Foraging ecology and use of space in wild golden lion tamarins (Leontopithecus rosalia)

In this paper we describe the use of space and feeding ecology of seven groups of golden lion tamarins observed for a total of 2,164 hr in Poço das Antas Reserve, Rio de Janeiro, Brazil. Relative to habitat availability in the home ranges of these groups, lion tamarins spent more time than expected in relatively undisturbed swamp forests and less time than expected in more degraded hillside and pasture habitats. Home range area was correlated with group biomass but not group size. Golden lion tamarins fed primarily on fruits and small animal prey, but relied heavily on floral nectar during seasonal periods of relatively low fruit availability. Compared to other New World monkeys, lion tamarins used larger home range areas and exhibited longer daily path lengths than would be predicted by group biomass alone. We suggest that this pattern of foraging and use of space may be explained by the relatively greater availability of cryptic prey and their microhabitats in forests that are flooded and/or have closed canopies than in forests that are in earlier stages of succession where prey may be more susceptible to desiccation during the dry season. Am. J. Primatol. 41:289–305, 1997. © 1997 Wiley-Liss, Inc.     

Sources of variability in numbers of live births in wild golden lion tamarins (Leontopithecus rosalia)

We examined the effects of several variables on the number of live births in multiparous females in a wild population of golden lion tamarins (Leontopithecus rosalia). Independent variables included the number of infants born to a female the previous breeding season, the number of infants weaned the previous breeding season, the female's age and body mass, the number of adult males and helpers in the group, and the inbreeding coefficient of the offspring. We also tested the hypothesis that trapping and chemical immobilization during pregnancy affected the number of live births. Female body mass was the only statistically significant predictor of the number of live-born infants in the current season when both first and second peaks were included. Characteristics that predicted higher numbers of infants in the first peak of a season were the number of infants born the previous season and the body mass of the female. The greater the number of infants born the previous season, the greater the number of infants born in the first peak of the current season. Factors positively correlated with the number of live births in the second peak within a season included the number of infants born the previous season, as well as the number of available helpers. Due to sample size constraints, the analysis of litters in the second peak did not include body mass of the female as a variable. Inbreeding and handling did not affect the number of live births. We found no evidence that current reproduction negatively impacts future reproduction in this species. We also found no evidence for an age-related reduction in fertility.     

Provisioning in wild golden lion tamarins (Leontopithecus rosalia): benefits to omnivorous young

Provisioning may act to cushion weaned young from dietary insufficiencyand errors during the period in which they are mastering complexforaging techniques or learning to identify appropriate dietaryitems. That is, young mammals who receive food from others maygain nutritional and/or informational benefits. I conducteda longitudinal study of 13 wild golden lion tamarins 11–56weeks of age in six groups to evaluate hypotheses regardingthe functions of provisioning. All members belonging to thisprimate taxonomic family (the Callitrichidae) are cooperativebreeders and are known to provision their young more frequentlythan do other primate species, except humans. My results, togetherwith experimental findings, suggest that juveniles receive bothnutritional and informational benefits from being provisioned.My juvenile study subjects received animal prey (invertebratesand small vertebrates) from others more frequently than plantresources (fruits and hardened exudates). Apparently difficult-to-handlefruits were more likely to be transferred than readily processedfruits. These results support the nutritional benefits hypothesisbecause the young received items, particularly lipid- and protein-richprey, that they might not otherwise have acquired. That juvenilesfed independently on, and were provisioned with, the same fruitson the same day is counterevidence to the nutritional benefitshypothesis, however. The informational benefits hypothesis wassupported because juveniles received a large variety of foods(including more than 20% of fruit species eaten) and receiveduncommon fruits that were easily acquired. Adults emitted food-offeringcalls to encourage the transfer of prey to juveniles, particularlywhen the prey was whole and alive.     

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.     

