Leaders of progressions in wild mixed-species troops of saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax), with emphasis on color vision and sex

Leadership of travel progression is an important aspect of group living. It is widely believed that trichromacy evolved to facilitate the detection and selection of fruit in the dappled light of a forest. Further, it has been proposed that in New World primate species, which typically contain a range of color vision phenotypes, at least one female in a group will be trichromatic (i.e., having three types of visual pigment, in contrast to the two types of pigment found in dichromatic individuals) and will lead the group to fruiting trees. We examine progression leadership within two wild mixed-species troops of saddleback (Saguinus fuscicollis) and mustached (Saguinus mystax) tamarins over a complete year. As whole units, the mixed-species troops were most frequently led by a mustached tamarin. This is the first time that mixed-species group leadership and individual leadership have been quantified in these tamarin species. In terms of single-species intragroup leadership, neither the visual status (dichromatic or trichromatic) nor the sex of individuals had a consistent effect across species. Saddleback tamarin groups were led by males more frequently than females, while evidence suggests that mustached tamarins may be female-led. The notion that all groups contain at least one trichromatic female that leads the troop to feeding trees was not supported.     

Long-term patterns of sleeping site use in wild saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax): effects of foraging, thermoregulation, predation, and resource defense constraints

Sleeping sites are an important aspect of an animal's ecology given the length of time that they spend in them. The sleep ecology of wild saddleback and mustached tamarins is examined using a long-term data set covering three mixed-species troops and 1,300+ tamarin nights. Seasonal changes in photoperiod accounted for a significant amount of variation in sleeping site entry and exit times. Time of exit was more closely correlated with sunrise than time of entry was with sunset. Both species entered their sleeping sites when light levels were significantly higher than when they left them in the morning. Troops of both species used >80 individual sites, the majority being used once. Mustached tamarins never used the same site for more than two consecutive nights, but saddlebacks reused the same site for up to four consecutive nights. Mustached tamarins slept at significantly greater heights than saddleback tamarins. There were consistent interspecific differences in the types of sites used. Neither the presence of infants, season, nor rainfall affected the types or heights of sites chosen. Sleeping sites were located in the central area of exclusive use more often than expected, and their position with respect to fruiting trees indicated a strategy closer to that of a multiple central place forager than a central place forager. These findings are discussed in light of species ecology, with particular reference to predation risk, which is indicated as the major factor influencing the pattern of sleeping site use in these species.     

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.     

Diet and feeding ecology of saddle-back (Saguinus fuscicollis) and moustached (S. mystax) tamarins in an Amazonian terra firme forest

The feeding ecology of two small-bodied primate species—saddle-back ( Saguinus fuscicollis auilapiresi ) and moustached tamarins ( S. mystax pileatus )—occurring in stable, mixed-species groups was studied in a terra firme forest site in the upper Urucu River, Amazonas, Brazil. Ecological data are based primarily on one mixed-species group of 5–8 saddle-back and 8–10 moustached tamarins. The overall vegetative and animal-prey components of each tamarin species' diet, their selection of food species, and the seasonal variation in their use of plant resources are described, and compared to those of callitrichids elsewhere. The extremely diverse diet of tamarins included at least 136 tree, 33 vine and liana, 12 epiphyte and nine shrub species, as well as a wide range of prey items. They fed primarily on ripe fruit pulp of most of these species for most of the year, but shifted to floral nectar and plant exudates of a few key plant species during the dry season. Taxonomic overlap in plant diet was nearly complete between the two tamarin species, but they diverged considerably in their prey capture techniques. Saddle-backs used the low forest understorey, and manipulatively searched for sedentary prey concealed within discrete, usually rigid, microhabitats, whereas moustached tamarins used the midstorey where they visually searched for mobile prey well exposed on foliage. These and other feeding and foraging patterns are discussed in the light of other callitrichid species studied to date.     

The behavioural ecology of mixed-species troops of callitrichine primates

This review summarizes information on the behavioural ecology of mixed-species troops (interspecific associations) formed by different species of callitrichines, small New World monkeys, in western and central Amazonia. The formation of mixed-species troops is an integral part of the biology of several species of this subfamily. Niche separation between associated species is obtained through vertical segregation which results in differences in the prey spectrum. The degree of niche separation is a predictor for the stability of mixed-species troops. Individuals may benefit from the formation of mixed-species troops through increased safety from predators, increased foraging efficiency, and/or increased resource defence. Costs of mixed-species troop formation are probably very low and mainly relate to patterns of interspecific behavioural interactions. We point to gaps in our knowledge and suggest pathways for future research into mixed-species troops.     

