The white-fronted spider monkey, Ateles belzebuth, is listed as ‘Endangered’ according to the IUCN classification. In Peru it is found in the departments of Loreto, San Martín, Amazonas and Cajamarca, but detailed data on its geographic distribution, population densities and conservation status are scarce. In order to obtain such information, we conducted transect censuses on the Río Aushiri and Río San Antonio (right bank of Río Napo), and between the Río Curaray and the Río Arabela and Río Nashiño, respectively, and made additional explorations on the northern and southern banks of the Río Marañón. We obtained 48 sightings along 761 km of census transect. Group size and population densities were lower in an area with high hunting pressure compared to areas with medium or low hunting pressure. Besides hunting, increasing deforestation is a major threat to the survival of A. belzebuth in Peruvian Amazonia.
The white-fronted spider monkey, Ateles belzebuth1, is 1 of 6 ateline taxa that occur in Peru [Aquino and Encarnación, 1994; Groves, 2001]. Because they are large, they are hunted extensively [Bodmer et al., 1997, 1999; Aquino et al., 2000a; Peres, 2000]. This has made A. belzebuth rare and it is now considered ‘Endangered’ (A2cd, decreasing population trend) [IUCN, 2012]. Detailed ecological and behavioural studies have been performed on this species, mainly in Colombia and Ecuador [Di Fiore et al., 2009; Blake et al., 2010; Stevenson and Link, 2010; for older references, see Campbell, 2008], but knowledge of A. belzebuth from Peruvian Amazonia is scanty and superficial. Even its geographic range in Peru is not well established, with errors or lack of precision found in distribution maps provided by Kellogg and Goldman , Hill , Aquino and Encarnación , Collins and Dubach  and Boubli et al. . These authors considered the areas between the rivers Napo and Putumayo and between the rivers Marañón, Huallaga and Aipena to be part of the distribution. Abundance data are only available for the Río Samiria and the Río Pucacuro [Aquino et al., 2000a, b; Aquino and Bodmer, 2006]. In the present study, therefore, we aim to: (1) define the geographic distribution, (2) obtain abundance and demographic data, and (3) identify threats to the survival of A. belzebuth in Peru. To these ends, expeditions and surveys were carried out between 2004 and 2009 in different areas of northern Peruvian Amazonia.
Transect censuses were carried out in January 2005 on the rivers Aushiri and San Antonio (right bank tributaries of the Río Napo), and in October-November 2007 and January-February 2008 on the Ríos Arabela, Curaray and Curaray-Nashiño. Detailed information on the geographic location, habitat types and a semiquantitative estimate of the degree of human disturbance at the 10 different survey sites are presented in table 1 and figure 1. High human disturbance in the Río Napo area is obvious from the many trails and camps used by hunters and loggers. The number of cartridges along trails and bony remains of animals, particularly primate and rodent skulls, and the intolerance of primates to approaches by humans are indicators of a strong hunting pressure in this area. In the Curaray-Nashiño and Curaray-Arabela areas, human disturbance is mainly due to logging. In both areas, camps were found close to the river banks, and 7- to 8-metre-wide trails for timber extraction extended up to 300 m into the forest interior. Hunting trails were few and never longer than 3 km in the Curaray-Nashiño area and very rare in the Curaray-Arabela area: consequently, primates were much more tolerant to the approaches of humans. Additional expeditions to verify the geographic distribution of A. belzebuth were made in several other areas between 2004 and 2009 (for details, see table 2).
In each of the 10 study sites 4 linear transects were opened, 3.0–4.0 km long in the Río Napo area, and 2.5–3.0 km long in the Curaray-Arabela and Curaray-Nashiño area. Two teams of experienced observers (a researcher and a field assistant) simultaneously walked different transects between 06.15 and 12.00 h (forward), and 14.00 and 17.00 h (return), respectively, at a speed of 1.0 km/h. Each transect was walked 2 or 3 times. Each time primates were encountered, species identity, perpendicular distance to the transect of the first individual detected, number of individuals detected, height and activity, and the presence of carried infants were noted. Complete counts of group size were obtained whenever possible. Given the fission-fusion organization of spider monkeys [Symington, 1990], these counts were generally foraging parties and probably not entire groups (‘communities’). In total 761 km of transect were walked (table 3).
