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.     

A case study employing operant conditioning to reduce stress of capture for red-bellied tamarins (Saguinus labiatus)

Traditional techniques used to capture New World monkeys, such as net capture, can induce high levels of acute stress detrimental to welfare. Alternatively, training nonhuman animals via operant conditioning to voluntarily participate in husbandry and/or veterinary practices is accepted as a humane process that can reduce stress and improve welfare. This study details the use of operant conditioning using positive reinforcement training (PRT) and target training to train a family of 5 captive red-bellied tamarins (Saguinus labiatus) in a wildlife park to voluntarily enter a transportation box and remain calm for 1 min after 54 training sessions. Observations of 2 unrelated net-capture processes provided measures of locomotion and vocalizations as indicators of stress behavior that were compared with those of the trained tamarins. Net-captured monkeys exhibited rapid erratic locomotion and emitted long, high-frequency vocalizations during capture whereas the trained tamarins exhibited minimal locomotion and emitted only 4 brief vocalizations (root mean square 35 dB) during capture. This indicates that the use of PRT considerably reduced potential for stress and improved welfare during the capture and containment of the tamarins.     

A Case Study Employing Operant Conditioning to Reduce Stress of Capture for Red-Bellied Tamarins (Saguinus labiatus)

Traditional techniques used to capture New World monkeys, such as net capture, can induce high levels of acute stress detrimental to welfare. Alternatively, training nonhuman animals via operant conditioning to voluntarily participate in husbandry and/or veterinary practices is accepted as a humane process that can reduce stress and improve welfare. This study details the use of operant conditioning using positive reinforcement training (PRT) and target training to train a family of 5 captive red-bellied tamarins (Saguinus labiatus) in a wildlife park to voluntarily enter a transportation box and remain calm for 1 min after 54 training sessions. Observations of 2 unrelated net-capture processes provided measures of locomotion and vocalizations as indicators of stress behavior that were compared with those of the trained tamarins. Net-captured monkeys exhibited rapid erratic locomotion and emitted long, high-frequency vocalizations during capture whereas the trained tamarins exhibited minimal locomotion and emitted only 4 brief vocalizations (root mean square 35 dB) during capture. This indicates that the use of PRT considerably reduced potential for stress and improved welfare during the capture and containment of the tamarins.     

Alu insertion loci and platyrrhine primate phylogeny

Short INterspersed Elements (SINEs) make very useful phylogenetic markers because the integration of a particular element at a location in the genome is irreversible and of known polarity. These attributes make analysis of SINEs as phylogenetic characters an essentially homoplasy-free affair. Alu elements are primate-specific SINEs that make up a large portion of the human genome and are also widespread in other primates. Using a combination wet-bench and computational approach we recovered 190 Alu insertions, 183 of which are specific to the genomes of nine New World primates. We used these loci to investigate branching order and have produced a cladogram that supports a sister relationship between Atelidae (spider, woolly, and howler monkeys) and Cebidae (marmosets, tamarins, and owl monkeys) and then the joining of this two family clade to Pitheciidae (titi and saki monkeys). The data support these relationships with a homoplasy index of 0.00. In this study, we report one of the largest applications of SINE elements to phylogenetic analysis to date, and the results provide a robust molecular phylogeny for platyrrhine primates.     

New World monkey phylogeny based on X-linked G6PD DNA sequences

The Platyrrhini, or New World monkeys, are an infraorder of Primates comprised of 16 genera. Molecular phylogenetic analyses have consistently sorted these genera into three groups: the Pitheciidae (e.g., saki and titi monkeys), Atelidae (e.g., spider and howler monkeys), and Cebidae (e.g., night monkeys, squirrel monkeys, and tamarins). No consensus has emerged on the relationships among the three groups or within the Cebidae. Here, approximately 0.8 kb of newly generated intronic DNA sequence data from the X-linked glucose-6-phosphate dehydrogenase (G6PD) locus have been collected from nine New World monkey taxa to examine these relationships. These data are added to 1.3 kb of previously generated G6PD intronic DNA sequence data [Mol. Phylogenet. Evol. 11 (1999) 459]. Using distance and parsimony-based techniques, G6PD sequences provide support for an initial bifurcation between the Pitheciidae and the remaining platyrrhines, linking Atelidae and Cebidae as sister taxa. Bayesian methods provided a conflicting phylogeny with Atelidae as outgroup. Within the Cebidae, a sister relation between Aotus and the Cebus/Saimiri clade is favored by parsimony analysis, but not by other analyses. Potential reasons for the difficulty in resolving family level New World monkey phylogenetics are discussed.     

