We studied a zone of sympatry between Alouatta seniculus and Alouatta palliata on the left bank of the Atrato River (Chocó). We located 110 groups of Alouatta, consisting of 81 groups of A. palliata and 29 groups of A. seniculus, recorded between 12 – 300 m a.s.l. Alouatta seniculus was associated principally with arracachal and panganal vegetation of alluvial soils alongside the Atrato River below 50 m altitude, and A. palliata was associated with upland vegetation of gallery forest, primary forest and secondary forest (20–300 m a.s.l.). The average number of animals per group of A. seniculus was 5.59 (range 2–7 individuals) while the average for A. palliata was 6.76 (range 2–18 individuals). No phenotypic evidence of hybridization was detected in contrast to other studies of hybridization of Alouatta. The condition of many of the forests in this study suggests the necessity of a conservation program in order to protect this unique zone of sympatry between the two species.
Alouatta is the most wide-spread Neotropical primate genus, distributed from southern Mexico to northern Argentina (Milton, 1980; Crockett, 1998). In Colombia two species are found that are generally allopatric, though there are poorly defined historic records and some recent observations that suggest a large sympatric zone between Alouatta palliata and A. seniculus for northern Colombia extending from the left banks of the Peye and Atrato in the Chocó department to the region around Cartagena, south to the río Sinú (Fig. 1). Whether A. palliata was at all common in northern Colombia east of the Atrato River can no longer be said; it is now very scarce in the region, perhaps having been largely displaced by A. seniculus which has a high tolerance for anthropogenic disturbances (Defler, 2012; Eisenberg, 1979). Three of the 14 recognized Alouatta species are known to have allopatric distributions with other Alouatta species (Crockett and Eisenberg, 1987). Small sympatric overlaps are known for Alouatta pigra and A. palliata in Central America (Horwich and Johnson, 1986), A. palliata and A. seniculus in Colombia (Hernández and Cooper, 1976) and A. caraya and A. fusca in northeast Argentina (Crockett, 1998).
This study was designed to describe and characterize the area of sympatric overlap between A. palliata and A. seniculus from a zone on the left bank of the Atrato River in the Darien, Colombia, and to search for phenotypical evidence of possible hybridization. We attempted to identify ecological factors characteristic of these species that could affect their distribution along the lower Atrato River. Alouatta seniculus persists at least sympatrically with A. palliata until the latitude of Quibdó (5°42′N) and, on the left bank of the lower Atrato river, A. palliata is present in the same region but on generally higher ground.
The Colombian Darién in northwestern Colombia is part of the Chocó biogeographic region, recognized for its strategic position as a bridge between Central and South America. The region comprises the Panamanian province of Darién and the northern Chocó of Colombia and includes a forested low mountainous frontier between Panamá and Colombia as well as extensive lowland swamplands on both sides of the Atrato River. The climate of the region studied is generally drier than other parts of the Chocó to the south and has a unimodal annual precipitation between 1,900– 3,100 mm, contrasting with the high precipitation of the central and southern portions of the department where the highest precipitations for any rain forest have been reported (13,300 mm in Lloró, south of Quibdó). Annual temperatures in the north are also higher at around 24° C in the lowlands, compared to further south (Rangel-Ch. and Arellano-P., 2004).
Topography is varied from a wide belt of wetlands along the Atrato river at near sea level to hills and low mountains, that gradually increase in height towards the Panama border, becoming the low mountains of the Serranía del Darien, with average heights of only 500 m but a maximum height of 1,875 m for the Cerro Tacarcuna. Originally the entire region was covered in thick forest that could be classified as bh-T in the Holdridge life-zone system (Holdridge, 1967), but currently the region is in rapid conversion of the natural vegetation to an anthropogenic landscape (Rangel-Ch., 2004a). Current forest cover in the study area up to the boundary of Los Katios National Park is limited to fragments of primary forest and secondary forest representing distinct floristic communities. The forest fragments are generally surrounded by pasturelands used for cattle as well as cultigens (corn, yams, manioc, rice, plantains and bananas, sugar cane and some coca leaf) and tree plantations (particularly of cativo Prioria copaifera, ceder Guarea aligero and roble Tabebuia rosed). The principal economic activities in the zone are cattle ranching and small scale lumbering.