Census and distribution of the golden lion tamarin (Leontopithecus rosalia)

During 1990–1992, a survey of the golden lion tamarin, Leontopithecus rosalia, was carried out throughout its known distribution area. Forest remnants were identified by visual interpretation of Landsat‐TM satellite images. Localities occupied by L. rosalia were first identified by interviews with local people. All forests more than 20 ha in size, and for which two or more interviews suggested the presence of the species, were surveyed using “play‐back” recordings of lion tamarin long calls. The total wild population of L. rosalia, including that of the Poço das Antas Biological Reserve, was estimated to be 562 individuals in 109 groups. The lion tamarins were generally found in four major areas of forest (six or more groups per forest, not including Poço das Antas), with a further 12 groups isolated in small forest patches. Currently the species' distribution is restricted to just four municipalities in the state of Rio de Janeiro: Silva Jardim, Cabo Frio, Saquarema, and Araruama. Although they are typically confined to lowland forest of <300 m altitude, L. rosalia was recorded at an altitude of 550 m in one locality. Average group size varied from 3.6 to 5.7 individuals, and densities from 0.39 groups/km² to 2.35 groups/km² (2.17 individuals/ km² to 8.53 individuals/km²). Six of the isolated groups found during the survey were successfully translocated to a forest of 2,400 ha. There is now also a significant population of reintroduced lion tamarins. Overall, however, the possibilities for further expansion of the wild population are severely limited. Am. J. Primatol. 59:29–44, 2003. © 2003 Wiley‐Liss, Inc.     

Phylogeny of lion tamarins (Leontopithecus spp) based on interphotoreceptor retinol binding protein intron sequences

The evolutionary relationships of the lion tamarins (Leontopithecus) were investigated using nuclear interphotoreceptor retinol binding protein (IRBP) intron sequences. Phylogenetic reconstructions strongly support the monophyly of the genus, and a sister relationship between the golden lion tamarin, Leontopithecus rosalia, and the black lion tamarin, L. chrysopygus, to the exclusion of the golden-headed lion tamarin, L. chrysomelas. The most parsimonious evolutionary reconstruction suggests that the ancestral lion tamarin and the common ancestor of L. rosalia and L. chrysopygus had predominantly black coats. This reconstruction is not consistent with a theory of orthogenetic evolution of coat color that was based on coat color evolution in marmosets and tamarins. An alternative reconstruction that is consistent with metachromism requires that ancestral lion tamarins had agouti hairs.     

Reproduction in captive lion tamarins (Leontopithecus): Seasonality,infant survival,and sex ratios

Diversity in reproductive and social systems characterizes the primate family Callitrichidae. This paper contributes to our appreciation of this diversity by presenting the first detailed comparative analysis of captive breeding in three species of lion tamarins (Leontopithecus chrysomelas, L. chrysopygus, and L. rosalia) housed at the Centro de Primatologia do Rio de Janeiro. The annual pattern of reproduction in all three species of Leontopithecus was markedly seasonal, with births occurring during the spring, summer, and fall months from August through March. While modal number of litters produced per female per year was 1, approximately 20% of breeding females produced two litters per year. The onset of breeding activity in years when two litters are produced was significantly earlier than in years when only one litter was produced. The cumulative number of offspring surviving to 3 months of age did not differ between years with one vs. two breeding attempts. Like other callitrichids, postnatal mortality was highest during the first week of life, and there were pronounced species differences in offspring survival through 1 year, with significantly lower survivorship in L. chrysomelas. Infant survivorship was affected by a number of experiential factors. Survivorship up to 30 days of life was higher in groups in which the breeding female had previous experience with infants as a nonbreeding helper than in groups in which the female lacked previous helping experience. Likewise, survivorship to 30 days of life was higher for infants born to multiparous females than for infants born to primiparous females. When parity and previous helping experience were analyzed concurrently, the lowest survivorship was associated with offspring produced by inexperienced primiparous females. Genus-wide, there was no significant departure from a 50:50 sex ratio at any point during the first year of life, nor was there evidence for differential mortality for male and female infants. However, L. chrysopygus produced significantly more male infants at birth (65:44) and had male-biased litters (approximately 60% males) throughout the first year of life, while L. chrysomelas showed a nonsignificant tendency toward female-biased litters. © 1996 Wiley-Liss, Inc.     

