Natural conceptual behavior in squirrel monkeys (saimiri sciureus): An experimental investigation

Natural conceptual discriminations have been tested in many different species, including pigeons and a variety of non-human primates. The ability of four male squirrel monkeys (Saimiri sciureus) to learn and use the natural concept ‘squirrel monkey’ was investigated in this study. After a training phase, subjects were presented with novel stimuli in transfer and test trials. All subjects performed at a rate significantly above chance on the first test trial (p<.001), indicating that squirrel monkeys can utilize natural concepts in the laboratory.     

Self-treatment of wounds by a capuchin monkey (Cebus apella)

A captive adult female capuchin monkey spontaneously manufactured and used tools to groom her vaginal area and four of her own wounds over a six-month period. The wounds apparently occurred during fights with other monkeys living in the same social groups. The monkey often groomed her vaginal area and wounds with tools she had coated with a sugar-based syrup. The monkey did not use tools to groom other body areas, nor did she use tools that were coated with substances other than syrup. This monkey’s unusual habit developed in the context of manufacturing and using tools in a feeding task. These observations demonstrate that the serendipitous performance of particular behaviours in appropriate contexts can lead to the discovery and practice of simple treatment of wounds by a monkey. The independent discovery of simple medicinal procedures in human cultures may have occurred in a similar manner. Such discoveries could have predated the development of sophisticated cultures in which medicinal practices were embedded and eventually recorded.     

Comparative molecular and three-dimensional analysis of the peptide–MHC II binding region in both human and Aotus MHC-DRB molecules confirms their usefulness in antimalarial vaccine development

A vaccine against malaria is desperately needed, and Aotus monkeys are highly susceptible to experimental infection with malarial parasites. A thorough analysis of this monkey’s immune system molecules was thus undertaken in our institute. Cloning and sequencing, followed by three-dimensional analysis, has revealed high homology with some HLA-DRB1 molecules in terms of their peptide binding region pockets. Molecules such as HLA-DRB1*03, 11, 08, and HLA-DRB1*04 are so similar to Aotus MHC-DRB molecules that peptides identified as binding to these molecules and inducing protective immunity in these monkeys could be used in humans without further refinement, while small modifications seem to be needed for those binding to HLA-DRB1*07, HLA-DRB1*15, 16, and HLA-DRB1*10-like molecules, making this New World monkey an excellent model for tailor-made vaccine development, especially against malaria.     

Reference strand conformational analysis (RSCA) is a valuable tool in identifying MHC-DRB sequences in three species of Aotus monkeys

The Aotus monkey has been of great value in the pre-clinical study of malaria vaccine candidates. Several components of this primate’s immune system have been studied and they display great similarity to their human counterparts. Cloning and sequencing studies have revealed extensive sequence polymorphisms in Aotus MHC-DRB with very high similarities to several human allelic lineages, grouping at least nine distinct MHC-DRB lineages. As the efficacy of peptide vaccines in this animal model may be strongly influenced by exon 2 MHC-DRB polymorphism, the availability of a reliable and rapid MHC-DRB typing method for three species of Aotus (Aotus nancymaae, Aotus vociferans and Aotus nigriceps) is necessary. Reference strand conformational analysis (RSCA) was used here for differentiating the distinctive Aotus MHC-DRB sequences’ mobility using five fluorescently labelled references proved to be very useful for resolving closely related sequences, establishing the number of sequences transcribed in a particular monkey and their identity. The RSCA method’s reliability in terms of identifying Aotus MHC-DRB sequences will facilitate evaluating individual responsiveness to vaccines and prompt studies associating susceptibility/resistance to infectious agents or auto-immune disease, for which Aotus monkeys may be considered to be an appropriate animal model.     

Normal hematological and plasma biochemical parameters of the captive bonnet monkey (Maccaca radiata)

The bonnet monkey is being increasingly used as a model in biomedical research. However, unlike the rhesus monkey, very little information on the hematological and biochemical characteristics of blood plasma is available. Comparative data on plasma biochemical parameters vis-a-vis rhesus and human is essential for utilization of this species in biomedical research. Efforts were made to determine selected serum enzymes, glucose, triglycerides, blood urea nitrogen, creatinine, total protein, albumin, cholesterol, bilirubin, calcium, phosphorus, sodium, magnessium, potassium and total erythrocyte count, total leukocyte count, hemoglobin, PCV, ESR, and differential leukocyte count in groups of juvenile and adult bonnet monkeys of both sexes. The monkeys exhibited similar values for all the parameters in comparison to rhesus and human except for alkaline phosphatase. The value for alkaline phosphatase was 3–5 fold higher when compared to concentrations seen in rhesus monkeys and human beings. The investigation also describes the variations seen between adults and juveniles, as well as between the sexes. The data presented is valuable for scientists using this species of monkey as a human surrogate model.     

