Distribution and abundance of sacred monkeys in Igboland,southern Nigeria

Although primates are hunted on a global scale, some species are protected against harassment and killing by taboos or religious doctrines. Sites where the killing of sacred monkeys or the destruction of sacred groves is forbidden may be integral to the conservation of certain species. In 2004, as part of a distribution survey of Sclater's guenon (Cercopithecus sclateri) in southern Nigeria, we investigated reports of sacred monkeys in the Igbo‐speaking region of Nigeria. We confirmed nine new sites where primates are protected as sacred: four with tantalus monkeys (Chlorocebus tantalus) and five with mona monkeys (Cercopithecus mona). During 2004–2006, we visited two communities (Akpugoeze and Lagwa) previously known to harbor sacred populations of Ce. sclateri to estimate population abundance and trends. We directly counted all groups and compared our estimates with previous counts when available. We also estimated the size of sacred groves and compared these with grove sizes reported in the literature. The mean size of the sacred groves in Akpugoeze (2.06 ha, n=10) was similar to others in Africa south of the Sahel, but larger than the average grove in Lagwa (0.49 ha, n=15). We estimated a total population of 124 Sclater's monkeys in 15 groups in Lagwa and 193 monkeys in 20 groups in Akpugoeze. The Akpugoeze population was relatively stable over two decades, although the proportion of infants declined, and the number of groups increased. As Sclater's monkey does not occur in any official protected areas, sacred populations are important to the species' long‐term conservation. Despite the monkeys' destruction of human crops, most local people still adhere to the custom of not killing monkeys. These sites represent ideal locations in which to study the ecology of Sclater's monkey and human–wildlife interactions. Am. J. Primatol. 71:574–586, 2009. © 2009 Wiley‐Liss, Inc.     

Distribution and abundance of patas monkeys (Erythrocebus patas) in Laikipia, Kenya, 1979-2004

Patas monkeys may be especially vulnerable to local extinction because they live in relatively small, female-philopatric groups at low densities and are strongly polygynous. We assessed a patas monkey population in Kenya's 9,700 km(2) Laikipia District over 25 years, using data collected in 1979-1981 and 1992-2004. The data were based on intensive observations of three study groups, "on the ground" counts, and surveys of Laikipia residents. In 1979-1981, a minimum of 415 patas monkeys lived in 14-15 groups. By 2000, the best estimate suggested 310-445 patas monkeys living in 13-17 groups over a greater surveyed area, suggesting that patas monkeys in Laikipia may have undergone a slight decline in numbers over time. Their distribution, however, was similar over time. The relative stability of this population has likely been the result of beneficial co-existence with large-scale cattle ranching. Outside Laikipia, substantial habitat alteration from rising human populations has coincided with the near disappearance of patas monkeys where they were previously more numerous. The small population in Laikipia, probably the largest remaining in Kenya, may therefore be critical to the continued existence of patas monkeys in that country and may be dependent on maintenance of large-scale ranches. Such land use provides patas monkeys with water and broad expanses of Acacia drepanolobium woodlands, the habitat to which patas are restricted in Laikipia.     

Seasonal variation of diet and food availability in a group of Sichuan snub-nosed monkeys in Shennongjia Nature Reserve, China

