Abstract
The yellow tailed woolly monkey (
Introduction
The yellow-tailed woolly monkey (
The Yellow-Tailed Woolly Monkey Project run by Neotropical Primate Conservation was initiated in 2007 [9]. Since its inception, the project has used the Critically Endangered
Horwich and Lyon [13] define Community Conservation (CC) projects as low budget projects that motivate and stimulate local people to assume ownership and responsibility over their natural resources. These projects concentrate on the smallest geographical scale, but have the potential to expand to regional level through reproducing initiatives in neighboring communities. They promote conservation through social values rather than through economic incentives, thus leading to stewardship of nature. Incentives such as economic alternatives are often integrated with the projects at later stages. Although these projects are very common in rural areas and predominantly successful, big conservation agencies seldom acknowledge or support them because of their relatively small scale and geographic isolation [13]. Seymour [14] suggested that the success of Community Conservation projects depends on the intrinsic capacity and traditions of the specific community to organize their resource use, rather than on the external project, and successful projects are therefore ‘discovered' rather than designed as such. Locally run conservation projects are increasingly common around the world [15–17] but get little attention in academic literature [17–20]. Shanee et al. [21] described local conservation initiatives in northeastern Peru, dividing them into formal conservation initiatives, including locally run protected areas registered with the government under any of the schemes permitted by law, and informal conservation initiatives, including voluntary agreements to control deforestation and/or hunting, which they define as landscape-level conservation initiatives. They suggest that combined formal and informal conservation initiatives offer important conservation opportunities [21].
Success in conservation projects is commonly measured by quantifying outputs and, preferably, outcomes [22, 23], often measured in non-biological terms. Quantifying success in biological terms in conservation projects can be difficult, as the time frames involved are often longer than many projects, and they can be cost dependent, putting them out of reach of smaller projects [22–27]. In community conservation projects, several previous studies have tried to quantify success in biological terms using measures such as deforestation rates and growth in local species populations, each showing varying levels of success [25, 28, 29].
The current study detects real changes in the population density of
Methods
Study Site
We conducted repeat census work of the 2008/09 survey, at the same site near the Centro Poblado La Esperanza, Amazonas department, in northern Peru [10]. The area is composed of ca. 700 ha of disturbed primary forest and regenerating secondary forest, interspersed with pasture (S 05°39'46“, W 77°54'32”). The study site is bounded by the main highway, Via Marginal, to the south; to the east and west by pasture and agricultural lands; and to the north it is contiguous with extensive forest reaching to the Rio Maranon (ca. 100 km). Since the last census, very little observable change in forest cover or land ownership has occurred. Three parcels of land (~ 60 ha) were sold or inherited during the intervening period, with some of these parcels being partially cleared. Also, a new dirt road was constructed near the survey site (Fig. 1), increasing rates of land transfers. This has so far not affected the area used in this study.

Location of study site in Amazonas department, northern Peru: showing villages, roads and rivers. Neighboring protected areas are shown to indicate the importance of the area for connectivity and as a buffer to these PA's.
The site was originally chosen for its location between three protected areas:
The land is titled to the
Community agreements
We employed commonly used CC methodologies such as local and regional awareness programs, voluntary agreements to control hunting and deforestation, small scale assistance programs and community involvement in research and conservation activities [9, 21, 28], making an effort to comply with the community's requests and ideas of how to achieve conservation rather than trying to impose outside ideas of how conservation should be administered. In 2008, the community asked to formally register a communally run private conservation area in an uninhabited area within the community. We were invited to different villages by local authorities to give conservation talks to explain the benefits of intact forests. Villagers were asked to vote for and sign voluntary pledges to set up systems of internal control of deforestation and hunting. Pledges were updated and re-signed whenever community authorities felt it was needed or when we requested. These conservation pledges and internal controls did not include any direct economic incentives or dedicated vigilance activities.
Voluntary pledges to not hunt threatened species were signed with the five annexes of the community closest to the study site, as well as in the community's general assembly. Agreements were made with the 11 land owners in the study site to allow transects to pass through their lands. Additionally, when land ownership had changed hands, permission was sought and granted by the new owner to continue our work.New land owners also signed the voluntary pledge in whichever village had jurisdiction over the lands. No direct economic incentives were provided to community members, but 17 local guides were rotationally employed as field assistants for field surveys as well as guides for tourists visiting the area. All field assistants and guides were selected from among the landowners or their relations.
