 49 sites were visited. Interviews were conducted at each site, and I walked pre-existing trails in secondary and primary forests, besides carrying out river censuses on the Río Cuyuni (Table 1, Fig. 1C). No transects were cut and only pre-existing trails were used (each walked just once) with the due permission of the owners or land managers. This field survey method (and the type of information recorded, see below) has been used in other rapid primate surveys in lowland South America (e.g., Heymann et al. 2002). Surveys covered approximately 790 km of roads, 55 km along the Río Cuyuní, and 22 km on pre-existing forest trails. When primates were seen, I recorded data on the behavioral activity, group size, height in the canopy, and sex/age composition of the group. Because of the large area to be covered in this rapid survey and the little time available, a more systematic census technique was impractical. Playback calls were used as an aid in locating tamarin populations, particularly in the Bochinche area where Linares (1998) reported them.

Interviews were conducted in 49 sites — towns and small caseríos (villages) located with a global positional system portable unit (Garmin GPS III) (Fig. 1C, Table 1) — to obtain information on the primate species present at each, their use by local communities (hunting, pets, use of body parts), and on perceptions of the behavior and ecology of the species. I avoided leading questions in order to avoid bias in the responses of the informants. In the initial questions I asked about the primates of the area, and their behavioral and physical descriptions, and only subsequently showed laminated color photocopies of primates in order to clarify their identity. I also included primates that have never been reported for this part of the Venezuelan Guayana (e.g., Callicebus lugens and Saimiri sciureus) to test the interviewees' knowledge. The informants were adult residents, including Amerindian capitanes (community leaders of the ethnic groups Kariña and Pemón), Amerindian and criollo (Venezuelan Creoles) local hunters, campesinos (criollo farmers), miners, loggers, local traders, Venezuelan national guards, Venezuelan and Guyanese Army soldiers, and Guyanese Carib Amerindians and Creoles.

Results

Only five primate groups were seen during the survey (Table 2). Four of these were A. seniculus and one P. pithecia. I heard red howler monkeys calls at six sites (Fig. 1C: numbers 1, 7, 21, 35, 39, and 47). The calls were heard mostly in the morning between 05:51 and 06:26, and later in the afternoon between 15:12 and 17:53.

Table 2.

Description of primate sightings (abbreviations: A = Adult, J = Juvenile, I = Infant, F = Female, M = Male, U = Unknown).

Ninety-seven people were interviewed at the 49 sites (Fig. 1C: 1–49; Table 1). All informants indicated that the only primate taxa in the region were P. pithecia, C. olivaceus and A. seniculus.

The following common names were obtained from the interviews:

Discussion

There was universal agreement among the informants as to the relative abundance of the three species: red howlers (Alouatta seniculus) > wedge-capped capuchin monkeys (Cebus olivaceus olivaceus) > white-faced sakis (Pithecia pithecia pithecia). The single saki sighting I achieved was of a multi-male and multi-female group of eight in an extremely degraded forest. There was an abandoned mining camp and evidence of a recent fire near the road. I was also told of P. pithecia living in a degraded forest on the outskirts of Tumeremo (c.10,000 inhabitants). The red howlers were seen in evergreen primary forests as well as in highly disturbed forests. These taxa were reported as the only primates present on the Guyana side of the Río Cuyuní. The informants indicated that white-faced sakis live in groups of two to nine individuals, while red howlers and wedge-capped capuchins form larger groups. I was also told that C. olivaceus and P. pithecia exploit guama trees (Inga spp., Leguminosae), and that wedge-capped capuchins tend to feed in slash-and-burn plantations.

Following the recommendation of Kinzey et al. (1988), I resurveyed an area they visited in 1988, on the upper Río Grande (Fig. 1C: 1–3). At the time of their study, they found white-faced sakis there. Fifteen years later, however I failed to observe any primates. I heard red howlers, and locals said that sakis and wedge-capped capuchins are often seen in the logged forest.

There was no evidence of the presence of Saguinus midas in the Bochinche area as reported by Linares (1998) (Fig. 1C, number 20 and adjacent sites). Here, local Kariñas and criollos identified just three primates, A. seniculus, C. olivaceus, and P. pithecia, with no reference of any animal similar to S. midas. Corroboration for the inexistence of S. midas in the region comes from Ochoa (2000), who worked on small mammal community structure in the Imataca region. He set up a trapping schedule for didelphids and small rodents that resulted in 10,320 trap nights (arboreal and terrestrial) using bananas as bait. The traps and bait were suitable for tamarins, but trapped none. He also spent 567 hours surveying mammals (diurnal and nocturnal) and his easternmost site was about 10 km west of Bochinche and found no evidence for the occurrence of tamarins. My attempts to locate them using Saguinus spp. and S. midas playback calls in secondary and primary forest around Bochinche also failed to detect any groups. A Guyanese Amerindian informant clearly indicated that tamarins occurred near the Essequibo River in Guyana, but not in the Río Cuyuní basin. This lends to support to Sussman and Phillips-Conroy's (1995) statement that this species does not occur west of the Essequibo River. Based on my survey, I suggest that S. midas is not present in the northeastern part of the state of Bolívar in Venezuela.

