The Azuero howler monkey, Alouatta coibensis trabeata, and the Azuero spider monkey, Ateles geoffroyi azuerensis, are endemic to the Azuero Peninsula, southwestern Panama, Central America and they are considered Critically Endangered. They are threatened by deforestation, poaching, and illegal trade. I carried out population surveys of the two subspecies from April 2001 to June 2009. The study covered potential habitats for these primates in the three provinces where they are believed to occur (Herrera, Los Santos and part of Veraguas). Surveys determined their occurrence and locations in each province. In all, 7,821 hrs were spent in survey activities. I used four methods: 1) Direct observation of presence/absence; 2) triangulations based on vocalizations; 3) strip-transect censuses, and 4) road counts. Forty-five Azuero howler monkey groups were seen and counted, totaling 452 individuals with a mean of 9.6 individuals/group, SE ±3.3 (range = 3–26). I estimate approximately 322 howler groups and c. 3,092 individuals remaining in the wild in the three provinces. For the Azuero spider monkey, 74 individuals in 10 sub-groups and five complete groups were counted directly, with a mean of 3.8 individuals/subgroup, SE ±0.6 (range 2–7) and a mean of 12.5 individuals/group, SE ±3.7 (range 10–22). Overall, I confirmed the existence of approximately 13 spider monkey subgroups and 145 individuals of A. g. azuerensis remaining in the wild in the provinces of Veraguas and Los Santos. It is already extinct in the province of Herrera. This study confirms that both subspecies are Critically Endangered. Each appears to have already experienced changes in group composition due to isolation and habitat degradation. Conservation measures based on educational awareness programs have been initiated.
Introduction
This is the first range-wide assessment of the distributions and populations of the Azuero howler monkey, Alouatta coibensis trabeata, and the Azuero spider monkey, Ateles geoffroyi azuerensis; endemic to the Azuero Peninsula of southwestern Panama (Froehlich and Froehlich 1987). Both are assessed as Critically Endangered on the IUCN Red List of Threatened Species (Cuarón et al. 2008). Surveys were carried out, using four conventional techniques to assess population parameters of the two subspecies. The aim was to calculate not only total numbers in Azuero but to obtain information on group characteristics, specifically their group structure, relating the findings to habitat size and other environmental variables. These two primates are among the most endangered in Panama, and the information obtained will provide a basis for the Fundación Pro-Conservación de los Primates Panameños (FCPP) and the Panama Environmental Authority (ANAM) to establish and enforce a conservation program. In this assessment I identify promising localities (e.g., villages, towns, protected areas) and primate populations for the development of long-term conservation projects and environmental education programs for local people (Jacobson et al. 2006). As stressed by Godfray and Crawley (2004), to improve conservation prospects of threatened wildlife in deforested regions such as the Azuero Peninsula, the remaining forests that still hold wild populations, need to be assessed to document the extent of environmental change that is taking place and responses to these changes by the endangered primate subspecies.
Methods
Study area
Azuero howler and spider monkeys are endemic to the Azuero Peninsula in the southwest of Panama. Annual average temperature is 28.1°C (range 22.5–33.7°C), and average annual rainfall is 1,410 mm/year (Navas et al. 2001). Azuero, encompassing the provinces of Herrera, Los Santos and the eastern part of Veraguas, is severely deforested. There is a dry season from December to April, and a rainy season from May to December (Suárez 1981). The lowlands are quite flat with small hills reaching 90 to 150 m above sea level (Méndez-Carvajal 2001). The El Montuoso Forest Reserve, at 900 m above sea level (Arcia et al. 2004), is in the highlands in the north, and the Cerro Hoya Natural Park (Cerro Hoya reaches 1,559 m above sea level) is in the southwest. Forests in the Azuero Peninsula remain mainly on hilltops and along rivers. The lowlands are dominated by pasture interspersed with forest patches that are connected in some areas by gallery forest and living fences. The tallest trees reach 15 to 20 m in the remnant forests and living fences that line the principal and secondary roads, delimiting the cattle ranches and pastures (Méndez-Carvajal 2001, 2008). Vegetation was classified and mapped using satellite data from GH NASA-Tele Atlas 2008 and Garmin Etrex (MapSource 6.15.4), along with information provided by the Panamanian Environmental Authority (ANAM) and the landowners. Statistical analyses were carried out using Excel, SPSS 16.0. Spearman's tests were applied to evaluate relationships between group size, forest height and the area of the habitat. The study area was divided into five regions (see Fig. 1, Table 1).
