Erratum to: The range of the golden-mantle tamarin, <Emphasis Type="Italic">Saguinus tripartitus</Emphasis> (Milne-Edwards, 1878): distributions and sympatry of four tamarins in Colombia,Ecuador, and northern Peru

A detailed understanding of the range of the golden-mantle tamarin, Saguinus tripartitus (Milne Edwards, 1878), in Amazonian Peru and Ecuador is of particular relevance, not only because it is poorly known but also because it was on the basis of its supposed sympatry with the saddleback tamarin (S. fuscicollis lagonotus) that Thorington (Am J Primatol 15:367–371, 1988) argued that it is a distinct species rather than a saddleback tamarin subspecies, as was believed by Hershkovitz (Living new world monkeys, vol I. The University of Chicago Press, Chicago, 1977). A number of surveys have been carried out since 1988 in the supposed range of S. tripartitus, in both Ecuador and Peru. Here we summarize and discuss these issues and provide a new suggestion for the geographic range of this species; that is, between the ríos Napo and Curaray in Peru and extending east into Ecuador. We also review current evidence for the distributions of Spix’s black-mantle tamarin (S. nigricollis nigricollis), Graells’ black-mantle tamarin (S. n. graellsi), and the saddleback tamarin (S. fuscicollis lagonotus), which are also poorly known, and examine the evidence regarding sympatry between them. We conclude that despite the existence of a number of specimens with collecting localities that indicate overlap in their geographic ranges, the fact that the four tamarin species are of similar size and undoubtedly very similar in their feeding habits militates strongly against the occurrence of sympatry among them.     

Field observations of the golden-mantled tamarin, Saguinus tripartitus, on the Río Curaray, Peruvian Amazonia

During a primatological survey on the Río Curaray in north-eastern Peruvian Amazonia, observations on the ecology and behaviour of the golden-mantled tamarin, Saguinus tripartitus, were made. Two groups consisting of 6 and 9 individuals were observed. The diet of one group that was observed in some detail consisted of fruit, insects (tettigoniid orthopterans) and gums. Patterns of height use were very similar to those observed in saddle-back tamarins, Saguinus fuscicollis. This similarity and the lack of evidence for sympatry with either S. fuscicollis or S. nigricollis lead to the suggestion that S. tripartitus should be reconsidered as a subspecies of S. fuscicollis rather than a species on its own; alternatively, other subspecies of S. fuscicollis should be raised in taxonomic rank.     

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.     

Mitochondrial phylogeny of tamarins (Saguinus, Hoffmannsegg 1807) with taxonomic and biogeographic implications for the S. nigricollis species group

Tamarins of the genus Saguinus, subfamily Callitrichinae, represent one of the most diverse primate radiations. So far, about 35 taxa have been described, but detailed information about their taxonomy and phylogeny is still lacking. To further elucidate the phylogenetic relationships and the biogeographic history within the genus, and to contribute to a more reliable classification of its taxa, we sequenced the complete mitochondrial cytochrome b gene and the hypervariable region I of the D-loop. Therefore, we mainly used fecal samples from wild tamarins collected during two expeditions to the Peruvian Amazon, an area of high tamarin diversity. Our data suggest that the numerous taxa of the S. nigricollis species group are derived from a common ancestor that separated from the other representatives of the genus ~10 mya. Most taxa of the S. nigricollis group form monophyletic clusters, which mainly originated in a single rapid radiation ~2.9 mya. S. fuscicollis and S. nigricollis appear as polyphyletic taxa, but we could identify various clusters, which are mainly consistent with differences in coat coloration. We could confirm most of the existing taxa as distinct entities and suggest species status for fuscicollis, illigeri, lagonotus, leucogenys, nigricollis, nigrifrons, tripartitus, and weddelli. Our genetic data do not support a separate status for melanoleucus and graellsi, but due to differences in fur coloration, we give them subspecies status. The species group most likely originated in western Amazonia and diversified during the decline of the Acre wetland and the formation of the Amazonian river system.     

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.     

Subspecific genetic differences in the saddle-back tamarin (Saguinus fuscicollis) postcranial skeleton

