Reproduction of the emperor tamarin (Saguinus imperator) in captivity,with comparisons to cotton-top and golden lion tamarins

Little information has been published on the reproductive biology and behavior of the emperor tamarin (Saguinus imperator). We analyzed twelve years of data on emperor tamarins at the Los Angeles Zoo and made comparisons with data on cotton-top tamarins (Saguinus o. oedipus) and golden lion tamarins (Leontopithecus rosalia) from the same collection. Secondary sex ratios did not differ significantly from 50:50. Births were not strictly seasonal for any species. The number of infants reared had a significant effect on interbirth interval for all species, with shorter intervals when only one or no infants were reared, but females did sometimes conceive early in lactation. In emperor tamarin families, all fathers and most older siblings carried new infants, usually beginning within a few days after a birth. Previous exposure to younger siblings did not appear to be critical to the development of competent parental behavior by zooborn emperor tamarin females.     

Disseminated lethal Encephalitozoon cuniculi (genotype III) infections in cotton-top tamarins (Oedipomidas oedipus)--a case report

For the first time, Encephalitozoon (E.) cuniculi genotype III ('dog strain') was verified in two cotton-top tamarins (Oedipomidas oedipus) by light microscopy, immunohistochemistry, electron microscopy, PCR and sequencing. The animals had a disseminated lethal infection with this protist. In earlier reports, genotype III had been found only in domestic dogs, man, emperor tamarins (Saguinus imperator) and golden lion tamarins (Leontopithecus rosalia). This investigation establishes now that the 'dog strain' can occur in cotton-top tamarins too. This is further evidence for the zoonotic potential of E. cuniculi. Furthermore, free E. cuniculi spores were identified also in blood vessels of several tissues. These findings indicate that during a disseminated infection E. cuniculi spores can occur in peripheral blood, too. We propose that blood should also be included in the investigations for the detection of microsporidia, so that a possible disseminated course of an infection can be detected.     

Social behavior of the emperor tamarin in captivity: Components of agonistic display and the agonistic network

Agonistic behavior was studied longitudinally for 16 months in an intact family groups of captive emperor tamarins (Saguinus imperator subgrisescens) using methods from quantitative ethology and social network analysis. A motivational analysis of the components of agonistic display revealed the relative strength of each component along a continuum from strongly dominant to strongly subordinate. Tabulations of exchanges of strongly dominant and strongly subordinate components in interactions among the tamarins revealed an agonistic network (“dominance hierarchy”) that approached, but did not quite reach, the ideal state of a transitive order (“linear dominance hierarchy”). The frequency with which individual tamarins long called and scent marked was not closely correlated with their position (“dominance rank”) in the agonistic network. Instead, individuals undergoing change in status long called and scent marked frequently, irrespective of their rank.     

Birth seasonality in cotton-top tamarins (saguinus oedipus) despite constant food supply and body weight

Goldizen et al. (1988) reported that wild saddle-back tamarins (Saguinus fuscicollis, Callitrichidae) show birth seasonality that is correlated with food supply and body weight. They suggested a sequence of ultimate causality in which shortage of food leads to reduced body weight which leads to timing of weaning and lactation when resources are more abundant. Cotton-top tamarins in captivity show birth seasonality despite constant food supply and body weight. Although natural availability of fruit and insects (which are key foods for tamarins) is related to rainfall, birth seasonality and body weight in captive cotton-top tamarins are unrelated to rainfall. The most likely proximate mechanism for seasonality of births in tamarins is photo-period, given existing data on populations living in natural and artificial lighting.     