Data collection
I report here on survey data collected over nine years—7,821 hours in the field from April 2001 to June 2009. Surveys were carried out on 121 days (10–15 days per year) (Table 2). Population densities were calculated by the number of individuals found divided by the size of each connected region; providing as such ecological densities, as indicated by Eisenberg (1979), Chapman et al. (1988) and Rudran et al. (1996).
Areas were selected on the basis of the presence of forest and information provided by the local people. Four methods were used in each survey area: presence/absence recording, strip transect, road count, and listening for calls and locating groups by triangulation. Besides seeing the primates, we recorded their presence through signs, which included smell, feces, tracks, chewed leaves, and calls (Rabinowitz 2003). Twelve strip transects were set up, each at least 1 km long, to cover the entire peninsula, following the recommendations of Ferrari (2002) and Carvalho-Oliveira et al. (2003) (Fig. 1). We carried out strip transects if the forest was at least 40 m wide. This method was used to survey gallery forest, living fences and patches of forest in fragments. Observations were made on foot between 08:00 and 12:00 hr and 14:00 and 18:00 hr. Speed of travel along the strip transects was 1 km/hr by foot. Eleven roads were also surveyed, averaging 26.6 km (range 18–34 km; n= 11). Each was surveyed by car twice a year; average speed was 15 km/hr.
The use of listening posts and triangulation to locate groups proved effective for howler monkeys in seven areas with isolated patches of forest (Fig. 1). Three listening posts were set up and manned from 04:30, for fixed periods in the morning, noon and late afternoon for at least three days in each area. We recorded the time and position of vocalizations using a GPS, and estimated the location of vocalizing groups using a compass-bearing and an estimated distance from the observer (Brockelman and Ali 1987; Aldrich et al. 2006). Whenever possible, the groups recorded were verified by direct observation later in the morning. They were counted and recounted at least twice each day while we stayed in the area. This process was repeated several times to ensure accuracy before an average group size and composition could be recorded (Milton 1992; Ferrari 2002). This method helped us to identify new groups unnoticed by our conventional strip transect method. Spider monkeys were detected with this method in previous surveys in the area of Chucantí, Darien (Méndez-Carvajal et al. 2010a). Black spider monkeys, Ateles fusciceps rufiventris, call almost every day throughout the day, and we expected the same behavior in Azuero. Azuero spider monkeys were, however, largely silent, probably because people chase them and sometimes shoot them. Azuero spider monkeys always fled when we found them, often subsequently mixing with groups of the similarly colored howler monkeys. They called so infrequently that this method proved impractical for this species in fragmented habitats.
Table 1.
Characterization of five Azuero regions divided in this study according to the provinces surveyed (see Fig. 1). Climatic and botanical information from Navas et al. 2001, Salazar-Allen (2001), and Arcia et al. 2004. Human population data from (González 2002).
For each group seen we recorded the group size and composition—adult male, adult female, juvenile and infant, following the classifications of Milton (1992) and Campbell and Gibson (2008). The number of groups detected was multiplied by the average group size for each area (Milton 1992). The combination of the four methods maximized our chances of detecting the groups remaining around the non-protected areas. The results from the different methods were analyzed separately but were complementary and allowed us to consolidate our information on the groups at each site.
