American Journal of Primatology 46:197–211 (1998)
Primate Diversity, Habitat Preferences, and Population Density Estimates in Noel Kempff Mercado National Park, Santa Cruz Department, Bolivia ROBERT B. WALLACE,1,2* R. LILIAN E. PAINTER,1,2 AND ANDREW B. TABER1 Wildlife Conservation Society, 185th Street and Southern Boulevard, Bronx, New York 2 Evolutionary Psychology and Behavioural Ecology Group, Department of Biology, University of Liverpool, Liverpool, England
1
This report documents primate communities at two sites within Noel Kempff Mercado National Park in northeastern Santa Cruz Department, Bolivia. Diurnal line transects and incidental observations were employed to survey two field sites, Lago Caiman and Las Gamas, providing information on primate diversity, habitat preferences, relative abundance, and population density. Primate diversity at both sites was not particularly high, with six observed species: Callithrix argentata melanura, Aotus azarae, Cebus apella, Alouatta caraya, A. seniculus, and Ateles paniscus chamek. Cebus showed no significant habitat preferences at Lago Caiman and was also more generalist in use of forest strata, whereas Ateles clearly preferred the upper levels of structurally tall forest. Callithrix argentata melanura was rarely encountered during surveys at Lago Caiman, where it preferred low vine forest. Both species of Alouatta showed restricted habitat use and were sympatric in Igapo forest in the Lago Caiman area. The most abundant primate at both field sites was Ateles, with density estimates reaching 32.1 individuals/km2 in the lowland forest at Lago Caiman, compared to 14.1 individuals/km2 for Cebus. Both Ateles and Cebus were absent from smaller patches of gallery forest at Las Gamas. These densities are compared with estimates from other Neotropical sites. The diversity of habitats and their different floristic composition may account for the numerical dominance of Ateles within the primate communities at both sites. Am. J. Primatol. 46:197–211, 1998. © 1998 Wiley-Liss, Inc.
Key words: primate diversity; habitat use; density; Bolivia INTRODUCTION Line transects have been extensively used throughout the forested tropics as a means of calculating the relative abundance and estimating the density of a wide variety of large (>1 kg) mammals [e.g., Emmons, 1984; Koster & Hart, 1988;
Contract grant sponsor: Wildlife Conservation Society. *Correspondence to: Robert B. Wallace, Evolutionary Psychology and Behavioural Ecology Group, School of Biological Sciences, Nicholson Building, University of Liverpool, Liverpool L69 3BX, UK. Email:
[email protected] Received 18 October 1997; revision accepted 12 May 1998
© 1998 Wiley-Liss, Inc.
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Karanth & Sunquist, 1992; White, 1994], particularly arboreal primates [e.g., Whitesides et al., 1988; Thomas, 1991]. However, it is widely recognized that this method provides at best only reasonable density estimates and longer term observational studies, based on the identification of all individuals in an area, are the only way to accurately assess population densities in a given area [Defler & Pintor, 1985; Brockelman & Ali, 1987]. A sampling effort which yields at least 40 and preferably 60–80 encounters for a given target species has been recommended [Burnham et al., 1980]. Nevertheless, useful comparisons between areas and/or habitat types have been possible with fewer encounters, and line transects have proved a popular compromise with many researchers due to the rapidity in which a relatively large area can be surveyed. Although Bolivia has recently been the focus of several primatological field studies, much of this attention has been directed toward true Amazonian forests in the northern regions of the country, particularly in Pando Department, where primate diversity is high and includes the endangered Goeldi’s monkey (Callimico goeldii) [Freese et al., 1982; Kohlhaas, 1988; Buchanan-Smith, 1991]. In contrast, primate diversity and distribution are largely undocumented in the extensive eastern regions of lowland Bolivia [but see an unpublished 1985 report to the New York Zoological Society by A.D. Brown and D.I. Rumiz; Braza & Garcia, 1988; Wallace et al., in preparation]. Here we present data concerning primate communities at two