Overt fatal and chronic subclinical Encephalitozoon cuniculi microsporidiosis in a colony of captive emperor tamarins (Saguinus imperator)

The course of an infection with the microsporidian Encephalitozoon cuniculi in a colony of captive emperor tamarins (Saguinus imperator) is described. In two litters, the infection was associated with overt disease and death of all infants. Immunohistochemistry for E. cuniculi showed generalized infections, and histopathologic evaluation revealed systemic vasculitis and disseminated mixed inflammatory cell infiltration with and without necrosis in several organs. Serologically, some of the juvenile animals presented with high titres for Encephalitozoon, while the adults had low titres. The E. cuniculi "dog strain" was identified by molecular means for the first time in Europe. The origin of the infection appeared to be a pair of breeding adults that originated from the US. Our data suggest that the organism persisted over years in the colony, and that subclinically infected animals most likely were involved in perpetuating the infection. Efforts should be made to ascertain if this microorganism is present in other captive populations of this endangered monkey species and to prevent its further spreading.     

Experimental field study of the relative costs and benefits to wild tamarins (Saguinus imperator and S. fuscicollis) of exploiting contestable food patches as single- and mixed-species troops

Several species of tamarins form stable mixed-species troops in which groups of each species feed, forage, rest, and travel together during much of the year. Although the precise set of factors that facilitate this ecological relationship remains unclear, predator detection and foraging benefits are presumed to play a critical role in maintaining troop stability. In this work we present data from an experimental field study designed to examine how factors such as social dominance and within-patch foraging decisions affect the costs and benefits to tamarins of visiting feeding sites as single- and mixed-species troops. Our data indicate that when they exploited contestable food patches (sets of eight feeding platforms, two of which contained a 100-g banana), each tamarin species experienced foraging costs when they arrived as part of a mixed-species troop. These costs were found to be less severe for emperor tamarins because they were socially dominant to saddle-back tamarins and could displace them at feeding sites. We conclude that the foraging benefits to tamarins residing in mixed-species troops are asymmetrical, and that at feeding sites in which the amount of food in a patch is insufficient to satiate all troop members, even minor differences in the timing of return to food patches and changes in troop cohesion have a measurable effect on the costs and benefits to participating tamarin species.     

Infant carrying in family groups of goeldi's monkeys (Callimico goeldii)

Goeldi's monkey (Callimico goeldii) is closely related to marmosets and tamarins. Like marmosets and tamarins, C. goeldii lives in family groups, and fathers and older offspring (helpers) participate in infant carrying. In contrast to the typical twin births in marmosets and tamarins, C. goeldii has only single offspring, and paternal carrying is delayed. We studied infant carrying following 26 births in eight groups of C. goeldii, testing hypotheses proposed in the literature on infant carrying in marmosets and tamarins. The infant was carried exclusively by the mother for the first 26.3 days after birth. Afterwards other group members participated in infant carrying. Whereas the C. goeldii mother is always the main carrier, the father does not always carry more than helpers. In contrast to other callitrichids, age and sex of sibling helpers was not found to have an effect on the participation in infant carrying. The participation in infant carrying in Callimico indicated intraindividual consistency, i.e., the amount of infant carrying performed by fathers and helpers following one birth correlated significantly with the amount of infant carrying of the same individuals following the next birth. We found a significant negative correlation between parental infant carrying and group size, indicating that helpers really do help, sharing the carrying burden with their parents. This is attributed to a clear trend for a reduction in maternal carrying in the presence of helpers, whereas fathers did not benefit from helpers. We conclude that the infant-carrying pattern in C. goeldii is different from the infant-carrying pattern in marmosets and tamarins. The main differences were that the mother instead of the father is the main carrier, and that there is a clear time delay between infant birth and when the father and helpers participate in infant carrying.     