Data Analysis
I calculated mean group size and composition for each subspecies. To estimate the total number of individuals of a subspecies present in a given area, I calculated densities as follows: Transects and Road counts: D = N/2WL; density (D) is found by dividing the number of individuals (N) recorded by twice the estimated detection distance (W) of the forest surveyed, multiplied by the length (L) of the transect.
For triangulation: D = fn/A; density (D) is found by multiplying the number of groups located by triangulation in a sampled area (N) by a correction factor for the bias that not all groups vocalize in the same sample period (f), divided by the study area (A) (Brockelman and Ali 1987).
Azuero howler monkey analysis
To estimate of the overall density for Alouatta coibensis trabeata, I used results of the two most effective methods applied for this survey: triangulation and strip transects. The total number of individuals was calculated using mean group size multiplied by the number of groups detected in connected forest. Using all relevant data, we tried to estimate the number of groups existing in the more isolated areas. Total population size was calculated using the criteria of Nichols and Conroy (1996). Thus, the equation used to calculate the total population of A. c. trabeata was based on a modification of the Eisenberg (1979) ecological formula with a canonical estimator as following:
where C is the total number of animals, β = Observation probability expressed as β = ŷ/χ, ŷ is the density of the incomplete population survey (Strip Transect), and χ the most accurate density of the complete survey (Triangulation); α = is the area sampled.
Azuero spider monkey analysis
The A. g. azuerensis population was estimated using two of the four methods applied for this survey. The most effective methods to detect Azuero spider monkeys were road counts and presence/absence, considering between them the presence/absence as the more complete and the road count as the less accurate method. We calculate their total population by the number of localities confirmed as “spider monkey present” and then, assuming at least one subgroup per locality, we multiplied the average subgroup size obtained by direct observations and determine the total population by the equation:
Table 2.
Summary of survey activities from 2001 to 2009. Average survey time was 12 hrs/day. P/A: Presence/absence; ST: Strip Transects; RC: Road counts; T: Triangulation. Regions described in Table 1.
where C is the total number of animals, β = Observation probability expressed as β = ŷ/χ, where ŷ is the density of the incomplete population survey (road counts) and the χ the most accurate density of the complete survey (presence/absence); α = is the area sampled.
Results
Total hours/effort invested in presence/absence recording, including informal interviews, for both species was 771.5 hours. Howler monkeys and spider monkeys occurred together in the following locations: Restingue, Cerro Culón, Rio Ventana, Tembladera, Punta Blanca, Cerro Hoya National Park, Cerro Moya, Jobero, Cambutal, Altos de Güera, Río Güera, La Tronosa Forestal Reserve, El Cortezo, Quema, Guánico, Tonosí, Cacao, Cañas, Venao, Los Pozos, Macaracas, Las Palmas, Llano de Piedra, Mogollón, Cerro Canajaguas, Cerro El Vijía, Valle Rico, La Miel, Valle de Tonosí, Flores (Los Santos), Oria, Río Purio, Los Ñopos, El Cacarañal, Macaraquitas, La Llanita, Buena Vista, Mariato, Arenas, and Flores (Veraguas) (Méndez-Carvajal 2008) (Table 3).
Populations by region
Northern Region: Herrera Province (lowland). The largest howler population was found in the northern lowland region; 261 howler monkeys in 11 groups. Group size averaged 23 individuals (range 15–39); all in highly fragmented forests. Average group composition was 6.0 males (25%), 7.8 females (32%), 6.6 juveniles (27%) and 3.4 infants (14%). The adult male/female ratio was 1:1.3, female/ juvenile 1:0.8, and female/infant was 1:0.4. Densities were 40.4 individuals/km2, and 1.7 groups/km2 (n=5; SD ±9.4) for 6.46 km2 forest surveyed. This population is not heavily hunted and has no natural predators, and the howlers appear to be overcrowded in the small fragments where they remain, facing, as they do, the difficulties of dispersing over wide expanses of pasture. Azuero spider monkeys were not found in this area.
Table 3.
