Introduction

Peru is one of the more active South American countries in primate research (PrimateLit, 1940–2010: 678 records), yet the Lower Urubamba Region (LUR, named for the Urubamba River) in the Department of Cuzco is underrepresented in the primate literature (PrimateLit, 1940–2010: 0 records). This is likely due to the lack of protected areas in the region and the LUR's many oil concession areas (Finer and Orta-Martínez, 2010), which can limit access. Primate records therefore come primarily from environmental consulting agencies and are in the form of environmental impact assessments (EIAs; Table 1). Because these reports are often the result of rapid assessments, species lists are produced primarily with indirect evidence (e.g. scat, vocalizations), and data on encounter rates and group sizes are limited.

Because the LUR lies at the base of the Andes Mountain Range, it exhibits high precipitation and great variation in elevation and topography (Alonso et al., 2001) promoting floral and faunal diversity (Gentry, 1988; Pacheco et al., 2009). There is much debate regarding the geographic distributions, names, and characteristics of the primate species likely to be found in the LUR and surrounding areas (e.g., for Callicebus spp. see Aquino et al., 2008; Defler, 2004; Hershkovitz, 1990; Heymann et al., 2002; van Roosmalen et al., 2002, among many others). The purpose of this paper is to document the primate species present in the LUR, report their encounter rates and group sizes, and present observations of other large mammal species encountered.

Study site

Covering approximately 60,000 ha, the LUR is bordered to the west by the Vilcabamba Mountains and to the east by the Urubamba Mountains. The study site is near the Pagoreni A natural gas well site, east of the confluence of the Camisea and Urubamba Rivers (11°42′ S, 72°48′ W; Fig. 1). Three habitat types—terra firme, riverine terrace, and mixed upland—have been described for the area, and Pagoreni A is in terra firme primary forest, dominated by Iriartea deltoidea (Araceae) and Pentagonia parvifolia (Rubiaceae) (Comiskey et al., 2001). In the region, the local Matsigenka people cultivate manioc, maize, plantains, and bananas using swidden agricultural techniques (Shepard and Chicchón, 2001) along the Camisea River, and subsistence hunting is legally practiced. The study area is in traditional Matsigenka territory, within oil concession lots 56 and 58, controlled by Pluspetrol. Repsol Exploración Perú is building a second pipeline from Pagoreni A to the Malvinas processing plant. We studied a 9.2 km section of the northern part of this proposed pipeline (Fig. 1) under a collaborative agreement with Repsol, and results presented here are part of a larger study on the impacts of pipeline construction on primates.

Table 1.

Summary of primate and mammal census data for the Lower Urubamba Region (LUR), Cordillera Vilcabamba (CV), and Manu National Park (MNP). The total number of mammal species registered in each study, both through direct (sighted or photographed) and indirect observations, are listed, as are the number of primate and other mammal species directly observed. The final column lists the primate species observed, and bold type indicates species also found at the study site. NR = not reported.

Methods

Primates were censused along eight transect trails perpendicular to the route of the planned pipeline, between 1.2 and 1.5 km in length (opened in March—May 2011) and along two transects on the proposed pipeline route 4.0 and 5.2 km in length (Fig. 1) during the dry (28 May-3 July 2011) and wet (13 October–24 November 2011) seasons. Transects were sampled between 700–1200 and 1300–1700 h. In the dry season, perpendicular transects were walked a total of 8 times each and in the wet season 20 times each. The pipeline trail transects were sampled 20 and 18 times each during the wet season only. A total of 467.6 km (dry season: 84 km; wet season: 383.6 km) were sampled. An additional 668.2 km (dry season: 259.3 km; wet season: 408.9 km) were sampled opportunistically during transit time to, from, and between transects. There were two field teams, each consisting of a Matsigenka guide, a primatologist (TG or FCR), and a field nurse. The team members walked transects at approximately 1.25 km per hour and upon encountering a group of primates recorded the following data: species, group size, sex-age composition of the group, height of the group in the canopy, and the location with a hand-held Garmin Map CSx or Cx GPS unit. When possible, primates were photographed to confirm species identifications. Groups that were heard but not seen (particularly Alouatta sara and Callicebus brunneus groups) were not included in data analysis because their exact location and group size could not be confirmed. We used group size and composition data, combined with the spatial distribution of sightings, to estimate the total number of distinct groups observed (Table 2). Group encounter rates (# seen per 10 km walked) were calculated for each species and compared to adjacent documented localities.

Figure 1.

Map of study area. Solid black lines indicate the 9.2 km portion of the proposed pipeline that was monitored and eight perpendicular transects that are at least one kilometer in straightline distance from the proposed pipeline.

Additionally, we placed Reconyx RC55 digital infrared trail cameras (Reconyx Inc., Holmen, Wisconsin, USA) along the pipeline route and perpendicular transects to document the presence of primates and other mammals. During the dry season, there were four cameras in five locations on the ground (87 camera trap nights) and five cameras in six locations in the canopy (89 nights). During the wet season, we placed six cameras in seven locations on the ground (157 nights).