The study area includes the municipalities of Acandí (8°32′ 00″N, 77°14′00″W) and Unguía (8°01′00″N, 77°04′07″W) [Colombian municipalities are similar to counties in the United States and include several towns and much countryside]. We selected ten localities because of confirmed presence of howlers and their locations, permitting reasonable access with manageable logistics. These localities were as follow: La Playona (Acandí), Balboa, Titumate, San Francisco, Tanela, Santa María la Nueva, Gilgal, Unguía and Los Katios National Park (Unguia). The particular characteristics of these localities are listed in Table 1. Data collection took place during the dry season between November, 2009 and February, 2010 (Table 1). The region has six sympatric species of primates; Alouatta palliata, Alouatta seniculus, Ateles geoffroyi rufiventris (=Ateles fusciceps rufiventris), Cebus capucinus, Saguinus geoffroyi and Aotus zonalis, but Ateles geoffroyi is becoming increasingly scarce due to hunting and habitat loss (Defler, in press-b).
Evaluating the species distribution
We used two methods to evaluate the distribution of the two species of Alouatta: unstructured interviews with local people and daily searches along paths and rivers (Pinto and Rylands, 1997; Iwanaga and Ferrari, 2002). The interviews consisted of questions about where groups had been seen, the color of their pelage and the type of vocalization. We also asked about hunting activities, the occupation of the interviewee and their time of residence in the area. People interviewed were principally subsistence hunters, small farmers, park guards and farm owners. Observations were made on foot and from boat. For each locality we noted GPS coordinates, number of individual primates observed, age-class, sex, pelage phenotype, height from ground when first observed, altitude over sea level, and the forest type. Individuals were classified as adults, subadults, juveniles and infants (Defler, 1981). We analyzed the coordinates of our observations using the program ArcGIS, version 9.3 (2008) in order to map them.
Forest habitat structure was classified and sketched by topography (hilly, hill top, sides of hills, lowland and swampy), forest type (primary, secondary, re-growth, special types of forest) and altitude above sea level. Vegetation structure was analyzed measuring DBH (diameter at breast height), tree height, and the identification of tree species. We measured tree height and DBH only from trees where the groups were first seen.
We completed 85 interviews and obtained 132 locations for Alouatta groups. We were able to locate 110 groups at these locations. The 110 groups totaled 672 individual howler monkeys of which 29 groups were A. seniculus and 89 groups were A. palliata.
For A. seniculus we found the 27 observed groups of the species in five different localities, confirming the presence of the species in four forest types varying in altitude from 7- 35 m a.s.l. (average = 19.3 m). Their distribution was restricted to floodable river plains and swampy lowlands. Eighteen of the 27 groups were seen on the left bank of the Atrato river in panganal (Raphia taedigera) associations in Katios National Park (Fig. 2).
Sampled localities and condition of forest.
The A. seniculus groups had an average of 5.59 +/- 2.08 (range 2–12 individuals) (Table 2). Two groups contained 11 and 12 individuals. The groups were made up of 1 or 2 adult males, 1–3 adult females and 1–3 subadults; the number of infants varied generally from 0–5. We observed two solitary adult males. The ratio of male adults to female adults was 1:1.1 and the ratio of adult females to immature (infant + juvenile) animals was 1:1.3. Pelage color was generally totally red-orange (Burnt Sienna to Mahogany Red or Chestnut according to Hershkovitz, 1949), although in some individuals there was some blackish coloring in the pelage that could not be closely observed due to the shyness of this species. Dark patches would suggest genetic introgression from A. palliata. We observed A. seniculus 55.2% of the time atop palm trees at an average height of only 12.5 m. Middle parts of the low forest at about 9.2 m were used about 44.8% of the time.
We observed A. palliata in nine localities, confirming the presence of this species in five types of forest. The altitude of these groups fell between 12– 400 m a.s.l. (average 94 m). They were principally observed in gallery forests and in old growth of secondary forest. The structure and composition of 76 groups of this species averaged 6.76 animals per group (range 2–18 individuals; DS: 3.6) (Table 3). Two groups had between 17 and 18 individuals. Groups usually had 1–3 adult males, 1–4 adult females, 1–3 subadults and from 0–3 immature animals for the 76 groups. The ratio of adult males to adult females was 1:1.5 and the ratio of adult females to immature animals was 1:0.99.
Usually the pelage of this species was totally black, although occasionally there were individuals with patches of brown on the flanks and the dorsal area. One male adult had whitish coloration in the mesial part of the tail. There was no pelage evidence of hybridization with A. seniculus on these animals. We observed a total of five solitary animals, three of which were males, one was a solitary female and one was a solitary subadult sex unknown. The solitary subadult A. palliata was heavily infested by bot flies (Alouattamyia baeri?). A. palliata was seen 77.8% of time at canopy height of 22.7 +/- 5.0 m while the undergrowth was used only 22.2% of the time with an average height of 9.5 m +/- 3.3 m.