field sites in Noel Kempff Mercado National Park, Department Santa Cruz, which were collected as part of a general mammalian survey [Painter et al., in preparation]. MATERIALS AND METHODS Study Area Noel Kempff Mercado National Park is situated on the Brazilian Shield geological formation in northeastern Santa Cruz Department, Bolivia. The Itenez River defines the park’s eastern and northern edges and marks the border with neighboring Brazil. Largely comprised of the Serrania de Huanchaca, a Precambrian table-mountain or mesa rising 200–400 m above the surrounding lowlands, the park covers 1,500,000 ha and contains an array of markedly differing habitat types, including open pampas, cerradâo forest, gallery forest, and various forms of tropical lowland forest. This lowland forest is broadly classified as Precambrian shield humid forest [Killeen et al., 1993]. While no meteorological data exist for the park itself, the region is characterized by a marked dry season in the austral winter, a mean annual temperature of 24o C, and annual precipitation of approximately 1,500 mm [Killeen, 1996]. Research was conducted at two sites within the park (see Fig. 1). For 15 months between September 1991 and November 1992 research was based at Lago Caiman (lat. 13°, 36′ S, lon. 60°, 55′ W), a large oxbow lake situated at the base of the northern tip of the Huanchaca escarpment and approximately 21 km up the Itenez River from the Flor de Oro tourist center. Trails totaling 46.6 km were distributed across an approximately 50 km2 area (see Fig. 2) and passed through a variety of distinct habitats. The following habitat types were recognized along the trails: 1. Tall forest was found on slightly undulating terrain with relatively deep and well-drained clay soils at the base of the escarpment. Emergent and canopy tree species such as Amburana cearensis, Parkia pendula,
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Fig. 1. Map of Noel Kempff Mercado National Park and locations of the two field sites: Lago Caiman and Las Gamas.
Enterolobium sp.(all Leguminosae), Pseudolmedia spp., Brosimum spp., Clarisia racemosa (all Moraceae), Qualea spp., and Erisma uncinatum (both Vochysiaceae) were typical and attained heights of up to 40 m. Palms such as Socratea exorrhiza and Euterpe precatoria, as well as smaller trees such as Theobroma speciosum (Sterculiaceae), Hirtella sp.(Chrysobalanaceae), Inga spp., Platypodium spp.(both Leguminosae), and Pourouma spp (Moraceae), were common in the subcanopy. 2. Low vine forest was found on well-drained slopes at the base of the escarpment. This habitat was characterized by large canopy and emergent trees such as Pseudolmedia spp., Casearia gossypiosperma (Flacourtiaceae), Sloanea spp.(Elaeocarpaceae), Celtis chipii (Ulmaceae), Sclerolobium spp.,
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Fig. 2.
Vegetation map of the Lago Caiman study site and the sampled transect trails.
Poeppigia procera (both Leguminosae), and Platypodium spp. that reached heights of up to 25 m, as well as by abundant Bignoniaceae vines. 3. Sartenejal forest was predominantly found along the forest–savanna border and in the vicinity of small forest streams. During the wet season, these areas became waterlogged due to heavy rains and were typified by small undulations that formed around the roots of larger canopy trees such as Alchornea sp.(Euphorbiaceae), Cariniana sp. (Lecythidaceae), Qualea
Primate Density in Northeastern Bolivia / 201
sp., Sloanea spp., Guatteria spp. (Annonaceae), Maquira sp. (Moraceae), Pourouma spp., Pseudolmedia spp., and Brosimum spp. that reached heights of 35 m. Palms such as Euterpe precatoria and Socratea exorrhiza were common in the subcanopy stratum. 4. Igapo forest was found on either side of the Itenez River. During the wet season (November–March), this forest was flooded, giving rise to a fairly open understory in the dry season. The canopy in this habitat was characterized by Macrolobium acaciifolium, Acosmium nitens (both Leguminosae), Ficus guianensis, Ficus trigona (both Moraceae), Hevea brasiliensis (Euphorbiaceae), and Cochlospermum orinicense (Cochlospermaceae) that reached heights of up to 30 m. The understory included Bactris gasipaes (Palmae), Mouriri apiranga (Melastomataceae), and Salacia elliptica (Hippocrateaceae). 