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.     

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 Use and Ranging Behavior of <Emphasis Type="Italic">Callimico goeldii</Emphasis>

We studied the diet, habitat use, and ranging behavior of 1 group of Callimico goeldii (callimicos) over 12 mo in northwestern Bolivia. The group’s diet was comprised of fungi (39%), fruits (31%), arthropods (14%), exudates (14%), and other matter (2%). Callimicos concentrated their ranging activities in secondary forest (50%), primary forest with dense understory (30%), and bamboo (17%) habitats. The group’s total home range was 114 ha; on average they used 38.4 ha/ mo and had a day range of 925 m. Monthly average day ranges—but not monthly home ranges—increased as frugivory declined, suggesting that subjects foraged on fungi and exudates by rechecking resources within a core area, making their day ranges longer than during months when they concentrated on fruit resources. The callimicos formed polyspecific associations with tamarins (Saguinus labiatus and S. fuscicollis) during 81% of observations. Day ranges increased in months with higher association rates which appears to result from the callimicos using a broader set of habitats when with tamarins than when alone. The ranging pattern of callimicos appears to be influenced primarily by 3 factors: their seasonal shift in diet requires that they forage in a variety of habitats across the year; their depletion of resources causes them to shift their core area over time; and their lack of territorial behavior eliminates the need to patrol boundaries as part of their daily movement. As a result, callimicos differ from many other callitrichids in their low ratio of day range length to home range size.     

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.     

Habitat Exploitation by Free-ranging Saguinus niger in Eastern Amazonia

We monitored the foraging behavior of the members of a group of black-handed tamarins (Saguinus niger) at a site in eastern Amazonia. Their diet was frugivorous-insectivorous, but also included pod exudate of Parkia pendula. The focal group used all 3 types of forest—primary, logged, and secondary— in all months, but differentially between seasons. In the dry season, tamarins spent more than half of activity time in primary forest and less than a third in secondary forest whereas during the wet season, the proportions were reversed. Data on resource abundance indicated that the shift in habitat preference is related to a seasonal change in the distribution of fruit sources, with a larger number of species and individuals fruiting during the wet season. We recorded no such variation in the abundance of arthropods. While using a larger area, including more secondary forest, during the wet season, the group traveled significantly shorter distances each day, reflecting the availability of a larger number of fruit sources. Overall, the results reemphasize the ecological and behavioral flexibility of Saguinus niger and their ability to cope with habitat disturbance.     

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.     

Comparative studies on vertical separation,foraging behavior and traveling mode of saddle-backed tamarins (Saguinus fuscicollis) and red-chested moustached tamarins (Saguinus labiatus) in Northern Bolivia

The author made comparative studies on the ecology of saddle-backed tamarins (Saguinus fuscicollis) and red-chested moustached tamarins (S. labiatus) on the upper Amazon in northern Bolivia. The unit group of both species of monkeys was a family group composed of two to seven individuals, but they often formed polyspecific associations comprising one such family group each. However, both species preferred different layers of forest for foraging insects and traveling.S. fuscicollis mainly utilized the lower layer of the forest and foraged large-sized insects lurking in tree hollows, whereasS. labiatus mainly utilized the middle layer of the forest and foraged small-sized animals on branches. These differences were more clearly noticeable in secondary forest than in primary forest.     

Tamarin polyspecific associations: Forest utilization and stability of mixed-species groups

Niche separation is likely to play a key role in the formation of mixed-species groups. Saddle-backed tamarins (Saguinus fuscicollis) were studied at three sites with different primate communities in northern Bolivia: (1) with red-bellied tamarins,S. labiatus; (2) with emperor tamarins,S. imperator; and (3) without a congeneric species. The degree of association is higher betweenS. labiatus andS. fuscicollis than betweenS. imperator andS. fuscicollis and is related to differences in forest utilization between associating pairs. Niche separation is found to be greater betweenS. labiatus andS. fuscicollis than betweenS. fuscicollis andS. imperator. The mean height and habitat utilization ofS. fuscicollis does not differ greatly across the three sites, nor does the height of tamarins in and out of association. It is concluded that combined with differences in body size and dietary overlap, vertical segregation plays an important role in tamarin polyspecific associations (increasing the potential of both foraging and anti-predatory benefits) and that this is not a consequence of vertical displacement ofS. fuscicollis by its dominant congeners.     