Saddle-back tamarins (Saguinus fuscicollis) have been differentiated into subspecies based on coat color and facial morphology. Morphology of first-generation genetic hybrids can provide an understanding of population differences and evolution that may otherwise be difficult to obtain. This study compares postcranial morphology in two hybrids of saddle-back tamarins (S. f. illigeri x S. f. lagonotus and S. f. illigeri x S. f. leucogenys) to the purebred subspecies. We examine whether postcranial morphology differs between the purebred subspecies and their hybrids, and whether hybrids exhibit heterosis indicative of genetic differences between the parental subspecies. Fifty postcranial dimensions, or traits, were measured on 287 S. fuscicollis skeletons. Measurements were corrected for sex differences and environmental differences (wild-derived or laboratory-born). Females were larger than males for most postcranial dimensions, especially in the pelvis. Significant environmental differences were found throughout the postcranial skeleton, with wild-derived animals generally larger than animals born in the laboratory. Significant heterosis was found for six postcranial traits in the S. f. illigeri x S. f. leucogenys cross, and heterosis was found for 15 postcranial traits in the S. f. illigeri x S. f. lagonotus cross. These results suggest that subspecies differences in skeletal morphology are generally due to genetic rather than environmental differences. The subspecies appear to represent geographic isolates that differ in gene frequencies and directional dominance for skeletal traits.     

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.     

Vertebrate predation by sympatric tamarins, Saguinus mystax and Saguinus fuscicollis

Vertebrate predation was examined in sympatric moustached tamarins (Saguinus mystax) and saddle-back tamarins (Saguinus fuscicollis) in the Amazon rainforest of northeastern Peru. Both species prey on frogs and lizards, and very rarely on nestling birds. As a result of divergent foraging strategies, S. mystax primarily exploited frogs at higher strata of the forest, while S. fuscicollis predominantly preyed on reptiles in the lower strata and on the ground. This difference may strengthen the niche differentiation between these two tamarin species that exists with regard to other prey.     

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.     

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.     

A case of syndactyly in the white-lipped tamarin Saguinus nigricollis.

A case of syndactyly in a captive bred white-lipped tamarin (Saguinus nigricollis) is reported which involved the fusion of metacarpals 3 and 4 of both hands. Variations in the vertebral formula among the parents and offspring were also found.     

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.     

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.     

Sleeping habits of tamarins, Saguinus mystax and Saguinus fuscicollis (Mammalia; Primates; Callitrichidae), in north-eastern Peru

The sleeping habits of moustached tamarins, Saguinus mystax , and saddle-back tamarins, Saguinus fuscicollis , were studied in northeastern Peru. Five types of sleeping sites were distinguished: 1) Jessenia bataua palms; 2) tree hollows; 3) dense tangles of vegetation; 4) crotches; 5) open horizontal branches. Both tamarin species used Jesseniu-palms most frequently. Tree hollows ranked second in the saddle-back tamarins, but were never used by moustached tamarins. Sleeping sites of moustached tamarins were located significantly higher than those of saddle-back tamarins. Jessenia -palms used by moustached tamarins were significantly higher than palms from a random transect sample, but this was not the case for Jessenia -palms used by saddle-back tamarins. For both species, concealment seems to be more important than height above ground. The maximum number of subsequent nights spent in the same sleeping site was two in moustached tamarins and six in saddle-back tamarins. The two tamarin species did not compete for sleeping sites. While the general pattern of sleeping site selection conforms to hypotheses predicting safety from predators as a major factor, differences between the two tamarin species reflect general niche differences between them. Most sleeping sites are located in exclusively used parts of the home range. Moustached tamarins generally use sleeping sites that are close to the last feeding site of the afternoon. The distance between simultaneously used sleeping sites of moustached and saddle-back tamarins are generally close together, which helps to minimize time spent out of interspecific association.     

Sexual dimorphism in responses to unfamiliar intruders in the tamarin, Saguinus oedipus

Aspects of social structure in group-living species can be inferred by observing the responses of individuals to unfamiliar animals. This study examined the responses of mated pairs of cotton-top tamarins (Saguinus oedipus oedipus) to presentation of either unfamiliar conspecifics or members of a related tamarin species, the saddle-back tamarin (Saguinus fuscicollis fuscicollis). Male and female responses to intruders differed: resident males threatened, displayed piloerection, approached, and attacked intruders, especially males, while resident females showed increases in suprapubic scentmarking in the presence of intruders. Both males and females discriminated between the species of intruders, exhibiting more threats, scent-marking, piloerection, and approaches in the presence of conspecific intruders. There are pronounced sex differences in the signals and behaviour patterns that are elicited in an aggressive or territorial encounter with unfamiliar conspecifics in this monogamous primate.     

Tamarins: Alpha female,queen bee or white rat?

The saddleback tamarin (Saguinus fuscicollis)combines a number of behavioral and physiological attributes which seem to violate “rules” of ethology. Of particular interest is the combination of facultative polyandry and high paternal investment. The social organization and breeding system of the tamarin also appear to combine reproductive restraint with an extremely high reproductive potential. These paradoxes may be resolved by noting that the combination of ecological circumstances and breeding systems has produced a species of limited genetic variability. Inclusive fitness is an important factor in situations of low genetic variability and may explain these apparent paradoxes.     

