The ecology of seed dispersal in two species of callitrichid primates (Saguinus mystax and Saguinus fuscicollis)

Data collected during a 12-month field investigation of mixed species troops of Saguinus mystax and Saguinus fuscicollis in the Amazon Basin of north-eastern Peru indicate that callitrichid primates play an important role in tropical forest seed dispersal. Moustached and saddle-back tamarins were observed to ingest seeds from a variety of tree and liana species and pass them unharmed. These seeds tended to be large and heavy, and passed through the tamarin digestive tract in one to three hours. Experimental plantings of defecated seeds yielded a germination success rate of 70%. The specific gravity of these seeds (weight/volume) was inversely correlated with passage time and apparently had an indirect influence on the distance that seeds were dispersed from the parent tree. In the case of three preferred fruiting species, Leonia glycycarpa, Pourouma sp., and Hippocrateaceae #283, the present distribution of adult trees closely resembled the pattern of the seed shadow created by Saguinus. Moustached and saddle-back tamarins appeared to be reliable and high-quality dispersal agents for a number of tree and liana species. In this role, they are likely to exert an important influence on the composition, distribution, and regeneration patterns of Amazonian rain forest.     

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.     

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.     

Demographic parameters and events in wild moustached Tamarins (Saguinus mystax)

This paper examines demographic events in the context of population structure and genetic relationships in groups of wild moustached tamarins (Saguinus mystax). We used a combination of long-term behavioral observations and genetic data from a total of eight groups from a population in northeastern Peruvian Amazonia. The mean group size was 6.0 (range = 4-9), including 2.5 adult males and 1.8 adult females. Within-group relatedness was generally high (r = 0.3), and most nonbreeding individuals were either natal or closely related to the respective same-sex breeder. The mean annual persistence of adults in the groups was 70% and 68% for males and females, respectively, and the reproductive tenure of one breeding pair lasted for at least 6 years. Migrations predominantly occurred after stability-disrupting events such as the immigration of new individuals and/or the loss of breeding individuals, or when groups were rather large. Migrations of both breeding and nonbreeding males and females occurred. Our results show that the hypothesis of Ferrari and Lopes Ferrari [Folia Primatologica 52:132-147, 1989] that tamarins live in smaller and less stable groups with lower relatedness compared to marmosets does not generally hold true. In contrast, we found that tamarin groups can consist of predominantly related individuals, and are stable as well. It is also apparent that a single demographic event can produce a chain of subsequent complex demographic changes.     

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.     

Composition and Proposed Nutritional Importance of Exudates Eaten by Saddleback (Saguinus fuscicollis) and Mustached (Saguinus mystax) Tamarins

I provide the first comprehensive data on the composition and mineral content of exudates eaten by saddleback (Saguinus fuscicollis) and mustached tamarins (S. mystax) and assess Garber's (1984; 1993) hypotheses on the potential nutritional importance of exudates in the diet of tamarins. In accordance with his initial findings, nutritional analyses show that the gums consumed are relatively high in calcium and may serve to balance a diet otherwise low in this mineral and high in phosphorus. However, the data on the seasonal variation in the amount consumed do not support the hypothesis that exudates are of particular nutritional importance during the later stages of gestation or lactation for saddleback or mustached tamarins.     

Sperm parameters and testicular volumes in Saguinus mystax

Adult male Saguinus mystax tamarins were evaluated for sperm parameters and testicular volumes. Sperm concentrations average 195.5 X 10(6)/cc with 41.7% motile sperm. Semen specimens were classified as normal, relative to sperm morphology, when 95% or more of the sperm in the specimen had normal morphology; 76% of the animals evaluated had normal semen specimens using this criterion. Testicular volumes averaged 726.9 mm3. A total of 50 infants were sired by 16 of these males during the period covered by this report.     

