New information about the distribution of Callicebus (Pithecidae, Primates) in northern Beni Department, Bolivia

Nueva información acerca de la distribución de Callicebus (Pithecidae, Primates) en el norte del Departamento del Beni, Bolivia

Jesus Martínez¹ & Robert B. Wallace^1,2

¹Wildlife Conservation Society, GreaterMadidi-Tambopata Landscape Conservation Program, Casilla 3-35181, San Miguel, La Paz, Bolivia.
Email: jmartinez@wcs.org Corresponding author ]]> ²Wildlife Conservation Society, 185th Street and Southern Boulevard, Bronx, Nueva York 10460, USA

Callicebus is one of the most diverse genera of primate in the Neotropics, including 30 recognized species of titi monkeys (Van Roosmalen et al. 2002, Wallace et al. 2006, Defler et al. 2010). In Bolivia, the distribution, diet and behavior of titi monkeys is poorly known and even the number and identity of species is unclear (Wallace et al. 2006, Martinez & Wallace 2010).

Two of the six species of titi monkeys recognized for Bolivia are endemic: Callicebus modestus (Beni titi monkey) and Callicebus olallae (Olallae's titi monkey), both locally named as "lucachis" (Hershkovitz 1988, Anderson 1997, Rylands et al. 2000, Van Roosmalen et al. 2002, Wallace et al. 2006, Martinez & Wallace 2010). Both species were categorized as Endangered (Veiga et al. 2008 a, b, Tarifa & Aguirre 2009).

Since original descriptions by Lönnberg (1939), taxonomic studies have consistently maintained these endemic monkeys as full species (Hershkovitz 1990, Kobayashi 1995, van Roosmalen et al. 2002). No new field data was available for these species until Felton et al. (2006) and Martinez & Wallace (2007) identified the physical diagnostic characteristics useful for field identification and reported new localities for both Callicebus endemics, establishing the principal limits of their distributional range in a restricted area within the forest patches of the western part of Beni Department, especially for C. olallae that is almost exclusively present along theYacuma river.

The northern limit remained unclear because ca. 185 km separates the northernmost record of C. modestus and the southernmost record of another species of Callicebus inhabiting the Amazonian forest of the northern region of Beni Department, previously assumed to be Callicebus brunneus (Hershkovitz 1990). Here we present observations of titi monkeys made in September 2008 evaluating the distribution of Callicebus in the northern part of the Beni Department of Bolivia.

Methods

The second survey area was around the Coquinal community at Rogaguado Lake (12°58'15.24" S, 65°51'33.30" W), located to the northwest of Santa Ana de Yacuma. Anecdotal evidence from two people who had heard Callicebus territorial calls (Y. Janco and M. Herrera pers. comm. 2007) suggested this forest area as potential habitat for Callicebus. Satellite imagery showing forest cover demonstrated that it is a relatively large but isolated forest patch surrounded by savannah and separated from other large forest patches by approximately 30 km (Fig. 1).

We searched for titi monkeys groups at each locality for four days. We consulted with local people about the best potential locations using pictures and recordings of their characteristic territorial calls. To observe Callicebus groups we firstly attempted to determine their location by their territorial calls early in the morning between 06:00-10:00 h corresponding with the highest vocal activity period (Kinzey 1981, Martinez & Wallace 2007). Vocalization playbacks were also used to promote vocal responses. Complementary searching was made during the afternoon (16:00-18:00 h). Once a group was located from vocalizations, we observed individuals with binoculars (Swift 10 x 42) and attempted to film them using a handheld video recorder (Sony Digital 8 Video Camera TRV 361). For each observed Callicebus group we noted the fur color patterns of the individuals, as well as group size, composition, height in the forest canopy, general habitat description, and geographic location (GPS Garmin III Plus).

To confirm the field species identifications, we compared video footage and descriptions of pelage with previous descriptions from Bolivian Callicebus species (Lönnberg 1939, Felton et al. 2006, Martinez & Wallace 2007, 2010). With the new Callicebus localities we actualized a distribution map for this genus in northern Beni Department.

Results

We identified two phenotypes of Callicebus. At Coquinal we observed six of twelve Callicebus donacophilus groups that were detected by vocalizations. Individuals showed characteristic grayish brown agouti pelage dorsally with the tail lighter than the body. This color pattern clearly contrasts with the reddish coloration of the body fur of both C. modestus and C. olallae, with the latter having a dark gray tail pelage.

The conspicuous white ear tufts and a similar coloration on the mouth area of the face, together with the light grayish coloration of hand and feet pelage were other features useful to distinguish this species from the endemic Callicebus that have relatively small ear tufts with a different gray tone on the fur of hands and feet. Juveniles of C. donacophilus also showed an almost white tail as well as characteristic head coloration patterns where white ear tufts are small and almost all of the face had abundant grayish fur, with only the eyes and part of the nose and mouth darker(endemic Callicebus juvenile heads have almost the same color pattern as adults). An important observation was the orange coloration in the ventral region of the body, arms and legs on some adult males, apparently a color variation related to the reproductive season (K. Dingess, pers. comm. 2007).

Currently the identity of this last species remains uncertain (Wallace et al. 2006, Martinez & Wallace 2010). Previous Callicebus taxonomic revisions reported C. brunneus (Hershkovitz 1990, Anderson 1997) or C. dubius (Van Roosmalen et al. 2002, Salazar-Bravo et al. 2003) as the expected titi monkey form in the northern Amazonian forests of Bolivia. However, the descriptions presented above do not correspond to either C. brunneus (Vermeer 2009) or C. dubius (van Roosmalen et al. 2002) and as such probably represents a different species (Martínez & Wallace 2010), possibly Callicebus toppini, known from locations north of the Madre de Dios River in neighboring southeastern Peru(Thomas1914, R. Wallace unpubl. data).