Age-sex composition for 29 groups of Alouatta seniculus in the Darien region of the Colombian Chocó.
Forests habitat structure
Generally A. palliata and A. seniculus were associated with different types of habitat. The wetlands of Darién are dominated by plant communities like the panganales, arracachales and cativales (very impacted due to lumbering of the tall cativo tree [Prioria copaifera, Rangel-Ch, 2004a]) that are found along edges and dikes of the Atrato river, sometimes at the base of hills and terraces. Panganales are dominated by the pangana palm (Raphia taedigerd), the suerdo (Ficus dendrosida, Cecropiaceae) and the chachafruto (Erythrina fusca, Fabaceae). In the medium stratum cativo (Prioria copaifera, Caesalpineaceae [an endangered tree species or EN in the IUCN system for Colombia], yarumo (Cecropia sp.) and guamo (Inga spp., Mimosaceae) are common. This type of forest is the most important for Alouatta senciculus and Cebus capucinus in the Darien region. Nevertheless it is one of the most transformed associations because of extraction of woody species and the opening of canals to drain flooded areas for use as pasture land.
Arracachales dominated by the widely distributed arracacho (Montrichardia arborescens, Araceae) is the principal association on the flood plain of the Atrato river. The arracacho (Montrichardia arborescens reaches 10–15 species per square meter with an average height of only 2 m (Plan de Manejo Katios, 2007). Arracachos grow in association with other dominant species such as Blechnum serrulatum, Acostichum aureum, Scleria secans, Scleria melaceuca and species of Thelytpteris and Panicum (Rangel-Ch, 2004a), often interspersed with ferns such as Macfadyena ungis. Alouatta seniculus using this community are easily seen because of the very low vegetation, in contrast to other vegetation types.
Rastrojo had a sometimes discontinuous, sometimes continuous canopy and thick undergrowth. Important tree species were Ficus spp. (Moraceae), cecropia (Cecropia sp., Cecropiaceae), hobo (Spondias mombin, Anacardiaceae), copey (Clusia sp., Clusiaceae), abarco (Cariniana pyriformis, Lecythidaceae), roble (Tabebuia rosea o Taebuia sp., Bignoniaceae), cedro (Cedrela cf. angustifolia, C. odorata, Meliaceae), cativo (Prioria copaifera, Caesalpinaceae), balso (Ochromoa pyramidale, Bombacaceae), ceiba (Ceiba pentandra, Bombacaceae), caracoli (Anacardium excelsum, Anacardiaceae), rubber (Castilla sp., Moraceae), churimo (Inga sp. probably I. edulis, Mimosaceae). Height of trees in this forest reaches 20–25 m, especially in the cases of Ceiba pentandra, Anacardium excelsium and facaranda caucana (Bignoniaceae). Rastrojos are often difficult of access because of the dense and closed vegetation, although some rastrojos were more open and especially exposed along the borders. These forests result from cutting the original forest for agriculture or other purposes and allowing a new forest to grow and mature on the same spot. Rastrojos were often isolated from other forest, requiring terrestrial travel for the Alouatta groups.
Altitudinal ranges of sampled sites and the number of sites with either presence or absence of the species.
Groups associated with forest types in the study area.
Gallery forests represented 25% of all observations of A. palliata. These primates were found alongside small rivers such as the Chugandi, Negro, Tanela, Tanelita, Cuti, Tibirri and the Titiza among others. Some groups were located in forest bordering very small streams and most of this forest was made up of tall (20–25 m) and continuous vegetation. Common trees of the gallery forest are balso (Ochromoa pyramidale, Bombacaceae), guaimaro (Brosimum alicastrum y B. guianense, Moraceae), cedro (Cedrela cf. angustifolia, C. odorata, Meliaceae), abarco (Cariniana pyriformis, Lecythidaceae), caracoli (Anacardium excelsum, Anacardiaceae). DBH's ranged from 0.63–2.67 m. Gallery forests have been conserved in most of the veredas (subdivision of a municipio in Colombia), since the inhabitants understand the importance for water quality.