Density Estimation
We conducted 13 months of field surveys, from May 2012 to February 2013, and April to June 2013. To make results from this survey comparable to the 2008–09 surveys, we replicated the same methods [10], reopening the four previously used transects. During the intervening years there were a number of landslips and changes in ownership, but minimal alterations in transect location were necessary (Fig. 2). We used a total of 9.1 km (Table 1) of transects. Transects radiated from a central camp at ca. 90° angles, with ca. 300 m between the camp and the start of the nearest transect. We measured and tagged transects every 50 m with high-visibility flagging tape. We walked transects in pairs of trained observers comprising one researcher and one local field assistant. Field trips lasted five days and were repeated every two weeks for the length of the survey. Each transect was walked twice on each field trip, once between 07:00 and 12:00 h and once between 11:00 and 16:00 h, with at least 24 hours between repeat walks on the same transect. Transect walks interrupted by heavy rains were abandoned, leaving an uneven sampling effort between transects. In total 329,150 m of reliable transect walks were completed (Table 1).

Transects used in this study (dashed lines indicate changes from previous study), showing neighboring villages and the path of the new road built between survey periods.
Transect lengths, sampling effort and detections during this survey.
Total number of sightings including audio and discarded detection events
We made repeat walks to maximize sampling effort on each field trip. Transects were walked at a maximum speed of 1.0 km/h (Average 0.9 km/h) to minimize background noise and increase detection probabilities. We did not include in the census data we collected on return walks, but we did use group counts to record group composition and calculate average group size for the area. On each transect we recorded the following data: weather conditions, species identity, group size and composition (we defined categories as adult male, adult female, juvenile male, juvenile female, undifferentiated juvenile, and nonlocomoting infant), location of detection along the transect, and perpendicular distance (PD) to first animal sighted. We allocated ~ 15 min (Avg 7 min) to obtaining group counts to gather accurate group spread estimates for use in adjusted strip width estimates [34]. Incomplete or inaccurate group counts and group spread estimates were discarded and replaced by the mean from all reliable counts during analyses. Single individuals are uncommon in the population and were not included in analysis, as we may have missed them on or near the transect line. We used χ2 tests to check for bias in detection between observers, field assistants, transects, month, and weather conditions.
As with the 2008–09 survey, we added an estimate of group spread to PD measurements to avoid overestimation of densities [35, 36] and right truncated detections from >100 m.. When possible we estimated group spread at each detection event. This differed from the 2008/9 survey when we did not collect data on group spread during detection events as collecting this data could have violated assumptions of transect methods [35]. We made these additional measurements to increase accuracy of density estimates. Also, the groups at the survey site are now habituated to the presence of researchers, reducing the likelihood of alarm calls or other behaviors affecting detection possibilities farther along the transect. We used the estimated radius to calculate adjusted PD measurements by adapting the method of Whitesides et al. [34]:
Where PD = perpendicular distance to first individual sighted, S = observer to first individual distance, r = one half mean group spread, P' = perpendicular distance from transect to group center. When the first individual sighted was directly over the transect, i.e.,; = 0°, θ = 90°, PD = 0, X = 0, then P' = 0. We used the transect-width estimation method of Whitesides et al. [34] to obtain an estimate of effective distance. This method has produced good estimates when tested against primate populations at known densities [34]:
where Nt = total number of sightings, Nf = number of sightings at less than half the fall-off distance (calculated as the 10-m interval at which the number of sightings was half or less than that of the previous interval), FD = fall-off distance, and D = effective distance. We then estimated the area sampled using the equation:
where S = estimated group spread in km, D = estimated effective distance, Lt = total sampling effort, and A = area sampled. We calculated group density using the equation:
where Gt = total number of sightings and A = estimated sample area.
We compared results from density estimates, group sizes and group compositions with results from previous surveys using tests with Yates correction for 2×2 contingency tables to see if observed differences were significant.