Due to the low number of encounters with A. belzebuth, we could not apply the software Distance [Laake et al., 1994]. Instead, we used the formula D = N/2dL [Burnham et al., 1980] to calculate group density D, where N is the number of groups encountered along transects, L the length (km) and d the mean perpendicular distance to the transect of the first animal sighted (= 26 m). The number of individuals per square kilometre was then calculated by multiplying D with the mean group size. We also calculated encounter rates as the number of sightings per 10 km of transect walked. In order to examine the effect of human disturbance on group size, we compared the mean group size between the different areas with a one-way ANOVA in Statistica 9.0.
Direct (sightings) and indirect evidence (interviews)2 for the presence of A. belzebuth during expeditions and surveys in combination with information during expeditions to the Ríos Yanayacu de Tutapishco, Tamboryacu and Santa María, all left bank tributaries of the Río Napo, between 1982 and 1987 [Aquino and Encarnación, 1986; Aquino et al., 1992, 2005a, b], surveys in the Río Samiria and Río Pucacuru areas [Aquino et al., 2000a, 2000b; Aquino and Bodmer, 2006] and information for the Laguna de los Cóndores and the Río Chilchos in the Departamento San Martín [Barrios et al., 2003] formed the basis for defining the geographic distribution of A. belzebuth in Peru as follows (fig. 2):
Northern Peru, in the Departamentos Loreto, San Martín, Amazonas and probably Cajamarca.
Departamento Loreto. Northern limit formed by the Río Napo, eastern limit by the Río Amazonas. South of the Río Marañón in a narrow enclave between the Río Huallaga and the Quebrada Caucho Grande to the west and the Río Samiria to the east; in this enclave, A. belzebuth occurs sympatrically with A. chamek [Aquino and Bodmer, 2006]. We also observed A. belzebuth in the forest interior along the Río Morona (locality Nueva Alegría; 1 group) and Río Chuinda (locality Puerto Requena; 2 groups) (table 2). For other localities, its presence or absence is based on interviews of locals.
Departamento San Martín. Between Cordillera Escalera in the north to the left bank of Río Mishollo in the south, and foothills of the eastern cordillera of the Andes in the west to the Río Huallaga in the east. In the area north of the Río Tocache, A. belzebuth probably occurs in sympatry with A. chamek.
Departamento Amazonas. From the border with Ecuador and the Departamento Cajamarca in the north to the right bank of Río Utcubamba (at the height of Choctamal) and the headwaters of the Ríos Jelache and Salas in the south. In the extreme south-east of this range, A. belzebuth occurs in sympatry with A. chamek; this is based on interviews with people in the montane forest areas who described two species of Ateles: north one with black fur and a creamy-yellow forehead, the other completely black. At Huamanpata, south of the Río Salas, people only reported a completely black spider monkey, i.e. A. chamek. South of Huamanpata, on the Río Chilchos, a tributary of the Río Jelache on the border between the Departamentos San Martín and Amazonas, A. belzebuth has been observed by Barrios et al.  at 1,620 m above sea level, but also pictures were taken at the same site of spider monkeys with fur coloration similar to hybrids between A. belzebuth and A. chamek at the Río Samiria [Aquino and Bodmer, 2006]. These data support the supposed sympatry between these two species in parts of the range.
Departamento Cajamarca. Probably both banks of the Río Chinchipe and its major tributaries.
We did not observe A. belzebuth in the area between the Cordilleras Cahuapanas and Escalera and the Río Marañón (microbasins of the Ríos Paranapura, Aipena, Potro, Aichiyacu and Cahuapanas). Older people (>50 years) emphasized that the only larger primate species that exist in this area are Lagothrix poeppigii and Alouatta seniculus.