Benefits of polyspecific associations for the Goeldi's monkey (Callimico goeldii).

Polyspecific associations are an important component of Callimico goeldii behavior and ecology. On average, Callimico goeldii was found in proximity to or in vocal contact with Saguinus troops (S. fuscicollis and S. labiatus) during 53% of all time intervals sampled. Polyspecific associations varied considerably between seasons, however, with association rates peaking during the wet-season month of February (89%) and declining in the dry season, with the lowest rate (13%) in July. The primary benefits of associations appear to be an increased use of the lower and middle canopy, and an increase in feeding behaviors during the wet season. Thus, Callimico goeldii appear to benefit most from associations during the wet season when fruits are its principal food source. Fruits are eaten more in the forest canopy than in the understory; thus, an increase in height use likely permits an increase in the fruit resources on which Callimico goeldii can forage and feed. In addition, Saguinus groups, with their smaller home ranges, are likely to be more knowledgeable than Callimico goeldii about the location and abundance of ripe fruits in their home ranges. Thus, Callimico goeldii may parasitize Saguinus for their fruit knowledge by following them through their ranges. In the dry season, limited dietary overlap between Callimico goeldii and Saguinus groups is likely to make associations less beneficial for Callimico goeldii as they adopt different foraging and ranging strategies.     

Foraging behavior of a tamarin group (Saguinus fuscicollis weddelli) and interactions with marmosets (Callithrix emiliae)

We present data on aspects of the behavioral ecology of a free- ranging group of Saguinus fuscicollis weddelliat a site in Brazilian Amazonia where a second callitrichid, Callithrix emiliae,is syntopic. Diet, activity patterns, and ranging behavior are broadly similar to those of S. fuscicollisfrom sites in Bolivia, Brazil, and Perú, though significant seasonal changes include an extreme and atypical form of ranging behavior in which they foraged in central-place fashion around a source of exudate—Parkia pendula. S. f. weddelliwas active at relatively low levels in the forest both in absolute terms and relative to C.emiliae, which appears to be an important factor in their niche partitioning. Association between the two species appeared to be less systematic overall than those observed between S. fuscicollisand congeners at other sites, though this may be partly a result of observation conditions. During the period of central-place foraging, the two species exhibited a high degree of association. Other characteristics of the behavior of S. f. weddelliat the study site include the frequent use of tree holes as sleeping sites.     

A comparative study of positional behavior in three species of tamarin monkeys

Tamarins of the genusSaguinus are small-bodied New World monkeys that exhibit clawlike or modified nails. Patterns of positional behavior and habitat utilization are presented for three species,Saguinus fuscicollis, S. geoffroy, andS. mystax. These data were collected on free-ranging tamarin populations in Panama and Peru. Despite considerable differences in body weight, all three species exhibited very similar patterns of positional behavior, with quadrupedal bounding and running accounting for 43 – 52% of travel time. Leaping was the second most common locomotor activity and accounted for 31 – 41% of travel. Although each species leaped principally on small supports in the perimeter of the tree crown, approximately 20% of all leaps inS. fuscicollis involved moderate to large sized vertical trunks located in the undercanopy. Leaping between trunks was rare in the two larger tamarin species. Measurements taken on live wild-trapped adults reveal that compared toSaguinus geoffroyi andS. mystax, S. fuscicollis is characterized by a long legspan and an especially long armspan. It is proposed that inS. fuscicollis, elongated forelimbs play an important role in maneuvering and rotating the body during the in-air phase of trunk-to-trunk leaping, and increase the breaking distance needed to decelerate the body upon impact. Additional relationships between body size, substrate preference, and positional behavior in callitrichines are discussed.     