Localities confirmed with presence/absence of A. coibensis trabeata and A. geoffroyi azuerensis, Azuero Peninsula, Panama. ? = probably present; +? = high probability of presence.
Continued
Continued
Table 4.
Total individuals detected of Alouatta coibensis trabeata, Azuero Peninsula, Panama. Confidence Level (95%), mean = 9.6 individuals/groups (3–26) (SD ±3.3).
Table 5.
Total individuals detected of Ateles geoffroyi azuerensis, Azuero Peninsula, Panama. Confidence Level (95%) mean = 10.2 individuals/groups (4–22) (SD±1.5) *See Table 1, **Calculated by locals and environmental authorities.
Northern Region: Herrera Province (highland). The howler population was estimated at 37 individuals in six groups, with an average of 6.1 individuals per group (range 5–12). The six groups averaged 1.83 males (30%), 2.5 females (40%), 1.0 juvenile (16.4%), and 0.8 infants (13.6%). The ratio of adult male/female was 1:1.36, female/juvenile was 1:0.4, and female/infant was 1:0.3. Densities were estimated at 0.52 individuals/km2 and 0.08 groups/km2 (n=6, SD ±3.6) over an area of 69.83 km2 (Table 4). Azuero spider monkeys were not found in this region but interviews assured us of their presence in the past. Locals told us that Azuero spider monkeys were present in the El Montuoso Forest Reserve about 20 years ago, but disappeared later with other animals such as jaguars; eliminated by poachers (Table 5).
Southern Region: Veraguas and Los Santos provinces — howler monkey population. The howler population was estimated to be at least 35 individuals in 11 groups, with an average of four individuals per group (range 1–12; n = 7), with 1.6 males (45%), 1.6 females (45%), 0.7 juveniles (2%) and 0.4 infants (1%). Relative densities were 5.1 individuals/km2 and 1.17 groups/km2 (SD ±5.5 for 6.78 km2). The ratio of adult males to females was 1:1, juveniles/females was 1:0.46, and females/infants 1:0.23. Densities were calculated based on the size of each patch of forest sampled, with 3.4 individuals/km2 and 0.94 groups/km2 for the area in the southwest (5.28 km2), and 13.3 individuals/km2 and 2.6 groups/km2 for the population in the southeast (1.5 km2).
Southern Region: Veraguas and Los Santos provinces — spider monkey population. Anecdotal reports from the communities of Ventana and Tembladera (Veraguas) indicated that spider monkeys occasionally traverse the area through the gallery forest and forest fragments close to the coast. They reported that spider monkeys inhabit mostly the upper forested slopes of the mountains, and are scarce in the lowlands. People from Ventana and Tembladera (Veraguas) told us that Azuero spider monkeys normally come down near to human settlements during the rainy season (middle of May to December). For Los Santos province, we found a total of 49 spider monkeys in four isolated groups (mean size = 10.2; range 4–22). The group composition average was 2 males (SD ±1.6; 40%), 2.2 females (SD ±1.5; 44%), 1.8 juveniles (SD ±1.5; 36%) and 1.5 infants (SD ±1.5; 30%) at Venao, La Zahina, Cañas, Flores of Tonosi and Pedasi District (Los Santos). The ratio of adult males to females was 1:1, and the female/infant ratio was 1:1.5 (n = 4; 95% confidence). Densities calculated were 7.3 individuals/km2 and 0.6 groups/km2 in 6.78 km2 (Table 5).
Eastern Region: Los Santos Province — howler monkey. Seventy-six howler monkeys were found in an area of 1.82 km2. There were 12 groups, and a lone juvenile female. The group composition averaged 1.6 males (21%), 3.8 females (50%), 0.6 juveniles (7.8%) and 1.6 infants (21%), and group size averaged 7.6 individuals (SD ±2.8, n = 10, range 3–12). The ratio of males/females was 1:2.3, juveniles/females 1:2.6, and infants/females with 1:0.42. Relative densities for the Eastern Region for Azuero howler monkeys were 42.6 individuals/ km2 and 5.5 groups/km2.
