Notes on the population and diet of Ateles geoffroyi vellerosus in a tropical rain forest of Oaxaca, Mexico
Teresita Ortiz-Martínez1,2 and Víctor Rico-Gray1
1
Departamento de Ecología Aplicada, Instituto de Ecología, A.C., Km 2.5 Carr. Antigua a Coatepec #351, Congregación El Haya, Xalapa, Veracruz 91070, México
2
Corresponding author: e-mail address: [email protected] (T. Ortiz-Martínez) Tel.: +52 (228) 842-1847, fax: +52 (228) 842-1847 ext. 4302
Key Words Ateles geoffroyi vellerosus; censuses; conservation; diet; Mexico; Oaxaca; tropical rain forest
This paper reports the findings of a brief study to estimate density, subgroup size and diet of spider monkeys (Ateles geoffroyi vellerosus) in a tropical rain forest of the state of Oaxaca, Mexico. For this state the study of primates is in the earliest stages. The current geographic distribution of these primates is being documented and no data on their population sizes are available. Regarding their diet little is known for this region (Ortiz-Martínez and Rico-Gray 2007) and for the rest of Mexico there are only few published reports (Watts and Rico-Gray 1987; Silva-López et al. 1993; Ramos-Fernández and Ayala-Orozco 2003). Because of the little attention focused to the primates living in Oaxaca and the extensive areas covered by tropical forest in this region, their study at this extent of their range has been largely recommended as a research priority (Estrada and Mandujano 2003).
Between June and December 2003 we collected data on monkeys in Cerro Chango communal protected area, in the north of the state of Oaxaca, Mexico. This is a 7km2 protected area of the community San José Río Manso located at 95°55' W and 17°42' N. The dominant vegetation type is tropical rain forest and altitude varies from 60 m to 130 m a.s.l. We conducted strip censuses along 4 km (perpendicular distance 30 m; area = 0.24 km2) of existing trails within the protected area. At least two observers, including one local guide, walked slowly along the trails, beginning at dawn. When monkeys were detected we recorded the number of individuals, sex and age classes. Considering the differences in their size and appearance, as has been described in other studies (e. g., Cant 1978), age was classified only in adults, juveniles and infants. The latter included both clinging individuals and individuals progressing independently during short moves. Subgroup size was determined according to the criteria employed by Cant (1978), where infants were included as members of the subgroup and one or more individuals in one contact counted as one subgroup. We analyzed only data of monkeys observed within the strip width along the census route. Density was estimated by dividing the number of these sights by the strip area, the latter was obtained by the multiplication of strip width by transect length. Mean densities of both individuals and subgroups of monkeys/km2 were derived from their estimation from the strip area. We based our population and subgroup size estimations on six days of complete observation. Observations of feeding were recorded by noting items and both species and local name of the ingested food. We complemented our observations by collecting and checking samples of feces from the forest floor. We obtained additional data on diet from local inhabitants who had observed these monkeys feeding in other contacts made prior to our survey. Samples of plants not identified during the field study were collected to be identified at the herbarium. Ingested seeds recovered from fecal material were identified by specialists to species level when possible.
We observed spider monkeys 22 times, six of these occurred outside the strip area, additionally we heard five subgroups. The density estimated was 54.9 individuals/km2 and
11.1 subgroups/km2. We observed two to four subgroups per day (average = 2.67 ± 0.82). Subgroups ranged from 1 to 13 individuals (4.9 ± 3.4). The proportions of age classes of individuals counted were: adults 0.68, juveniles 0.15, and infants 0.16. Adult sex ratio was 1:2.11 and adult female to immature was 1:0.84; these ratios were derived from the 10 completely identified subgroups (62.5%). Spiders monkeys fed from 16 plant species belonging to 11 families (Table 1). Of these, 75% were trees and the remaining 25% included one epiphyte, one vine, one shrub, and one non-identified species. During the study monkeys fed mostly on fruits.