Role of spatial memory in primate foraging patterns: Saguinus mystax and Saguinus fuscicollis

From field data collected in the Amazon Basin of northeastern Peru, I present evidence that moustached (Saguinus mystax) and saddle-back (Saguinus fuscicollis) tamarins maintain detailed knowledge of the distribution and location of many tree species in their home range. During the wet season months of October through December 1984, fruits and exudates from 20 tree species and over 150 individual trees accounted for 75% of plant feeding time. These trees exhibited a patchy distribution; mean nearest-neighbor distances between trees of the same species averaged 148 meters. Moustached and saddle-back tamarins visited an average of 13 trees per day, concentrating their feeding efforts on 4–11 individual trees from a small number of target species. In 70% of all cases the nearest tree of a given species was selected as the next feeding site. Movement between these sites was characterized by relatively straight-line travel. It is argued that S. mystax and S. fuscicollis offset the patchiness component of the fruit and exudate part of their diet through goal-directed foraging and an ability to compare accurately the distances and directions from their present location to a large number of potential feeding trees.     

Effect of Resting Patterns of Tamarins (<Emphasis Type="BoldItalic">Saguinus fuscicollis</Emphasis> and <Emphasis Type="BoldItalic">Saguinus mystax</Emphasis>) on the Spatial Distribution of Seeds and Seedling Recruitment

The spatial distributions of dispersed seeds have important evolutionary consequences for plants. Repeated defecations in sites frequently used by seed dispersers can result in high seed concentrations. We observed the resting behavior of a mixed-species group of tamarins in Peru and recorded the occurrence of seed dispersal (over 8 mo) and seed fate (over 11–22 mo) to determine whether the location and use of resting sites influenced the spatial distribution of dispersed seeds and seedlings. The tamarins rested mostly on trees (Saguinus fuscicollis: 60.6%, S. mystax: 89.2%) and dead trunks (S. fuscicollis: 24.4%) and used 61% of their resting sites repeatedly. During both the dry and wet seasons, tamarins dispersed significantly more seeds within resting areas (0.00662 and 0.00424 seeds/m², respectively) than outside them (0.00141 and 0.00181 seeds/m²). Seed survival and seedling recruitment did not differ significantly between resting and other areas, resulting in a higher seedling concentration around the resting sites. Seed density did not increase with the duration or the frequency of use of the resting sites but did increase when we pooled the seasonal resting sites together in 50 m × 50 m quadrats, ultimately causing a clumped distribution of dispersed seeds. The use of resting sites in secondary forest, particularly during the dry season, allows the creation of seedling recruitment centers for species coming from the primary forest. Our findings show that tamarin resting behavior affects the spatial distribution of dispersed seeds and seedlings, and their resting sites play an important role in plant diversity maintenance and facilitate forest regeneration in degraded areas.     

Distribution and Forest Utilization of Saguinus and Other Primates of the Pando Department, Northern Bolivia

We carried out a 4-month census of primates in the Pando Department of northern Bolivia with special emphasis on Saguinus species. Contrary to a previous report by Izawa and Bejarano (1981), there was no evidence for the presence of the two populations of Saguinus mystax that they reported, or that Lagothrix occurs in the Pando. In addition, we found the distribution of Saguinus imperator to be more restricted than they suggested. We confirm the presence of Cebuella south of the Río Tahuamanu (cf. Brown and Rumiz, 1986) and report two new locations for Callimico goeldii. We present data on group sizes, habitat utilization, and locomotor behavior of the primates and compare them with previous studies in the Pando. Differences in body size, diet, foraging techniques, and vertical use of the forest appear to be key factors in both sympatry and in the formation of polyspecific associations.     