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.     

Social interaction with non-averse group-mates modifies a learned food aversion in single- and mixed-species groups of tamarins (Saguinus fuscicollis and S. labiatus)

For social species, being a member of a cohesive group and performing activities as a coordinated unit appear to provide a mechanism for the efficient transmission of information about food. Social learning about food palatability was investigated in two captive primates, Saguinus fuscicollis and S. labiatus, which form stable and cohesive mixed-species groups in the wild. We explored whether an induced food aversion toward a preferred food is modified during and after social interaction with non-averse conspecifics or congeners. Sets of intra- and interspecific pairs were presented with two foods, one of which was considered distasteful by one of the pairs (the other was palatable), and their behavior was compared pre-interaction, during interaction, and post-interaction. For the aversely-conditioned individuals of both species, the change in social context corresponded to a change in their preference for the food that they considered unpalatable, regardless of whether they had interacted with a conspecific or congeneric pair, and the change in food preference was maintained post-interaction. In a control condition, in which averse individuals did not have the opportunity to interact with non-averse animals, S. fuscicollis sampled the preferred food, but not as quickly as when given the opportunity to interact. We conclude that the social learning demonstrated here may allow individual tamarins to track environmental change, such as fruit ripening, more efficiently than asocial learning alone, because social learners can more quickly and safely focus on appropriate behavior by sharing up-to-date foraging information. Furthermore, since the behavior of congeners, as well as conspecifics, acts to influence food choice in a more adaptive direction, social learning about food palatability may be an advantage of mixed-species group formation to tamarins of both species.     

Hand specialization, sympatry, and mixed-species associations in callitrichines

Hand morphology in callitrichines (i.e., tamarins, marmosets, and Goeldi's monkey) is correlated with positional and foraging behaviors. This study examines hand shape in callitrichines using an allometric approach. It addresses a series of questions relating hand anatomy, insect foraging behavior, and resource partitioning in callitrichines. The main questions are: 1. Do the hands of Leontopithecus differ in shape from all other callitrichine taxa allowing it to perform highly manipulative prey foraging behaviors? 2. Are the hands of Saguinus fuscicollis adapted to manipulative foraging, and are they functionally similar to Leontopithecus' hands? 3. Is hand morphology in S. fuscicollis more similar to the hand morphology of sympatric tamarin species with whom it does not form mixed species troops (S. nigricollis and S. tripartitus) than to those sympatric tamarin species with whom it does form mixed troops (S. mystax, S. labiatus, and S. imperator)? Measurements of hand length (HL), width (HW), and thickness (HT) were taken from 1350 museum specimens of callitrichines (Callithrix, Cebuella, Leontopithecus, Saguinus, and Callimico), squirrel monkeys (Saimiri), and owl monkeys (Aotus). The analysis indicates that hand shape covaries with foraging strategy. Specifically, the hands of Leontopithecus are adapted for manipulative foraging and are relatively longer and more slender than the hands of other callitrichines. A similar pattern is observed in the hands of S. fuscicollis, S. tripartitus and S. nigricollis. These latter species, however, differ significantly in shape from all other tamarin species. Large differences in hand morphology are observed among tamarin species that form mixed-species troops. These anatomical differences may permit resource partitioning and coexistence among these closely related taxa. Hand shape, expressed as log HLGM (logged hand length divided by the geometric mean of all measurements), is a good predictor of manipulative and non-manipulative prey foraging techniques employed by callitrichines.     

Modeling monkeys: A comparison of computer-generated and naturally occurring foraging patterns in two species of neotropical primates

We present a series of computer-generated foraging models (random movement, olfactory navigation, and spatial memory) designed to examine the manner in which sensory cues and cognitive skills might be used by rainforest monkeys to locate patchily distributed feeding sites. These simulations are compared with data collected in the Amazon Basin of northeastern Peru on the foraging patterns of two species of neotropical primates, the moustached tamarin monkey (Saguinus mystax) and the saddle-back tamarin monkey (Saguinus fuscicollis). The results indicate that, although tamarins may rely on olfactory cues to locate nearby feeding sites, their foraging patterns are better explained by an ability to maintain a detailed spatial map of the location and distribution of hundreds of feeding trees in their home range. There is evidence that such informationis retained for a period of at least several weeks and is used to minimize the distance traveled between widely scattered feeding sites. The use of computer simulations provides a powerful research tool for generating predictive models regarding the role of memory and sensory cues in animal foraging patterns.     