Conservation Status and Threats to Survival
Both in the areas of detailed population surveys and in the other areas that were explored to verify the geographic distribution, the following human activities were identified that do or potentially can threaten the survival of A. belzebuth: hunting, deforestation for pasture, agriculture and timber extraction. Major populations of this species remain principally in those areas that are either remote (headwaters of rivers) or difficult to access (aguajales). In Loreto, this conforms to a narrow strip along the border with Ecuador with the headwaters of the Ríos Nashiño and Curaray (affluents of the Río Napo), Tangarana, Baratillo, Corrientes and Macusari (tributaries of the Río Tigre), Chapuli, Chuinda y Sicuanga between the Ríos Pastaza and Morona, and the Cordillera Campanquiz between the Ríos Morona and Santiago. In the Departamento San Martín, A. belzebuth is relatively abundant in the Parque Nacional del Río Abiseo, and in the Departamento Amazonas; major concentrations occur south of the Marañón between the upper course and headwaters of the Ríos Imaza and Nievas, and north of the Marañón between the Ríos Santiago and Chinchipe close to the Ecuadorian border. Finally, the aguajales on the left bank of the Río Samiria in the Reserva Nacional Pacaya-Samiria harbour populations of A. belzebuth.
Sighting Rates, Population Densities and Party Size
In total 48 groups of A. belzebuth were encountered during the transect surveys. Sighting rates were low in the Río Napo area, and 3–4 times higher in the Curaray-Nashiño and Curaray-Arabela areas, respectively (table 3). Similarly, population density was low in the Río Napo area, and higher in the other two areas (table 3).
Party size did not differ significantly between areas (F2, 13 = 2.36, n.s.). Nevertheless, mean and maximum party sizes were lowest in the area with the highest degree of human disturbance (Río Napo; table 3). The discrepancy between the Río Napo area and the other two areas might even be stronger, since larger parties of A. belzebuth are usually more dispersed, making reliable counts more difficult. In the area of moderate human disturbance, the two smallest parties (5 and 6 individuals, respectively) were encountered along small streams, i.e. areas where exposure to humans is potentially higher.
The geographic distribution of A. belzebuth outlined here contrasts with previous distribution maps by Kellogg and Goldman , Hill , Aquino and Encarnación  and Collins and Dubach : (1) the species is absent from areas north of the Ríos Napo and Amazonas; (2) the species is also lacking from the area defined by the Ríos Marañón and Huallaga in the north and east, respectively, and the Cordilleras de Cahuapanas and Escalera in the west and south. For this second area, the lack of sightings during expeditions is corroborated by information from local hunters who maintained that the species occurs only on the western and southern slope of the two Cordilleras, in the Departamentos Amazonas and San Martín, respectively. We currently lack an explanation for this ‘lacuna’ in the distribution of A. belzebuth. Such ‘lacunae’ have also been reported for Ateles marginatus and Lagothrix cana from Brazilian Amazonia [Iwanaga and Ferrari, 2002; Ravetta and Ferrari, 2009] and may be more common than appreciated so far in the geographic distribution of many New World primates [Palminteri, 2010; Palminteri et al., 2011]. While local absence can often be explained by extinction due to excessive hunting [Peres, 1990; Nuñez-Iturri and Howe, 2007], local and regional lack of a species may also relate to fine-grained and often unrecognized habitat factors [Ravetta and Ferrari, 2009; Palminteri, 2010].
Habitats occupied by A. belzebuth in Peru are varied and comprise both inundated forests and dense aguajales, high-ground forest, and premontane forest up to around 1,800 m above sea level. However, throughout its range, populations are threatened – to different degrees – by human activities like hunting (both subsistence and commercial), deforestation, logging, mining and petroleum exploitation. The latter threat may become increasingly strong. In many areas that have been licensed for oil exploitation, activities will start or will increase with the opening of heliports, installation of housing areas, opening of transects for seismic explorations, and the seismic explorations themselves. Seismic transects will also increase access to hunters and illegal loggers.
