Introduction
Primates are characterized by a morphology and anatomy that clearly shows adaptations for an arboreal life including climbing, brachiating and swinging abilities (Chivers, 1991). Marked terrestrial habits are present in some Catarrhini members such as Mandrillus, Papio and Macaca in the Old World. Observations of terrestrial behaviors were also reported for some essentially arboreal Neotropical primate species such as Alouatta, Cebus, Ateles and Brachyteles to obtain some food, water or minerals and/or for geographic dispersion (Dib et al., 1997; Emmons, 1999; Mandujano et al., 2004; Almeida Silva et al., 2005; Campbell et al, 2005; Mourthe et al., 2007; Pozo-Montuy & Serio-Silva, 2007). This last point is very important in fragmented forest habitats where monkeys move on the ground to reach new patches of forest but in so doing expose themselves to increased predation risks. As such, increases in forest fragmentation may affect primate conservation and survival beyond just the immediate effects of habitat loss.
Olalla brother's titi monkey (Callicebus olallae) has one of the most restricted distribution ranges of Neotropical primate species inhabiting a small naturally fragmented forest-savanna area in the southwestern portion of the Beni department in Bolivia, almost exclusively within the riverine forest of Yacuma River. Initial work on this species concentrated on their distribution, demography and taxonomy (Barreta et al., 2007; Felton et al., 2006; Lopez-Strauss & Wallace, in prep; Martinez & Wallace, 2007). To better understand the ecological requirements of this primate a behavioral ecology survey was initiated in 2007. In this note we present a series of observations concerning terrestrial movements of these monkeys obtained during this study.
Methods
The study site was at La Asunta, a cattle ranch located along the Yacuma River where, according to previous distributional knowledge, a number of C. olallae groups occurred (Figure 1). Two general types of forest habitats are present: gallery and fragmented forest, with the latter more evident at greater distances from the river. In July 2007 two groups inhabiting gallery forest and fragmented forest respectively, were chosen for study. Primate observations were made from 06:30 to 18:00 h, searching for study groups at sunrise and then attempting to follow them all day. We registered places visited frequently by the groups in order to record resting, feeding and sleeping sites.
Results
Observations 1 and 2
Early on in the habituation phase, the original fragmented forest group of five individuals (Quinteto, Fig. 1) abandoned their territory when two groups one of squirrel monkeys (Saimiri boliviensis) and another of night monkeys (Aotus azarae) arrived in the forest patch. Individuals of this group were observed travelling to and between several of the forest patches adjacent to their original site, covering distances by ground of 5 to 20 m. During these displacements, the titi monkeys remained some time at the edge of the forest before jumping to the ground and jumping quickly with arms and legs moving together and the tail lifted. Upon reaching the adjacent forest patch the leading titi monkey, usually the adult male, waited for the rest of the group in a tree on the edge of the patch before together moving off in the forest.
Similar observations were recorded for gallery forest group (Rio group, Fig. 1) following the burning of a grassland area next to the forest, which forced the two adult individuals of the group to search for a new territory. The two monkeys were observed travelling along the ground between forest patches covering greater distances than in the previous case (around 40 m) due the isolation of forest islands although they looked for forest connections to avoid the ground whenever possible.
Observation 3
As the original groups mentioned in observations 1 and 2 were not yet habituated, other groups were selected for study in fragmented and gallery forests, Pistero and Ribereño, respectively. The Pistero group inhabited a highly fragmented forest area consisting of several forest islands located near each other including three larger islands. Initially, this group was observed in the largest forest patch with the highest trees and this was assumed to be the group's entire home range. However, during the course of the study we observed the group in neighboring and isolated forest islands accessible only by ground displacements (Figure 2). Terrestrial displacements were first confirmed when the group was spotted moving along a wire fence located in the middle of the group territory dividing two cattle camps. When terrestrial the monkeys showed the same jumping style of movements previously described. In total, we obtained 100 observations of these terrestrial movements from September 2007 to March 2008. The mean distance covered was 10 m (DS=4; range 5 –16 m), and although these displacements represent a low proportion of the total movement records (7 %), it is significant for a Neotropical primate. Finally, of 11 sites where terrestrial movements were reported in the Pistero group territory, in all except three cases the movements were in both directions (see white arrows in Fig. 2).
Conclusions
Titi monkeys are arboreal and previous studies on the diverse Callicebus genus show very low percentages of activities made at ground level related principally to individuals playing, falling and casual predation of insects (1%, Kinzey, 1981). According to their distribution, most of the Callicebus species inhabit continuous forest areas with high vegetation density (Anderson, 1997; Hershkovitz 1990; Martinez & Wallace, 2010; Van Roosmalen et al., 2002). The naturally fragmented forest-savanna inhabited by C. olallae (Martinez & Wallace, 2007) clearly necessitates frequent terrestrial travel during ranging behavior, as was previously suggested by Felton and colleagues (2006) and confirmed by our observations. Even if individuals inhabit large continuous forest areas, eventually they may need to travel terrestrially to look for new areas when they reach sexual maturity and form new groups (Kinzey, 1981 ; Wright, 1986). In all cases the monkeys travelled the shortest terrestrial route between neighboring forested areas showing an evident effort to reduce the predation risks associated with terrestrial travel. The first two observations where longer distances were covered must represent extreme risks given the small size of these primates and the diverse carnivore community associated with these forests. Indeed, when isolated small trees are on pathways to large forest areas, the monkeys climb them making their displacement in stages instead of passing directly from one forest patch to another.
In naturally fragmented habitats, terrestrial movements of monkeys may not always be related to terrestrial-based feeding or drinking behavior but also due to ranging requirements. As the world's forests become more fragmented due to human intervention these terrestrial movements may become more commonplace in primate species that normally occur in more continuous forests increasing exposition to predation risks.