Eastern Region: Los Santos Province — spider monkeys. We found one group composed of three subgroups of Azuero spider monkeys in this region with 25 individuals seen, in the area of La Miel, Las Tablas, and the Tonosi Valley, about 2 km from the town of Flores. Average group size was 12, and subgroup size 6.2, sharing the same area with Azuero howler monkey groups. The density in the three locations was 13.7 individuals/km2, 0.5 groups/km2, and 2.2 subgroups/km2, respectively. Subgroup composition averaged 2.0 adult males, 2.3 adult females, 1.3 juveniles, 1.3 infants (range 3–14, SD ± 1.5, n = 3) for a total area of 1.82 km2. These monkeys are indirectly connected between the Río Oria Arriba and Oria Abajo via the La Palma Bridge as far as the forest of Cerro El Montuoso, Las Tablas District.
Western Region: Southern Veraguas Province. We observed 43 Azuero howler monkeys in five groups. The groups averaged 1.5 males (13.9%), 5.2 females (48.8%), 3 juveniles (13.9%) and 2.5 infants (23.2%). The adult male/ female ratio was 1:3.5, female/juvenile 1:0.4, and females/ infant 1:0.5. Densities calculated were 17.2 individuals/km2 and 2 groups/km2 (n = 4; SD ±5.5) in 2.5 km2. Spider monkeys were reported by the locals, and around 50 individuals were confirmed for Cerro Hoya National Park, Arenas, Quebro and Restingue including Cerro Culón (Table 5).
Total population of the Azuero howler monkey
We recorded 433 Azuero howler monkeys from 87.39 km2 of fragmented forest from 2001 through 2009 (Table 4). Forty-three groups provided an overall density of 5 individuals/km2 and 0.5 groups/km2 for the entire forested area of the Azuero Peninsula (n = 32, SD ±2.4). Overall, group composition averaged 2.5 adult males, 4.3 adult females, 1.92 juveniles and 1.88 infants. The mean group size was 9.6 (range 3–26). According to the equation, Ň = 433/(1)0.14, we estimate a total of 3,092 individuals remaining in the wild.
Total population of the Azuero spider monkey
We recorded 74 Azuero spider monkeys, with five groups detected and/or counted directly, and six indirectly (Table 5). There are evidently no spider monkeys remaining in Herrera province, the northern part of the Azuero Peninsula, but remnant and diminished populations survive in the southern (southeastern and southwestern) parts of the peninsula (Méndez-Carvajal and Ruiz-Bernard 2009). The Cerro Hoya National Park is their main stronghold (Rowe 2000; Cuarón et al. 2008), and our efforts were concentrated mostly in remnant forests. We found the Azuero spider monkeys surviving in the remnant patches close to the Cerro Hoya National Park and La Tronosa Forest Reserve, and we also confirmed their presence in the surrounding secondary forest, living fences and forest patches throughout the southeastern part of the peninsula, including the gallery forest and coastal forests (Fig. 1). The spider monkeys were difficult to observe in the wild, but using presence/absence detection we obtained a total of 13 localities where their presence was confirmed; in seven of them we obtained direct counts. Conservatively, we can assume at least one subgroup is present in each of the other six (widely separated and isolated) areas. Adding 50 to the number of individuals recorded in the southeastern gallery forested areas (74 individuals), 124 individuals was the number detected during our surveys. Applying the formula β = 124/(1)0.85, I estimate a total of 145 Azuero spider monkeys remaining in the wild.