The use of vocal signals in the social play of barbary macaques

Field studies in various species ofMacaca (Cercopithecidae) provided evidence for specific visual displays that typically accompany playful interactions. The aim of our study was to examine whether and when playing individuals would use auditory displays, i.e. vocalizations that often occur during social play as well. The study was conducted on a population of semi-free Barbary macaques (Macaca sylvanus) with a special focus on the composition and dynamics of playful wrestling (synonymous term: ‘rough-and-tumble play’). Analyses of dyadic encounters between subadult males allowed us to distinguish five types of playful behaviours and three types of vocalizations. The latter were clearly linked to encounters where effects of visual signals were impaired, e.g. during close body contact. During wrestling, vocalizations tended to increase in the beginning of an encounter, whereas the last seconds of wrestling often showed a decline in vocalization rate. Our results allowed us to conclude that these vocalizations may supplement or in many cases even substitute interactional effects of visual signals, e.g. the ‘play face.’     

Capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>) modify their own behaviors according to a conspecific’s emotional expressions

Understanding conspecifics’ emotional states is important for managing social interactions. We examined whether capuchin monkeys modify their own behaviors in response to a conspecific’s emotional expressions. Six monkeys saw a demonstrator monkey responding emotionally to an object in a container; the subject monkeys could not see the object. The subjects reached for the container more frequently when the demonstrator showed an emotionally positive expression than when she showed an emotionally neutral or negative expression. This is the first report that New World monkeys are sensitive to the emotional valence of conspecifics’ emotional expressions. The finding is consistent with the hypothesis that monkeys can recognize emotional meanings in others’ expressions, an ability previously attributed only to humans and great apes.     

Behavioral and hormonal aspects of reproduction in captive goeldi’s monkeys (Callimico goeldii) in a comparative and evolutionary context

The fate of most nonhuman primate species is intimately related to man. The increasing encroachment on the natural habitat has resulted in the decimation and even near extinction of some species. Along with this development, the basic concept in many modern zoos has changed from one of merely display to self-perpetuating units. Primate research facilities are orienting their research programs towards reproductive physiology and behavior in an effort to provide basic knowledge of reproduction in these species. This increased emphasis in the area of reproductive biology and the various efforts to improve breeding of these mostly endangered primates in captivity has stimulated the author to write this review. It represents an attempt to provide the reader with basic background information relating to the endocrinology and behavior of reproduction in the clawed New World monkeys as it exists at the time of publication. The intermediate evolutionary position ofCallimico goeldii between the clawed New World monkeys and the ‘true New World monkeys’ and our relatively poor knowledge about reproduction and behavior in this particular species fully justifies the focus on Goeldi’s monkey in this essay. This review is an attempt to provide a brief history of previous studies but also the basis for research in the future. The current status of knowledge of the small-bodied clawed monkeys is also discussed in an evolutionary context, with an emphasis on the different reproductive strategies in this dynamic group of primates. The outcome, not surprisingly, confirms the unique position ofCallimico goeldii in its social, ecological, and evolutionary environment.     

A primate survey in northern Bolivia,with special reference to Goeldi’s monkey,Callimico goeldii

We conducted a 5-month survey on primates, with special attention to Goeldi’s monkey (Callimico goeldii),in the rainforest of northwestern Bolivia. Goeldi’s monkey is one of the least documented of all South American primates, and very little is known about its distribution. We report observations on distribution, abundance, and habitat of Callimico goeldiiand other primates, incidental sightings of other mammals, and preliminary behavioral observations on Callimicoand on two associated callitrichid monkey species: Saguinus fuscicollisand S. labiatus.We found a locality that appears to be particularly suitable for detailed field observations on Callimico on the north bank of the lower Río Tahuamanu. The fieldwork was carried out by A.C.; the analysis of the vocalizations, by T. G.     