Based on transect method, the density estimated for spider monkeys in Cerro Chango is similar to those found in Tikal protected area, Guatemala (45 ind/km2 in Coelho 1976; 56.4 ind/km2 Estrada et al. 2004). These densities represent an average size within the range reported for Ateles geoffroyi in other sites in México (27.11 and 14.52 ind/km2 in Gonzalez- Kirchner 1999; 17.0 and 17.2 ind/km2 in Estrada et al. 2004; 6.3 and 87 ind/km2 in Ramos- Fernández and Ayala-Orozco 2003), Guatemala (26 ind/km2 in Cant 1978), and Costa Rica (6-9 ind/km2 in Freese 1976; 6 and 8-10 ind/km2 in Pruetz and Leasor 2002). Extreme population densities of these monkeys are found in highly fragmented and isolated habitats (0.22 ind/km2 Estrada and Coates-Estrada 1996; 150 and 114 ind/km2 in Silva-López et al. 1993). Several studies have documented that extinction (Corlett and Turner 1997) and low densities of monkeys are expected consequences of habitat reduction and degradation, isolation, and hunting (Estrada and Coates-Estrada, 1996), while high densities are the temporal effect of overcrowding in remaining habitat (Marsh et al. 1987; Pruetz and Leasor 2002).
Spider monkeys in Cerro Chango were observed in subgroups of 1 to 13 individuals, but small subgroups consisting of no more than six monkeys were more frequently observed, as found in other sites in Mexico (González-Zamora 2003; Ramos-Fernández and Ayala-Orozco 2003). The average subgroup size of these monkeys is more like those reported for Muchukux, Quintana Roo (4.55 in Gonzalez-Kirchner 1999) and Tikal, Guatemala (4.7 in Estrada et al. 2004), where the average size is around 5 ind/km2. Most reports for the species show that lower and higher mean subgroup sizes are found in both extensive (3.82 and 4.3 in Cant 1978; 4 in Silva-López and Jiménez-Huerta 2000; 7.7 and 5.6 in Estrada et al. 2004) and fragmented forest (6.25 and 5.76 in Silva-López et al. 1993; 3.82 in Gonzalez- Kirchner 1999; 5.76, 5.87, and 3.6 in Silva-López et al. 2001; 2 and 3.3 in Pruetz and Leasor 2002; 4 in González-Zamora 2003), thus we still lack clear relation in response to habitat suitability differences (Serio-Silva et al. 2006).The sex ratio of adult males to females in this study is consistent with those found in extensive forest tracts such as Calakmul, Mexico (1:2.07 in Estrada et al. 2004) and Tikal, Guatemala (1:2.23 in Coelho 1976; 1:1.76 in Cant
result is also similar to those of the Yucatan Peninsula, Mexico (1:0.87 in Serio-Silva et al. 2006), Calakmul, Mexico (1:0.74 in Estrada et al. 2004) and Tikal, Guatemala (1:0.68 in Coelho 1976; 1:0.71 in Estrada et al. 2004), as found in fragmented sites of Sierra de Santa Marta, Mexico (1:0.76 in Silva-López et al. 2001) whose ratio of around one immature per adult female suggest a reproductively active population.
Spider monkeys (Ateles geoffroyi) spend large proportions of their feeding time eating fruits, in comparison to other plant items such as leaves and flowers (Milton 1981; Chapman 1987). From the data obtained during this study, monkeys consumed the fruits of 15 plant species and leaves of only one species. Based on this evidence the diet of these monkeys was primarily frugivorous as has been reported elsewhere. However, long-term studies on this monkey are necessary to document their foraging choices with more precision. Regarding information from local inhabitants, three of seven species they reported monkeys ate were confirmed during our field work, and only one (Pouteria sapota) has been not documented before from the study of spider monkeys elsewhere. This adds to the evidence that local inhabitants can provide reliable information to the investigations of target species (Zinner et al. 2001; Radhakrishna et al. 2006). Of the 16 foraged species that we reported here, seven have not been published before as food used resource for A. geoffroyi (Chapman 1987; Van Rosmalen and Klein 1988; Watts & Rico-Gray 1987; García-Orduña 2003; González-Zamora 2003; Ramos-Fernández and Ayala-Orozco 2003; Ortiz-Martínez and Rico-Gray 2007) (Table 1). Of these seven species, only Monstera sp. (Van Rosmalen and Klein 1988) and
Celtis iguanae (Van Rosmalen and Klein 1988; Suárez 2006), have been reported as food
species for the genus Ateles elsewhere.
