The Equivocal Relationship Between Territoriality and Scent Marking in Wild Saddleback Tamarins (<Emphasis Type="Italic">Saguinus fuscicollis</Emphasis>)

Researchers have often assumed that scent marking serves a territorial function in callitrichines, although some controversy exists. To fulfill such a function, scent marks should 1) prevent intrusions, 2) ensure access to feeding resources, 3) enable avoidance of intergroup encounters, or 4) play an important role in the aggressive encounters between groups. We studied 13 saddleback tamarins (Saguinus fuscicollis) belonging to 3 free-ranging groups, which formed mixed-species troops with moustached tamarins (S. mystax) in the Amazonian rain forest of Peru. None of the predictions were confirmed. The tamarins used a border-marking strategy, marking more on the periphery of their territory. However, feeding trees in overlap and encounter areas received more scent marking but were still visited by neighboring groups. Intergroup encounters occurred more often than expected, and scent-marking frequency was not higher during them than when no other group was present. It appears that instead of defending a territory in the classic sense, the tamarins are optimizing signal transmission by depositing their scents where the probability of detection by neighbors is higher. Saddleback tamarins may use shared areas of their home ranges to exchange information with neighboring groups, perhaps regarding reproductive opportunities.     

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.     

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.     

Diet, foraging, and use of space in wild golden-headed lion tamarins

Lion tamarins (Callitrichidae: Leontopithecus) are small frugi-faunivores that defend large home ranges. We describe results from the first long-term investigation of wild golden-headed lion tamarins (L. chrysomelas; GHLTs). We present data about activity budgets, daily activity cycles, diet, daily path length, home range size, home range overlap, and territorial encounters for three groups of GHLTs that were studied for 1.5-2.5 years in Una Biological Reserve, Bahia State, Brazil, an area characterized by aseasonal rainfall. We compare our results to those from other studies of lion tamarins to identify factors that may influence foraging and ranging patterns in this genus. Ripe fruit, nectar, insects, and small vertebrates were the primary components of the GHLT diet, and gums were rarely eaten. Fruit comprised the majority of plant feeding bouts, and the GHLTs ate at least 79 different species of plants from 32 families. The most common foraging sites for animal prey were epiphytic bromeliads. The GHLTs defended large home ranges averaging 123 ha, but showed strong affinities for core areas, spending 50% of their time in approximately 11% of their home range. Encounters with neighboring groups averaged two encounters every 9 days, and they were always aggressive. Data about time budgets and daily activity cycles reveal that the GHLTs spent most of their time foraging for resources or traveling between foraging sites distributed throughout their home ranges. The GHLTs spent much less time consuming exudates compared to lion tamarins in more seasonal environments. Additionally, the GHLTs had much larger home ranges than golden lion tamarins (L. rosalia), and did not engage in territorial encounters as frequently as L. rosalia. GHLT ranging patterns appear to be strongly influenced by resource acquisition and, to a lesser extent, by resource defense.     

Social and seasonal influences on reproductive biology in male moustached tamarins (Saguinus mystax)

In several primate taxa there is evidence that the social and physical environment can exert a significant effect on reproductive behavior and biology. In this paper we examine social and physiological factors influencing group composition and reproduction in free-ranging moustached tamarin monkeys (Saguinus mystax mystax). This species is characterized by cooperative care of the young and a breeding system that includes both polyandrous and polygyandrous matings. Body measurements collected on adult males residing in multimale groups indicate marked within-group differences in testes volume. In 12 of 17 groups examined, testes volume of at least two resident adult males differed by 21–174%. Among these males, testes volume was not correlated with either body weight or adult age class. We also examine whether factors such as time of year had an effect on reproductive condition. An analysis of body measurements of 128 adult male and 127 adult female moustached tamarins, wild-trapped and released in northeastern Peru, indicates cyclic changes in genital size. For males, mean monthly testes volume in July (712 mm³) was twice that recorded in June (351 mm³). Females exhibited a similar pattern. Although endocrine information on intra- and intersexual social effects on fertility are unavailable for S. mystax, given the high degree of social cooperation and lack of overt aggression among adult male group members, we offer the possibility that resident male moustached tamarins compete for access to the groups' lone breeding female through socially induced reproductive suppression and sperm competition. © 1996 Wiley-Liss, Inc.     