Deforestation is a major threat in the Departamentos San Martín and Amazonas, where land is increasingly cleared for cattle ranging and agriculture, but also for the extraction of commercially valuable timber. Where forest remains, it is highly fragmented, and even if populations of A. belzebuth could survive in such fragments (which is doubtful), in the long term the lack of gene flow would result in population extinction.
The effect of hunting and habitat disturbance on populations of A. belzebuth is obvious from our results on population density. Group densities were about 50% and individual densities 70–80% lower in the area with the highest degree of hunting and disturbance (Río Napo). Densities of A. belzebuth in the Curary-Arabela and Curaray-Nashiño areas are higher than those on the Río Pucacuru (0.16 groups/km2, 0.8 individuals/km2 [Aquino et al., 2000b]) and those of A. belzebuth and A. chamek on the Río Samiria (A. belzebuth: 0.2 groups/km2, 1.0 individual/km2, A. chamek: 0.06 groups/km2, 0.5 individuals/km2 [Aquino and Bodmer, 2006]), both areas with a moderate to strong hunting impact. In a more strictly protected area, the Parque Nacional del Manu, population densities of A. chamek are considerably higher than those reported here (28–31 individuals/km2 [White 1986; Symington, 1988a]). The effect of hunting on population densities is in line with findings for other atelines throughout Amazonia [Peres, 1990, 2000; Souza-Mazurrek et al., 2000; Nuñez-Iturri and Howe, 2007]. However, population densities of spider monkeys may also be influenced by habitat quality [Symington, 1988a]. The effect of hunting was also obvious from responses to the presence of observers: spider monkeys in the Curaray-Arabela and Curaray-Nashiño areas tolerated and even approached observers, dropping and throwing branches towards them.
Larger parties in the areas with low or moderate human influence (Curaray-Arabela and Curaray-Nashiño) seem to suggest that hunting may also affect party size. However, this effect is probably less clear than this observation might indicate. Party sizes at the Curaray-Arabela and Curaray-Nashiño are larger than those of A. belzebuth and A. chamek in the Reserva Nacional Pacaya-Samiria (5.1 and 7.3, respectively; strong hunting pressure in the past [Aquino and Bodmer, 2006]), higher than those reported for A. chamek in the Parque Nacional del Mánu (3.2 [White, 1986]; 3.65–4.05 [Symington, 1990]; almost no hunting pressure), but similar to those of A. chamek in the Sierra de Contamana (13 [Aquino et al., 2005a]; almost no hunting). However, since party size may vary seasonally as a function of resource availability [van Roosmalen, 1985; Symington, 1988b; Chapman, 1990], differences in party size may emerge if surveys in different areas are made in different seasons and may not always indicate real differences.
We are grateful to the following organizations and institutions: Consultora Daimi Perú SAC for providing us with the opportunity to participate in the wildlife evaluation in the Curaray-Arabela and Curaray-Nashiño areas as part of the Environmental Impact Studies (Estudio de Impacto Ambiental) for the oil concession for Lot 67; the Faculty of Forestry Science of the Universidad Nacional de la Amazonía Peruana in Iquitos for allowing us to participate in the wildlife evaluation on the rivers Pastaza and Morona as part of the Zonificación Ecológica Económica; the Instituto de Investigaciones de la Amazonía Peruana in Iquitos for entrusting one of us (R.A.) with the wildlife evaluation in the departments of Amazonas, San Martín and Loreto, also as part of the Zonificación Ecológica Económica; the Proyecto Peruano de Primatología for facilitating the primate surveys on the Río Aushiri and Río San Antonio; the Iquitos branch of the Instituto Nacional de Desarrollo for providing the opportunity for wildlife evaluation along the Río Algodón. Finally, we thank 4 anonymous reviewers for their very helpful and constructive comments.
We follow the taxonomy of Groves  who recognizes 7 species of the genus Ateles but are aware that separation of A. belzebuth and A. chamek may not be definitive.
We asked local people to describe in detail primate species they know from their area.