The Cerro Chango communal land protected area forms part of a larger extension of tropical forest in the north of the state of Oaxaca. At this region is found the westernmost verified distribution for neotropical primates and has been identified as one of the important areas for primate conservation and research in Oaxaca (Ortiz-Martínez et al. unpublished data). Private and communal land protected areas implies a commitment to conservation and management, and sustainable uses are recommended to obtain economical benefits. The attractive landscape of the communal land of San José Río Manso and its biological diversity, provides it with a great potential for the development of ecotourism. Although monkeys are protected against hunting, selective logging of trees for construction and other uses can be permitted under local controlled limits. Some of the tree species important for human activities also represent important food sources for monkeys, such as Dialium
guianense (paque), Manilkara sapota (chicozapote) and Pouteria sapota (mamey).
Therefore, the identification of tree individuals and species used by monkeys for foraging provided data to support decisions on the use and management of the forest inhabited by the monkeys.
Acknowledgements
We are grateful to the local authorities and inhabitants of San José Río Manso, Oaxaca, particularly to Abel Toledo Méndez and Francisco Vargas, for their permission, logistical support and assistance during the field study. Javier Sandoval, Paloma Mejia, and Stephanie Weisgerber are thanked for their help at various stages of this research. Gonzalo Castillo and Claudia Gallardo are thanked for their help in determining the plant species. We are grateful to Cliona Maher who improves the English version of our manuscript. We thank COPLADE and the government of the state of Oaxaca for digital geographic information. We thank IDEA WILD for the donation of equipment to aid our research. We thank the staff of PNUD Chinantla region for its assistance during the study. We were supported by the Instituto de Ecología, A.C. (902-16-335), CONACYT (which awarded a scholarship -171209- to TOM) and CONAFOR-Oaxaca. The latter was obtained thanks to Conserva, A.C.
References
Cant J.G.H. 1978. Population survey of the spider monkeys Ateles geofrroyi at Tikal, Guatemal. Primates 19:525-535.
Corlett R.T. & Turner I.M. 1997. Long term survival in tropical forest remnants in Singapore and Hong Kong. In: (W.F. Laurance and R.O. Bierregaard Jr. eds) Tropical forest remnants: ecology, management and conservation of fragmented communities. Chicago University Press. pp. 333-345.
Chapman C.A. 1987. Flexibility in diets of three species of Costa Rican primates. Folia Primatol. 49:90-105.
Estrada A. & Coates-Estrada R. 1996. Tropical rain forest fragmentation and wild population of primates at Los Tuxtlas, Mexico. Int. J. Primatol. 17: 759-783.
Estrada A., Luecke L., Van Belle S., Barrueta E. & Rosales M. 2004. Survey of black howler (Alouatta pigra) and spider (Ateles geoffroyi) monkeys in the Mayan sites of Calakmul and Yaxchilán, Mexico and Tikal, Guatemala. Primates 45:33-39.
Estrada A. & Mandujano S. 2003. Investigaciones con Alouatta y Ateles en México. Neotrop. Primates 11:147-156.
Freese C. 1976. Censusing Alouatta palliata, Ateles geoffroyi, and Cebus capucinus in the Costa Rican dry forest. In: (Thorington R.W. and Heltne P.G. eds) Neotropical Primates. National Academy of Sciences, Washington, D. C. pp. 4-9.
García-Orduña F. 2003. Comparación de las estrategias de forrajeo de Ateles geoffroyi
vellerosus y Alouatta palliata mexicana en un fragmento de selva en la Sierra de Santa
González-Zamora A. 2003. Patrones de utilización de fragmentos de selva por el mono araña Ateles geoffroyi vellerosus en el sur de Veracruz. [Thesis] Instituto de Ecología, A. C. Xalapa, México.
Gonzalez-Kirchner J.P. 1997. Habitat use, population density and subgrouping pattern of the Yucatan spider monkey (Ateles geoffroyi yucatanensis) in Quintana Roo, Mexico. Folia Primatol. 70:55-60.
Marsh C.W., Johns A.D. & Ayres J.M. 1987. Effects of habitat disturbance on rain forest primates. In: (C.W. Marsh and R.A. Mittermeier, eds) Primate conservation in the tropical rain forest. Alan R Liss, New York. pp 83-107.
Milton K. 1981. Food choice and digestive strategies of two sympatric primate species. Am. Nat. 117:496-505.