Seasonal influence on reproduction in chimpanzees of gombe national park

Although wild chimpanzees are not seasonal breeders, there are seasonal effects on several aspects of chimpanzee reproduction. I examined the seasonal incidence of anogenital swelling in cyclic, pregnant, and acyclic female chimpanzees in Gombe National Park, May 1975–April 1992, and surveyed important reproductive events to determine whether there is a seasonal effect. I analyzed data by season (wet vs. dry) and seasonal quarter;early dry season = May–July;late dry = August–October;early wet = November–January;late wet = February–April. When data for the 17 years are combined, the percentage of females in each reproductive state remains consistent throughout the year. In a given month, 30–35% of subjects were in the cyclic category, 11–15% were pregnant, and 54–61% were acyclic. Cyclic females showed full swelling more often during the late dry season. Pregnant females exhibited anogenital swelling more often during the late dry and early wet seasons. Acyclic females also exhibited a seasonal effect with more anogenital swelling during the late dry season. There is no seasonal difference in frequency of live births (dry, 20;wet, 23). However, the timing of conception showed a seasonal effect (dry, 32;wet, 16). Consistent with earlier reports, the onset of postpartum cycles is highly seasonal;30 occurred during dry season, 9 during wet season. The occurrence of first full swellings for young females is also concentrated in the late dry season. It appears that the dry season is a time of great change for Gombe chimpanzee reproductive physiology. Previous studies indicated that seasonal changes in food availability play a role in increasing group size during the dry season and social contact between females can enhance cyclicity. Accordingly, I suggest that seasonal changes in diet may play a role, either directly (food content) or indirectly (social contact), to alter reproductive physiology.     

Assessing habitat utilization by neotropical primates: a new approach

This study aims to ascertain habitat utilization, in relation to forest structural variation, by a multi-species group of primates in tropical lowland rainforest in Southeast Peru during dry season. A new approach to assessing habitat utilization was used. Habitat variation was described by structural and indicator variables collected in quadrats along transects through a study area within Terra Firme and Floodplain forest. Variables were grouped into ‘factors’ accounting for most of the variation by means of a Principal Components Analysis (PCA). Presence or absence of the primates within the quadrats, assessed by repeat transect surveys, was taken to indicate habitat preferences. Discrimination between the habitat and forest structure in areas of primate presence as opposed to absence was carried out by means of Discriminant Function Analysis (DFA). This highlighted patterns in most utilized habitat. Vertical utilization of the forest was also assessed along with presence in bamboo and general activity on encounter. Suggestions of habitat preference and utilization are made for each of the six sympatric species studied, based on significantly discriminating habitat factors, vertical stratification on encounter and relationships with bamboo.Saguinus fuscicollis andCebus moloch appeared as habitat generalists.Cebus apella, Saimiri sciureus, andAotus spp., exhibited varying degrees of preference for habitat factors suggesting disturbed forest,Cebus albifrons was more generalistic but with a possible association with primary, naturally disturbed forest.C. appella was encountered in Terra Firme forest significantly more than in Floodplain. ForS. sciureus, C. moloch, andC. apella, upper understory was the most utilized forest layer, forC. albifrons, middle canopy and forS. sciureus andAotus spp., lower understory. Both positive and negative relationships with bamboo were highlighted. Significant positive relationships betweenAotus spp., and bamboo suggest dense bamboo stands provide important daytime resting sites for this nocturnal species.C. moloch was also shown to utilize bamboo whereasS. fuscicollis appeared to actively avoid it. High levels of conformity with past studies in terms of habitat utilization patterns described for the species studied supports the conclusion that the methods used in this study provide an effective means of assessing primate habitat utilization within complex habitat.     