Use of spatial, visual, and olfactory information during foraging in wild nocturnal and diurnal anthropoids: A field experiment comparing Aotus, Callicebus, and Saguinus

Early in their evolution, the ancestors of anthropoid primates radiated from a nocturnal to a diurnal niche. Foraging during the night differs from foraging during the day in terms of the availability of light and color cues, and in the movement of odor molecules through the canopy. In this study, we compared the ability of nocturnal and diurnal New World monkeys to use perceptual cues (i.e., the sight or smell of food) and spatial information (place predictability) in within-patch foraging decisions. An experimental field study was conducted on wild groups of night monkeys (Aotus nigriceps), tamarins (Saguinus imperator imperator and S. fuscicollis weddelli), and titi monkeys (Callicebus cupreus) at the Zoobotanical Park/UFAC, Rio Branco, Brazil. Our research design included the construction of feeding stations located in the home range of the study groups. Each feeding station consisted of eight visually identical feeding platforms located in a circular arrangement. In all test settings, two platforms at each feeding station contained a food reward (banana), and the remaining six platforms contained a sham reward (yellow plastic or inaccessible banana). In the night-monkey experiments, each feeding platform was illuminated by a 40-W red bulb to aid the researcher in observing their behavior. When the location of reward sites was predictable over time, individuals in all four species successfully relocated food rewards based solely on spatial information. Each species was also successful in using visual information to distinguish real from sham food rewards. However, only night monkeys and one group of emperor tamarins used olfactory information alone to locate food rewards. Overall, the species' performances did not clearly differentiate Aotus from diurnal New World primates in these experiments.     

Foraging and Spatial Memory in Wild Weddell’s Saddleback Tamarins (Saguinus fuscicollis weddelli) When Moving Between Distant and Out-of-Sight Goals

Two main types of cognitive maps, route-based and coordinate-based, have been proposed to explain how animals navigate through their environments. We examined patterns of feeding and ranging in Weddell’s saddleback tamarins (Saguinus fuscicollis weddelli) in northern Bolivia to assess which type of cognitive map best explains the tamarins’ movement patterns in large-scale space, e.g., when moving between distant and out-of-sight goals. We observed the tamarins for 236 h over the course of 32 d and used a GPS unit to record the location of nighttime sleeping sites and feeding trees and the locations of individuals at 10-min intervals. Based on an evaluation of 109 travel segments of >20 m in which the monkeys traveled from the tree of one major feeding species to another without stopping to rest, forage for insects, or interact with neighbors, we calculated a circuity index (actual distance traveled divided by the straight-line distance) of 1.43. We also plotted the monkeys’ daily movement patterns using GIS software. These analyses showed that tamarin travel was not random, that a limited set of route segments (N?=?29) was reused on multiple occasions, and that certain areas of the forest appeared to serve as switch points (N?=?9) where the monkeys reoriented travel. These results support the contention that the tamarins encoded the spatial relationships among many feeding and sleeping sites in their home range, and navigated in large-scale space using a route-based spatial representation. These results are consistent with those reported for a variety of primate taxa, suggesting that many primate species reuse a familiar set of travel routes and switch points to orient in large-scale space.     