We studied the diet and food availability of a group of Sichuan snub-nosed monkeys for 14 months (July 2003 to September 2004, except for February) in the Shennongjia Nature Reserve, China. This species is primarily a lichen eater, with lichens (Usneaceae) accounting for 43.28% of feeding records (n=3,452). Other food types in the diet were young leaves (28.71%), fruits or seeds (14.57%), buds (5.36%), mature leaves (3.51%), herbs (2.09%), bark (1.36%), and flowers (1.13%). The monkeys used 23 plant species. Their diet showed a complicated seasonal variation: the monthly diet varied from primarily lichens in November-April, to a mixture of leaves and lichens in May-July, to a mixture of fruits or seeds and lichens in August-October (the latter depended on annual fruit and seed availability). The proportion of fruits or seeds in the diet was negatively correlated with that of lichens, which suggests that the monkeys prefer fruits or seeds to lichens when all of these items are available. The fruit or seed availability varied greatly between the two study years. The proportion of lichens, young leaves, flowers, and fruits or seeds in the diet was positively associated with their availability. The monkeys appeared to be selective feeders. They preferred 10 tree species for plant parts, and nine tree species for lichens. The selection index of tree species for lichens was positively related to lichen coverage per branch on tree species, demonstrating that the monkeys preferred tree species with abundant lichens, as well as dead trees for lichens. The results suggest that dead-tree harvesting in the reserve could significantly reduce the quality of habitat for these monkeys, and should therefore be prohibited. Connus controversa, Cerasus discadenia, Salix willichiana, and Malus halliana should be conserved as top priority species because the monkeys preferred them for both their vegetative parts and the lichens that grow on them.     

Spontaneous tool use by wild capuchin monkeys (Cebus libidinosus) in the Cerrado

Among primates, only chimpanzees and orang-utans are credited with customary tool use in nature. Among monkeys, capuchins stand out with respect to the number of accounts of tool use. However, the majority of capuchin tool use observations reported in nature is anecdotal or idiosyncratic. In this report, we documented the stone pounding of dry fruits (Hymenea courbaril and Acrocomia aculeata) in two wild free-ranging groups of Cebus libidinosus in the Brasilia National Park, a preserved area representative of the Cerradobiome of Central Brazil. In 2004, we noted 2 episodes at which 4 monkeys used stones to crack open nuts. In 2005, we recorded 5 pounding episodes involving 2 different monkeys. Observations of tool use over the course of 2 consecutive years by some individuals, as well as other indirect evidence, indicate that this behaviour could be habitual in the studied groups. We propose that the probability of the emergence of the use of pounding stones as tools may be dependent on the ecological variables that influence the degree of terrestriality and extractive foraging and the complex interaction of these factors.     

Can proboscis monkeys be successfully maintained in captivity? A case of swings and roundabouts

Although most western zoos have experienced difficulties in maintaining proboscis monkeys, the Singapore Zoo has managed to sustain a social group of proboscis monkeys housed in a large naturalistic exhibit since 1998. Within 3 years after the monkeys were brought to the zoo, five offspring were produced, all of which survived. Natural forest vegetation from 20 plant species was provided along with a staple diet of about seven different species on a daily basis. The calcium and sodium contents of the plant items consumed by monkeys in the Singapore Zoo were similar to those in the diet of wild proboscis monkeys in Borneo. However, the levels of other minerals, such as iron, magnesium, manganese, potassium, zinc, and phosphorus, were significantly lower in the natural vegetation consumed by the monkeys compared to the wild diet. Food supplements such as primate biscuits, cod liver oil, boiled egg, multivitamins, and mineral syrup further ensured a more balanced diet for the captive monkeys. The data presented here show that zoos can maintain these rare Colobine monkeys successfully by provide them with a natural diet, along with appropriate husbandry and hygiene practices, minimal human interference, and applied nutritional science. The husbandry and nutritional management model presented in this paper could be of use to other institutions around the world. Zoo Biol 23:533–544, 2004. © 2004 Wiley-Liss, Inc.     

云南富合山地区滇金丝猴游走模式的季节性差异

从 2 0 0 0年 11月至 2 0 0 2年 1月 ,我们在云南富合山 (99°2 0′E ,2 6°2 5′N)记录了滇金丝猴 (Rhinopithe cusbieti)的游走以及其他行为 ,以描述猴群行为模式的季节性变化及其对温带环境的适应。由于季节间行为方式的相似 ,我们将冬季和春季、夏季和秋季的数据合并表述。猴群终年以取食树叶为主 ,多在过夜地附近活动。在冬 -春季 ,猴群一般在低海拔的南部地区活动 ,同时缩短日行走距离 ,花费较多的时间取食树叶、竹叶和竹笋 ;而在夏 -秋季猴群的活动模式与冬 -春季相反 ,并取食大量果实。我们将富合地区猴群的季节性游走模式以及食性看作是食物供给和温度变化之间折中的结果 ,这些行为特征和其它温带灵长类的相似。此外 ,过夜地的分布也会影响猴群利用家域内各方格的方式     

