Primates of the Río Curaray,Northern Peruvian Amazon

We conducted a short survey of primates along the Río Curaray in the northern Peruvian Amazon, emphazing rare, threatened or little known species. Contrary to Thorington, (Thorington, R. W., Jr., 1988, Am. J. Primatol. 15:367–371), we found no evidence for sympatry between Saguinus tripartitus and Saguinus fuscicollis, with the former being restricted to the north bank and the latter to the south bank of the Río Curaray. The Curaray also separates two species of Pithecia. The height above ground at which species were encountered increased with body size, providing evidence for vertical stratification within the primate community. The Curaray area still has rich primate diversity compared to other areas in the northern Peruvian Amazon, even though larger species, such as the spider monkeys, are hunted.     

Vigilance in Single- and Mixed-Species Groups of Tamarins (Saguinus labiatus and Saguinus fuscicollis)

By forming larger sizes of groups, individuals benefit from a decrease in vigilance, but the collective vigilance of the group as a whole is not compromised. We examined whether this group size effect is apparent in mixed-species groups of red-bellied tamarins (S. labiatus) and saddleback tamarins (S. fuscicollis) which form stable and permanent associations in the wild. We studied general vigilance and responses to hidden threatening stimuli in five captive groups of each species, while they were housed in single- and mixed-species groups. For vigilance, the individual rate was lower in the larger mixed-species groups than in the smaller single-species groups. In addition, the amount of time when at least one individual was vigilant was higher in mixed-species groups. This suggests that the tamarins alter their vigilance behavior in the presence of the other species. In response to hidden threats, both species performed brief vigilance checks and frequencies of checking did not differ in single- and mixed-species groups. However, both species had a significant reduction in the mean duration per check, and there was a reduced total amount of time spent vigilance checking in the mixed-species groups compared to the single-species groups, demonstrating the group size effect. Overall the mixed-species groups had a higher number and mean duration of checking than the smaller single-species groups. Given that the two species share a common set of predators, and respond to each other's alarm calls, these findings provide strong evidence that individuals of both tamarin species may be able to benefit from forming mixed-species groups via improved vigilance and monitoring of threats.     

Composition and Nutritional Characteristics of Fungi Consumed by Callimico goeldii in Pando, Bolivia

Though ≥22 species of Primates consume fungi, most do so at low rates, comprising <5% of their feeding time. Goeldi's monkeys (Callimico goeldii), spend up to 29% of their feeding time year-round consuming fungal sporocarps, the fruiting bodies of fungi. We provide comprehensive data on the nutritional characteristics of 4 species of fungi consumed by Callimico goeldii (Ascopolyporus polyporoides, Ascopolyporus polychrous, Auricularia auricula, and Auricularia delicata). The composition of the fungi is similar to that of other fungi: predominantly fiber (66.2–83.0% dry matter) with small amounts of sugar (2.0–5.6% dry matter) and crude fat (0.9–1.6% dry matter). Though the crude protein content is substantial (5.5–13.4% dry matter), much of the nitrogen in the fungi is not likely to be available to Callimico goeldii because it is associated with indigestible food components or is in nonprotein form. The mineral content of the fungi are within the normal range for fungi generally and the calcium-to-phosphorus ratio is low (0.07–0.25). Fungi appear to be a low-quality food resource for Callimico goeldii and may contribute to their relatively large home ranges and low population density compared to other Callitrichinae. Research on the ability of Callimico goeldii to digest fungi is needed to understand fully the nutritional value of fungi to them. We discuss adaptations Callimico goeldii may have for improving their ability to obtain nutrients from fungi and potential ecological correlates of mycophagy.     

Distribution and density of Callimico goeldii in the Department of Pando, Bolivia

A survey of the distribution and density of Callimico goeldii was conducted at five sites across northwestern Bolivia, in the Department of Pando. C. goeldii was found at two sites north of the Manuripi River, with high densities at one site located along the Acre River. Estimates of habitat availability at these sites suggest that C. goeldii reaches high densities in areas with low human density and well established and extensive bamboo forests. These results, when reviewed with those of prior studies, indicate that the patchy distribution of C. goeldii in Pando is a result of both riverine barriers and the availability of bamboo habitat.     