Acoustic structure of long calls in free-ranging groups of golden lion tarnarins,Leontopithecus rosalia

Like many other callitrichids, golden lion tamarins, Leontopithecus rosalia, emit Long Calls. Recordings of four free-ranging groups were made to explore different types of Long Calls. Three Long Call types were identified acoustically, and analyzed sonographically. The calls usually started with an Introductory Syllable (a chirp, a trill, or a whine) which was followed by either one, two, or three different phrases in a fixed sequential order. Each of the three phrases was unique and contained a typical number of syllables of characteristic shape, frequencies, and durations. Possible functions of these calls are discussed. © 1994 Wiley-Liss, Inc.     

Immigration in wild groups of golden lion tamarins (Leontopithecus rosalia)

Seventeen territorial groups of wild golden lion tamarins were monitored for periods of 10–76 months. Immigration into established groups was rare (0.48 immigrating individuals per group per year) and occurred mostly in the context of replacement of breeding individuals. Nonreplacement immigration events usually occurred in conjunction with some other change in group composition (e.g., an emigration or another immigration). Aggression by resident tamarins toward potential immigrants appeared to be the proximate factor limiting movement into groups. Most such aggression was intrasexual, but potential female immigrants were sometimes chased by male as well as female residents. Immigration was highly male biased (85% of individuals). Factors possibly contributing to this bias were inheritance of breeding positions by adult daughters (reducing female and increasing male immigration opportunities), ability of males but not females to join groups already containing a same-sex breeding individual, and the fact that potential female immigrants appeared to face some intersexual as well as intrasexual aggression. Male and female roles in the maintenance of a monogynous mating system are considered in light of these results. Contrasts with data from intruder studies on captive golden lion tamarins [French & Inglett, Animal Behaviour 37:487–497, 1989] are discussed. © 1996 Wiley-Liss, Inc.     

Characteristics of reproductive biology and proximate factors regulating seasonal breeding in captive golden-headed lion tamarins (Leontopithecus chrysomelas)

Reproduction is highly demanding in terms of energy expenditure, and the costs and benefits associated with postponing or investing in a reproductive effort are crucial determinants of an individual's fitness. Understanding the reproductive potential of a species under varying ecological conditions offers important insights into the dynamics of its social system. This study provides the first detailed analysis of the reproductive potential of wild- and captive-born golden-headed lion tamarins (Leontopithecus chrysomelas) under captive conditions, based on studbook data compiled during 1984-2000. Litters produced by wild-born females breeding in captivity are similar in size to litters observed in the wild, but smaller than litters of captive-born females. The more stringent ecological conditions experienced by wild-born females during maturation may result in a lifelong effect on litter size. However, interbirth intervals are shorter for wild-born than captive-born females. The relatively smaller burden of infant care that results from having smaller litters may allow wild-born females to sustain the next pregnancy sooner. Reproduction in the Brazilian captive population is highly seasonal for both wild-born females and females born in captivity in Brazil. Changes in photoperiod over a year provide a proximate explanation for changes in the proportion of conceptions and births per month. Outside Brazil, breeding occurs year-round, and no clear birth peak is apparent. Information from field reports that could be used to relate this finding to ecological factors, such as resource availability, is unavailable.     

Food transfers in wild and reintroduced golden lion tamarins,Leontopithecus rosalia

We collected data from wild and reintroduced golden lion tamarins (Leontopithecus rosalia) to describe the behavior of donor and recipient during food transfers, evaluate the effect of supplemental feeding on food transfer behavior, and examine various hypotheses concerning the function of food transfers in primates. Behavioral observations were conducted on 12 groups of tamarins with young (N = 30) between the ages of 1 week and 1 year old. Results show that food transfers involve various behaviors, from steals by recipients to offers by donors; transfers mostly derive from adults and are directed at immature weaned young (between 3 and 9 months old); and that most items transferred were prey or fruits that require skill to process. Eleven percent of food transfers were preceded by an adult vocalization specific to that context, whereas 86% were preceded by conspicuous infant vocalizations and begging behavior. The most common vocalizations were loud and atonal (rasps) and broad banded frequency modulated (trills). Infants born to reintroduced parents vocalized less, whereas reintroduced adults vocalized more before transferring food than their wild counterparts. Reintroduced adults and young received more food transfers (4.4 per hr) than did wild‐born adults and young (2.2 per hr). Our findings suggest that food transfer in golden lion tamarins is best understood as provisioning of young that have not fully developed foraging skills to ensure they get the necessary resources for growth and survival. Am. J. Primatol. 48:305–320, 1999. © 1999 Wiley‐Liss, Inc.     