Endometriosis: clinical monitoring and treatment procedures in Rhesus Monkeys

The National Institute on Aging (NIA) sponsored a workshop on September 8, 2004, to discuss the incidence, diagnosis, and clinical treatment of endometriosis in rhesus monkey colonies. Because of the growing number of aging studies using rhesus monkeys, this disease has become more prevalent as monkeys are living into advanced ages in captivity. The objective of the workshop was to gather information from various NIA-supported aging rhesus colonies on the incidence, clinical manifestations, indicators for early detection, and possible treatment options for endometriosis. Participants outlined a course of action for the effective management of this disease that would best maintain the integrity of long-term aging studies.     

Terrestriality and tree stratum use in a group of Sichuan snub-nosed monkeys

Morphological characters allow the Sichuan snub-nosed monkey (Rhinopithecus roxellana) to use multiple tree levels, but very few studies have quantified the terrestriality and tree stratum use of the species. I investigated the terrestriality and tree stratum use in a group of the monkeys from July 2003 to September 2004 (except February) in the Qianjiaping area of Shennongjia Nature Reserve, China. I collected data on the vertical position of individual monkeys in forest in relation to behavior types, diet, age/sex classes, vegetation types, tree height, and distribution of predators. The monkeys were much more arboreal than they were thought to be. They spent 97.1% of their time in trees (n=21,234 records) and 2.9% on the ground, and mainly used the middle (74.4%) and upper strata (17.4%). The monkeys displayed all behavioral types except searching in the middle and upper strata. The percentage of use of a stratum (except the low stratum) varied among months, and there was a difference in the percentage of use of a stratum among age/sex classes and between vegetation types. Approximately 94.2% of trees used by the monkeys were >6 m tall. They mainly fed on lichens, young leaves, mature leaves, flowers, fruits or seeds, and buds in the middle and upper strata, bark in the low and middle strata and herbs on the ground. Wolf (Canis lupus), leopard (Panthera pardus), and golden eagle (Aquila chrysaetos) are predators threatening the survival of individual monkeys in the study site. The results suggested that the seasonal vertical distribution of food items eaten in forest, predators, and vegetation types had important effects on the terrestriality and tree stratum use of the monkeys.     

Effect of different primate species on germination of Ficus (Urostigma) seeds

We examined the germination of Ficus seeds (subgenus Urostigma) after defecation by six primate species (New World monkeys, Old World monkeys, and apes). Seeds from figs (control) and primate feces were placed in a thermostatically controlled chamber for 30 days. Seeds defecated by Alouatta palliata, A. pigra, and Cercopithecus aethiops showed significantly higher germination rates than control seeds. In addition, seeds from A. palliata feces germinated significantly faster than control seeds and seeds from C. aethiops and Pan troglodytes. These differences may be due to the different digestive characteristics of the six primate species. Zoo Biol 23:273–278, 2004. © 2004 Wiley‐Liss, Inc.     

Cathemerality and lunar periodicity of activity rhythms in owl monkeys of the Argentinian Chaco

Although most South American owl monkeys are mainly nocturnal, Aotus azarai azarai of the Argentinean Chaco regularly shows diurnal activity. In this study we examined the strong influence of moonlight on its diurnal and nocturnal activity, as well as the interaction of moonlight effects with other exogenous factors. We analyzed long-term automated activity recordings obtained with accelerometer collars from 7 owl monkeys during 2003 and 2004. Our data show marked lunar periodic and seasonal modulations of the owl monkeys' activity pattern. On full moon days they were active throughout the whole night and displayed reduced activity during the day. With a new moon, activity decreased during the dark portion of the night, peaked during dawn and dusk and extended over the bright morning hours. Waxing and waning moons induced a significant increase in activity during the first and the second half of the night, respectively. During the cold winter months the monkeys displayed twice as much activity throughout the warmer bright part of the day than during the rest of the year. These findings indicate that A. a. azarai is mainly a dark-active species, but is still able to shift a considerable portion of activity into the bright part of the day if unfavourable lighting and/or temperature conditions prevail during the night.     