5. Semideciduous forest was a broad habitat classification representing the upland forests of the study site including cerradâo forest. This was the dominant vegetation found on the top of the northern regions of the Huanchaca escarpment as well as on lower surrounding hills. The canopy of this habitat ranged between 10 and 20 m and included species such as Schinopsis sp. (Leguminosae), Jacaranda sp. (Bignoniaceae), Sterculia apetala (Sterculiaceae), and Crepidospermum sp. (Burseraceae). The understory included Talisia esculenta (Sapindaceae), Roupala montana (Proteaceae), and Abuta grandiflora (Menispermaceae). The second field site, Las Gamas (lat. 14°, 48′ S, lon. 60°, 23′ W), was around an abandoned airstrip situated on top of the table-mountain in the southern region of the park and was visited for 5 weeks during March/April 1993. Trails were located in three patches of gallery forest and totaled 10.3 km in length (see Fig. 3). Two of these gallery forest patches, patch A (approximately 41 ha) and patch B (approximately 50 ha), were relatively small, isolated, and surrounded by open grassland and a variety of cerrado scrub vegetation types. The larger third patch, patch C (approximately 1,535 ha), was located on the edge of the escarpment, with one side bordering the lowland forest below. The canopy of this patch often reached 30 m and was characterized by Aspidosperma cf. marcgravianum (Apocynaceae), Erisma uncinatum, and Qualea sp. [Arroyo Padilla, 1995]. Other dominant tree species included Miconia chrysophylla (Melastomataceae), Pseudolmedia cf. rigida, and an unidentified Lauraceae [Arroyo Padilla, 1995]. The understory was typified by Psychotria sp. (Rubiaceae), Cordia nodosa (Boraginaceae), Vitex sp. (Verbenaceae), and Ouratea sp. (Ochnaceae) [Arroyo Padilla, 1995]. Methods Population density estimates were determined using line transect methodology [Burnham et al., 1980; Brockelman & Ali, 1987]. Transects were conducted by one to three observers in fair weather conditions along established trails. At Lago Caiman, 503.5 km of line transect were conducted between 6:00 and 11:15 h and 15:00 and 18:00 h. At Las Gamas, 50.4 km were walked between 6:30 and 12:15 h. Details regarding the location, length, and replication of transect trails and habitats present on each trail are listed in Table I. Although each transect walk did not necessarily total the trail length, efforts were made to sample all sections of the trails evenly. Each transect was independent because at least 2 days passed before a trail was resampled. The rate at which transects were walked ranged between 1 and 3 km/h and depended on trail conditions. Periods of walk-
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Fig. 3.
Vegetation map of the Las Gamas study site and the three sampled gallery forest patches.
ing were regularly interspersed with brief listening stops to increase the probability of detecting cryptic primate groups. The following information was recorded for all primate groups encountered on transect: species, group size (and, where possible, age/sex composition), date and time detected, observation duration, transect position, habitat type, perpendicular distance from the transect trail to the estimated geometric centroid of the group, and vertical position of the group in forest strata. Only “good” observations were used for estimat-
Primate Density in Northeastern Bolivia / 203 TABLE I. Details of Transect Routes, Sampling Effort, and Habitat Types at Lago Caiman and Las Gamas* Trail name Lago Caiman Flor de Oro Paralela Marimono Serrania Lomas La Vista Itenez Total
Number of walks
Trail length
Total distance (km)
25 23 27 24 13 5 13
7.6 7.9 10.5 10 2.9 3.1 4.6
85.36 110.16 116.11 98.18 34.7 13.34 45.65
130
46.6
503.5
Las Gamas Patch A Patch B Patch C
4 4 18
1.02 2.01 7.25
4.08 4.02 42.3
Total
26
10.28
50.4
Habitat types censused Low vine, tall, and sartenejal forests Low vine, tall, and sartenejal forests Low vine, tall, and sartenejal forests Semideciduous and low vine forests Semideciduous forest Semideciduous forest Igapo forest
Gallery forest Gallery forest Gallery forest
*Each transect walk did not necessarily total the trail length; thus, the product of trail length and number of walks does not always equal the total distance censused for each trail.