Paternity and kinship patterns in polyandrous moustached tamarins (Saguinus mystax)

We studied patterns of genetic relatedness and paternity in moustached tamarins, small Neotropical primates living in groups of 1–4 adult males and 1–4 adult females. Generally only one female per group breeds, mating with more than one male. Twin birth are the norm. In order to examine the genetic consequences of this mating pattern, DNA was extracted from fecal samples collected from two principal and six neighboring groups. DNA was characterized at twelve microsatellite loci (average: seven alleles/locus). We addressed the following questions: Do all adult males have mating access to the reproductive female of the group? How is paternity distributed across males in a group? Can polyandrous mating lead to multiple paternity? Are nonparental animals more closely related to the breeders than to the population mean? And, are mating partners unrelated? Breeding females mated with all nonrelated males. In at least one group the father of the older offspring did not sire the youngest infant although he was still resident in the group. We also found evidence for multiple paternity in a supposed twin pair. Yet, within each group the majority (67–100%) of infants had the same father, suggesting reproductive skew. Relatedness within groups was generally high (average R = 0.31), although both nonrelated males and females occurred, i.e., immigrations of both sexes are possible. Mating partners were never found to be related, hence inbreeding seems to be uncommon. The results suggest that while the social mating system is polyandry, paternity is often monopolized by a single male per group. Am J Phys Anthropol, 2005. © 2004 Wiley-Liss, Inc.     

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.     

Polymorphic microsatellite loci for the mustached tamarin (Saguinus mystax) and their cross‐species amplification in other New World monkeys

We isolated and characterized 10 polymorphic microsatellite loci for the mustached and cotton‐top tamarin (Saguinus mystax and S. oedipus) and also tested their applicability in other New World monkey genera. Six loci proved to be variable in Cebus apella and Saimiri sciureus/S. boliviensis, respectively. We also show that faeces‐derived DNA is suitable for polymerase chain reaction (PCR) analyses of a primate taxon that gives birth to twins with individuals exhibiting a haematopoetic chimaerism. The microsatellite fingerprint patterns do not display a complex mixture of the PCR‐products derived from the alleles of both dizygotic twins, but exhibit the constitutive alleles of one sibling only.     

Geophagy in moustached tamarins,Saguinus mystax (platyrrhini: Callitrichidae), at the Río Blanco,Peruvian Amazonia

During a field study at the Río Blanco in northeastern Peru between June and September 1990, moustached tamarins (Saguinus mystax) were observed to feed on soil material on three different occasions. Soil was taken directly from bare spots of surface soil (two observations) and from the broken mound of leaf-cutting ants (Atta sp.; one observation). Exposed surface soil is rare throughout the study area. Geochemical analyses of the soils that were consumed showed elevated concentrations of several elements in the ant mound sample compared to the other two soil samples. The most likely hypothesis for the function of soil feeding in moustached tamarins is that it serves in mineral supplementation.     

Reproduction of wild-caught tamarins (Saguinus mystax mystax) under laboratory conditions

The reproductive performance of tamarins (Saguinus mystax mystax) under laboratory conditions was evaluated. Fifteen of 20 male-female pairs were fertile and produced 30 live births during an observation period of 3.5 years. Twenty-six breeders (65%) and 12 offspring (40%) more than 3 years old were alive at the termination of the reporting period.     

Prey foraging of red titi monkeys, Callicebus cupreus, in comparison to sympatric tamarins, Saguinus mystax and Saguinus fuscicollis

We compared the prey capture strategies of red titi monkeys, Callicebus cupreus, with those of sympatric mustached, Saguinus mystax, and saddleback tamarins, Saguinus fuscicollis, to examine whether animal prey is important in niche differentiation between these Neotropical primates. We collected data on strata and substrate use during foraging, on prey searching and capturing, and on prey type of two C. cupreus groups and one group each of S. mystax and S. fuscicollis during a 5-month field study in northeastern Peruvian Amazonia. Our results showed that C. cupreus differed both from S. mystax and S. fuscicollis in prey capture strategies: (1) C. cupreus used lower forest strata for prey search and capture than S. mystax and higher forest strata than S. fuscicollis. (2) C. cupreus captured prey on a higher variety of substrates than S. mystax and more often on open microhabitats compared to S. fuscicollis. (3) C. cupreus captured prey more often directly than S. mystax and rarely by manual search, in contrast to S. fuscicollis. (4) C. cupreus fed exclusively on arthropods and focused on Hymenoptera, in contrast to both tamarin species that focused on Orthoptera and included vertebrates in their diet. These findings indicate that animal prey plays a role in niche differentiation between C. cupreus and S. fuscicollis/S. mystax and might facilitate the coexistence of these three sympatric species.     