Associations Between Golden-Headed Lion Tamarins and the Bird Community in the Atlantic Forest of Southern Bahia

We examined the presence of birds accompanying and foraging in proximity to golden-headed lion tamarins at Una Biological Reserve, Bahia, Brazil. We followed 3 groups of golden-headed lion tamarins over 3 yr. We noted all birds ≤5 m of a lion tamarin during 20-min observation periods. We found 11 different bird species in the presence of the lion tamarins. We most often found insectivores, such as woodcreepers and nunbirds, in association with them, eating prey the tamarins flushed. Associations were most frequent in mature and shade-cocoa forests. The group that spent most of its time in mature and shade-cocoa forest was also the group that foraging birds followed most frequently. Differences in resource availability among forest types, such as the abundance of microforaging environments, may affect the frequency and diversity of birds seen in association with golden-headed lion tamarins.     

Dietary Differences Among Sympatric Callitrichinae in Northern Bolivia: Callimico goeldii,Saguinus fuscicollis and S. labiatus

Studies of sympatric species can provide important data to define how dietary and habitat requirements differ among them. I collected dietary data during a first yearlong comparative study of wild groups of Callimico goeldii, Saguinus labiatus and S. fuscicollis. Dietary overlap was highest between Saguinus fuscicollis and Saguinus labiatus throughout the year, and lowest between Saguinus labiatus and Callimico goeldii. All three species had high dietary overlap in February and March when a few abundant fruit species dominated their diets. Although all three species rely heavily on many of the same fruits and arthropods, there are several important distinctions among their diets. Surprisingly, Callimico goeldii consume large quantities of fungus throughout the year: 29% of annual feeding records. Mycophagy is more frequent in the dry season when fruits are scarce. In contrast, Saguinus labiatus rarely eat fungus during the period of fruit scarcity, and instead rely on nectar, a resource never exploited by Callimico goeldii. Saguinus fuscicollis also rely on nectar during periods of low fruit availability and increase their intake of arthropods and exudates. During April, a period of fruit scarcity, exudates comprise >50% of the feeding records of Saguinus fuscicollis. The use of different food resources during fruit scarcity, and differences in the heights at which each species feeds and forages appear to define a distinct ecological niche for each of them and allow them to maintain long-term associations throughout the year. Furthermore, I hypothesize that the limited distribution of Callimico goeldii may result from their restriction to forests that have high disturbance rates, where microhabitats appropriate for fungal growth are abundant, but which also contain abundant fruit and insects.     

Craniometric sexual dimorphism inLeontopithecus Lesson, 1840 (Callitrichidae, Primates)

Lion tamarins are among the World's most critically endangered primates. Many studies have been produced under guidance of the International Management Committees for the preservation and management of these tamarins. Primates present morphological sexual differences in a wide range of characteristics, including cranial morphology. Studies of sexual dimorphism in the cranial morphology of theLeontopithecus are few in number and contradictory in their results. In order to check for the existence of sexual dimorphism in lion tamarins the present study analyzed 17 craniometric distances on 56 crania of three species of lion tamarins (Leontopithecus): 20L. rosalia (14 females and 6 males); 13L. chrysomelas (6 females and 7 males); and 23L. chrysopygus (8 females and 15 males). All crania are housed in the CPRJ-FEEMA collection (Primatological Center of Rio de Janeiro) and came from animals born in captivity.L. chrysopygus was more sexually dimorphic (10/17 measurements, 59%) thanL. chrysomelas (9/17 measurements, 53%) orL. rosalia (7/17 measurements, 41%). In all three species, male values are greater than the female ones, except for orbital breadth (m7) inL. rosalia. However, this distance is not sexually dimorphic in this species. This study reveals that some cranial distances, especially in the facial region, are sexually dimorphic in lion tamarins.     