Seasonal variations of fecal progesterone and 17beta-estradiol in captive female black-handed spider monkeys (Ateles geoffroyi)

A number of studies in free-ranging and captive spider monkeys (Ateles spp.) have shown that this genus is able to reproduce throughout the entire year. Nonetheless, it is still controversial whether births, and therefore conceptions, tend to be more frequent during certain seasons. In the present study, we monitored changes in fecal 17beta-estradiol and progesterone for approximately 1 years in five female black-handed spider monkeys (Ateles geoffroyi) kept in captivity in Mexico City. The objective was to determine whether hormone concentrations and menstrual cycles of summer and autumn accounted for a greater chance of conception than those of winter and spring, consistent with birth patterns previously reported. We collected fecal samples from the five monkeys almost daily for 1 year (March 2004 to February 2005) and used radioimmunoassay of fecal extracts to determine concentrations of 17beta-estradiol and progesterone. Concurrently, menstrual cycle phases were determined by cytological evaluation of vaginal swabs. Periovulatory 17beta-estradiol concentrations were significantly higher in autumn than in winter, spring or summer. Moreover, as evidenced by progesterone peaks, most of the summer-autumn menstrual cycles were ovulatory; in contrast, most of the winter and spring cycles were anovulatory. In conclusion, our data supported the notion that, although not a strictly seasonal reproducer, the black-handed spider monkey is more likely to conceive at the end of the rainy season and throughout autumn.     

Interaction of music and emotional stimuli in modulating working memory in macaque monkeys

Background music is one of the most frequently encountered contextual factors that affect cognitive and emotional functions in humans. However, it is still unclear whether music induces similar effects in nonhuman primates. Answering this question might bring insight to the long‐lasting question regarding the ability of nonhuman primates in perceiving and dissociating music from other nonmusical acoustic information. In the present study, macaque monkeys were trained to perform a working memory task that required matching visual stimuli. These stimuli had different emotional content (neutral, negative, and positive). Monkeys performed the task within different background acoustic conditions (music, same‐intensity noise, and silence). We hypothesized that the auditory stimuli might interact with emotional information of visual stimuli and modulate monkeys’ performance. Furthermore, if the effects of music and noise on monkeys’ behavioral measures differ it would mean that monkeys perceived and processed music differently. We found that, monkeys committed more errors and were slower when they encountered stimuli with negative or positive emotional content. In the presence of music, the influence of emotional stimuli on monkeys’ performance significantly differed from those of the neutral stimuli, however, in the presence of noise, the effects of emotional stimuli on monkeys’ performance were not distinguishable. The dissociable effects of music and noise on monkeys’ performance show that the effects of emotional stimuli were dependent on the background acoustic conditions. Our findings indicate that background music and the same‐intensity noise were differentially perceived by monkeys and influenced their cognitive functions.     

Locomotion and habitat use of Stampflii's putty-nosed monkey (Cercopithecus nictitans stampflii) in the Taï National Park, Ivory Coast