Look before leaping: foraging selectivity of capuchin monkeys on acacia trees in Costa Rica

Acacia trees in Costa Rica have an obligate mutualism with three species of Pseudomyrmex ants, which vigorously defend their host tree from insect and mammalian herbivores. Depending on the size and species of ant colony, individual acacia trees may be differentially protected. For animals able to discern between weakly and highly aggressive ant colonies, costs of ant stings from less active colonies might be offset by nutritional value acquired from feeding on acacia fruit or ant larvae in swollen thorns. We examined foraging selectivity of capuchin monkeys on acacia trees in Santa Rosa National Park, Costa Rica. We measured four characteristics of the acacia trees from which capuchins fed and of acacias immediately adjacent to those in which the monkeys fed: diameter at breast height (DBH), accessibility, species of closest tree and ant species present. We found that capuchins prefer to forage in acacias that are large and accessible. We also made two measurements of ant colony activity on each tree, one before and one after disturbing the ant colony. We found that the three species of mutualistic ants differ in baseline activity levels and that mutualistic ants are more active than non-mutualistic ant species found in acacia trees. We also found that capuchins foraged more frequently in trees colonized by non-mutualistic ants, but the explanatory value (r ²) of this model was low. Furthermore, monkeys did not discriminate between acacias on the basis of baseline ant activity or the ant colony’s response to disturbance. We conclude that these monkeys select acacia trees in which to forage based on characteristics of the trees rather than the ants. In addition, our study suggests that white-faced capuchins act as predators on the acacia ants but they probably benefit the dispersal and reproductive success of acacia trees. Capuchins may in fact function as an additional mutualistic partner for acacia trees via seed dispersal, but they must overcome the ants’ defense of the trees to do so.     

Hearing and communication in blue monkeys (Cercopithecus mitis)

Hearing and vocal communication in blue monkeys (Cercopithecus mitis) was studied within an ecological context. Field measurements of the acoustical characteristics of the blue monkey's natural habitat were conducted in the Kibale forest (Uganda) and in Kakamega forest (Kenya). Measurements of background noise levels indicated that vocal communication pitched in the 100–1000-Hz frequency band would be relatively unimpeded by disruptive background noises. Furthermore, measurements of the propagation rate of audio signals indicated that calls pitched in the 125–200-Hz region penetrated the forest with minimal decrement in amplitude. Tests of the blue monkey's acoustic sensitivyty and range of hearing were conducted in the laboratory with standard audiometric procedures. Hearing in the blue monkey was characterized by a U-shaped function, with maximum sensitivity of about 5 dB SPL spanning a four-octave range from 1 to 16 kHz. The hearing of blue monkeys was superior to human hearing for tones below 500 Hz and above 8 kHz in frequency. A comparative analysis of primate hearing indicated that the blue monkey was approximately 18 dB more sensitive to low-frequency tones than the comparably sized, semi-terrestrial rhesus monkey (Macaca mulatta). Furthermore, blue monkeys exhibit phonatory specializations for vocal production in this relatively unused, low-frequency band of 125–200 Hz. These specializations for low-frequency vocal production and low-frequency hearing collectively act to increase the effective distance of long-range acoustic communication in the forest canopy.     

Report on the distribution,population, and ecology of the yunnan snub-nosed monkey (Rhinopithecus bieti)

The Yunnan snub-nosed monkey (Rhinopithecus bieti), an endangered species in China, has received more protection in theory than in practice. Therefore it is on the very verge of extinction. The population of the species was estimated less than 2,000 individuals spread in 19 distinct groups. It was confirmed that the monkey was confined to the Yunling Mountain System, the area between the Yangtze River (Changjiang, aka Jinshajiang) to the east and the Mekong River (Lancangjiang) to the west. We further concluded that a lowland belt to the east, about 100 km long and 20 – 30 km wide was not suitable habitat for the monkeys, and appeared to serve as the natural ecogeologic barrier for the species. Our results indicated that the southern limit of the distribution was at Longma (26°14′N), and that the northern limit of the distribution was at Xiaochangdu (29°20′N). The distribution area of the species was substantially smaller than previously estimated. There were substantial ecological differences between the southern and northern parts of the species range. The monkey was found only in fir-larch forest.     