A field study on the red-bellied tamarin,Saguinus l. labiatus,in Bolivia

A 5-month field study was conducted on red-bellied tamarins,Saguinus labiatus labiatus, in the Pando Department of northern Bolivia. Group sizes ranged from 5 to 10 animals, and each group associated with a group of saddle-backed tamarins,Saguinus fuscicollis weddelli. Members of three groups were trapped and marked and data were collected by radiolocation. The average range size used over 10 days was 19 ha. On average the groups entered about 29% of their range each day and had a mean daily path length of about 1487 m. The groups used a number of different sleeping sites within their ranges. They fed on a variety of different fruits and also on nectar from flowers, resin, and insects. Areas within the home range which were used significantly more than expected were generally those in which one or more of the following existed: a sleeping site, an intergroup encounter site, or a site where the group took shelter during an extended period of heavy rain.     

A New Subspecies of <Emphasis Type="Italic">Saguinus fuscicollis</Emphasis> (Primates,Callitrichidae)

Saddleback tamarins (Saguinus fuscicollis, S. melanoleucus, and S. tripartitus) occur in the upper Amazon, west of the rios Madeira and Mamoré–Guaporé to the Andes. They currently comprise 13 species and subspecies in Bolivia, Brazil, Colombia, Ecuador, and Peru. Here we report on a previously undescribed subspecies of Saguinus fuscicollis from the interfluvium of the lower rios Madeira and Purus in the central Amazon of Brazil. It is a distinct form with a very pronounced mottling on the back giving the appearance of a saddle, a characteristic shared by the 3 species, and the reason for their collective common name. The lack of a white superciliary chevron and its highly mottled ochraceous-dark brown to black saddle that extends from the scapular region to the base of the tail distinguish the new taxon from Saguinus fuscicollis weddelli. The latter characteristic also distinguishes it from another saddleback tamarin (Saguinus fuscicollis ssp.) that has been reported immediately to the south of its range in the same interfluvium. We compare pelage coloration, external characters and craniometric measurements with its geographically closest relatives, Saguinus fuscicollis weddelli and S. f. avilapiresi, and indicate its probable geographic distribution in a small area between the rios Madeira and Purus, just south of the Rio Amazonas.     

Census,habitat preference,and polyspecific associations of six monkeys in the Lomako Forest,Zaire

This paper reports preliminary data on a number of poorly known cercopithecids inhabiting the Lomako Forest, Zaire. Data include those on density, biomass, group size, the relationship between group type (mono vs. polyspecific) and forest type (mixed primary, secondary, monodominant primary, and swamp), and vertical stratification. Species examined are Colobus angolensis, Cercocebus aterrimus, Cercopithecus wolfi, Cercopithecus ascanius, Cercopithecus neglectus, and Allenopithecus nigroviridis. The density and biomass for the Lomako Forest anthropoids (excluding Cercopithecus neglectus and A. nigroviridis) are 165 ind/km² and 1,034 kg/km², respectively. Cercopithecus wolfi and Colobus angolensis are found in group sizes similar to those reported from other sites while Cercopithecus ascanius, Cercocebus aterrimus, and A. nigroviridis display group sizes unique to the Lomako. While Colobus angolensis, Cercocebus aterrimus, Cercopithecus ascanius and Cercopithecus wolfi were found, to varying extents, in all four forest types, Cercopithecus neglectus and A. nigroviridis inhabited only swamp forest. The different species sort out along vertical continua both within and between the four forest types. © 1994 Wiley-Liss, Inc.     