Stampflii's putty-nosed monkeys Cercopithecus nictitans stampflii are large, rare, poorly known guenons with a discontinuous distribution in West Africa. Putty-nosed monkeys occur at low densities in Ivory Coast's Tai National Park where they are believed to have migrated from less forested regions north of the park (Eckardt and Zuberbühler: Behav Ecol 15 (2004) 400-411). In this article, we compare the positional behavior of Putty-nosed monkeys to that of three other guenon species in the Tai Forest and provide an additional test of the relationship among locomotion, body size, maintenance activity, and habitat use in generalized arboreal quadrupeds. Our results indicate that putty-nosed monkeys confine the great majority of their locomotion to the main canopy where most movement occurs on boughs and branches. Comparison of overall locomotor frequencies across the four Tai guenon species reveals a general pattern; quadrupedalism accounts for at least 70% of the total profile, climbing ranges between 15 and 20%, and leaping accounts for 5-10% of total movement. The overall locomotor consistency among the taxa, especially between putty-nosed and Diana monkeys, is significant considering marked interspecific differences in support preference and strata use.     

Age-related changes in diurnal rhythms and levels of gonadotropins, testosterone, and inhibin B in male rhesus monkeys (Macaca mulatta)

Testosterone shows circadian rhythms in monkeys with low serum levels in the morning hours. The decline relies on a diminished frequency of LH pulses. Inhibin B shows no diurnal patterns. In elderly men, the diurnal rhythm of testosterone is blunted and inhibin levels fall. Here we explore whether aging exerts similar effects in the rhesus monkey. We collected blood samples from groups of young (6-9 yr) and old (12-16 yr) male rhesus monkeys at 20-min intervals for a period of 24 h under remote sampling via a venous catheter. We determined moment-to-moment changes in plasma levels of testosterone, FSH, and LH by RIA, and of inhibin B by ELISA. We found significant diurnal patterns of testosterone in both groups. The circadian rhythm in testosterone was enhanced in older monkeys. Testosterone levels and pulse frequencies dropped significantly below those of young monkeys during midday hours. Diminished pulse frequency of LH appeared to be responsible for the midday testosterone decrease in old monkeys, while LH and testosterone pulse frequency did not change in young monkeys at corresponding time points. Old monkeys showed extended periods of LH-pulse quiescence in the morning and midday hours. Inhibin B and FSH levels were generally lower in old monkeys compared with the young group, but neither inhibin B nor FSH showed circadian rhythms. We conclude from these data that old rhesus monkeys have a more prominent circadian rhythm of LH and testosterone resulting from an extended midday period of quiescence in the hypothalamus-pituitary-gonadal axis.     

Social behavior and gender in biomedical investigations using monkeys: studies in atherogenesis.

We review the use of socially housed cynomolgus monkeys (Macaca fascicularis) in biomedical research with emphasis on studies of atherosclerosis, particularly in the two specific domains of atherosclerosis investigation for which nonhuman primates are especially well-suited as animal models: gender differences and psychosocial influences. We found that the presence of normal ovarian function prevented exacerbation of diet-induced coronary artery atherosclerosis in female monkeys. However, any manipulation or condition which impaired ovarian function tended to diminish or abolish this "female" protection. Among group-housed female monkeys, low social status was accompanied by ovarian dysfunction and, not surprisingly, by exacerbated coronary artery atherosclerosis as well. Surgical menopause (ovariectomy) also induced exacerbation of coronary atherosclerosis in monkeys, a situation which was prevented by estrogen replacement therapy. Conversely, pregnancy (a hyperestrogenic state) resulted in markedly diminished atherosclerosis. A somewhat different pattern of atherogenesis emerged among socially-housed males. Here, socially dominant animals developed exacerbated coronary artery atherosclerosis, but only under conditions of social stress (viz., disruption caused by periodic reorganization of social group membership). We hypothesized that exposure to repeated group reorganizations provoked activation of the sympathetic nervous system among dominant animals; in turn, the hemodynamic and metabolic concomitants of sympathetic activation may have damaged the coronary arteries of these monkeys, potentiating atherogenesis. To test this hypothesis, males were housed in unstable social groupings, with half of the monkeys administered a beta-adrenergic blocking agent (to attenuate heart rate and blood pressure responses to stress). The beta-blocker inhibited atherosclerosis, but only among those animals behaviorally predisposed to develop exacerbated lesions (i.e. dominant monkeys). These results support the view that monkeys are suitable research models of atherosclerosis, a disease that affects millions of humans.     