Seed dispersal by sympatric tamarins,Saguinus mystax and Saguinus fuscicollis: diversity and characteristics of plant species

In a comparative study of Saguinus mystax and Saguinus fuscicollis, we examined the spectrum of plant species whose seeds are dispersed by these two tamarin species. We characterize these plants in terms of life form, fruit colour, pulp consistency and seed dimensions. The tamarins disperse a much broader spectrum of plant species than previously reported (88 of the total of 155 species exploited for fruit). While the distribution over plant life form, fruit colour and pulp consistency is identical between dispersed plant species and the overall spectrum of consumed plant species, clear differences exist in all seed parameters (length, width, height, volume, mass) except specific weight between dispersed and non-dispersed plant species for both tamarin species. Plant and fruit characteristics and seed parameters of dispersed plant species do not differ between S. mystax and S. fuscicollis, suggesting that their ecological and evolutionary interaction with plants is very similar or identical.     

Patterns of range use,range defense,and intergroup spacing in moustached tamarin monkeys (Saguinus mystax)

In this paper we examine patterns of group spacing and habitat utilization in neighboring groups of marked free-ranging moustached tamarin monkeys (Saguinus mystax) inhabiting Padre Isla, a small island in the Amazon Basin of northeastern Peru, and describe the set of behavioral mechanisms used by tamarins to maintain the spatial isolation and social integrity of individual groups. Specifically, we address a series of questions regarding the importance of resource defense, mate defense, and territorial defense in intergroup interactions. From June through November 1990, we recorded 67 intergroup interactions involving members of our two main study groups. These interactions occurred at a rate of .14/observation hour and were of two general types. Vocal battles averaged 18 min in duration and were characterized by a series of high frequency, short syllable, long calls that were exchanged between groups separated by distances of greater than 25 m. Aggressive encounters averaged 26 min in duration and involved visual contact, alarm calls, scent marking, and sequences of chases and retreats. Intergroup confrontations did not cluster around the perimeter of a group's home range, and there was no evidence that moustached tamarins patrolled range borders. Our data indicate that 35% of aggressive encounters occurred in the vicinity of major feeding trees. Priority access to these sites is likely to have an important influence on tamarin foraging success. Mate defense and the exploration of new breeding opportunities also appear to be important functions of intergroup conflicts. Not only did the frequency of aggressive encounters increase during breeding periods, but three-fourths of all observed copulations occurred during or within 30 min of an encounter. Given the high degree of reproductive competition reported among tamarin females and the time and energy group members devote to intergroup aggression, maintaining access to a stable home range and the resources contained within that range appear to be critical functions of moustached tamarin social interactions.     

Races of the emperor tamarin,Saguinus imperator Goeldi (Callitrichidae,Primates)

The two described subspecies of the emperor tamarin,Saguinus imperator imperator Goeldi andSaguinus imperator subgrisescens Lönnberg are defined and compared, the geographic range of each plotted.     

The Evolutionary History and Genetic Diversity of Kinkajous, <Emphasis Type="Italic">Potos flavus</Emphasis> (Carnivora,Procyonidae)

The genus Potos (Procyonidae) is currently recognized as a monotypic genus comprising the single species Potos flavus, the kinkajou. Kinkajous are widely distributed throughout forested habitats of tropical Central and South America, extending from eastern Brazil across central Bolivia, eastern Peru, northern Ecuador, Guianas, Suriname, Venezuela, Colombia, and then through Central America and into western Mexico. The taxonomic history of the species is complex, with seven or eight subspecies historically recognized to acknowledge the phenotypic variation among populations. In this study, the systematics and the evolutionary history of Potos flavus were investigated based on the mitochondrial gene cytochrome b, including specimens from a large range of localities, covering most of the distribution of the species, from central Middle America (Costa Rica and Panama) through South America (Ecuador, Peru, Bolivia, Brazil, Guyana, and French Guiana). Analyses of 30 Potos flavus sequences showed 27 haplotypes that were grouped in five main clades in all phylogenetic analyses. These clades suggested a high geographic structure with specimens from (1) Costa Rica, (2) Guianas and North Brazil, (3) North Peru, (4) Ecuador and Panama, (5a) interfluves Branco-Negro rivers in the Brazilian Amazon, (5b) Eastern Atlantic Forest, (5c) Amazonian lowlands east Negro river including Bolivia, Peru, and West Brazil. Each of these clades differs from 4.5 % to 9.3 % in their genetic distance estimates, which suggests that the specific status of some of these lineages should be reconsidered. Divergence dating and biogeographic analysis suggested that crown Potos diversified in the Miocene-Pliocene in South America, and geographic barriers, such as savannas and rivers, may have played a significant role in the kinkajou diversification.