Secondary growth forests showed various states of succession. Disturbances that created clearings modify the structure of the original forest allowing the growth of many pioneer species. Common trees growing in secondary growth forests (similar to rastrojo) were cedro (Cedrela cf. angustifolia, C. odorata, Meliaceae), copey (Clusia sp., Clusiaceae), palma mil pesos (Jessenia bataua, Araceae), cuipo (Cavanillesiaplatanifolia, Bombacaceae), guamo (Inga spp, Mimosaceae), copey (Clusia sp., Clusiaceae) , yarumo (Cecropia spp., Cecropiaceae), balso (Ochromoa pyramidale, Bombacaceae) , tachuelo (Zanthoxylum grandifolum, Rutaceae) and churimo (Inga edulis, Mimosaceae). These forests were usually surrounded by pasturelands used by cattle.
Primary forests were often disturbed due to logging so that species with low economic value predominated, even though three strata of trees existed. The highest stratum consisted of emergent trees up to 20–25 m, dominated by species such as higuerón (Ficus sp., Moraceae), cedro (Cedrela cf. angustifolia, C. odorata Meliaceae), caracolí (Anacardium excelsum, Anacardiaceae), hobo (Spondias mombin, Anacardiaceae), almendro (Dipteryx oleifera, Fabaceae) and cordoncillo (Piper imperialis, Piperaceae) among others. This forest type characteristically contained climbing plants and lianas, and very little undergrowth.
Of six forest types, A. palliata was found in five and A. seniculus in four (Table 5). A. palliata was mostly in second growth and gallery forests and never in the arracachal associations (Montrichardia arborescens). We observed one group of A. palliata in panganal (Raphia taedigerd). In contrast, A. seniculus commonly used the panganal association and was seen very rarely in second growth (rastrojo) (Table 5). We never observed either species of Alouatta in tree plantations or in other crops, in contrast to Cebus capucinus, which we observed several times in both forest plantations and other cultivars.
This study confirms the sympatry between A. seniculus and A. palliata along the west bank of the Atrato river and formally register other sites east of the Atrato river, but we cannot confirm hybridization between the two species. According to local information, sympatry between the two species continues upriver to an undetermined point along the Atrato river. Hybridization is not well-known in Alouatta. A study of Alouatta sympatry describes hybridization between A. caraya and A. clamitans in a group of eight individuals observed near the Paraná river in Brazil, in the ecotone between rain forest and the Cerrado, showing intermediate morphological variation (Aguiar et al., 2007). Another study in Tabasco, Mexico, reported hybridization of individuals with a mosaic of morphological characteristics between A. palliata and A. pigra. These included individuals living in various grades of disturbed vegetation and that had characteristics of both species (Cortes-Ortiz et al., 2007). Also, hybridization is known in captivity between A. caraya and A. guariba (de Souza et al., 2010).
The two species of Alouatta in this study are not completely syntopic; their habitat preferences seem to overlap somewhat, affording some contact. According to Agostini et al. (2010) in undisturbed habitat the two species could be avoiding competition, employing strategies associated with different diets and different habitat use when in sympatric contact (Lehmann, 2004). Given the differences detected in the use of distinct types of forest in this research and a lack of clear-cut morphological evidence for hybrids, we suspect that the two species maintain effective separation. Further to the east in the highly disturbed and fragmented Colombian Caribbean there may be animals with mixed phenotypes (obs. pers. A. Flórez and F. Garcia-Castillo) and these animals should be studied, especially in Cordoba (Fig. 1). Bicca-Marques et al. (2008) indicate that the habitat and utilization of resources are not considered factors that maintain a separation of species of Alouatta. Other authors consider that disturbed habitats can play a fundamental role in the sympatry and overlap of species' ranges (Aguiar et al., 2007, 2008; Agostini, 2010). The situation of the Darien is of a disturbed habitat. Colonization has led to changes in vegetation cover resulting in much pastureland for cattle ranching and disturbed vegetation (Plan de Manejo Katios, 2007). Accordingly it seems logical that these activities might influence contact between the two species.
In the Chocó A. palliata was present at all sites sampled from sea level to above 300 m, although its presence in panganal was minimal. But Alouatta seniculus was absent on the sides of hills from primary and secondary forest, although this species has been found up to 3,200 m in the Colombian Andes and is found in many types of primary forests in the lowlands of Amazonia, as well as gallery forest in Orinoquia and sub-Andean forests in Quindío (Hernández and Cooper, 1975; Gaulin and Gaulin, 1982; Izawa, 1988; Defler, 1981, 2010; Stevenson et al., 1991). In the Darien A. seniculus is restricted to swampy forest, panganales especially along the borders of rivers (Neville 1972; Defler 2010) and it is limited to elevations below 50 m. These uses of particular habitats clearly show there to be a minimum of distribution overlap in the Chocó.