ing primate group sizes. Good observations were those in which the observer gained a prolonged view of the troop, allowing an accurate count with a reasonable certainty that no additional unobserved individuals were present. The vertical position of each primate troop encountered was classified as in either the upper levels of the forest (emergents, upper and middle canopy), medium levels (subcanopy and understory), or lower levels (shrub layer) or as terrestrial. Additionally, all nontransect incidental observations were noted and appropriate parameters recorded. Transect information was analyzed using the DISTANCE computer program which employs Fourier Series transformations [Laake et al., 1991; Buckland et al., 1993]. The independence of observations on a given transect was maintained by excluding any observation of the same species that occurred within 200 m of an original observation. Due to problems of data heaping, perpendicular distances were grouped for analysis, which provided more accurate fits to the various estimator models used in the DISTANCE analysis. Heaping was largely a result of the difficulty in accurately assessing, in dense forest vegetation, the geometric centroid of an observed primate group. Similarly, as seemed appropriate for each primate species, perpendicular distance data were truncated to remove outliers from the analysis. To determine the proportion of habitat types occurring along the transect trails, a habitat classification, using the habitats described above, was assigned every 100 m along each trail. Due to logistical constraints and the desire to assess specific habitat types, some transect trails were placed within certain habitats and not distributed in a random fashion. Thus, the proportion of habitat occurring along the trails does not necessarily reflect the relative abundance of the Igapo forest and semideciduous forest habitats within the study area. Statistical analysis follows Siegel and Castellan [1988], and significance levels were set at the P < 0.05 level. RESULTS Primate Diversity During the study, the following primate species were registered at Lago Caiman: silvery marmoset (Callithrix argentata melanura), owl monkey (Aotus
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azarae), brown capuchin monkey (Cebus apella), black howler monkey (Alouatta caraya), red howler monkey (Alouatta seniculus), and black spider monkey (Ateles paniscus chamek). Four additional primate species were registered on the Brazilian side of the Itenez River during the course of this study: dusky titi monkey (Callicebus brunneus), bare-eared squirrel monkey (Saimiri ustus), monk saki monkey (Pithecia irrorata), and red-faced bearded saki monkey (Chiropotes albinasus) [Wallace et al., 1996]. At the Las Gamas study site, the following primates were registered: Aotus azarae, Cebus apella, Alouatta caraya, and Ateles paniscus chamek. Habitat Preferences To assess habitat preferences of Cebus apella and Ateles paniscus chamek at Lago Caiman, the only species for which sufficient transect sightings were made for this analysis, we used transect encounter rates for these monkeys and the proportions of the total transect distance in each habitat. We first checked that the perpendicular sighting distances for each species were not significantly different across habitats including the gallery forest at Las Gamas (Kruskal-Wallis; Cebus apella: KW = 5.317, D.F. 4, P > 0.05; Ateles paniscus chamek: KW = 6.567, D.F. 4, P > 0.05). This ensured that over a standard transect distance the area censused in each habitat was similar. The distribution of transect kilometers and primate sightings for each habitat, and the resulting encounter rates, expressed as number of groups/10 km censused, are listed in Table II. Despite slight variations in encounter rates within each habitat type, Cebus apella showed no significant habitat preferences at Lago Caiman (X2 = 5.21, D.F. 4, P > 0.05). In contrast, Ateles paniscus chamek displayed highly significant habitat preferences (X2 = 79.02, D.F. 4, P < 0.001). Spider monkey groups were encountered predominantly in tall forest and to a lesser extent Sartenejal forest but were infrequently observed in semideciduous and low vine forests. Although spider monkeys were not encountered in Igapo forest during censuses, they were sighted incidentally in this habitat on five occasions. There were insufficient transect sightings to test for habitat preferences in the other primate species at Lago Caiman; nevertheless, it is instructive to consider all primate observations, both transect and nontransect. The red howler monkey (Alouatta seniculus) was exclusively encountered (n = 20) in Igapo forest along the Itenez River. Similarly, although Alouatta caraya (n = 9) was observed once in the table-mountain’s semideciduous forest and once in low vine forest on TABLE II. Transect Observations and Encounter Rates of Cebus apella and Ateles paniscus chamek Across Habitats at Lago Caiman* Cebus apella
Ateles paniscus
Habitat type
Trail (km)
Transect (km)
n
ER
n
ER
Tall forest Low vine forest Sartenejal forest Igapo forest Semideciduous forest
11.25 9.2 6.6 4.6 14.95
110.71 160.15 57.57 45.65 129.42
11 16 9 8 9
0.99 1.00 1.56 1.75 0.70
41 6 14 0 5
4.42 0.46 2.49 — 0.45
Overall 46.6 X2 test on habitat preference
503.5
53 1.06 X2 = 5.21, d.f. 4 (P > 0.05)
66 — X2 = 79.02, d.f. 4 (P < .001)
*ER, encounter rate expressed as number of groups encountered per 10 km of trail censused.