Diet of Pacific sleeper shark, a potential Steller sea lion predator, in the north-east Pacific Ocean

Pacific sleeper sharks Somniosus pacificus were captured near Steller sea lion Eumetopias jubatus rookeries during the period when Steller sea lion pups are most vulnerable to Pacific sleeper shark predation (first water entrance and weaning). Analysis of stomach contents revealed that teleosts were the dominant prey in August and cephalopods were the dominant prey in May ( n = 198). Marine mammals were found in 15% of stomachs regardless of season, but no Steller sea lion tissues were detected. Molecular genetic analysis identified grey whale Eschrichtius robustus and harbour seal Phoca vitulina remains in some Pacific sleeper shark stomachs. Most mammals were cetacean and at least 70% of the cetaceans were probably scavenged. Although Pacific sleeper shark and Steller sea lion ranges overlapped, so predation could potentially occur, the diet study suggested that predation on Steller sea lions is unlikely, at least when pups first enter the water or during weaning. Harbour seals were infrequent prey and may have been consumed alive. Pacific sleeper sharks consume fast-swimming prey like Pacific salmon Oncorhynchus sp., most likely live animals rather than scavenged animals. Pacific sleeper sharks appeared to be opportunistic consumers of the available prey and carrion, feeding both on the bottom and in the water column, and their diet shifted to teleosts and cetacean carrion as the fish grew larger.     

Optimal foraging theory predicts effects of environmental enrichment in a group of adult golden lion tamarins

The success of environmental enrichment programs in effecting specific changes in the behavior of captive animals has not always been uniform. Separate studies demonstrated both an increase in food competition and a decrease in food competition among captive group-living primates upon introduction of foraging devices. The objectives of this study were to measure the effects of variation in resource distribution and availability on food competition in a group of captive adult golden lion tamarins (Leontopithecus rosalia). The resource variables chosen were suggested from optimal foraging theory. The energy invested to obtain an item influenced food transfer and aggressive behaviors while food abundance did not. All individuals obtained an equivalent number of items over the course of the experiment from the foraging device, even though some tamarins obtained most of their food rewards directly from the device while others received their food rewards primarily through food transfer from other group members. Because the monkeys appeared highly motivated to obtain food from the test apparatus and did not habituate to it, the foraging device used in this experiment could be used as regular environmental enrichment for golden lion tamarins. One way to circumvent potentially unacceptable rates of aggression, with this or any feeding protocol that increases foraging task complexity and search time, may be to provide more than one foraging device per group. Zoo Biol 17:231–244, 1998. © 1998 Wiley-Liss, Inc.     

西双版纳尚勇亚洲象的食物组成与取食生态

于1998—2000在西双版纳国家级自然保护区尚勇子保护区的自然生境中,通过对亚洲象取食植物调查和粪便分析,了解亚洲象的食物组成与取食习性。结果显示,野外跟踪调查共记录有106种植物被亚洲象所取食。其中有83种出现在象的粪便中,这些种类分别属于：禾本科8种（10．0％）、桑科7种（9．9％）、蝶形花科4种（8．4％）、五加科3种（6．6％）、葡萄科3种（5．7％）、夹竹桃科3种（4．6％）、芭蕉科1种（4．2％）、姜科3种（3．7％）、紫金牛科3种（3．6％）、蔷薇科3种（3．6％）、大戟科5种（3．3％）、榆科2种（3．O％）、含羞草科4种（2．9％）13个植物科。根据食物中所占的比率,桑科的榕属（Ficus）、禾本科的竹类（Bambusoideae）、小果野芭蕉（Musa acuminate）和莠竹（Microstegium ciliatum）是亚洲象的主要食物资源。在觅食过程中,亚洲象取食包括乔木、藤本灌木和草本等各种生活型的植物,其中先锋种所占比率（59％）高于后续种;选择性啃食枝条的植物种类（77种）高于牧草式取食的种类（6种）。亚洲象取食植物种类的月变化与月平均温度和月降雨量成负相关,旱季取食植物种类高于雨季。本研究对制定保护区野生动物管理策略,以及解决保护区周边日趋恶化的人象矛盾,具有一定的参考价值。     

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.