The use of forest strata by A. palliata and A. seniculus is related principally to the food supply, solar exposure and locomotion (Braza et al., 1981; Lehmann, 2004). These animals prefer forest with adequate connectivity between canopies (Neville, 1972; Izawa, 1976) and tall trees, generally of 20–25 cm diameters or more (Gómez-Posada et al., 2007). The observations of A. palliata and A. seniculus in this research showed a preference of these primates for upper strata. During the study, A. palliata groups were found 77.8% of the time in the canopy. They were only found in underbrush when they were eating from low trees or resting in shade (Palma, 2005). Groups of A. seniculus were seen in the low canopy 55% of the times observed where they generally were eating or resting. The middle stratum was used for travel (Izawa, 1976; Braza et al., 1981). They were not observed in tall emergent trees in this study, a contrast to some other studies (Defler, 1981, 2010). The forests that were sampled contained plant species that already have been reported as being highly important for the diet of the two species of Alouatta (Neville et al., 1988). These generally correspond to the Moraceae (usually the most important family in the diet of Alouatta) (Milton, 1980; Crockett and Eisenberg, 1987), including especially Ficus spp, Cecropia spp. as some of the most important genera (Milton, 1980; Gaulin and Gaulin, 1982; Crockett and Eisenberg, 1987; Gómez-Posada et al., 2007; Giraldo et al., 2007).
Studies of A. seniculus suggest that this species is more a generalist than is A. palliata and usually does not depend on one type of habitat in particular (Neville, 1972; Stevenson et al., 1991; Julliot, 1996; Bicca-Marques, 2003). Other authors report preferences of the species for specific types of vegetation found at riversides, on river terraces, and in transitional forests and forest of Igapó during the dry season (Palacios and Rodríquez, 2001; Iwanaga and Ferrari, 2002) where they consume species such as Cecropia sp. and Ficus sp. and new leaves (Stevenson et al., 1991). The densest populations known are found in the llanos of Colombia and Venezuela (Crockett and Eisenberg, 1987; Defler (in press-a). In this study A. seniculus was associated with vegetation that is frequently inundated and where the species Raphia taedigera, Erythrina fusca and Cecropia sp. were found. Such associations reached heights of only 8–9 m and did not have a continuous stratum along the edge of the Atrato river. This primate was also associated with the plant species Welfia regia and Prioria copaifera and the animals were often syntopic with Cebus capucinus. River and lake-side preferences of A. seniculus in eastern Colombia have also been described where no second species of Alouatta is present (Defler, in press-a)
A. palliata has demonstrated its capacity for surviving in fragmented habitats (Crockett and Eisenberg, 1987; Clarke et al. 2002; Rodríguez-Toledo et al., 2003; Bicca-Marques, 2003). In this study this species seemed quite habituated to human beings, since during the majority of observations they continued their activities without being disturbed by our presence. Nevertheless, hunting of A. palliata in some parts of the Darien is reported to be very high, since they are avidly pursued by members of various indigenous ethnic groups such as the Cunas and Emberas (com. pers. various interviewees). Hunting pressure on A. seniculus is medium to high along the banks of the Atrato River, according to comments from locals. In other cases, for example around the Ciénega de Ungía and because of the low vegetation, the animals are harassed and chased as a diversion, causing fear towards humans in both cases (probably always a reasonable response).
The Darien was considered one of the 17 most critical areas in the world for conservation, according to the concept first developed by Myers (1988), underlining the importance of conservation planning and resource management in local development. Human activities compromise the continued presence of howlers in this region, and data on hunting, descriptions of habitat alteration and diseases are relevant for the management and conservation of these species over time. Studies of the ecology of closely related sympatric species represent a challenge, since these relationships are not commonly found in all habitats and their ecological relationships are not always evident. It is particularly important to integrate the demographic history and population structure of these primates to be able to monitor the changes that occur over time (Crockett, 1998; Rodríquez et al., 2003; Asencio et al., 2009; Defler, 2010). It is fundamental to define the technical and scientific criteria to be included in any resource planning and to include the active participation of communities in any region for the success of any future studies that facilitate the conservation of these species in the future.
Sara Zuñiga Leal especially thanks her mother, Alexandra Leal, who has supported her in these and all of her formation. We thank the people of the Chocó region, UAES-PNN (Colombian Parks Service), Katios National Park, Lilia Cordoba and relatives for their support at all time. We also thank Jaime Burbano for orientation using ArcGis and Marcela Fonseca, Maritza Larrota and Silvana García for their support. Thomas Defler thanks the Universidad Nacional de Colombia for support during the writing of this article.
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