Responses of Captive Single- and Mixed-Species Groups of Saguinus to Novel Nonthreatening Objects

The provision of novel objects allows one to probe for behavioural differences among species. This is particularly relevant when studying species that form mixed-species groups, as divergent responses may provide clues to the advantages that individuals gain from associating. We compared the responsiveness to novel objects in captive single- and mixed-species groups of saddleback (Saguinus fuscicollis) and red-bellied (Saguinus labiatus) tamarins to determine the influence of a congener. We tested groups with novel objects placed near the top, the middle, and on the floor of their enclosures and measured latency to approach and touch them. We tested predictions related to differences in lifestyle patterns under natural conditions. As we predicted, S.labiatus, which usually occur at a higher mean height in the forest than their congeners, responded to objects placed near the top of the enclosure significantly quicker in both single- and mixed-species groups. S. fuscicollis responded to objects placed on the floor quicker, and in mixed-species groups S. fuscicollis approached them before S. labiatus did. There were specific differences in median touch–approach time (T-A): Saguinus fuscicollis had a shorter T-A time than that of S. labiatus, which can be related to their manipulative foraging style. Reaction times decreased in mixed-species trials for both species, suggesting that the reaction of one species may effect the congener. Both species may benefit through association, though the dominance of Saguinus labiatus over S. fuscicollis may limit the advantages to S. fuscicollis. Over all our study supports the idea that cross-specific social facilitation is an important consequence of mixed-species groups of Saguinus.     

Population Sizes and Distribution of Primates in the Lower Tana River Forests,Kenya

We studied the population size and distribution of diurnal primates in the lower Tana River forests, Kenya. They are the only remaining habitats for 2 threatened primates: the Tana River red colobus (Procolobus rufomitratus) and the Tana River crested mangabey (Cercocebus galeritus galeritus). We conducted censuses in 73 forest patches from January through March 2001. We estimate population size of the red colobus to be 788 individuals in 82 groups and that of the crested mangabeys to be 2,070 individuals in 59 groups. The data suggest that over a 7-year period (1994-2001), there was an 18% increase in the crested mangabey population and a 5% decline in red colobus numbers. Further, the red colobus range has expanded both north and south, whereas that of crested mangabeys has only expanded south. Fifty-six percent of crested mangabeys and 46% of red colobus groups were inside the Tana River Primate National Reserve (TRPNR). Other primates encountered included 170 groups of Sykes' monkeys (Cercopithecus mitis), 70 groups of yellow baboons (Papio cynocephalus) and 4 groups of grivets [Chlorocebus (Cercopithecus) aethiops]. Mean group densities of the 2 endangered primates and of baboons were higher inside than outside the TRPNR, reinforcing the importance of TRPNR for their conservation. An intervention program is required to stem further decline in the red colobus population and to protect small isolated groups in forest patches outside TRPNR.     

Contributions to infant care in captive cotton-top tamarins (Saguinus oedipus): The influence of age,sex, and reproductive status

Marmosets and tamarins are characterized by a reproductive strategy that includes twinning, and a communal rearing system in which infant care is shared among all group members, both breeders and nonbreeding helpers (often older offspring). In order to test some predictions about the extent to which different age-sex classes should invest in infants, contributions to infant carrying and food-sharing by all family members were measured in captive groups of cotton-top tamarins (Saquinus oedipus) ranging in size from 2 to 12 independent individuals. Fourteen litters were observed from birth to 12 weeks. Carrying by mothers decreased steadily over the study period, while carrying by fathers and other offspring increased for 3–5 weeks, then declined. Infants spent more time carried by siblings than by either parent, but parents did more carrying than individual siblings and, also, shared more food with infants. Older siblings contributed more care than younger siblings did. Adult sons carried infants more than adult daughters did, but immature daughters carried more than immature sons did. However, adult daughters actively offered food to infants more than any other class of helper did. These results were interpreted in the light of hypotheses concerning the reproductive and dispersal strategies of callitrichid species.     

A primate survey in northern Bolivia,with special reference to Goeldi’s monkey,Callimico goeldii

We conducted a 5-month survey on primates, with special attention to Goeldi’s monkey (Callimico goeldii),in the rainforest of northwestern Bolivia. Goeldi’s monkey is one of the least documented of all South American primates, and very little is known about its distribution. We report observations on distribution, abundance, and habitat of Callimico goeldiiand other primates, incidental sightings of other mammals, and preliminary behavioral observations on Callimicoand on two associated callitrichid monkey species: Saguinus fuscicollisand S. labiatus.We found a locality that appears to be particularly suitable for detailed field observations on Callimico on the north bank of the lower Río Tahuamanu. The fieldwork was carried out by A.C.; the analysis of the vocalizations, by T. G.     