Population recovery in the moustached tamarin (Saguinus mystax): Management strategies and mechanisms of recovery

In 1978, 66% of the individuals of Saguinus mystax and 9.5% of Saguinus fuscicollis were cropped from a population at the Yarapa river, Peru. The effects of cropping on the remaining tamarin population were evaluated by conducting censuses in 1981 and 1982 and by trapping and release of Saguinus mystax in 1981. Three hundred kilometers of trail were covered in the censuses, and all the groups within the 1.9-km² study area were located. Within three years after cropping, the population of S. mystax had increased by 124%, more than double the size left in 1978. Increased reproductive rate, early breeding, and reduced infant mortality contributed to the recovery. On the other hand, S. fuscicollis had decreased by 12% in the three years following the cropping but had increased in the fourth year to a level slightly below the precropping density. The cropping of more S. mystax than S. fuscicollis might have contributed to the decline of the latter. The cropping of a sizable percentage of S. mystax from a natural population does not seem to impair its recuperative powers. It may take longer than four years for a population exhibiting high density, such as that at the Yarapa site, to recover completely.     

Dentition of moustached tamarins (Saguinus mystax mystax) from Padre Isla, Peru, part 1: quantitative variation

Analyses of dental variation in geographically restricted, wild populations of primates are extremely rare; however, such data form the best source for models of likely degrees of variation within and between fossil species. Data from dental casts of a geographically restricted population of moustached tamarins (Saguinus mystax mystax) from Padre Isla, Peru, document high levels of dental variability, as measured by coefficients of variation, in a nonsexually dimorphic species, despite its isolation and small population size. Like other primates, moustached tamarins show lower variability in the dimensions of the first molars and increased variability in the dimensions of the final molars in the toothrow. Moustached tamarins from Padre Isla have a distinctive pattern of variability in the remaining teeth, including more stable tooth lengths in the anterior and posterior portions of the toothrow, and more stable tooth widths in the midregion of the toothrow. High variability in incisor width may be due to age effects of a distinctive diet and pattern of dental wear.     

Interspecific variation of scent-marking behaviour in wild tamarins, Saguinus mystax and Saguinus fuscicollis.

The scent-marking behaviour of sympatric moustached, Saguinus mystax, and saddle-back tamarins, Saguinus fuscicollis, was compared in order to explore interspecific differences and potential sources of variation. The author examined basic patterns of scent marking (types, intensity, complexity), substrate use (type, orientation, height), and social patterning of scent marking in three groups of S. mystax and one group of S. fuscicollis at the Estación Biológica Quebrada Blanco, Peruvian Amazonia. S. mystax and S. fuscicollis differed significantly in the relative frequency of different types, and in the intensity and complexity of scent marking. Only S. fuscicollis showed allomarking. They also differed significantly in the type, orientation and height of substrates used for scent marking which corresponded to general differences in substrate use. In S. fuscicollis, but very rarely in S. mystax, two or more group members marked the same site sequentially or simultaneously. 'Collective scent marking', i.e. simultaneous scent marking by most or all group members, occurred only in S. fuscicollis. Since both tamarin species live sympatrically in mixed-species groups, ecological factors are unlikely to account for the differences found in scent-marking behaviour (except for differences in substrate use). They probably relate to as yet unknown differences in social and reproductive strategies of the two species.     

A field study of Geoffroy's tamarin (Saguinus geoffroyi) in Panama

A 3-month field study was conducted in Panama to determine presence and relative abundance of Saguinus geoffroyi, the Geoffroy's tamarin, and status of its habitat (see Acknowledgments for taxonomic note). This primate has a wide geographical distribution in eastern Panama; however, local distribution is highly variable. Tropical forest habitat is rapidly being converted for agriculture and timber. Areas where human access was strictly limited showed tamarin densities significantly greater than in less protected areas. Disturbance has a distinct impact on population densities. There may also be a relationship between tamarin abundance and specific types of vegetation. Future actions regarding the conservation of S. geoffroyi and its habitat are recommended.