Group size for both observed species varied between two and four individuals. For C. donacophilus, adult individuals were always present in the groups (62.5% of age composition, n=16), accompanied by juveniles and subadults (25.0% and 12.5% of age composition respectively). The observed Callicebus sp. group had only an adult pair.

The Australia locality is situated in the southern part of the northern Amazonian forests of Bolivia where the landscape consists of several forest islands with high densities of vines and a dense understory surrounded by natural grasslands. Overall tall forests dominated (canopy reaches ca. 25 m), but forests inhabited by Callicebus were lower in stature (canopy ~15 m) and usually located at the forest borders near grassland, where relatively higher densities of "motacú" palm trees (Attalea phalerata) occurred compared to the taller forest.

Groups of C. donacophilus at Coquinal also occurred in lower forests (canopy ~13-14 m) near the lakeshore, although the taller forests at Coquinal were relatively low (canopy~15 m). One group of C. donacophilus was observed in secondary forest next to a manioc crop where vines occurred in high densities. All groups of both species were located in the canopy level at an average height of 13.6 m for C. donacophilus and 15 m for the Callicebus sp. group.

Local people of Coquinal reported the presence of three other primate species Aotus sp., Alouatta caraya, and Sapajus apella, but we did not observe or hear any of these species. At Australia Saimiri boliviensis and S. apella were observed and Alouatta sp. heard. Local people also reported the presence of Aotus sp., and rarely Cebus albifrons.

Discussion

The new register for the unidentified Callicebus at Australia, further suggests that El Candado to the south of the Beni Department's Amazonian forest (Martinez & Wallace 2007) may constitute the northern distributional limit of C. modestus. Even though the gallery forest of the Biata river connects the forests of El Candado and Australia, local information from Porvenir (Fig. 1) suggests that no titi monkeys are present until El Candado. Also, our field observations in Porvenir zone suggest that this gallery forest area may not be suitable for Callicebus due to low vine densities, and as such this zone may constitute a barrier separating C. modestus from the unidentified Callicebus species.

The presence of C. donacophilus at Rogaguado lake is somewhat surprising given the relative isolation of this forest from others where this species has been registered. The Amazonian forest north of this lake is the nearest major forest block and it is actually connected by the narrow gallery forest of the Yata river. However, the absence of the Callicebus sp. from Australia at Rogaguado suggests that this gallery forest may not serve as a corridor. The nearest records of C. donacophilus to Coquinal are at Venecia ranch south of the Maniqui river(Anderson 1997) and at the Huacaraje community near Blanco river on the opposite side of the Mamoré river (Martínez & Wallace 2007), perhaps suggesting that historically forest connections existed between Rogaguado and the southern forests (Fig. 1). Paleo-geographical studies of the forest-savanna complex including archeological aspects related to ancient grassland management need to be taken into account in future explanations of Callicebus distributions in the Beni Department.

The new C. donacophilus record (Fig. 1) helps to clarify the northeastern distributional limit for C. modestus because of the absence of Callicebus in the heavily fragmented forest outside of the lake system to the east of the Santa Rosa - Riberalta road, as well as previous surveys in similar forest types to the east side of the Mamoré river where Callicebus were also absent (Fig. 1; Martinez & Wallace 2007).

Residents of Coquinal practice subsistence hunting including Sapajus apella, but they do not hunt C. donacophilus. In general, C. donacophilus shows a high level of tolerance to human presence (Martínez & Wallace 2010), although children at Coquinal do occasionally throw objects at Callicebus to stop their territorial calls that are considered noisy. Even though the intention seems not be to hurt them, this persecution may produce behavioral changes and the groups nearest to the community ceased calling at the minimum sound of people. Nevertheless, forest conversion for manioc crops is the major threat at Coquinal compared to hunting.

Local people at Australia reported higher hunting levels, which included titi monkeys. According to older residents, several Callicebus groups inhabited forests immediately adjacent to Australia 20 years ago, but due to hunting pressure towards this species mainly related to obtaining bait for fishing these groups gradually disappeared. This may explain the highly evasive behavior displayed by Callicebus groups and other primate species (S. boliviensis and S. apella), making prolonged observations challenging as previously reported for other nearby areas (Martínez & Wallace 2007).

Conclusions

We present a new record for C. donacophilus representing their northernmost distributional limit and an interesting case of population isolation, perhaps related to human activities. Similarly we report a new observation of the still unidentified Callicebus sp. that inhabits the Amazonian forests of northern Bolivia.

Crucially, this survey also provides us with a more complete picture (Fig.1) of the general distribution of the Bolivian endemic titi monkeys, Callicebus olallae and C. modestus. With no new northern localities found for these endemic primates, we can confirm the zone of El Candado community as the northern limit for C. modestus (Martínez& Wallace 2007), allowing us to improve conservation assessments for both endemic species and reinforce conservation initiatives against threats to this primate genus and their habitat. Finer scale distributional evaluations that consider titi monkey presence in different forest types are now required to determine and confirm appropriate conservation activities for the endemic primates and their habitat that are threatened by increasing deforestation levels in Bolivia (Martínez & Wallace 2010).

Acknowledgements

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Nota recibida en: Julio de 2012.
Manejada por: Jaime Jiménez.
Aceptada en: Diciembre de 2013.