Transfer of the Nonmatch-to-Goal rule in Monkeys across Cognitive Domains

To solve novel problems, it is advantageous to abstract relevant information from past experience to transfer on related problems. To study whether macaque monkeys were able to transfer an abstract rule across cognitive domains, we trained two monkeys on a nonmatch-to-goal (NMTG) task. In the object version of the task (O-NMTG), the monkeys were required to choose between two object-like stimuli, which differed either only in shape or in shape and color. For each choice, they were required to switch from their previously chosen object-goal to a different one. After they reached a performance level of over 90% correct on the O-NMTG task, the monkeys were tested for rule transfer on a spatial version of the task (S-NMTG). To receive a reward, the monkeys had to switch from their previously chosen location to a different one. In both the O-NMTG and S-NMTG tasks, there were four potential choices, presented in pairs from trial-to-trial. We found that both monkeys transferred successfully the NMTG rule within the first testing session, showing effective transfer of the learned rule between two cognitive domains.     

Cross-genus adoption of a marmoset (Callithrix jacchus) by wild capuchin monkeys (Cebus libidinosus): case report

We report a case of interspecies adoption of an infant marmoset (Callithrix jacchus) by wild capuchin monkeys (Cebus libidinosus). The marmoset was an infant when it was first observed in the capuchin group on 3 March 2004. Since it first appeared it has been observed informally and frequently. In January 2005 systematic observations were made of the marmoset and a capuchin of similar age. Throughout its period of adoption the marmoset appeared to be socially integrated into the group, benefiting from nurturant behaviors exhibited by two successive adoptive "mothers" and pronounced tolerance from all members of the group. This case highlights the flexibility of both Callithrix and Cebus in accommodating variable social behaviors and other characteristics (including size) of social partners.     

Effects of estradiol and aging on fine manual performance in female rhesus monkeys

Aging is characterized by a progressive deterioration of motor function related to dysfunctions of the nigrostriatal system. Because estrogen has been reported to protect dopaminergic neurons and to improve the motor deficits associated with Parkinson's disease, we hypothesized that it would partially reverse the age-related decline of motor function in normal aging. We tested the effects of estrogen treatment and withdrawal on fine motor performance in five aged (21-24 years old) and five young (6-9 years old) ovariectomized female rhesus monkeys. The tests required the monkeys to use each hand to retrieve a Life Saver candy from metal rods bent in shapes of different complexity. Monkeys were tested twice a week for 8 consecutive weeks, during treatment with placebo or ethinyl estradiol (EE(2)) in alternating 14-day blocks. Each behavioral test was videotaped and subsequently scored for the duration and the success of the first trial on each shape. Both groups of monkeys improved rapidly with practice in speed and success of retrieval. The older monkeys were slower but as successful as the young monkeys in retrieving the candy. The left hand was faster than the right hand for both the aged and young females. We failed to detect any effect of EE(2) treatment on speed or success of retrieval in either group. These results confirm the slowing of fine motor performance with aging in female rhesus monkeys. They also indicate that estradiol, at least as administered in this study, does not benefit fine manual performance.     

Perception of shape-from-motion in macaque monkeys and humans

Motion is one of the most efficient cues for shape perception. We conducted behavioral experiments to examine how monkeys perceive shapes defined by motion cues and whether they perceive them as humans do. We trained monkeys to perform a shape discrimination task in which shapes were defined by the motion of random dots. Effects of dot density and dot speed on the shape perception of monkeys were examined. Human subjects were also tested using the same paradigm and the test results were compared with those of monkeys. In both monkeys and humans, correct performance rates declined when density or speed of random dots was reduced. Both of them tended to confuse the same combinations of shapes frequently. These results suggest that monkeys and humans perceive shapes defined by motion cues in a similar manner and probably have common neural mechanisms to perceive them. Electronic Publication