Abundance, diversity, and patterns of distribution of primates on the Tapiche River in Amazonian Peru

This work presents data on the relative diversity, abundance, and distribution patterns of primates in a 20 km2 area of the Tapiche River in the Peruvian Amazon. Population data were collected while the study area was both inundated and dry (March to September 1997) using conventional line-transect census techniques. Survey results reflected the presence of 11 primate species, but population parameters on only eight of the species will be presented, including saddleback tamarins (Saguinus fuscicollis), Bolivian squirrel monkeys (Saimiri boliviensis), brown capuchins (Cebus apella), white-fronted capuchins (Cebus albifrons), monk sakis (Pithecia monachus), red titi monkeys (Callicebus cupreus), red uakaris (Cacajao calvus), and red howler monkeys (Alouatta seniculus). Woolly monkeys (Lagothrix lagotricha), night monkeys (Aotus nancymaae), and pygmy marmosets (Callithrix pygmaea) were also seen in the area. The data for the smaller-bodied primates is similar to that reported almost 18 years earlier, but the data for the larger-bodied primates reflect a loss in the number of animals present in the area. Pressure from hunters and the timber industry may account for declining numbers of large-bodied primates, while it appears that natural features peculiar to the conservation area contribute to the patchy pattern of distribution.     

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.     

Preparing New World monkeys for laboratory research

New World monkeys represent an important but often poorly understood research resource. The relatively small size and low zoonotic risk of these animals make them appealing as research subjects in a number of areas. However, historic portrayal of many of these species as difficult to manage and handle is one of the factors that has limited their use. Basic guidelines are provided on management and handling approaches for the New World monkeys most commonly used in research: marmosets, squirrel monkeys, owl monkeys, and titi monkeys. Topics include transport and acclimation to a new facility, location changes within a facility, diet changes, removal from and return to social groups, capture and restraint, handling for anesthesia, postprocedural monitoring, and staff training.     

Effects of duration of separation on responses to mates and strangers in the monogamous titi monkey (Callicebus moloch)

Adult male and female titi monkeys form an intense social bond characterized by high levels of affiliative interactions between pairmates and agonistic responses to strangers. In natural settings, separation between mates can vary from brief periods, as when mates drift apart during feeding, to permanent separation, occasioned by desertion or death. In this study we asked how different durations of separation altered the behavior of male and female titi monkeys (Callicebus moloch). We compared the effects of brief separation such as might occur incidentally during feeding (1–2 h) with prolonged separation such as might occur if one partner died or deserted (5 days). Effects were observed during a 30 min reunion of pairmates or during a 30 min encounter with a stranger of the opposite sex. Following brief separation, interactions between mates and between strangers clearly differed in measures of affiliation, but not in behaviors indicative of arousal. Following prolonged separation, measures of arousal increased with both mated pairs and strangers. Females tended to interact more readily with a stranger following prolonged separation than after brief separation, but interactions between mates were essentially unchanged and differed substantially from those between strangers. The data suggest that the pair bond persists in titi monkeys after prolonged social isolation, despite increased interest in interacting with potential new partners. Am. J. Primatol. 43:225–237, 1997. © 1997 Wiley-Liss, Inc.     

Behavioral modifications in northern bearded saki monkeys (<Emphasis Type="Italic">Chiropotes satanas chiropotes</Emphasis>) in forest fragments of central Amazonia

We investigated behavioral differences among seven groups of northern bearded saki monkeys (Chiropotes satanas chiropotes) living in five forest fragments and two areas of continuous forest at the Biological Dynamics of Forest Fragments Project study area, located approximately 80 km north of Manaus, Brazil. We collected data in six research cycles from July–August 2003 to January 2005–April 2006. When bearded saki monkeys were present in a study area, we followed the group from dawn until dusk for three consecutive days. Every 5 min, we conducted behavioral scans of all visible individuals. There was a positive relationship between forest size and group size, but animals in the small forest fragments lived at greater densities. Bearded saki monkeys in the smaller fragments spent more time resting, less time traveling, and less time vocalizing, but there was no relationship between forest size and the amount of time spent feeding. Our results indicate that the main behavioral differences among the groups are related to the amount of forest resources (e.g., fruit trees, space) available to the monkeys in the smaller fragments, as well as the resulting smaller group sizes. We stress the need to preserve large tracts of forest and provide connectivity between forest patches.     