Recognition of facial expressions in a Japanese monkey (Macaca fuscata) and humans (Homo sapiens)

Recognition of facial expressions by a Japanese monkey and two humans was studied. The monkey subject matched 20 photographs of monkey facial expressions and 20 photographs of human facial expressions. Humans sorted the same pictures. Matching accuracy by the monkey was about 80% correct for both human and monkey facial expressions. The confusion matrices of those facial expressions were analyzed by a multi-dimensional scaling procedure (MDSCAL). The resulting MDS plots suggested that the important cues in recognizing facial expressions of monkeys were “thrusting the mouth” and ‘raising the eyebrows.” Comparison of the MDS plots by the monkey subject with those by human subjects suggested that the monkey categorized the human “happiness” faces. This may suggest that the monkey has an ability to recognize human smile face even though it is learned. However, the monkey did not differentiate the human “anger/disgust” faces from the human “sad” faces, while human subjects clearly did. This may correlate with the lack of eyebrow movement in monkeys.     

Primate numts and reticulate evolution of capped and golden leaf monkeys (Primates: Colobinae)

A recent phylogenetic study of langurs and leaf monkeys of South Asia suggested a reticulate evolution of capped and golden leaf monkeys through ancient hybridization between Semnopithecus and Trachypithecus. To test this hybridization scenario, I analysed nuclear copies of the mitochondrial cytochrome b gene (numts) from capped, golden and Phayre’s leaf monkeys. These numts were aligned with mitochondrial cytochrome b sequences of various species belonging to the genera Semnopithecus and Trachypithecus. In the phylogenetic tree derived from this alignment, the numts fell into three distinct clades (A, B and C) suggesting three independent integration events. Clade A was basal to Semnopithecus, and clades B and C were basal to Trachypithecus. Among the numts in clades A and C were sequences derived from species not represented in their respective sister mitochondrial groups. This unusual placement of certain numts is taken as additional support for the hybridization scenario. Based on the molecular dating of these integration events, hybridization is estimated to have occurred around 7.1 to 3.4 million years ago. Capped and golden leaf monkeys might have to be assigned to a new genus to reconcile their unique evolutionary history. Additionally, northeast India appears to be a ‘hot spot’ for lineages that might have evolved through reticulate evolution.     

Considerations for using occupancy surveys to monitor forest primates: a case study with Sclater’s monkey (<Emphasis Type="Italic">Cercopithecus sclateri</Emphasis>)

Count-based indices and distance sampling are widely used to monitor primate populations. Indices are often confounded by variation in detectability, whereas distance sampling is generally ineffective with species that flee or hide from observers and where it is difficult to accurately measure detection distances. We tested occupancy modeling as a means to monitor Sclater’s monkey (Cercopithecus sclateri), an endemic of Nigeria. We evaluated effects of survey methodology, habitat, and human disturbance on detection probability and site occupancy. Average detectability was high (p = 0.81), but varied substantially between two observers. Occupancy was highest in areas with intermediate levels (20–40%) of farmland and secondary forest, and was unaffected by human disturbance. Sampling plots (4 and 6.25 ha) did not concurrently contain >1 monkey group, were likely closed to monkey movements during the replicate surveys of each plot, and were spatially separated so that it was unlikely the same group was observed in >1 plot. These conditions enabled the conversion of occupancy to group density. Scaled to 6.25 ha, model-weighted occupancy averaged 0.230 (SE 0.103), yielding an estimate of 3.7 groups/km² (95% CI 1.4–7.7 groups/km²). Because some groups straddled plot boundaries, we assumed that half of these groups were inside the plots, resulting in an adjusted estimate of 3.1 groups/km². Our results illustrate that occupancy can be suitable for monitoring vigilant forest primates where detection distances are difficult to measure. However, special attention is required to choose spatial and temporal scales that accommodate the method’s closure and independent-detection assumptions.     

Owl monkey MHC-DRB exon 2 reveals high similarity with several HLA-DRB lineages

One hundred and ten novel MHC-DRB gene exon 2 nucleotide sequences were sequenced in 96 monkeys from three owl monkey species (67 from Aotus nancymaae, 30 from Aotus nigriceps and 13 from Aotus vociferans). Owl monkeys, like humans, have high MHC-DRB allele polymorphism, revealing a striking similarity with several human allele lineages in the peptide binding region and presenting major convergence with DRB lineages from several Catarrhini (humans, apes and Old World monkeys) rather than with others New World monkeys (Platyrrhini). The parallelism between human and Aotus MHC-DRB reveals additional similarities regarding variability pattern, selection pressure and physicochemical constraints in amino acid replacements. These observations concerning previous findings of similarity between the Aotus immune system molecules and their human counterparts affirm this specie’s usefulness as an excellent animal model in biomedical research.Experiments carried out in this work complied with current Colombian Ministry of Health law and regulations governing animal care and handling.An erratum to this article can be found at     