The possibility of Aotus occurring in the region, as was suggested by Kinzey et al. (1988) for the area of Río Grande, might be a reference to another nocturnal mammal. In many of the sites I surveyed the kinkajou (Potos flavus) was classified as a monkey. In the Venezuela Guayanan region it is referred to as the mono güinche and ueshé (in Kariña), while on the Guyanese side of the Río Cuyuní it is called night monkey or night traveler. In many cases, it was described as nocturnal, solitary, or living in pairs, marroncito (light brown) or amarillento (yellowish) and with cara de perro (dog-face), clearly indicating the kinkajou. An informant who knew this animal from western Venezuela called it cuchi-cuchi, which is the common name for P. flavus in the country. I also presented photographs of Aotus to the informants and they failed to recognize it. Bodini and Pérez-Hernández (1987) and Ford (1994) reported that the range of Aotus does not extend to this region. In two interviews, the three-toed sloth (Bradypus tridactylus) and the silky anteater (Cyclopes didactylus) were also classified as monkeys.

Linares (1998) indicated the presence of black spider monkeys (Ateles paniscus) in the Río Cuyuní area. He reported a sighting of four individuals in 1967 on the upper Río Cuyuní, and an observation in 1979 of a solitary individual near San Martín de Turumbán (Fig. 1C: number 29), which is very close to Anacoco (Fig. 1C: numbers 27, 28). In Anacoco, I saw wild P. pithecia and A. seniculus (Fig. 1C: Table 2). All informants in Anacoco and San Martín de Turumbán indicated that Ateles did not occur in the area. They included two Guyanese who knew black spider monkeys from the Potaro and Essequibo rivers in Guyana, but said they did not occur in Venezuela. One informant I interviewed on the upper Río Cuyuní clearly identified the three common primates of the area: P. pithecia, A. seniculus, and C. olivaceus, and the spider monkey. He said he had seen a pair in 1996 (Fig. 1C: number 36) and clearly described them as an Ateles, emphasizing their particular physical characteristics, a grayish color, and giving the Spanish name, mono araña. In El Dorado, I was also informed of a spider monkey- like primate, which was very rare but apparently existed in the Alto Paraguán of the Río Yuruán, a tributary of the upper Río Cuyuní (Fig. 1C). Kinzey et al. (1988) reported the possibility of Ateles near the Río Supamo, a tributary of the Río Yuruán, between the Río Caroní and the Río Cuyuní. Considering the color description of the Río Cuyuní specimen, its proximity to the Río Supamo basin, and the distribution of A. paniscus in Guyana, it is probable that rare, small, isolated populations of spider monkeys inhabit the Venezuelan Río Cuyuní basin, but this demands further investigation. Although reported absent from the Iwokrama Reserve west of the Essequibo River by Lehman (2000), a large population of black spider monkeys was studied in this reserve by Barth Wright (pers. comm. 2005), indicating that northwestern Guyana may be more densely populated with A. paniscus than previously believed, and that this species may well have crossed into this part of Venezuela (B. Wright pers. comm. 2005).

The only records of pet monkeys were four wedgecapped capuchins (C. olivaceus). Two were found in criollo villages (Fig. 1C: numbers 17, 24): an infant and an adult owned since it was young. A juvenile was being kept as a pet in a Pemón village, and another was in a Kariña village where I obtained the partial skeleton of an immature C. olivaceus pet (Fig. 1C: numbers 44, 18). Capuchins are the preferred primate pets in the region, and generally captured when young, after killing the mother. I was also told of a female P. pithecia that had been sold for about US$25, and another person informed me that white-faced saki tails are used for making key chains. Based on my interviews, primates were rarely preferred bush meat. Some locals argued that they look too much like humans, and informants alleged that rodents and ungulates, particularly agoutis (Agouti paca) and tapirs (Tapirus terrestris), were relatively abundant and preferred game animals in the region. Gold miners, on the other hand, reported hunting red howler because of its carne roja (red meat), but indicated that they tend to be rare near the mines.

Cattle ranching and habitat fragmentation are widespread in the region, especially in the area of Altiplanicie de Nuria- Tumeremo and the middle Río Botanamo. Forest patches are common, as are recently burned cleanings. Mining and logging are apparently reducing primate populations from the Río Botanamo to the Venezuelan-Guyanese border due to habitat loss and the creation of roads and trails in the Imataca forest, which provide for incursions of human disturbance and hunting. The consequences of such activities need to be studied in order to evaluate their effects on the primate communities and the implications for the conservation of the primates and forests of the Guianas in general.

Primate biogeographic studies are particularly needed in different areas of western Guyana, particularly in the Barama, Down Cuyuni, and Mazaruni river basins. This region is located between the east of the surveyed area in this project (the Venezuelan-Guyanese border in the Río Cuyuní basin) and the Potaro and Essequibo Rivers (Guyana), west of the regions surveyed by Lehman (2000) and Barnett et al. (2000). As such it fills a gap in our knowledge of the distribution and conservation status of the primates in the western Guianas. My findings reinforce the observed pattern of a gradual drop in primate diversity from east to west in the Guiana Shield, probably because of the existence of major rivers acting as biogeographic barriers such as the Essequibo (see Sussman and Phillips-Conroy 1995). It was possible to fully document the presence of only three primate species (A. seniculus, C. olivaceus and P. pithecia) in the northeastern part of the Venezuelan Guayana (= western Guianas), contrasting as such with the eight primates reported for eastern Guyana and Suriname (Lehman 2000; Boinski 2002). More surveys in isolated areas of the Guianas should be conducted to fully understand the primate biogeography of this broad region.