Food patch structure and plant resource partitioning in interspecific associations of amazonian tamarins

ávila-Pires’ saddle-back tamarins (Saguinus fuscicollis avilapiresi) and red-cap moustached tamarins (S. mystax pileatus), coexisting in highly stable mixed-species groups, overlapped considerably in their use of plant food resources at an Amazonian terra firme forest site. Overlap between food types consumed by the two species was particularly high during periods of lowest fruit availability, when they resorted to a common food supply, primarily the pod exudates of two emergent species of legume trees (Parkia nitida andParkia pendula) and nectar ofSymphonia globulifera. Within-group interspecific competition did not covary with independent measures of resource availability, contrary to predictions based on resource partitioning models. A greater number of both saddle-back and moustached tamarins were able to feed for longer patch residence periods within larger and more productive food patches, whereas small and clumped patches could be monopolized by the socially and numerically dominant moustached tamarins to the physical exclusion of the smaller-bodied saddle-back tamarins. Overall rates of interspecific aggression were extremely low, however, partly because patches that could be monopolized contributed with a minor proportion of either species’ diet. Saddle-backs foraged at lower levels in the understory and encountered smaller food patches more often, whereas moustached tamarins foraged higher and encountered more larger patches in the middle canopy. Although the two species led one another to differently-sized patches, moustached tamarins initiated most feeding bouts and encountered significantly larger and more productive patches that tended to accommodate the entire mixed-species group. Disadvantages of exploitative and interference feeding competition over plant resources, and advantages of shared knowledge of food patches, are but one component of the overall cost-benefit relationship of interspecific associations in tamarins.     

Factors Affecting Group Spread within Wild Mixed-Species Troops of Saddleback and Mustached Tamarins

We examined group spread and interindividual spacing within wild mixed-species troops of saddleback (Saguinus fuscicollis) and mustached (Saguinus mystax) tamarins. Mustached tamarin groups were spread over larger areas than those of saddleback tamarins. Group size and behavior affected group spread and interspecific proximity: larger groups of both species were dispersed over greater areas, and the larger troop had the lowest degree of interspecific proximity. Behavior also affected group spread and interspecific proximity: when traveling individuals were spread over a larger area, and the distance between heterospecifics was greater than when stationary. We examined spatial proximity using data on the distance from nearest neighbor. Overall, distance to nearest neighbor was not affected by group size. Based on specific behaviors, foraging saddleback tamarins were significantly nearer conspecifics than to mustached tamarins. Tamarins have polymorphic color vision, and trichromats—having 3 types of visual pigment—versus dichromatic individuals—with two types of pigment—may be better at perceiving yellow or russet colored predators and conspecifics than their dichromatic counterparts are. Color vision status affected spatial positioning, with vigilant trichromats being further from their neighbors than their dichromatic conspecifics were. We discuss the findings with respect to the ecology of the species. Specifically, interspecific differences in group spread and spatial proximity are related to differences in the supports used, and the effect of troop size on interspecific proximity is related to increased resource competition. The finding that trichromats are further from their neighbors represents the first example of a behavioral correlate of color vision ability in a wild species with polymorphic color vision, and is explained through the perception of predation risk.     

Body weights in mixed species troops of Saguinus mystax mystax and Saguinus fuscicollis nigrifrons in Amazonian Peru

An investigation of body weights of members of mixed species troops of Saguinus mystax mystax and Saguinus fuscicollis nigrifrons was conducted at the Rio Blanco Research Station in northeastern Peru. A total of 107 adult and subadult tamarin monkeys were trapped, measured, and released. Data collected indicate that mean body weights for adult male and female moustached tamarins are 564 gm and 626 gm, respectively, whereas for adult saddle-back tamarins these values are 412 gm and 411 gm. Subadults weighed 11-27% less than adults. Body weights recorded in this study are significantly greater than those previously reported for tamarins of the same species and age living in other areas of Amazonian Peru. We hypothesize that, in the case of moustached and saddle-back tamarins, advantages associated with feeding and foraging in mixed species troops facilitate greater efficiency in resource monitoring and result in the maintenance of larger body weights.     