<Emphasis Type="Italic">Cebus apella</Emphasis> Tolerate Intermittent Unreliability in Human Experimenters

Monkeys form expectations for outcomes based on interactions with human experimenters. Capuchins, a cooperative New World monkey species, not only anticipate receiving rewards that the experimenter indicates, but also apparently anticipate rewards based on what the experimenter has given to their partners. However, this could be due to subjects responding to either outcomes or experimenters. Here we examine whether capuchins will continue to interact with human experimenters who are occasionally unreliable. We tested 10 monkeys with a series of familiar human experimenters using an exchange task. The experimenters had never before participated in exchange studies with these monkeys, hence the monkeys learned about their behavior during the course of testing. Occasionally experimenters were unreliable, failing to give a reward after the monkey returned the token. The monkeys did recognize these interactions as different, responding much more quickly in trials following those that were nonrewarded than in other situations with the same experimenter. However, subjects did not change their preference for experimenters when given the opportunity to choose between the unreliable exchanger and another exchanger, nor did subjects learn to prefer reliable experimenters from watching other monkeys’ interactions. Instead, subjects returned the tokens to the same location from which they received it. These results indicate that capuchins may not be sensitive to isolated instances in which experimenters are unreliable, possibly because of a strong bias to returning the token to the location from which it was donated.     

Frequent insectivory by two guenons (Cercopithecus lhoesti and Cercopithecus mitis) in the Kalinzu Forest, Uganda

I investigated the feeding ecology of lHoests monkeys (Cercopithecus lhoesti) and blue monkeys (Cercopithecus mitis) in the Kalinzu Forest, Uganda. Although forest guenons are generally thought to be frugivores or folivores, these two guenons spent a large proportion of their time feeding on invertebrates. The lHoests monkey and the blue monkey spent as much as 66 and 50% of their time on insectivory, respectively. These proportions of time spent on invertebrate feeding are higher than those reported elsewhere for forest guenons. LHoests monkeys mainly utilized the area near the ground for invertebrate feeding, while blue monkeys utilized the area around 20 m above the ground. It seemed that guenons have an ability to change their diet according to the environment.     

How Reliable are Density Estimates for Diurnal Primates?

Primate population assessments provide the basis for comparative studies and are necessary prerequisites in determining conservation status. The most widely used assessment method is line transect sampling, which generates systematic data quickly and comparatively inexpensively. In contrast, the presumably most reliable method is long-term monitoring of known groups, which is both slow and costly. To assess the reliability of various analytical methods, we compared group and population densities for white-handed gibbons (Hylobates lar carpenteri) and Phayre’s leaf monkeys (Trachypithecus phayrei crepusculus) derived from transect walks with those from long-term group follows at Phu Khieo Wildlife Sanctuary, Thailand. Our assistants and we regularly walked a 4-km transect over 30 mo (480 km total), resulting in 155 gibbon sightings and 125 leaf monkey sightings. We then estimated densities via 1) DISTANCE and 2) the Kelker method based on perpendicular distances (PD) or animal-to-observer distances (AOD). We compared the 3 estimates to values based on known home ranges (95% kernels), accounting for home range overlap, combined with group size data. Analyses of line transect data consistently overestimated group densities for both species, while underestimating group size for leaf monkeys. Quality of results varied according to the group size and spread of each species. However, we found, in accordance with previous studies, that values derived via AOD (or its derivations) matched most closely with population estimates based on home range data.     

Reintroduction of the rare damselfly <Emphasis Type="Italic">Ischnura gemina</Emphasis> (Odonata: Coenagrionidae) into an urban California park

Habitat degradation led to local extinction of the San Francisco forktail damselfly (Ischnura gemina) in Glen Canyon Park, San Francisco, California. In this study, we reintroduced I. gemina into Glen Canyon after the damselfly’s habitat was restored. Upon release, we carried out a mark- release-recapture study to monitor the damselfly’s population dynamics. Our data were compared to two “baseline” studies on I. gemina, conducted in the park prior to the damselfly’s demise. Our recapture rates were significantly lower than the prior studies due to a large initial decline in marked individuals upon release. Despite a lower recapture rate, the reintroduction was initially successful since the damselflies reproduced throughout the summer and the following year. However, the population failed to persist during the second year when the habitat became degraded with excess vegetation. Future success is contingent on the continual management and upkeep of the habitat.