Spatial patterns of scent marking in wild moustached tamarins, Saguinus mystax: no evidence for a territorial function

I investigated whether scent marking has a territorial function in wild moustached tamarins. I examined the spatial distribution of scent marking within the home ranges of four groups of this neotropical primate and tested predictions from Gorman & Mills' (1984, Journal of Zoology,202, 535-547) model for border and 'hinterland' marking. Although home ranges were economically defensible, no evidence was found for increased marking along the territorial boundary or in areas of home range overlap, but there was also no evidence for hinterland marking. Observed distributions of scent marking in exclusively used and overlapping areas of the home range did not deviate from distributions that would be expected if scent marking occurred at random (expectation based both on size of area and on frequency of quadrat occupation), and there was a strong correlation between frequency of quadrat occupation and frequency of scent marking per quadrat. These results indicate that scent marking has no territorial function in moustached tamarins. This is in line with mainly qualitative findings from the majority of other studies on wild marmosets and tamarins. These and other findings on scent marking in moustached tamarins suggest that this behaviour functions mainly in intersexual communication. Copyright 2000 The Association for the Study of Animal Behaviour.     

Social behavior of wild moustached tamarins,Saguinus mystax,at the Estación Biológica Quebrada Blanco,Peruvian Amazonia

The social behavior in two small, polyandrous groups of moustached tamarins, Saguinus mystax, was studied at the Estación Biológica Quebrada Blanco in northeastern Peru. Allogrooming was the most obvious type of social interaction. Grooming relations were characterized by a strong asymmetry. In both groups, one adult male contributed about 70% of all allogrooming given (in terms of time spent grooming) and allocated his allogrooming evenly to all other group members. Grooming relations between the second adult male and other group members were less intensive. Intragroup agonistic interactions were infrequent, and most of them occurred in the context of feeding on small food resources (fruit, exudate) and during intergroup encounters. Sexual behavior was rare, but at least in one group a tendency existed for the principal groomer to be somewhat more active than the other male. Results are compared with data from other field studies on callitrichid social behavior. Although the label polyandrous correctly describes the demographic structure of many groups, it is not clear whether it is sufficient for understanding the patterning of social relations and thus the social organization of tamarins. © 1996 Wiley-Liss, Inc.     

Aggressive intergroup encounters in two populations of Japanese macaques (Macaca fuscata)

It is predicted that variation in intergroup relationships in group living primates reflects the cost and benefit of resource defense. We tested the applicability of the model by examining population difference, group difference, and seasonal difference in behaviors during intergroup encounters in two populations of Japanese macaques (Macaca fuscata), one of six groups from Yakushima Island, and the other of three groups from Kinkazan Island. We found that the nature of intergroup encounter varied with group identity, reproductive seasonality, and population. Yakushima groups showed aggressive behaviors more frequently than did Kinkazan groups and the difference was consistent with the food competition model, both because of the involvement of females, and because home ranges were smaller on Yakushima than on Kinkazan, and thus more defensive. Both sexes of animals participated in aggressive interactions, but males were more aggressive than females. Furthermore, Yakushima population showed more agonistic intergroup behaviors during the mating season than the non-mating season. Also during the encounters, intergroup mating was observed, but only in Yakushima. It is concluded that intergroup relationships reflect the mate guarding behavior by group males. However, the agonistic relationship during non-mating season, especially that of among females, is also consistent with the food competition model. It is also noted that males' behavior toward other groups can also be interpreted as a form of investigative behavior before possible transfer into a new group.     

Characterization and Social Correlates of Fecal Testosterone and Cortisol Excretion in Wild Male <Emphasis Type="Italic">Saguinus mystax</Emphasis>

Reproductive success in male primates can be influenced by testosterone (T) and cortisol (C). We examined them in wild Saguinus mystax via fecal hormone analysis. Firstly, we wanted to characterize male hormonal status over the course of the year. Further we tested the influence of the reproductive status of the breeding female, social instability, and intergroup encounter rates on T levels, comparing the results with predictions of the challenge hypothesis (Wingfield et al., 1990). We also tested for interindividual differences in hormonal levels, possibly related to social or breeding status. We collected data during a 12-mo study on 2 groups of moustached tamarins at the Estación Biológica Quebrada Blanco in northeastern Peru. We found fairly similar T and C levels over the course of the year for all males. Yet an elevation of T shortly after the birth of infants, during the phase of ovarian inactivity of the groups breeding female, was evident. Hormonal levels were not significantly elevated during a phase of social instability, did not correlate with intergroup encounter rates, and did not differ between breeding and nonbreeding males. Our results confirm the challenge hypothesis (Wingfield et al., 1990). The data suggest that reproductive competition in moustached tamarins is not based on endocrinological, but instead on behavioral mechanisms, possibly combined with sperm competition.     