Sleeping Site Selection by the Golden-handed Tamarin Saguinus midas midas: The Role of Predation Risk, Proximity to Feeding Sites, and Territorial Defence

Tamarin monkeys, of the genus Saguinus , spend over half their lives at arboreal sleeping sites. The decision as to which site to use is likely to have considerable fitness consequences. These decisions about sleeping sites by three troops of golden-handed tamarin Saguinus midas midas were examined over a 9-mo period at a rainforest site in French Guiana. Data are presented on the physical nature of sleeping sites, their number, position within home ranges, and pattern of use and reuse, aspects of behaviour at retirement and egress, and predation attempts on the study troops. Cumulative plot analysis indicated that a tamarin troop used 30–40 sleeping sites in a 100-day period, approximately half of which were used very infrequently, so that consecutive reuse was never greater than three nights. Sleeping trees were superior in architectural parameters and liana weight to non-sleeping trees. There were no more sleeping sites than expected within the home range boundary region of the tamarins or in areas of overlap with the home ranges of neighbouring troops. Tamarins selected sleeping sites nearest to the last feeding site of the day on 25% of occasions. The study troops engaged in a number of activities that may reduce predation risk; raptor attacks on the study troops over 9 mo were frequent but unsuccessful. Tamarins often visited a sleeping site several hours before arrival, and were more likely to visit a site before use if they had not used it recently. The decision to select a sleeping site therefore involved knowledge of the previous frequency of use of that site.     

Troop-specific responses to long calls of isolated tamarins (Saguinus mystax)

Recently captured moustached tamarins (Saguinus mystax) were briefly separated from other members of their troop. Most separated animals emitted long calls that were, in general, similar in acoustic structure to those of sympatric tamarin species while retaining species distinctiveness. Individual differences also appeared in call structure. The long calls of a separated animal were responded to almost entirely by members of the animal's own troop rather than by other troops, and reciprocal calling occurred among troop members significantly more often than expected by chance. Although there was no evidence of troop-specific call structure or dialect, there were troop-specific responses to the calls of separated tamarins. This response implies the existence of a stable and integrated troop structure that allows troop members to learn and to respond to the individual specific features of each troop member's calls.     

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.     

Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipus) and saddle-back (S. fuscicollis) tamarins

Patterns of morphological variation play an important role in evolutionary diversification and are critical to an informed interpretation of interspecific differences. When patterns of genetic variation have not diverged substantially, it is possible to reconstruct the differences in selection which gave rise to morphological differences among extant species. Morphological variation patterns are compared between two tamarin species, the cotton-top tamarin (Saguinus oedipus) and the saddle-back tamarin (S. fuscicollis illigeri). Genetic, phenotypic, and environmental variance/covariance and correlation matrices were obtained for a series of 39 cranial characters in each species (cotton-top tamarin, N = 328; saddle-back tamarin, N = 209) and for the species combined using crania from individuals of known genealogical relationship. After accounting for the effects of estimation error on measures of matrix similarity, patterns of phenotypic, genetic, and environmental variation and correlation were found to be very similar across species and among the types of variance within species. Taking the saddle-back tamarins as the standard, cotton-top tamarins have been selected for an enlarged anterior temporalis attachment area and increased facial prognathism. In primates, an enlarged anterior temporalis muscle is associated with incisive food preparation, especially at wide gape.     

Ring-Tailed Lemur Home Ranges Correlate with Food Abundance and Nutritional Content at a Time of Environmental Stress

In order to determine whether ring-tailed lemurs (Lemur catta) adapt their ranging and select an optimal diet at a time of food shortage, we observed two adjacent troops in Berenty Reserve, Madagascar for over 250 h. The troops, created by a recent fission, ranged through closed canopy gallery forest next to a river and open forest away from the river. We conducted the study in September–October, 2000, normally a time of seasonally low resource availability, which was intensified by damage from a previous windstorm and recent drought. To examine the impact of environmental stress, we mapped their ranging patterns, intertroop encounters, feeding patches, siesta trees, and sleeping trees. We then correlated their ranging and feeding behavior with nutritional analyses of leaves and fruit from tamarind trees located in different parts of their ranges. One of the troops, D1A, ranged farther into open forest than previously. However, the range for troop D1B and the closed canopy portion of D1A's range were located in traditional positions for historical troops D and E. Both troops ate significantly more mature leaves from the tamarind trees in the closed canopy forest, where the leaves had significantly higher nutritional content (water and protein) than that of open forest samples. They fed on tamarind fruit significantly more often in the open forest away from the river, where it was more abundant. The lemurs selected a diet that maximized leaf water and protein and ranged where fruit was most abundant but at high energetic costs for troop D1A.     