Habitat Utilization of Three Sympatric Cheirogaleid Lemur Species in a Littoral Rain Forest of Southeastern Madagascar

I compared the habitat utilization in 3 sympatric species of Cheirogaleidae (Microcebus murinus [81 g], Cheirogaleus medius [183 g] and Cheirogaleus major [362 g]) in a littoral rain forest in southeastern Madagascar during 3 rainy seasons. Females of promiscuous Microcebus murinus had small home ranges and the males had large overlapping home ranges. Home ranges of family groups of monogamous Cheirogaleus medius and C. major overlapped extensively. Home ranges of all 3 species overlapped completely in the study area but home range sizes differed among species and correlate positively with body masses. Male Microcebus murinus slept in open vegetation (79%) and alone (71%), whereas female M. murinus and family group members of Cheirogaleus spp. preferred communal sleeping in tree holes. There are significant interspecific differences in the choice of sleeping sites: smaller lemurs chose smaller trees and used more sleeping sites than larger lemurs did. Species also differed significantly in the vertical dimension of forest utilization: Cheirogaleus major used the upper part of the trees, C. medius used the middle parts, and Microcebus murinus used the understory during nocturnal activities. The 3 species differed mainly in vertical habitat utilization and showed vertical stratification.     

A new species of Mesopropithecus (Primates, Palaeopropithecidae) from Northern Madagascar

We diagnose new subfossil specimens belonging to the extinct palaeopropithecid, Mesopropithecus,from several caves at the Ankarana massif in northern Madagascar. They include three partial crania with mandibles, and the first vertebrae, ribs, clavicle, pelvis, ulna, and hand and foot bones of Mesopropithecusever found. Several other postcranial elements are known for this northern variant of Mesopropithecusand for previously described species from central and southern Madagascar. The new materials cannot be accommodated in either currently recognized species of this genus and are,hereby, given the name Mesopropithecus dolichobrachion. M. dolichobrachionis the second new species of extinct subfossil lemur to be found in the caves of Ankarana. It is unlike the two previously described species of this genus primarily in its larger size, different limb proportions, and aspects of its long bone morphology. Most notable is the fact that this is the only species of Mesopropithecuswith the forelimb longer than the hind limb— hence the name, the “long-armed” Mesopropithecus.Various characteristics place M. dolichobrachionphenetically closest (of species belonging to Mesopropithecus)to Babakotia radofilai, Archaeoindris,and Palaeopropithecus.If these similarities are derived specializations rather than primitive for palaeopropithecids, a new generic name will be required.     

Forest use and activity patterns of Callimico goeldii in comparison to two sympatric tamarins, Saguinus fuscicollis and Saguinus labiatus

Callimico goeldii, Saguinus fuscicollis, and S. labiatus are sympatric in northern Bolivia and differ from each other in patterns of spatial and structural use of their environment. C. goeldii has a home range five times larger than that of mixed-species troops of S. fuscicollis and S. labiatus. The larger overlapping home range of C. goeldii allows it to move among Saguinus troops, giving it access to a wide range of different microhabitats. All three species use the most common microhabitat in the area, primary forest with dense understory, more than any other microhabitat type. C. goeldii habitat use varies by season, with bamboo and Heliconia microhabitats used more during the dry season. Each species shows preferences for different height classes: C. goeldii is found almost exclusively in the understory, S. fuscicollis uses the understory and middle canopy, and S. labiatus is found mostly in the middle canopy. These height class preferences are reflected in each species' locomotor styles, with C. goeldii showing the highest rates of vertical clinging and leaping, and S. labiatus showing the highest rates of branch-to-branch leaping and quadrupedal movement. The results suggest that C. goeldii may be restricted to forests with dense understory and a mosaic of other microhabitats. Furthermore, C. goeldii does not appear to use its tegulae for large branch foraging, but rather for vertical clinging and leaping between small vertical supports.     