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.     

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.     

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

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

The Function of Howling in the Ring-Tailed Lemur (Lemur catta)

Long calls are sex-specific vocalizations used for mate attraction or mate defense in many animal species. Ring-tailed lemurs (Lemur catta), female-dominant strepsirrhines, have a male-specific long call termed a howl, with proposed functions that have never been empirically tested. I aimed to investigate why ring-tailed lemur males howl and to test whether the mate defense and mate attraction hypotheses for long-calling were applicable to this species. From March to July 2010, I collected 600 h of focal data on 25 males aged ≥3 year at Beza Mahafaly Special Reserve, Madagascar. I observed each male continuously for 30 min at a time and noted all agonism using one–zero sampling at 2.5-min intervals. I calculated male dominance rank from these data. I recorded days when female estrus occurred and noted howling and intergroup encounters using all-occurrences sampling. Howling rate was not significantly related to female estrus or male dominance rank, providing no support for the mate attraction hypothesis or the intragroup mate defense hypothesis. In contrast, the intergroup mate defense hypothesis was strongly supported. During intergroup encounters, male howling rate significantly increased compared to howling rate at times without other groups present, and a greater number of males participated in multimale howling choruses when compared to times without nongroup members present. My results suggest that male ring-tailed lemurs howl to advertise their presence and location to other groups, but not to male or female members of their own group. Howling could discourage male immigration by advertising the number of males already present in a group. Long calls are used for similar mate defense purposes during intergroup encounters by other primates, including Thomas langurs (Presbytis thomasi) and chacma baboons (Papio ursinus).     

The Perception of Sex-specificity in Long Calls of the Tamarin (Saguinus labiatus labiatus)

Long calls given by red-chested moustached tamarins (Saguinus l. labiatus), typically 1–2 s in duration and made up of individual syllables, reveal distinctive sex-specificity as well as population and individual differences in their acoustic structure. Distributions of male calls and female vocalizations are discrete with regard to two acoustic parameters, i.e. number of syllables and mean inter-syllable intervals. Mean number of syllables produced in a given time is much greater in male than in female calls. I played back synthetic versions of the long calls varying in mean inter-syllable intervals to captive tamarins and found that the sex differences were encoded in a relatively simple acoustic form. The tamarin is able to identify the sex of unfamiliar calling conspecifics by voice alone.     

Intergroup relations and home range use in Verreaux's sifaka (Propithecus verreauxi)

Relationships between neighboring groups feature prominently in socioecological theory, but few empirical studies have focused on the effects of neighbors on the behavior of primates. Interactions between neighboring groups are most conspicuous during intergroup encounters, but the likelihood of encounters with neighbors can also affect ranging and activity patterns indirectly, and, as a result, behavioral patterns in areas of exclusive use may differ from those in overlap areas of adjacent home ranges. The aim of this study was to examine intergroup relations and spatial variation in home range use in Verreaux's sifaka (Propithecus verreauxi) during the annual mating season. Based on 230 hr of focal animal data collected from ten members of five adjacent groups, we found that behavioral patterns and patterns of resource utilization were not markedly different between areas of exclusive use and overlap areas of adjacent home ranges. Group cohesion tended to be higher in overlap than in core areas, but the proportion of time spent resting and foraging did not differ between these two areas. However, dominant males exhibited a higher scent-marking rate in overlap areas. Observations during intergroup encounters revealed that chases between males occurred frequently, whereas fights involving physical contact were not observed. We also found that the intergroup dominance hierarchy depended on the relative group size or the number of males in each group, with groups of lower dominance rank exhibiting a tendency to sleep proportionally more often in their core areas. The results of this study suggest that in primate species with a moderate level of intergroup aggression, such as Verreaux's sifaka, the possibility of encountering neighbors in areas of home range overlap does not exert strong influence on their behavior and resource utilization.     