Results and discussion

During the dry season, we documented eight species of primates. These species were also confirmed in the wet season in addition to a single subadult female Ateles chamek (Fig. 2; Table 2). Encounter rates were highest for the two Saguinus spp. and the two Cebus spp. Callicebus brunneus, Alouatta sara, and Pithecia irrorata were seen relatively infrequently. Aotus nigriceps was only seen on four occasions; however, this low encounter rate is likely a byproduct of strictly diurnal sampling. Group sizes were similar to those reported from other sites for both Saguinus spp, C. brunneus, and P. irrorata. Groups of Cebus spp., however, were small compared to group sizes documented in the literature (Table 2). In either or both of the seasons, infants and/ or juveniles were observed in groups of all species except C. brunneus.

More species of primates were observed during this study than in previous studies in the area (Table 1). However, with the exception of the two Saguinus spp., encounter rates were low compared to nearby protected areas (Table 2). Primate species not observed but considered potential inhabitants of the area include: Cebuella pygmaea, Saimiri boliviensis, and lagothrix cana. Appropriate data were not gathered during this study to determine whether these species are absent for ecological reasons. However, given that sampling intensity was relatively high and data were gathered during two seasons, it is unlikely they simply went undetected. Low encounter rates and group sizes may be attributable to various causes including ecological factors and human impact. While these factors were not specifically addressed by this study, human impact is indeed a possibility. Although construction of the original Pluspetrol pipeline from Pagoreni to Malvinas was completed in 2008, maintenance of the pipeline and well requires the continuous presence of personnel along with associated frequent helicopter traffic, resulting in a notable human presence in the area. Separate from this disturbance, legal subsistence hunting by local communities has been documented to have a significant influence on abundance and diversity of local primates in the Amazon (Naughton-Treves et al., 2003) and this could be a factor in the LUR as well.

Table 2.

Primates observed during study period both on transect walks and during walks to reach sampling sites (total). Mean group size (with all age classes), range, and estimated number of groups observed are based on total sightings. Encounter rates (ER) are based only on transect walk sightings. References for species identifications include names of experts consulted. Group sizes and ER for nearby protected areas Manu National Park (MNP) and Los Amigos Conservation Concession (CICRA) are presented for comparison.

Figure 2.

Images from Pagoreni A the nine species observed: A. Callicebus brunneus (sexes unknown), B. Pithecia irrorata (female?), C. Aotus nigriceps (sex unknown), D. Saguinus Imperator (male?), E. Saguinus fuscicollis (sex unknown), F. Cebus apella (sub-adult male), G. Cebus albifrons (juvenile), H. Alouatta sara (male), and I. Ateles chamek (female). Photos: TG: A, B, D, G, H; FCR: E, I; Camera trap (taken 2013): C, F.

Table 3.

Non-primate mammal species registered during the study either through direct observations or photographs from camera traps.

Ateles chamek and lagothrix cana are the two most preferred edible primate species for the Matsigenka people in Manu National Park, followed by Alouatta seniculus (sara in the present study), Cebus apella, and C. albifrons (da Silva et al., 2005; Shepard, 2002). In the present study, the absence of L. cana and encounter rates of the other species are consistent with this preference pattern of primate consumption. A. chamek and A. sara were seen infrequently, and while both Cebus spp. were among the four most frequently sighted, encounter rates and group sizes were lower than other sites, particularly for C. apella. In contrast to the larger bodied primates, both Saguinus spp. were relatively abundant and showed higher encounter rates than reported in Manu National Park (Table 2). Both small body size and high fertility (twinning every six months) likely contribute to this phenomenon. According to da Silva et al. (2005), Matsigenka hunters only take Saguinus, Callicebus, and Pithecia spp. on occasion because of their small body size. Abundances of Saguinus spp. may therefore be an example of density compensation, wherein abundances of smaller and medium-bodied species increase given an absence of larger-bodied species, a pattern that has been associated with hunting pressure (Barrera Zambrano et al., 2008; Peres and Dolman, 2000). Alternatively, a preference among Saguinus spp. for disturbed and secondary habitat (Garber, 1993; Oliveira and Ferrari, 2008), such as that created by the nearby pipeline, may also explain higher numbers of these two species. Low encounter rates of Pithecia irrorata and Callicebus brunneus may be have to do with lack of habituation and a resulting cryptic anti-predator response (Gleason and Norconk, 2002; Terborgh, 1983), which likely reduced detectability for observers.

Regarding non-primates, eighteen additional large mammal species were documented in the area (Table 3). Procyon cancrivorus was recorded for the first time in the area, and both large felids (Puma concolor and Panthera pardus) were photographed, along with Leopardus pardalis. Other documented species of interest include Priodontes maximus and Tapirus terrestris, both of which are listed as vulnerable on the IUCN Red List (Naveda et al., 2008; Superina et al., 2010). T. terrestris and felid tracks were seen almost daily, and Cuniculus paca, Myoprocta pratii, Mazama americana, and Pecari tajacu were recorded frequently in the camera traps. This potentially high diversity and abundance of terrestrial large mammals, despite the low abundances of large bodied primates, requires further investigation.