Biochemical diversity and genetic distance in two species of the genusSaguinus

A comparative study of 20 blood genetic systems was performed on three populations of genusSaguinus: S. fuscicollis weddelli, S. midas niger, andS. midas midas. Some markers are useful for the characterization of the two species.ADA ⁵, ADA⁶, CA2³, CA2⁴, andES2 ² occur only inS. fuscicollis whileADA ⁴is fixed inS. midas. S. midas midas showed heterozygosity value comparable to those previously obtained for the genusAlouatta. Estimates of genetic distance betweenS. fuscicollis andS. midas species of about 14% are in accordance with those referred to in the literature for interspecific differences. Genetic distances between subspecies ofSaguinus midas were nearly 3%, which is within the range for subspecies.     

The Impact of Annual and Seasonal Rainfall Patterns on Growth and Phenology of Emergent Tree Species in Southeastern Amazonia,Brazil

Understanding tree growth in response to rainfall distribution is critical to predicting forest and species population responses to climate change. We investigated inter‐annual and seasonal variation in stem diameter by three emergent tree species in a seasonally dry tropical forest in southeast Pará, Brazil. Annual diameter growth rates by Swietenia macrophylla demonstrated strong positive correlation with annual rainfall totals during 1997–2009; Hymenaea courbaril growth rates demonstrated weak positive correlation, whereas Parkia pendula exhibited weak negative correlation. For both Swietenia and Hymenaea, annual diameter growth rates correlated positively and significantly with rainfall totals during the first 6 mo of the growing year (July to December). Vernier dendrometer bands monitored at 4‐wk intervals during 3–5 yr confirmed strong seasonal effects on stem diameter expansion. Individuals of all three species expanded in unison during wet season months and were static or even contracted during dry season months. Stems of the deciduous Swietenia contracted as crowns were shed during the early dry season, expanded slightly as new crowns were flushed, and then contracted further during 3–5 wk flowering periods in the late dry season by newly mature crowns. The three species’ physiographic distribution patterns at the study site may partially underlie observed differences in annual and seasonal growth. With most global circulation models predicting conditions becoming gradually drier in southeast Amazonia over the coming decades, species such as Swietenia that perform best on the ‘wet end’ of current conditions may experience reduced growth rates. However, population viability will not necessarily be threatened if life history and ecophysiological responses to changing conditions are compensatory.     

The impact of cropping on wild populations of Saguinus mystax and Saguinus fuscicollis in Peru

A transect census technique was used to estimate the population densities of Saguinus mystax and Saguinus fuscicollis at two sites in Peru. Cropping of these two species had occurred five years before the census at one site and two years before at the other. The populations of S. mystax at both sites had recovered completely from cropping, and the relationship between S. mystax and S. fuscicollis had not been altered at one site and had been reversed in favor of S. mystax at the other.     

Seasonal patterns of diet and ranging in two species of tamarin monkeys: Stability versus variability

From June through December, data were collected on the diet and ranging patterns of moustached (Saguinus mystax) and saddle-back (Saguinus fuscicollis) tamarin monkeys in the Amazon Basin of northeastern Peru. During this 7-month period, insects and nonleguminous fruits accounted for 83% of tamarin feeding and foraging time. Despite marked seasonal variation in rainfall and forest productivity, patterns of habitat utilization, day range, dietary diversity, resource exploitation, and activity budget remained relatively stable throughout the year. Moustached and saddle-back tamarins appear to solve problems of food acquisition and exploit patchily distributed feeding sites using a relatively limited set of foraging patterns. In general, these primates concentrate their daily feeding efforts on several trees from a small number of target plant species. These feeding sites are uncommon, produce only a small amount of ripe fruit each day, and are characterized by a high degree of intraspecific fruiting and flowering synchrony. Trees of the same species are frequently visited in succession, and individual feeding sites are revisited several times over the course of 1–2 weeks. This type of foraging pattern occurred during both dry and wet seasons and when exploiting fruit, nectar, legume, and exudate resources. Seasonal variation in the percentage of feeding and foraging time devoted to insectivory was also limited. In this investigation, there was no consistent evidence that temporal changes in overall forest fruit production had a major impact on the feeding, foraging, or ranging behavior of either tamarin species.