Discussion
Distribution
Cattle pasture and farmland dominate the landscape of the Azuero Peninsula, largely replacing the original forest (Heckadon-Moreno 2001). The most heavily disturbed parts are in central and northern Azuero, with urbanization more widespread and large areas of monoculture crops, besides cattle ranching (Suárez 1981). Despite this, Alouatta c. trabeata, generally scarce by any standards, was found to be widespread and occupied several different habitat types, from sea level to 1500 m. My results show evidence of a significant presence of Azuero howler monkeys and spider monkeys in forest patches with such as Anacardium excelsum, Bursera simaruba, Cecropia spp., Ceiba pentandra, Enterolobium cyclocarpum, Ficus spp., Manguifera indica, Inga vera, Pachira spp., and Spondias mombin (see Table 6); species that are generally conserved by the Azuerense campesinos as living fences on their cattle ranches (Méndez-Carvajal 2008). Previous reports of A. c. trabeata and A. g. azuerensis (Brandaris 1983; Rowe 2000) also found them surviving in extensively deforested areas of cattle ranches and gallery forest.
Alouatta c. trabeata is not restricted to the Cerro Hoya National Park. It would seem, on the other hand, that A. g. azuerensis, no longer occurs in El Montuoso Forest Reserve (EMFR), thought to be an important protected area for this species by Cuarón et al. (2008). The Azuero howler monkey is common in riparian forest and is often sighted moving through gallery forest, living fences and patches of forest of the natural reserves of Azuero (Méndez-Carvajal et al. 2004; Méndez-Carvajal 2005; Méndez-Carvajal and Ruiz-Bernard 2009). The Azuero spider monkey has been extirpated from the El Montuoso Forest Reserve (EMFR) and non-protected areas in Herrera province; it is now found only in the southern part of the peninsula, including the Mariato District (Veraguas province), Cerro Hoya National Park and La Tronosa Forest Reserve (Los Santos province) (Méndez-Carvajal and Ruiz-Bernard 2009). Deforestation and hunting has severely reduced and fragmented the ranges of A. c. trabeata and A. g. azuerensis in the region, mainly by eliminating suitable habitat, most particularly along the middle and northern parts of Azuero.
Table 6.
Common trees species identified for the study areas surveyed and observed to be used by Azuero primates, Azuero Peninsula, Panama. A) Northern Region (1); B) Northern Region (h); C) Southern Region; D) Eastern Region; E) Western Region. Species of trees confirmed, according to Pérez and Deago (2001), Garibaldi et al. (2004), and Agustin Somoza in Méndez-Carvajal (2005).
The extirpation of A. g. azuerensis from the El Montuoso Forest Reserve shows that its occurrence in a protected area is no guarantee of its survival. The Azuero spider monkey was hunted out by indigenous people and farmers. Hunting pressure seems to be less, however, for A. c. trabeata, and the howler monkey is evidently more adaptable than the spider monkeys.
The forests harboring A. c. trabeata and the Panamanian white-throated capuchin, Cebus capucinus imitator, in the southwestern part of the peninsula are classified as evergreen subtropical lowland and montane forest, but in the southeast semideciduous and largely secondary forest prevail (Garibaldi et al. 2004; Pérez and Deago, 2001). Important for these species and for A. g. azuerensis in the south is the Cerro Hoya National Park, and the riparian vegetation along the Ventana town border as far as Cambutal, then following the mangroves of the southeastern coast of Azuero mixing with the gallery forest and patches of forest near the coast in the vicinity of Tonosi, Venao, Cañas as far as Pedasi (Fig. 1).
Population estimates for the Azuero howler and Azuero spider monkey
The population estimates for the howler and spider monkeys from Azuero have changed from previous calculations made in 2008 (Méndez-Carvajal and Ruiz-Bernard 2009). The estimate for the spider monkey has increased slightly, from 117 to 145 individuals still surviving in Azuero. That for the howlers, on the other hand has dropped with an increase in the area covered by the surveys, from 4,214 in 2008 to around 3,092 (Méndez-Carvajal 2008). Not all the locations surveyed had both species; howler monkeys demonstrated better plasticity in deforested zones, as found by Clarke et al. (2002) and Baumgarten and Williamson (2007). Alouatta does better than Ateles in fragmented habitats.