Predation risk and the interspecific association of two Brazilian Atlantic forest primates in Cabruca agroforest

Forming interspecific associations is one of many strategies adopted by primates in order to avoid predation. In addition to improved predator detection and avoidance, benefits of interspecific associations relate to improved foraging efficiency. In this study we tested these two hypotheses explaining associations between the endangered golden-headed lion tamarin, Leontopithecus chrysomelas and the sympatric Wied's marmoset, Callithrix kuhlii. We estimated predation risk by recording the number of encounters between lion tamarins and potential predators in cabruca agroforest (shaded cacao plantation) and in mosaic forest (a mix of cabruca, primary and secondary forest). To evaluate if the association between the two species was related to foraging benefits we recorded the number of associations between the two species when the lion tamarins were eating and when they were not eating. To test if the association occurred to improve predator detection and avoidance, we evaluated if associations between the species were more frequent in areas with higher predation risk and during the part of the day when predation risk is higher. We also compared the number of associations 3 months before birth events and 3 months after, when the lion tamarins are more susceptible to predation. Predation risk, mainly by raptors, was significantly higher in cabruca than in mosaic forest (0.17 and 0.05 encounters with predators per hour of observation, respectively). Associations were significantly more frequent after birth events and during the part of the day when predation risk was also higher (5-6 am until noon). We did not observe any direct evidence of foraging-related advantages of interspecific associations for the lion tamarins. The tamarins did not associate more when they were foraging. Our findings suggest that lion tamarins are more exposed to predation in cabruca than in mosaic forest and associations between lion tamarins and Wied's marmosets are related to predation avoidance.     

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.     

Mating patterns in the golden lion tamarin (Leontopithecus rosalia): continuous receptivity and concealed estrus

Sociosexual behavior was monitored on a daily basis for 3 months in 5 pairs of golden lion tamarins (Leontopithecus rosalia). Urine samples were collected daily from each female and urinary estrogen cycles were determined by radioimmunoassay. Mounts and copulations were observed during all phases of the estrogen cycle. Peaks or regular cycles in sexual behavior were not documented. There were no significant changes in affiliative behavior by females or males that were associated with changes in urinary estrogen values. A negative relationship between pair bond duration and frequency of sexual interactions was observed: newly established pairs exhibited 2-6 times more frequent sexual behavior than a long-established pair. The lack of a conspicuous sexual signal in female golden lion tamarins may be related to a pattern of continuous sexual receptivity. Both reproductive patterns, concealed estrus and continuous receptivity, are explicable in relation to either monogamous or polyandrous mating systems.     

A comparison of diamino- and diamidocarbenes toward dimerization

In this study, we compare the dimerization of N,N’-diamidocarbene with that of N-heterocyclic carbene (NHC). Less interaction occurred between the filled lone pair of nitrogen and the unfilled lone pair of the carbenic center for a N,N’-diamdiocarbene than did in a saturated NHC because of the resonance between the lone pair of nitrogen and a carbonyl group. Therefore, a N,N’-diamidocarbene exhibits less singlet-triplet splitting. The less singlet-triplet splitting in a heterocyclic carbene containing nitrogen, the more exothermic the dimerization, which is consistent with the conclusion of Thiel et al. (Chem Phys Lett 217:11–16, 1994).

Breeding of the cotton-top tamarin Saguinus oedipus oedipus: A comparison with the common marmoset

A colony experienced in the successful breeding of thecommon marmoset acquired 15 cotton-top tamarins for breeding purposes over a period of 2 yrs. Data are presented on the breeding of the cotton-top and compared with the breeding of the common marmoset. The tamarins did not breed as successfully as the common marmosets. There were several reasons for this: Cotton-tops took longer to produce young on initial pairing, had a longer birth interval, and showed a high incidence of suspected infanticide and parental neglect. These factors are thought to be largely responsible for the relatively low reproductive potential of the cotton-top in captivity.     

A multiyear survey of helminths from wild saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins

The establishment of baseline data on parasites from wild primates is essential to understand how changes in habitat or climatic disturbances will impact parasite–host relationships. In nature, multiparasitic infections of primates usually fluctuate temporally and seasonally, implying that the acquisition of reliable data must occur over time. Individual parasite infection data from two wild populations of New World primates, the saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarin, were collected over 3 years to establish baseline levels of helminth prevalence and parasite species richness (PSR). Secondarily, we explored variation in parasite prevalence across age and sex classes, test nonrandom associations of parasite co‐occurrence, and assess the relationship between group size and PSR. From 288 fecal samples across 105 individuals (71 saddleback and 34 emperor tamarins), 10 parasite taxa were identified by light microscopy following centrifugation and ethyl‐acetate sedimentation. Of these taxa, none were host‐specific, Dicrocoeliidae and Cestoda prevalences differed between host species, Prosthenorchis and Strongylida were the most prevalent. Host age was positively associated with Prosthenorchis ova and filariform larva, but negatively with cestode and the Rhabditoidea ova. We detected no differences between expected and observed levels of co‐infection, nor between group size and parasite species richness over 30 group‐years. Logistic models of individual infection status did not identify a sex bias; however, age and species predicted the presence of four and three parasite taxa, respectively, with saddleback tamarins exhibiting higher PSR. Now that we have reliable baseline data for future monitoring of these populations, next steps involve the molecular characterization of these parasites, and exploration of linkages with health parameters.     

Behavioral effects of introducing pied tamarin (Saguinus bicolor) to black howler monkey (Alouatta caraya) and white-faced saki (Pithecia pithecia) in a zoological park

Mixed-species primate exhibits are becoming more common in zoological parks as a means to display a diverse array of animals both more naturalistically and with more economy of space. Here, we describe behavioral changes during the introduction process of a pair of pied tamarins (Saguinus bicolor) to an established group of black howler monkeys (Allouatta caraya) and white-faced saki monkeys (Pithecia pithecia). Data were collected during six phases, representing introductions among the various species and to exhibit space and off-exhibit holding. The pied tamarins were consistently the most active of the three species. Although activity levels of the howler and saki monkeys remained constant throughout, that of the tamarins declined as the introduction progressed. Several episodes of aggression between the tamarins and the sakis were observed, but did not coincide with patterns predicted by previous intra-specific introductions. The three-species mix remained stable for several months; however, escalating aggression ultimately led to the removal of the sakis from the mixed-species exhibit. Despite our mixed results, we contend that only through continued trials, coupled with careful and systematic monitoring, can we ultimately identify stable mixes of species.     

Correlates of molt in golden lion tamarins (Leontopithecus rosalia)

In this paper we describe the timing and correlates of molt for a native population of golden lion tamarins (Leontopithecus rosalia). We conducted 820 examinations of 267 adult tamarins over a 7.75 year period to determine the annual molting cycle in this population. Dorsal molt was an annual event for most individuals in the study population; however, 10% of sampled individuals apparently molted twice in a 12 month period. Duration of molt was estimated at 5–6 weeks. The proportion of samples in which tamarins were in molt was significantly greater during the wet season than the dry season and positively correlated with mean monthly precipitation and minimum temperature but not tamarin births, suggesting an environmental component to timing of molt. We found no sex differences in the occurrence of molt during wet or dry seasons. However, the relative frequency of samples in molt was significantly less for gravid females than for nongravid females. In four polygynous groups, socially dominant females gave birth before subordinate females, and younger reproductive females completed molt before older reproductive females. © 1995 Wiley-Liss, Inc.     

The formation of a new gibbon group

Families of gibbons and siamang were studied in lowland dipterocarp forest at Kuala Lompat, Pahang, Malaysia between January and July 1973. In April a lone male gibbon (who had previously been a frequent associate of a lone male siamang) attracted a female gibbon and the two animals called together in chorus. The new pair were immediately attacked and separated by a long-established neighbouring family of gibbons. Four days later the new pair reformed and despite further fierce attacks from their neighbours remained together and gradually established their own territory. The lone siamang also attracted a female into his range. The new siamang pair stayed together for most of four days but eventually the female left his range and did not return. Generalisations are made concerning the way that new hylobatid groups become establilished.     

Do female tamarins use visual cues to detect fruit rewards more successfully than do males?