Coping with Forest Fragmentation: The Primates of Kibale National Park,Uganda

A goal of conservation biology is to determine which types of species are most susceptible to habitat disturbance and which types of disturbed habitats can support particular species. We studied 20 forest fragments outside of Kibale National Park, Uganda, to address this question. At each patch, we determined the presence of primate species, tree species composition, patch size, and distance to nearest patch. We collected demographic, behavioral, and dietary data for Abyssinian black-and-white colobus (Colobus guereza). Black-and-white colobus and red-tailed guenons (Cercopithecus ascanius) were in almost all fragments; Pennant's red colobus (Procolobus pennantii) and chimpanzees (Pan troglodytes) were in some fragments; and blue monkeys (Cercopithecus mitis) and gray-cheeked mangabeys (Lophocebus albigena) were absent from all fragments. No species characteristics—home range, body size, group size, or degree of frugivory—predicted the ability of species to live in patches. No characteristics of patches—area, distance to the nearest patch, distance to Kibale, or number of food trees present—predicted the presence of a particular species in a patch, but distance to Kibale may have influenced presence of red colobus. Black-and-white colobus group size was significantly smaller in the forest patches than in the continuous forest of Kibale. For a group of black-and-white colobus in one patch, food plant species and home range size were very different from those of a group within Kibale. However, their activity budget and plant parts eaten were quite similar to those of the Kibale group. The lack of strong predictive variables as well as differences between other studies of fragmentation and ours caution against making generalizations about primate responses to fragmentation.     

Densities of Two Frugivorous Primates with Respect to Forest and Fragment Tree Species Composition and Fruit Availability

Conservation of wildlife populations requires extensive knowledge of their habitat requirements, efficient methods to evaluate habitat quality, and an understanding of the value of fragments and edges. Kibale National Park, Uganda has areas that differ in the densities of 2 species of frugivorous monkeys—Cercopithecus mitis and Lophocebus albigena—including one on an edge and forest fragments outside the park that lack both species. We compared the basal area densities of important food trees with primate densities. The density of Cercopithecus mitis correlates most strongly with the basal area density of all types of food trees combined. The density of Lophocebus albigena does not correlate with the basal area densities of any category of food trees or with fruit availability. An index of their density—number of groups seen per km walked—correlates to fruit availability but with marginal significance. Lack of a relationship between the basal area densities of food trees and density of Lophocebus albigena may be the result of a mismatch in scale between the forest area measured and their large home ranges. We compared the unused area of forest to the other areas of the forest and the fragments and found it had higher basal area densities in all food tree categories for both species than the fragments and lower basal area densities of most categories than the other parts of the forest, indicating that the fragments are poor quality and would probably be unused even if dispersal were likely.     

Reactions of wild tamarins,Saguinus mystax andSaguinus fuscicollis to avian predators

During a field study in northeastern Peru, the reactions of a group ofSaguinus mystax on Padre Isla and of a mixed-species troop ofS. mystax andSaguinus fuscicollis at the Río Blanco to raptorial and other birds were observed. Alarms that are specific to flying stimuli were elicited by birds of prey, but other birds that do not represent a threat to the tamarins also caused alarm calls. Alarm events (i.e., instances when one or more alarm calls were given) were observed at rates of 0.3/hr (Padre Isla) and 0.5/hr (Río Blanco). Rates of alarm events significantly increased after the birth of an infant in the Padre Isla group and after the attack of an ornate hawk-eagle (Spizaetus ornatus) on the Río Blanco group. Reactions to alarming stimuli/alarm calls ranged from looking up to falling down from trees. The modification of the tamarins' behavior by the potential presence of aerial predators indicates that raptors represent an important predatory threat to tamarins.