Ortiz-Marínez T. & Rico-Gray V. 2007. Spider monkeys (Ateles geoffroyi vellerosus) in a tropical deciduous forest in Tehuantepec, Oaxaca, Mexico. Southwest. Nat. 52:393-399. Pruetz J.D. & Leasor H.C. 2002. Survey of three primate species in forest fragments at La
Suerte Biological Field Station, Costa Rica. Neotrop. Primates 10:4-9.
Ramos-Fernández G. & Ayala-Orozco B. 2003. Population size and habitat use of spiders monkeys at Punta Laguna, Mexico. In: (L.K. Mash, ed) Primates in fragments: ecology and conservation. Kluwer/Plenum Press, New York. pp. 191-209.
Radhakrishna S., Goswami A.B. & Sinha A. 2006. Distribution and Conservation of
Nycticebus bengalensis in Northeastern India. Int. J. Primatol. 27:971-982.
Silva-López G., Benítez-Rodriguez J. & Jiménez-Huerta J. 1993. Uso del hábitat por monos araña (Ateles geoffroyi) y aullador (Alouatta palliata) en áreas perturbadas. In: (R.A. Medellín and G. Cevallos, eds) Avances en el estudio de los mamíferos de México. pp 421-435.
Silva-López G. &, Jiménez-Huerta J. 2000. A study of spider monkeys (Ateles geoffroyi
vellerosus) in the forest of the crater of Santa Marta, Veracruz, Mexico. Neotrop. Primates
8:148-150.
Silva-López G., Mota Gill J. & Sánchez-Hernández A. 2001. Composición sexo-edad en grupos de monos araña, Ateles geoffroyi vellerosus Kellog y Goldman (1944), de México y Guatemala. Foresta Veracruzana 3:41-46.
Serio-Silva, J., Rico-Gray V. & Ramos-Fernández F. 2006. Mapping primate populations in the Yucatán Peninsula, México: A first assessment. In: (A. Estrada, P. A. Garber, M. Pavelka, L. Leucke, eds) New perspectives in the study of Mesoamerican Primates: Distribution, Ecology, Behavior and Conservation. Springer, New York, pp. 489-511. Suarez S.A. 1996. Diet and travel costs of spiders monkeys in a nonseasonal, hyperdiverse
Van Roosmalen M.G.M. & Klein L.L. 1988. The spider monkeys, genus Ateles. In: (R.A. Mittermeir, A.B. Rylands, A.F. Cohimbra-Filho and G.A.B. da Fonseca, eds) Ecology and Behavior of Neotropical Primates. Academia Brasileira de Ciencias, Rio de Janeiro. pp. 455-3537.
Watts E. & Rico-Gray V. 1987. Los primates de la península de Yucatán, México: estudio preliminar sobre su distribución actual y estado de conservación. Biótica 12:57-66.
Zinner D., Peláez F. & Torkler F. 2001. Distribution and habitat associations of baboons (Papio hamadryas) in Central Eritrea. Int. J. Primatol. 22:397-413.
Table 1. Plant species used by Ateles geoffroyi as food in the rain forest of San José Río Manso, Oaxaca, Mexico.
Family Species Local name Part
eaten
Record Typea
Anacardiaceae Spondias mombin Jobo Fruit F
Annonaceae Annona sp. Anona Fruit F
Araceae Monstera sp. b - Leaf D
Arecaceae Desmoncus orthacanthosb Bejuco Fruit F
Cecropiaceae Cecropia obtusifolia Chancarro Fruit R
Euphorbiaceae Omphalea oleifera b - Fruit D
Fabaceae Not identified - Fruit F
Leguminosae Dialium guianense Paque Fruit R/F
Moraceae Brosimum alicastrum Ojoche Fruit R/D
Moraceae Ficus sp. Amate Fruit R/D
Sapotaceae Manilkara sapota Chicozapote Fruit R
Sapotaceae Pouteria campechiana Zapote negro Fruit R
Sapotaceae Pouteria sapota b Zapote mamey Fruit R
Sapotacea Sideroxylon tempisque b Zapotillo Fruit F/D
Ulmaceae Ampelocera hottlei b Cautivo Fruit F
Ulmaceae Celtis iguanaea b Bejuco Fruit F
a
Record type: F, feces; D, direct observation; R, reported by local inhabitants. b
CAPÍTULO VI