Role of loud calls in brown howlers,Alouatta fusca

The loud calls of brown howler monkeys were studied during a year at the Santa Genebra Reserve, in southeastern Brazil. The study group emitted roars and barks on a total of 47 occasions, the majority of which (92%) were restricted to intergroup visual encounters. Loud calls were also elicited by the roars of distant groups (6%) and during intragroup agonistic interactions (2%). Intergroup visual encounters (n = 42) occurred predominantly in seldom used quadrats of the study group home range. In these instances, the loud calls were produced chiefly by the adult male alone (69% of cases), while the study group's two adult females joined the male in the remaining cases. Intergroup physical aggression, such as chase and displacement, was observed during 15 encounters (35% of cases). A dawn chorus does not occur in Santa Genebra—the loud calls were heard most frequently in mid-morning and again during mid-afternoon—and they were more abundant during the dry season, when the availability of food (new leaves) in the forest was lower. The data presented here provide some support for the hypothesis that roars of howler adult males are used in assessment of opponents, providing an alternative to energetically expensive chases and fights. However, given the relatively high rate of physical aggression observed during intergroup encounters, a result probably related to the high density of howlers and the consequent high frequency of intergroup encounters observed in this forest (0.7/day), ritualized aggression, in the form of loud calling, is apparently often insufficient to settle disputes. © 1995 Wiley-Liss, Inc.     

Demographic and reproductive patterns in moustached tamarin monkeys (Saguinus mystax): Implications for reconstructing platyrrhine mating systems

In this paper we address a series of questions concerning reproductive opportunities, kinship, dispersal, and mating patterns in free-ranging moustached tamarin monkeys (Saguinus mystax). Between 1980 and 1990 information on group size, composition, and migration patterns was collected on marked groups of moustached tamarins inhabiting Padre Isla, an island in the Amazon Basin of northeastern Peru. In 1990, 86% of 114 animals residing in 16 social groups were trapped, examined, and released. Mean group size was 7.0, including 2.2 adult males and 2.0 adult females. None of these groups was characterized by a single adult male-female pair. In groups with more than one adult female, only the oldest female produced offspring. An examination of dispersal patterns indicates that transfers between groups were common and fell into several categories, including immigration of individual males and females, simultaneous transfer of pairs of subadult and/or adult males (sometimes relatives) into the same social groups, and group fissioning in which males and females of the splinter group join another small social group. We have no unambiguous cases of 2 adult/subadult females migrating together into the same social group. All 6 groups for which reproductive data were available were characterized by either a polyandrous or polygynous (polygyandrous) mating pattern. The results of this study indicate that moustached tamarins reside in small multimale multifemale groups that are likely to contain both related and unrelated adult group members. Kinship and social ties among males appear to be stronger and more longlasting than kinship and social ties among females. We contend that the modal mating system of moustached and many other tamarins is not monogamous, and offer the possibility that cooperative infant care and mating system flexibility in callitrichines evolved from a polygynous mating pattern. © 1993 Wiley-Liss, Inc.     

Intergroup encounters in wild white-faced capuchins (Cebus capucinus)

Wrangham (1980) hypothesized that knowledge of the nature of intergroup encounters is crucial to understanding primate social relationships and social organization. I studied a single social group of wild white-faced capuchins over a period of 26 months and observed 44 encounters between social groups during 3703 hr of observation. All intergroup encounters consisted of predominantly hostile social interactions. However, nonaggressive interactions between males of different social groups occurred in a few cases. Adult males were the sole participants in 39 encounters and the primary participants in all 44 encounters. The alpha male was the most frequent participant. High-ranking females participated aggressively in five encounters, and low-ranking females never participated. There was no stable intergroup dominance hierarchy. I hypothesize that the need for male-male cooperation in intergroup aggression is an important factor influencing the quality of intragroup male-male relationships. Behavior during intergroup encounters is consistent with the idea that intergroup behavior is related to male reproductive strategies, but inconsistent with the idea that intergroup aggression is related to female defense of resources. The possibility that males are “hired guns” (Wrangham, 1980) cannot be ruled out.     

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

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