Population densities
Densities of A. c. trabeata of 0.52 individuals/km2 for the northern highlands and 2.2 individuals/km2 for the lowlands are evidently low when compared to estimates in other areas; for example, A. palliata in Los Tuxtlas, Mexico, with 23 individuals/km2 (Estrada and Coates-Estrada 1996); La Selva, Costa Rica, with 12.2 individuals/km2 (Fishkind and Sussman 1987), and Barro Colorado Island, Panama, with 91.7 individuals/km2 (Milton 1992). One possible factor in this is that A. coibensis has a tendency to live in smaller unimale-multifemale, groups than A. palliata elsewhere in Mesoamerica (Méndez-Carvajal and Serio-Silva 2011). The difference in population densities between highland and lowland areas may be related to lower nutrient availability at higher altitudes (600–1,559 m above sea level) where temperatures are lower (Chapman and Balcom 1998). Morales-Jiménez (2002) found differences in group sizes for Alouatta seniculus in the Andes, with 3.1 individuals/group in high elevations, and 6.9 individuals/group in the lowlands, similar to our groups. Our survey found no effect of elevation on population density (Spearman rank correlation coefficient 0.045, n=31, p = 0.811). For highlands in Azuero (600 m), lower densities of howlers could be caused by hunting; for food in the Sonadora area behind the EMFR (northern region, highland), and also in the Cerro Hoya National Park for traditional medicinal potions, influenced directly by the Ngäbe Buglé indigenous people (Torres de Araúz 1980).
In the eastern region, the densities of A. c. trabeata were 42.6 individuals/km2, but much lower on the western side of Azuero at 17.2 individuals/km2. This could be explained by the connectivity of living fences, widespread on the western side; allowing the monkeys to move more easily through the landscape. Even if howler monkeys adapt well to surviving in disturbed forests (Ferrari 2002), overcrowding with the lack of migration is a problem. The local people on the east side of the Azuero Peninsula are more tolerant and protective of howler monkeys and exploit the forest fragments less for such as charcoal and medicinal products.
Azuero spider monkeys with 1.4 individuals/km2 for fragmented habitat suffer more from hunting pressure and the use of the forest patches by people (Méndez-Carvajal and RuizBernard 2009). Densities in this study were similar to those in other areas where they are hunted; for example, Boca de Cupe, Darien, Panama, with 3.6 individuals/km2; (Moreno-Ruíz 2006), and lower than those recorded from Tikal, Guatemala (A. g. yucatanensis) with 24 individuals/km2 (Cant 1990). Densities of A. g. frontatus have been estimated at 9 individuals/km2 in the Santa Rosa Natural Park, in Costa Rica (Freese 1976). Except for the Río Oria and La Miel area, the Azuero spider monkey has been found only as family groups (male, female, juvenile and infants), contrasting with a typical spider monkey sub-grouping system (Carpenter 1935; Aureli and Schaffner 2008).
Group composition: Azuero howler monkey
The Azuero howlers in the lowlands tended to have larger groups. The howlers from the Northern (lowland) community had an average of 23.8 individuals/group (15–39) (Méndez-Carvajal 2005), which is high when compared with the average of the Azuero howler populations elsewhere with 6.1–10.0 individuals/group (3–12) (Méndez-Carvajal et al. 2004). Due to the abundance of trees reported as potential resources for howlers in the Azuero area, we could expect them to be more abundant with larger groups in the Northern region (lowland), as was found on Barro Colorado Island (BCI) Panama. Statistical analysis of Azuero howler group structure vs. habitat size was applied in this study using Spearman's test, showing a positive correlation (-4.50, n=31, p = 0.011), confirming the hypothesis that groups in the eastern region are a slightly more connected through small patches (linear shape home-ranges), while the Northern region groups are more isolated (Fig. 1).