Primate Density in Northeastern Bolivia / 205
one of its slopes, seven (77.8%) sightings of this species were in Igapo forest in the Lago Caiman vicinity. These two congeners had sympatric distribution in this region: at Flor de Oro both species frequented Igapo forest on the opposite bank of the Itenez River, and on three occasions groups of each species were observed in close proximity, once in adjacent Ficus sp. trees. For Callithrix argentata melanura, low vine forest appeared to be the most important habitat, accounting for 77.8% of all sightings (n = 9). Incidental nocturnal observations registered Aotus azarae in tall forest and low vine forest at Lago Caiman. Although at Las Gamas only one forest habitat type was surveyed, censuses were conducted in separate patches of gallery forest which differed both in size and geography. In the two smaller and isolated patches (approximately 50 ha), primate groups were never encountered on transects and overall were only observed on three occasions: Alouatta caraya was observed twice in patch B, and Aotus azarae was heard calling once in patch A. In the third and larger patch C (approximately 1,535 ha), which also bordered the lowland forest below the escarpment, Cebus apella was observed once during censuses, with a resulting encounter rate of 0.24 groups/10 km censused, and five times overall. Ateles paniscus chamek was encountered on 15 occasions during censuses, an encounter rate of 3.55 groups/10 km censused, and on 28 occasions overall. Although samples are small, it appears that both these species were absent in the smaller and isolated gallery forest patches. However, if we include the transect kilometers from these patches, resulting encounter rates drop to 0.2 groups/10 km for Cebus apella and 2.98 groups/10 km for Ateles paniscus. Vertical Strata Clear differences in forest strata use existed among the primate species at the study sites. Callithrix argentata melanura (n = 8) was exclusively encountered in the middle levels of the forest. Aotus azarae (n = 9) also showed a preference for this forest stratum, with 77.8% of sightings at this level and the remaining two observations in the upper strata. Cebus apella (n = 114) seems to be much more of a generalist, with 43.9% of sightings in the upper strata and 50% in the middle levels of the forest. Additionally, on six occasions Cebus apella was observed in the shrub layer and once on the ground in semideciduous forest. The two Alouatta species were also found predominantly in the middle and upper levels of the forest, although A. seniculus (n = 20) was once observed drinking from a beach on the Itenez River in the dry season. Spider monkeys (n = 175) clearly preferred emergent trees and upper and middle canopy strata of the forest, with upper levels accounting for 90.9% of sightings and the remaining observations in the middle stratum. Average Group Size The observed mean group size for Callithrix argentata melanura was 6.2 individuals (n = 5, SD ±1.9, range 4–9). Aotus azarae had a mean group size of three individuals (n = 3, SD ±1.7, range 2–5). The two species of howler monkey showed similar mean group sizes: Alouatta caraya at four individuals (n = 3, SD ±2.6, range 1–6) and A. seniculus at 3.3 individuals (n = 18, SD ±2, range 1–7). Cebus apella had the largest mean group size of the primate species examined, with nine individuals (n = 47, SD ±5.7, range 1–25). Ateles paniscus chamek showed highly variable subgroup size, with a mean of 6.2 individuals (n = 96, SD ±5.3, range 1–30). For Ateles paniscus chamek, we also calculated the mean adult/
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subadult subgroup size by eliminating dependent offspring from the analysis. This resulted in a mean adult/subadult subgroup size of 4.5 individuals; thus, juveniles and infants made up approximately 28.4% of the total population in the Lago Caiman vicinity. In addition, for those species with sufficient encounters, we examined variations in mean group size across the recognized habitat types at Lago Caiman and Las Gamas. Cebus apella showed no significant differences in group size between habitats (Kruskal-Wallis; KW = 6.603, D.F. 5, P > 0.05). For Ateles paniscus, however, habitat type had a significant effect on observed subgroup size (Kruskal-Wallis; KW = 12.133, D.F. 4, P< 0.02). In low vine forest, the mean subgroup size for Ateles paniscus was 4.6 individuals (n = 7, SD ±4, range 1–13), in tall forest the mean was 5.8 individuals (n = 55, SD ±4.2, range 1–20), and in gallery forest the mean was 3.6 individuals (n = 16, SD ±2.2, range 1–7). Sartenejal forest displayed the highest mean subgroup size, with 10.7 individuals (n = 12, SD ±8.5, range 2–30), with semideciduous forest approaching this at 7.5 individuals (n = 4, SD ±6.6, range 2–17). Population Density Estimates Population density estimates were possible only for Cebus apella and Ateles paniscus due to insufficient transect sightings for the other primate species within the park. Since the encounter rates for Cebus apella were not significantly different between habitats, we calculated the overall density at the Lago Caiman study site using transect encounters in all habitats. Perpendicular distance data were truncated at 36 m on either side of the transect, which resulted in a total of 53 sightings. Of the various estimator models tested within the DISTANCE program, the uniform cosine model provided the best fit to the data and resulted in an overall density estimate of 14.1 Cebus apella individuals/km2 (confidence limits, 7.8–25.5). Due to significant differences in encounter rates between habitats, an overall population density estimate was not possible for Ateles paniscus. Instead, we estimated the density of spider monkeys for three amalgamated lowland habitat types for which the trails had been randomly placed: low vine forest, Sartenejal forest and tall forest. The perpendicular distance data were truncated at 45 m on either side of the transect, which resulted in a total of 61 sightings. Again the uniform cosine model provided the best fit to the data, resulting in a density estimate of 32.1 Ateles paniscus individuals/km2 of lowland forest (confidence limits, 21.9–47.0). This results in a density estimate for spider monkey adults/ subadults of 23 per km2, calculated by subtracting the proportion of juveniles. DISCUSSION In terms of species number and composition, the primate community within Noel Kempff Mercado National Park is similar to other documented areas in eastern Santa Cruz Department [Braza & Garcia, 1988; Wallace et al., in preparation]. Callithrix was observed infrequently at Lago Caiman (0.1 groups encountered per 10 km censused), as is the case at several nearby locations [Wallace et al., in preparation]. Their apparent preference for lower vine forests and mean group size in this region is comparable to several other studies on congeners [Stevenson & Rylands, 1988]. The Aotus genus is known to occur in a variety of habitats in the Neotropics, and the mean group size of three individuals at Lago Caiman is similar to other reported sites [Robinson et al., 1987].
Primate Density in Northeastern Bolivia / 207
The apparent absence of the two howler monkey species from the majority of the habitats considered is surprising given Alouatta’s well-documented habitat adaptability [Crockett & Eisenberg, 1987] and numerical dominance in several Neotropical primate communities with few species [Emmons, 1984]. Interestingly, sloths also appear scarce and were not observed at either field site. The lack of arboreal folivores within the nonriverine forests may be a feature of the Brazilian Shield, given their absence or scarcity in other nearby areas [Painter et al., in preparation]. Possible explanations for this absence are the floristic composition of these forests and/or poor nutrient background of the soils of this region [PLUS-CORDECRUZ, 1994], which may limit folivory as a dietary niche. Similarly, Alouatta seniculus is reported as widespread in Colombia but rare away from rivers and lake shores [Defler, 1994]. Recently, Peres [1997] demonstrated that distance from a major white water river, forest structure, seasonality, and correlates of soil fertility were useful in predicting the density of howler monkeys in Brazilian Amazonia once hunting pressure had been controlled for and also noted the lack of other arboreal folivores in low density howler monkey sites. The habitat adaptability of Cebus apella is thought to be related to its generalist diet; capuchins opportunistically consume fruit, flowers, leaves, palm nuts, and insects [Terborgh, 1983]. The population density estimate (14.1 individuals/ km2), mean group size, and variability in group size of Cebus apella at Lago Caiman is similar to previous studies [see Robinson & Janson, 1987; Janson, 1988]. Nevertheless, the Lago Caiman density estimate is considerably less than the 38.9 individuals/km2 reported during less extensive surveys in the southern regions of the park [Braza & Garcia, 1988]. For Cebus and Ateles, the size of the two smaller gallery forest patches at Las Gamas may prevent groups of a viable