Primates are unique among eutherian mammals for possessing trichromatic colour vision. It is generally proposed that trichromacy evolved to aid detection of ripe fruits against mature foliage. However, while trichromacy is routine in all Old World monkeys and apes (the catarrhines), a cone opsin polymorphism in New World monkeys (the platyrrhines) results in foraging groups with mixed capacities for chromatic distinction. Although 50-66% of female platyrrhines are trichromatic, all males are dichromatic. Here, we test the hypothesis that trichromatic platyrrhines use visual cues to detect fruit rewards more successfully than do males. Specifically, we ask whether female emperor tamarins, Saguinus imperator imperator, and saddleback tamarins, S. fuscicollis weddelli, are the first members of their foraging group to locate food patches; and, furthermore, whether they are more successful than males in using colour, shape and size cues to discriminate between sham and reward feeding sites. Our results show that females and males do not differ in their ability to locate or discriminate between feeding sites. We conclude that trichromatic vision in female tamarins does not confer an advantage for detecting yellow fruit rewards against mature foliage. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Spontaneous tool use in captive, free-ranging golden lion tamarins (Leontopithecus rosalia rosalia)

Two types of tool use were observed in eight captive, free-ranging golden lion tamarins (Leontopithecus rosalia rosalia). All eight individuals used twigs and/or radio collar antennae to pry bark from trees and probe crevices, presumably for invertebrates. Three individuals used tools for grooming. In two animals, antennae were used as grooming tools while the third individual used a stick while grooming. The complexity of the free-ranging environment may have played a role in the expression of tool use behavior in these animals, as tool use has never been observed in captive tamarins living in traditional enclosures or wild tamarins. Social transmission may be one of the mechanisms responsible for the acquisition of tool use — six of the eight tool users resided in two social groups, and the only two individuals that used antennae as grooming tools were a bonded pair. These are the first published observations of tool use by golden lion tamarins or any callitrichid in a non-experimental setting and provide further data supporting the theory of a link between extractive foraging and tool use.     

Investigation of Beckett–Casy model 3: Synthesis of novel naltrexone derivatives with contracted and expanded D-rings and their pharmacology

Novel naltrexone derivatives 7 and 8 with contracted and expanded D-rings were synthesized to investigate the importance of orientation of lone electron pair on the nitrogen for binding abilities to the opioid receptor. Compound 7 showed almost no binding affinity, whereas compound 8 was comparable to naltrexone (6) in binding affinity. Conformational analyses and NOE experiments in D₂O of compounds 6–8 suggested that the lone electron pairs of compounds 6 and 8 with respective six- and seven-membered D-rings would project in the pseudo-axial orientation, whereas compound 7 with five-membered D-ring would have the lone electron pair directing in pseudo-equatorial position. These results strongly supported the proposal that the axial orientation of the lone electron pair on nitrogen would provide sufficient binding abilities to the opioid receptor and that the 15–16 ethylene moiety in the morphine structure would play a role in fixation of the lone electron pair in the axial direction rather than interaction with the putative cavity in the Beckett–Casy model.     

A quantum chemistry evaluation of the stereochemical activity of the lone pair in Pb<Superscript>II</Superscript> complexes with sequestering ligands

The stereochemical activity of the lone pair on Pb^II complexes is assessed using several theoretical methods, including structural analyses, computations of Fukui functions, natural bond orbitals, electron localization function, investigation of the electron density and of its laplacian. The attention is focused on four octadentate N-carbamoylmethyl-substituted tetraazamacrocycles of various ring sizes ranging from 8 to 14 atoms associated with the Pb^II cation. The theoretical study illustrates the geometrical constraints imposed by the ring structure which limits the spatial development of the lone pair but without fully preventing it. For a given coordination number, the lone pair activity is strongly correlated to the geometry of the ligand and in particular to the size of the cage that the ligand forms around the Pb^II cation. Some limitations of the theoretical tools used are also evidenced, among them the necessity to sample around a critical point instead of just analyzing its nature. In the case of the laplacian of the electron density, a visualization method is introduced to moderate the results based only on the nature of a critical point. These limitations should also be related to the difficulty to extend the lone pair concept for the heaviest atoms of the classification.