Group structure presented differences in the male/female ratio, and was found to be more uni-male than multi-male, contrary to the first report of the Azuero howler monkeys in the Northern region (lowland) (Méndez-Carvajal 2005). The group composition was similar to that found for A. c. coibensis on Coiba Island, with 1.8 for males and 2.8 for females (Milton and Mittermeier 1977; Méndez-Carvajal et al. 2010b).
Group composition: Azuero spider monkey
The subgroup size average of the Azuero spider monkey, 3.8 individuals/subgroup, is comparable with that found for A. fusciceps rufiventris at 4 individuals/subgroup (MéndezCarvajal et al. (2010a), and 3.5 individuals/subgroup for Venezuelan A. hybridus (see Cordero-Rodríguez and Biord 2001). Ateles g. azuerensis was found in smaller groups (12 individuals/group) in forest patches in the southern area; La Miel, Flores, Oria and Cañas. Total size of groups of Azuero spider monkeys could be considered low in devastated areas if we compare them with averages found in protected areas such as Calakmul Reserve or Quintana Roo, Mexico (28.5 individuals/group) (Ramos-Fernández et al. 2003; Estrada et al. 2004), Barro Colorado, Panama (24 individuals/group) (Di Fiore and Campbell 2007) and Ateles fusciceps rufiventris from Chucanti-Darien, Panama, with average of 30 individuals/group (Méndez-Carvajal et al. 2010a).
Conservation Status
Deforestation has been the principal threat to these subspecies. Land use in Azuero is agricultural. If the region is well supported economically, based on small, medium or large businesses, subsistence hunting could be minimal. Previous questionnaires given out before the start of this project in 2001 found that monkeys are not a vital resource for Azuero locals (Ruiz-Bernard et al. 2010). Environmental education and awareness programs informing the communities of the value of their forests and living fences, and of the ecological role of the primates, could be highly positive for the conservation of the region's primates. It will be important to set up a permanent monitoring program for the two primates and their habitats.
Our informal interviews with the people from the communities revealed two issues of relevance: (1) the lack of any informative material that values the region's fauna and flora, and (2) the lack of interest in protecting wildlife, especially these monkeys which are considered to be little more than crop pests. The Fundación Pro-Conservación de los Primates Panameños (FCPP) has been offering educational talks to elementary schools and colleges to create a basic conservation understanding for the future generations of the Azuero people (Ruiz-Bernard et al. 2010). FCPP is still monitoring the groups found in the natural reserves of Azuero.
Acknowledgments
This long-term survey is a voluntary effort of the author as a pioneer conservation initiative for these two Panamanian endemics under the auspices of the Fundación Pro-Conservación de los Primates Panameños (FCPP). The following institutions supported this project: Primate Conservation Inc., Idea Wild, the Mohamed bin Zayed Species Conservation Fund, Rufford Small Grants Foundation, Florida Museum of Natural History, Ford Motor Company, and Wild Futures. I thank the Panamanian Environmental Authority (ANAM) for providing permission to perform this research and allowing the use of their facilities in some of the study areas on Azuero Peninsula. I am grateful to professors, Simon Bearder, Anna Nekaris and Corri Waitt of Oxford Brookes University for their support and advice. I also thank Ivelisse Ruiz-Bernard, Somaly Silva, Valeria Franco, Glenis De León, Kenia Sánchez,Yarelis González, Jorge Garzón, Robert Duarte and Alejandro Garrido, for assistance in the field, and Guido Berguido for his help with the scientific station in Panama City. Noel Rowe and Russell Mittermeier were generous in supporting this project, and I am grateful to the locals of Azuero Peninsula, especially Didio González, Tacho González, and the Méndez and De León families. My special thanks to Katharine Milton and Anthony Rylands, for their help in reviewing and editing the article, and for their technical support. This research complied with protocols approved by the guidelines (University Code of Practice on Ethical Standards for Research Involving Human Participants) of the School Research Ethics Office, Oxford Brookes University, United Kingdom, and also with the legal requirements of the Republic of Panama.