Forest cover change mapping
We estimated changes in land cover over the period between surveys using high resolution satellite images for the years 2007 and 2013. For the 2007 period we used a LandSAT 5 TM (Thematic Mapper) image, and for 2013 we used a LandSAT 8 OLI (Operational Land Imager) image, both at 30 × 30 m resolution (both Path/Row 009/064). The LandSAT 5 image was chosen to avoid problems with data gaps in the SLC-off (Scan Line Corrector) LandSAT 7 images for this year. All data were projected on UTM 18S (datum WGS84). A major challenge for remote sensing in montane forest areas is the level of continuous cloud cover [37]. We selected images that had < 20% cloud cover, as 100% cloud free images were not available for these time periods. Prior to analysis we checked both images for positional error, but georectification was not necessary as error between the images was less than one pixel (error ~ 15 m). We then made a cloud cover mask combining both years, which was then applied to both images. Using the Image Classification tool in ArcGIS 10.0 with Spatial Analyst extension [38], pixels in the 2007 image assigned one of seven categories based on a band 3, 4, 2 false color image and an NDVI (Normalized Difference Vegetation Index) using a band 3, 4 (Red, Near infra-red) combination: Forest; Pasture;
To investigate the effect on our population density estimates of possible in-migration of outlying groups and individuals of
To compare deforestation rates among our study site, outlying areas, and the regional and national averages, we calculated annual deforestation rates from official figures [42, 43] for Amazonas and San Martin Regions of Peru, which cover the majority, ~ 90 %, of the species range [44]; we then compared these with our estimates from the study site using χ2 tests.
Results
Between the two census periods, behavioral work on
The project also yielded the creation of a Private Conservation Area (ACP), La Pampa del Burro, on community lands and managed by a committee of community members. The ACP is < 1 km north of the census survey area. It covers 2,776 ha, composed of white sand forest with smaller areas of montane forests that are habitat for
Mean population densities and group compositions from each census year.
Χ2 test
Mann-Whitney U test
Density estimates
We detected
We estimated group spread at a diameter of 29.83 m (SE15.49). This gave an effective distance for transect-width estimation method of 21.8 m, and estimated densities of 1.28 (SE 0.2) groups/km2 and 14.45 (SE 3.3) individuals/km2. Group and individual densities increased by 18.8 and 35.9 %, respectively. We estimated the total number of groups that include all or part of their territory within the 700 ha of the study site, using density estimates obtained from the line transect survey at 8.7 groups.
Tests for differences in
Forest cover change mapping
Using a maximum home range estimate of 174 ha from published estimates from our survey site [41], we generated a buffer of ~ 10 home range diameters (10,000 m), giving a 37,860 ha polygon around the survey site, an area of ~ 218 home ranges (Fig. 3). Our estimate of deforestation for 2013 was 9,959 ha, representing an increase of 0.52 % (Table 3) using a LandSAT 8 image (Fig. 3). Using the two home range buffer generated a polygon of 979 ha, an area of ~ 5.6 home ranges. Our deforestation estimates for 2007 and 2013 were 87 and 93 ha respectively, representing an increase of 0.61 % (Table 3). Using χ2 tests, the change in land cover in our estimated area of low influence was not significant (χ2 = 0.99, df = 1, P < 0.32). Using the probable influence area, there was also no significant difference found in the amount of deforestation between 2007 and 2013 (χ2 = 0.1, df = 1, P = 0.75). Annual deforestation rates over both areas of influence estimate were 0.09 % and 0.1 %, respectively.

Map of landcover change in the area surrounding the study site between surveys. Map shows the two buffers used to represent different levels of influence on local populations of
Variable deforestation estimates between 2007 and 2013.
Annual deforestation rates for Amazonas and San Martin over the period 2005–2011,calculated from official figures [42, 43], were 0.18 % and 0.62
Discussion
The results of this study showed increases in both individual and group densities over those found in the previous 2008/9 survey [10]. Although neither change was significant in itself, there was a significantly greater increase in individual densities than in group densities. The overall average group size increase was also significant. When changes in individual age-sex classes were examined separately, significant increases were only found in the juvenile and non-locomoting infant categories. These increases suggest that the majority change is from natural population increase and not due to in-migration of individuals or groups from outside the study area. By replicating as exactly as possible the methods of the previous survey [10], we have traded increased comparability for possible improvements in survey methods. This was necessary because variation in census results are typically due to differences in methodologies [45].