Extension of the Geographical Range of White-browed Titi Monkeys (<Emphasis Type="BoldItalic">Callicebus discolor</Emphasis>) and Evidence for Sympatry with San Martin Titi Monkeys (<Emphasis Type="BoldItalic">Callicebus oenanthe</Emphasis>)

White-browed titi monkeys (Callicebus discolor) have one of the largest distribution ranges of all titi monkey species, occurring from central Peru to southern Colombia. During a long-term study on the distribution of titi monkeys and other primates in Peru, we conducted extensive surveys in the San Martin Department of northeastern Peru. We encountered Callicebus discolor at the left bank of the Huallaga River, where the species most probably lives in sympatry with endemic San Martin titi monkeys (Callicebus oenanthe). Our study reveals an important extension of its formerly known distribution range. Massive deforestation activities in the region make studies on the habitat preferences of both species difficult, as most titi monkeys are confined to the remaining small remnants of the original forest. Urgent conservation measures are necessary to preserve the last lowland forests of San Martin.     

Color discrimination by the cotton-top tamarin (Saguinus oedipus oedipus) and its relation to fruit coloration

Old World monkeys and apes have been reported to differ from New World monkeys in their abilities to discriminate colors across the visible spectrum. Old World monkeys and apes (Macaca, Pan, Pongo) discriminate colors quite accurately, while some New World monkeys studied (Saimiri, Cebus) have shown lower sensitivity to and poorer discrimination of long wavelength light. This study examined the color discrimination ability of another New World primate, the cotton-top tamarin, Saguinus oedipus oedipus (family Callitrichidae). The tamarins were trained to discriminate a set of Munsell color chips, both within the same hue category and from the 2 hue categories on either side of the training hue. Results indicated that the cotton-top tamarin can make accurate discriminations across the visible spectrum. Human subjects were tested under similar conditions in order to compare their color discrimination abilities to those of the tamarins. The tamarins and human subjects had the most difficulty discriminating the same hues. The discrimination abilities of the monkeys were assessed in relation to the coloration of fruits eaten in a natural environment. A list of the species of fruits commonly eaten by various species of New World monkeys was compiled and the coloration of fruits at maturity was noted. It was found that most New World primate species eat fruits whose mature coloration ranges across most of the spectrum.     

Can Auditory Playback Condition Predator Mobbing in Captive-reared <Emphasis Type="Italic">Saguinus oedipus</Emphasis>?

Captive reintroductions often suffer high mortality, with predation as one source. Many species learn about predators; thus training captive-born animals to recognize predators may increase survivorship. We adapted variants of methods developed for birds to attempt to condition monkeys to mob a predator. Captive-reared cotton-top tamarins (Saguinus oedipus) did not differentiate between a snake and a rat, confirming previous research that naïve cotton-top tamarins do not fear snakes. Tamarins then viewed a living snake during playback of mobbing calls. In posttests, tamarins did not mob the snake. We then eliminated the pretest to avoid potential habituation and placed a stillborn tamarin with the snake in an attempt to heighten arousal. In posttests, tamarins again did not mob the snake, although they did increase their rates of calls, indicating mild arousal. Overall, none of 8 groups of cotton-top tamarins learned to mob a predator. Potential reasons for failure include conditioning multiple subjects at once and the lack of an experienced demonstrator. Observing a demonstrator was not necessary for birds to acquire mobbing, but may be necessary for tamarins.     

An experiment on the relation between the feeding speed and the caloric intake through leaf eating in Japanese monkeys

In order to know the bioenergetic effect of leaf eating in Japanese monkeys experiments were conducted on caged animals. Two monkeys from the Koshima troop were fed with leaves in a cage shortly after their capture. The monkeys were tested to determine in what duration they could fulfill their daily energy requirements by solely leaf eating or by solely wheat eating. Twelve hours of feeding solely on leaves did not fulfill the monkeys' maximum daily intake, whereas 4 hr of feeding solely on wheat satisfied their daily energy requirements. The ratio of the daily intake to the daily energy consumption was 90% for leaf eating and 120% for wheat eating. It is difficult for Japanese monkeys to fulfill their daily energy requirements by leaf eating only. Thus, the combination of fruits (nuts) and leaves must be necessary for their energy intake. These facts are to be considered in the studies of feeding activity, food abundance, or the home range size.     