size taking hold [see Lovejoy et al., 1986]. The third patch was considerably larger and floristically different [T. Killeen, personal communication] and bordered the continuous forest below the escarpment, with some areas being forested steep slopes. Seasonal movements between the continuous forest below and the upland gallery forest would be theoretically possible, especially as we have observed Ateles and Alouatta caraya climbing 200 m cliffs in the Lago Caiman vicinity. It is important to underline the brevity of the field work at Las Gamas and the limitations this imposes on data interpretation. Clearly, Ateles was abundant in patch C during the surveys; however, this abundance may be a seasonal phenomenon. The preference for the tall forest and structurally similar Sartenejal habitats displayed by Ateles at Lago Caiman mirrors the results from previous studies in Colombia and Peru [Klein & Klein, 1976; Terborgh, 1983]. In Surinam, van Roosmalen [1985] describes Ateles as preferring high forest with only occasional forays into other forest types when a particularly abundant fruit resource is seasonally available. The overall observed mean subgroup size of 6.2 individuals, or 4.5 adults/subadults, is higher than reported for longer term studies on congeners in Colombia, Guatemala, Surinam, Peru, and Costa Rica [McFarland Symington, 1988a; Chapman, 1990]. In addition, proportions of juveniles/infants reported at three of the above sites are similar to that presented here [van Roosmalen, 1985; McFarland Symington 1988b; Chapman, 1990]. The variability in observed subgroup size and the differences in subgroup size between habitats are as expected considering the well-documented fission–fusion social system of this genus [van Roosmalen, 1985; Chapman, 1990; McFarland Symington 1988c]. The lowland forest density estimate for Ateles at Lago Caiman of 32.1 individuals/km2 is one of the highest reported in the literature [McFarland Symington, 1988a]. The only study which documented a higher density estimate, 84.5 individuals/km2, was conducted in the southern regions of Noel Kempff Mercado Na-
208 / Wallace et al.
tional Park [Braza & Garcia, 1988]. Braza and Garcia [1988] fail to detail the analytical methods used to reach this estimate, but, due to the small number of encounters in the study (n = 11), their estimate should be treated with caution. Regardless, the subgroup encounter rates reported for Lago Caiman (1.86 for the three lowland habitats) and those calculated from Braza and Garcia [1988] (11 encounters in 45 km of transect, giving 2.44 groups/10 km) are similar. Given that this region represents a southern limit for this genus, these encounter rates are perhaps surprising, especially when one considers that in nearby areas encounter rates are appreciably lower than those reported for the park [Wallace et al., in preparation]. McFarland Symington [1988a] assessed several factors which might explain differences in Ateles population densities among four Neotropical sites and suggested that while community effects such as the abundance of arboreal frugivorous competitors and potential predators may be contributory factors, they failed to explain the observed variation. Noel Kempff Mercado National Park holds a full complement of larger predators, with jaguar (Panthera onca), puma (Puma concolor), harpy eagle (Harpia harpyja), and crested eagle (Morphnus guianensis) all present [Killeen, 1996]. Thus, while we have no data regarding the relative abundances of these predators, it seems that a lack of predation is an unlikely explanation for the high Ateles densities within the park. In terms of primate community structure, the Guatemalan and Costa Rican study sites which have high densities of Ateles and low primate diversity [McFarland Symington 1988a, Chapman 1990] appear similar to Lago Caiman. These observations suggest that the number of frugivorous primate competitors present in an area may be inversely correlated with spider monkey densities. However, as McFarland Symington [1988a] noted, the Peruvian site rather contradicts this hypothesis, as it features high spider monkey densities and a rich primate assemblage. Floristic diversity, habitat productivity, and related factors such as the amount and seasonality of rainfall also failed to explain population densities [McFarland Symington, 1988a]. Initially, this may appear surprising, since in general food availability is considered the ultimate limiting factor on primate population density, though other factors, such as access to water, climate, disease, and