Assuming observed increases were from natural population growth, an increase of ~ 35% in just five years is high, but possible. Assuming that
An interesting observation of this study is the increase in group spread recorded in the 2013 survey. This could be because of differences in resource production between survey years due to greater/lower rainfall and/or solar radiation. Such differences could be responsible for the small increase observed in group densities, as larger groups will be more conspicuous, increasing the possibility of detection. However, this will not have an effect on individual densities, particularly within age-sex classes. Surveys from other less disturbed areas have recorded larger groups than those found at our study site, up to 20–30 individuals in the
Our analysis of annual deforestation rates in the survey area showed no significant increase in forest loss over either of our influence thresholds. The average annual deforestation rates for our threshold areas were also much lower than the official regional estimates for Amazonas and San Martin (0.18 and 0.62% respectively). Although all observed differences in forest cover and deforestation rates were not significant, deforestation in our area was lower than the average across the species range. This difference is more interesting when put into the local context. In the period between surveys a new road was built bordering the survey site, allowing the first vehicular access to nearby forested areas. Roads are a common cause of deforestation and forest degradation [50–52] through intensified migratory agriculture and logging [53], increased forest fires [54], and wildlife traffic [55, 56]. Humid montane forests are especially vulnerable to the ravages of road construction, placing specialized species at great risk [50]. Studies conducted in the Upper Huallaga river basin have shown a high probability of deforestation in strips of up to 10 km on either side of roads, an effect that only diminishes when valleys are particularly steep [57]. In lower Amazonia, deforestation can reach up to 100 km from paved highways [58, 59]. Similarly, Jerozolimski and Peres [60] found that hunting can occur anywhere within 9 km of any access point. Amazonas and San Martin had already lost the majority of their primary forest cover prior to our work, whereas our survey site still retains 74% primary forest cover.
Shanee
In a similar project in La Primavera, Peru [21, 61], we have been working on the creation of a 7,174 ha Conservation Concession, Sun Angel's gardens, administered by a local association. In addition to local support of the new reserve, the villagers of the four surrounding villages have signed agreements to control hunting and deforestation in all the surrounding areas, covering ~ 80,000 ha. Local people reported that white bellied spider monkey (
Informal conservation efficiency is hard to measure because of inexact geographic limits and difficulties in long-term monitoring of forest growth and populations of wildlife. Such long-term projects are unfeasible for many NGOs, as funders generally require quick and conclusive results [62–64]. The essence of landscape-level conservation is its large geographical extension and the inclusion of populated areas. It is mainly informal and therefore has no legal standing against national and regional development plans or against continuous immigration to an area. Moreover, it does not offer complete protection for forests and in most cases will not benefit wildlife that need large areas of undisturbed primary forest. It therefore is generally a complementary activity in combination with the creation of better protected, intangible private and state-run protected areas to efficiently protect a range of species [65]. Wildlife can quickly return to non-hunted areas, giving local people a sense of success and pride. This type of conservation also avoids the bureaucratic processes required by the state. Informal conservation initiatives can be implemented on individual, communal or regional levels [21]. They do not require a consensus, bureaucracy, or the cooperation of authorities.
Implications for conservation
This is one of the few existing studies of the impact of locally run, landscape-level conservation initiatives on local fauna. It shows that low-cost, community-based conservation projects offer valid conservation opportunities for threatened species. Due to the very small range and intensity of anthropogenic threats (Fig. 4) in the densely populated habitat of the Critically Endangered

Clockwise from top right: Adult male
We urge conservation theoreticians and practitioners to be much more attentive to local conservation rationales and methodologies and work as much as possible with existing cultural organizations, while we hope that funding agencies and the public will be more willing to donate to small scale, local, or locally-focused NGOs.
Footnotes
Acknowledgements
We thank all the students, volunteers, staff and local guides for their help in the field, particularly Nestor Allgas and Alejandro “Apu” Alarcon. This work was funded by Neotropical Primate Conservation, thanks to grants from Primate Conservation Inc., The National Geographic Society, International Primate Protection League – UK, The Monkey Sanctuary Trust/Wild Futures, Apenhuel Primate Conservation Trust, Le Conservatoire pour la Protection des Primates, International Primate Protection League - US, Community Conservation, and the Margot Marsh Biodiversity Foundation. We thank Direccion General Forestal y de de Fauna Silvestre/Ministerio de Agricultura for permits to carry out this work (Autorización N° N