Individuality in the vocalizations of infant and adult coppery titi monkeys (Plecturocebus cupreus)

As social animals, many primates use acoustic communication to maintain relationships. Vocal individuality has been documented in a diverse range of primate species and call types, many of which have presumably different functions. Auditory recognition of one's neighbors may confer a selective advantage if identifying conspecifics decreases the need to participate in costly territorial behaviors. Alternatively, vocal individuality may be nonadaptive and the result of a unique combination of genetics and environment. Pair-bonded primates, in particular, often participate in coordinated vocal duets that can be heard over long distances by neighboring conspecifics. In contrast to adult calls, infant vocalizations are short-range and used for intragroup communication. Here, we provide two separate but complementary analyses of vocal individuality in distinct call types of coppery titi monkeys (Plecturocebus cupreus) to test whether individuality occurs in call types from animals of different age classes with presumably different functions. We analyzed 600 trill vocalizations from 30 infants and 169 pulse-chirp duet vocalizations from 30 adult titi monkeys. We predicted that duet contributions would exhibit a higher degree of individuality than infant trills, given their assumed function for long-distance, intergroup communication. We estimated 7 features from infant trills and 16 features from spectrograms of adult pulse-chirps, then used discriminant function analysis with leave-one-out cross-validation to classify individuals. We correctly classified infants with 48% accuracy and adults with 83% accuracy. To further investigate variance in call features, we used a multivariate variance components model to estimate variance partitioning in features across two levels: within- and between-individuals. Between-individual variance was the most important source of variance for all features in adults, and three of four features in infants. We show that pulse-chirps of adult titi monkey duets are individually distinct, and infant trills are less individually distinct, which may be due to the different functions of the vocalizations.     

Positive reinforcement training in rhesus macaques—training progress as a result of training frequency

Positive reinforcement training (PRT) efficiency was examined as a function of training frequency in 33 pair‐ or triple‐housed female rhesus macaques. The animals were trained three times a week, once a day or twice a day, using PRT and a clicker as a secondary reinforcer. All animals were trained on 30 sessions, with an average of 5 min per training session per animal. The behaviors, trained in succession, were Targeting (reliably touching and following a Target); Collaborating (dominant animals allowing subordinates to train while stationing); Box‐training (accepting being enclosed in a small compartment while responding to Target training) and initial Injection training. Fulfilled criteria for Targeting were obtained in 32/33 animals in a median of nine training sessions. Collaboration was obtained in 27/33 animals in a median of 15 training sessions. However, only four animals completed Box‐training during the 30 training sessions and started Injection training. When comparing training success in terms of number of training sessions, training twice a day was less efficient than the other two treatments. In terms of daily progress, our results suggest that from a management perspective, daily training is more conducive to quick training success than thrice weekly training. In addition, in this study no further advantages could be gained from training twice a day. Am. J. Primatol. 71:373–379, 2009. © 2009 Wiley‐Liss, Inc.     

Travel and Spatial Patterns Change When <Emphasis Type="Italic">Chiropotes satanas chiropotes</Emphasis> Inhabit Forest Fragments

Previous studies have used home range size to predict a species’ vulnerability to forest fragmentation. Northern bearded saki monkeys (Chiropotes satanas chiropotes) are medium-bodied frugivores with large home ranges, but sometimes they reside in forest fragments that are smaller than the species’ characteristic home range size. Here we examine how travel and spatial patterns differ among groups living in forest fragments of 3 size classes (1 ha, 10 ha, and 100 ha) versus continuous forest. We collected data in 6 research cycles from July–August 2003 and January 2005–June 2006 at the Biological Dynamics of Forest Fragments Project (BDFFP), north of Manaus, Brazil. For each cycle, we followed the monkeys at each study site from dawn until dusk for 3 consecutive days, and recorded their location. Although bearded saki monkeys living in 10-ha and 1-ha fragments had smaller day ranges and traveled shorter daily distances, they traveled greater distances than expected based on the size of the forest fragment. Monkeys in the small fragments revisited a greater percentage of feeding trees each day, traveled in more circular patterns, and used the fragments in a more uniform pattern than monkeys in the continuous forest. Our results suggest that monkeys in the small fragments maximize their use of the forest, and that the preservation of large tracts of forest is essential for species conservation. Species with large home ranges sometimes inhabit forest fragments, but doing so can alter behavior, demographics, and ecology, and the monkeys may be vulnerable to stochastic events.