predation, are certainly important [Dunbar, 1987]. However, as Cant [1980] has argued, this limitation is not a reflection of the overall annual productivity of a habitat, which may far exceed the energetic requirements of the resident primate community [e.g., Coelho et al., 1976]. Rather, populations are constrained by resource density at times of relative food scarcity. These relative resource droughts may be seasonal in nature or products of rarer “ecological crunch” events [cf. Wiens, 1977], such as the lack of fruiting in certain “keystone” resources [cf. Terborgh, 1986], massive forest fruit failures, or severe climatic conditions [Dittus, 1977; Cant, 1980; Foster, 1982; Terborgh, 1986]. The fruit resources which make up the majority of spider monkey diets are relatively scarce compared to other potential primate dietary constituents, ephemeral in nature, and patchily distributed, and they are known to seasonally fluctuate in density [Leigh & Windsor, 1982; Howe, 1984; Richard, 1985]. Given the apparent importance of keystone resources for tropical forest frugivores, we tentatively suggest that the diversity of floristically different habitats available at the Lago Caiman site offers a year-round abundance of fruit resources. Indeed, all semideciduous forest observations of Ateles occurred in a 2 month period (October–November 1992), suggesting a seasonal use of this habitat. This explanation may also account for the larger Ateles subgroup sizes ob-
Primate Density in Northeastern Bolivia / 209
served in less preferred habitats. Preliminary results from a recently completed ecological study of a spider monkey community at Lago Caiman suggest that seasonal use of different habitats is an important feature of spider monkey ecology in this region [Wallace, unpublished data]. This argument would also apply to the Las Gamas site and Braza and Garcia’s [1988] surveys in the south of the park and may go some way in explaining the clear numerical and biomass dominance of Ateles within the primate communities at these sites. CONCLUSIONS 1. Primate diversity and species composition at Noel Kempff Mercado National Park was typical of the northeastern regions of Santa Cruz Department, Bolivia. 2. Callithrix argentata melanura was infrequently encountered at Lago Caiman and preferred low vine forest. Incidental observations registered Aotus azarae in low vine, tall, and gallery forests of the park. 3. The park includes two species of Alouatta which displayed narrow habitat use at Lago Caiman. Alouatta seniculus was exclusively encountered in Igapo forest, where it is sympatric with A. caraya. Alouatta caraya was the only diurnal species encountered in the smaller patches of gallery forest at Las Gamas. 4. At Lago Caiman, Cebus apella showed a generalized use of habitat and vertical strata. The population density estimate for this site was 14.1 individuals/km2. Cebus was infrequently encountered in the larger patch of gallery forest at Las Gamas. 5. The population density estimate of 32.1 individuals/km2 for Ateles paniscus chamek in lowland forest at Lago Caiman is one of the highest reported in the literature. Ateles clearly preferred tall and structurally similar Sartenejal forests and was predominantly encountered in the upper levels of the forest. The encounter rate for Ateles at Las Gamas was also particularly high in the larger patch of gallery forest. 6. The diversity of floristically different habitats is suggested as an explanation for the numerical dominance of Ateles within the primate communities at both field sites. ACKNOWLEDGMENTS The research was funded as part of a grant to A. Taber from the Wildlife Conservation Society (WCS). Considerable logistical support was gratefully received from F.A.N. (Fundación Amigos de la Naturaleza) at the administrative level in Santa Cruz and while in the field from all those resident at Flor de Oro, particularly the park guards. Thanks also go to Robin Foster, who visited the Lago Caiman field site and provided invaluable information regarding the vegetation of the predominant habitat types. John Robinson and four anonymous reviewers provided valuable comments on earlier drafts of the manuscript. Assistance in the field was capably provided by several Bolivian undergraduate students, particularly Jose-Carlos Herrera. REFERENCES Arroyo Padilla, L. Estructura y composición de una isla de bosque y un bosque de galería en el Parque Nacional Noel Kempff Mercado. Graduate thesis, Universidad Autónoma Gabriel Rene Moreno, Santa Cruz, 1995.
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