Use of Social and Ecological Information in Tamarin Foraging Decisions

A major consequence of group living is that foragers may rely on social information in addition to ecological information to locate feeding sites. Although conspecifics can provide cues as to the spatial location of food patches, individual foraging decisions also must include some assessment of the likelihood of obtaining access to a resource other group members seek. This likelihood differs in the 2 models generally proposed to explain intragroup social foraging: the information-sharing model and the producer-scrounger model. We conducted an experimental field study on wild groups of emperor (Saguinus imperator) and saddleback (S. fuscicollis) tamarins to determine the foraging strategies adopted by individual group members and their relationship to social rank, food intake, and the ability to use ecological and social information in making intra-patch foraging decisions. Individual tamarins applied different behavioral strategies compatible with a finder-joiner paradigm to solve foraging problems. About half of the individuals in each study group initiated 74%–90% of all food searches and acted as finders. Most alpha individuals adopted a joiner strategy by monitoring the activities of others' to obtain a reward. The individual arriving first at a reward platform enjoyed a finder's advantage. Despite differences in search effort, both finders and joiners presented similar abilities in learning to associate ecological cues with the presence of food rewards at our experimental feeding stations. We conclude that within a group foraging context, tamarins integrate social and ecological information in decision-making.     

Predation on Orthoptera and other orders in insects by tamarin monkeys, Saguinus mystax mystax and Saguinus fuscicollis nigrifrons (Primates: Callitrichidae), in north-eastern Peru

Kaytydids and related insects are an important component in the diets of moustached ( Saguinus mystax mystax ) and saddle-back tamarins ( Saguinus fuscicollis nigrifrons ). Based on preliminary data of captured prey, trends suggest that partitioning occurs regarding orthopterans as a limited food resource. Of species caputre as prey, only three were shared by both tamarin species. Saddle-back tamarins appeared to specialize more on understorey species (0-4 m), concentrating on pseudophylline katydids. Moustached tamarins incorporated a greater percentage of phaneropterine katydids from the lower to middle canopy into their diet of insects. Although most prey species were exposed to view during the diurnal feeding period of the tamarins, only the saddle-back tamarin fed on katydids that spend the day concealed from view within dead curled leaves. Differentiation of the prey spectrum may represent a critical pattern of niche differentiation in these two sympatric tamarin species, which show a high overlap in their plant food resources.     

The influence of flocking on the foraging behaviour of the chough (Pyrrhocorax pyrrhocorax) and the Alpine chough (P. graculus) coexisting in the Alps

We studied the flocking and foraging behaviour of the chough Pyrrhocorax pyrrhocorax and the Alpine chough P. gruculus coexisting in the south-western Italian Alps in order to evaluate the costs and benefits of foraging in single- and mixed-species flocks.
In the single-species context, flock size significantly affected the foraging behaviour of the Alpine chough; in larger flocks, the birds stayed for a shorter time in a patch and fed more quickly than in smaller flocks. Flock size did not significantly affect the foraging behaviour of the chough, probably because of the small number of individuals per flock.
The propensity for mixed-species flocking was rather low. The observed frequencies of single-species flocks of choughs and Alpine choughs were significantly higher than those expected on the basis of random flocking, whereas the observed frequencies of mixed-species flocks of the two species were lower than those expected. The stay times became significantly shorter for the chough in the presence of the Alpine chough. Moreover, feeding rates of the Alpine chough were significantly lower in the presence of the dominant chough.
The present study does not confirm the hypothetical foraging advantages of flocking. In single-species flocks, the benefits for the Alpine chough (higher feeding rates in larger flocks) were roughly compensated by the costs (shorter stay times in larger flocks), whereas the chough apparently neither gained benefits nor endured costs.
In mixed-species flocks, the Alpine chough sustained costs due to a reduction of feeding rates and the chough suffered costs due to a reduction of stay times. Hence, on average, single-species flocking gives no evident foraging advantages to either the chough or the Alpine chough, whereas mixed-species flocking provides some disadvantages for both species.