Behavioral responses of Barbary macaques (Macaca sylvanus) to variations in environmental conditions in Algeria

In this study, the behavioral responses of Barbary macaques to seasonal and interhabitat variations in resource availability were analyzed over an entire annual cycle. Two groups, one in an evergreen cedar–oak forest (Djurdjura) and the other in a deciduous oak forest (Akfadou), were observed. In this paper, references to data on resource availability published elsewhere are made. Time budget has been studied. Variations in foraging and moving time, in day–range lengths, and in time moving in trees have been considered to estimate the variations in foraging effort and thus energy expenditure. Great monthly variations in foraging effort and other activities were observed in both habitats. In early spring, when resource availabilities were maximal, foraging effort was low while monkeys maximized their feeding time (about 5 h/day). In June, during the peak of the birth season and the rearing period, monkeys minimized their feeding time to the benefit of social interactions (to 1.6–2.7 h/day), whatever the food availability, which was low in Akfadou and high in Djurdjura. In addition, foraging effort remained low in Djurdjura, while it increased in Akfadou. Thus, at the beginning of the dry summer period, monkeys in Akfadou were in a less favorable position than those in Djurdjura. At both sites, in periods of food shortage in summer or in winter, monkeys displayed two different strategies. In the former case, their foraging effort increased, while in the second one it remained relatively low. Whatever the foraging effort, monkeys did not reach the same amount of feeding time as in early spring. In the poorest site of Akfadou, foraging effort was globally greater than in the richest site of Djurdjura, especially for adults. At both sites, adult males spent more time feeding than juveniles and less time in social interactions. Results are discussed according to rearing period, temperatures, and day length constraints. The limits of adaptability to different habitats are considered in light of the demographic parameters. Am. J. Primatol. 43:285–304, 1997. © 1997 Wiley-Liss, Inc.     

Trichoepithelioma in a Barbary ape (Macaca sylvanus): review of cutaneous tumors in nonhuman primates and case report

A cutaneous tumor was surgically removed from a 10-year-old, male Barbary ape (Macaca sylvanus). Histologically, the tumor was primarily adnexoid in nature and contained structures that resembled abortive hair follicles. The tumor was diagnosed as a trichoepithelioma.     

Genetic differentiation within and between isolated Algerian subpopulations of Barbary macaques (Macaca sylvanus): evidence from microsatellites

This study of wild-living Algerian Barbary macaques ( Macaca sylvanus ) was designed to examine genetic variability in subpopulations isolated in residual forest patches, in an attempt to obtain data on the effects of habitat fragmentation. The wild population of this species (estimated at a maximum of 15 000) is vulnerable and this study therefore has direct relevance for conservation measures. Data from five microsatellite loci were analysed for 159 individuals from nine different groups living in four isolates in Algeria. Genetic polymorphism was found to be relatively high (4–12 alleles per locus) compared with other genetic markers used in previous studies of this species; mean expected heterozygosity was 65%. The four isolates are all genetically distinct ( F _ST = 0; P < 0.001). Indeed, the results suggest that dispersal is limited even between some social groups within a single isolate. Genetic distances based on models not assuming stepwise mutation ( F _ST and chord distance) gave very similar results and are highly correlated with geographical distances within one isolate but not between isolates. This may indicate that isolation by distance exerts a significant influence within an isolate but that genetic drift prevails between the four isolates. After allowing for variation in sample size, we found no evidence of reduced allelic diversity within small isolates that may have been separated for 250 years or more. The surviving population of Algerian Barbary macaques taken as a whole still shows marked variability in microsatellite alleles, but maintenance of genetic variability over the long term will surely require effective protection of all isolates.     

Triadic interactions in captive Barbary macaques (Macaca sylvanus,Linnaeus, 1758): “Agonistic buffering”?

This study presents data on the expression of male-immature triadic interactions, previously termed agonistic buffering, in a captive Macaca sylvanus group. Agonistic buffering has been hypothesized as inhibiting or modifying the expression of aggression. This was tested by examining (1) the dominance ranks of the animals involved in the triadic interactions, (2) the events preceding and following the triadic interactions, and (3) the presence of an infant in nonagonistic encounters between juvenile, subadult, and adult males. The results obtained do not support the hypothesis of agonistic buffering as the single explanation for triadic interactions, but emphasize the contextual variability in the expression of these triadic interactions.     

Testing the reliability of noninvasive genetic sampling by comparing analyses of blood and fecal samples in Barbary macaques (Macaca sylvanus).

Genetic studies of wild animal populations are often hindered by difficulties in obtaining blood samples. Recent advances in molecular biology have allowed the use of noninvasive samples as sources of DNA (e.g., hair or feces), but such samples may provide low-quality DNA and prevent the determination of true genotypes in subsequent DNA analysis. We present a preliminary study aimed at assessing the reliability of using fecal samples for genotyping in Barbary macaques (Macaca sylvanus). The test was performed on samples of blood and feces from 11 captive animals, using three dinucleotide microsatellites. The CTAB DNA extraction method was found to be the most relevant for Barbary macaque feces, yielding successful amplification at all loci for 70% of PCRs. All the fecal samples tested gave correct genotypes at least once for each locus when referenced against blood-derived genotypes. An average of 18.3% of PCRs displayed spurious genotypes (false homozygous or false allele). The minimum theoretical probability required to obtain a 100% accurate genotype is 0.74, based on the criterion that a correct genotype is assessed only if it was observed at least twice. The observed probability of obtaining a correct genotype from three PCRs, based on our genotyping results, was greater (0.81 on average) than the minimum threshold. In conclusion, our comparison of blood and fecal samples showed that fecal sampling is a reliable tool for the further study of wild Barbary macaque populations.     

Behavior, Diet, and Movements of the Sulawesi Crested Black Macaque (Macaca nigra)

We present the first field study of activity budgets, diet and ranging patterns of the Sulawesi crested black macaque, Macaca nigra, one of seven macaque species endemic to Sulawesi, Indonesia. We studied three crested macaque groups, ranging in size from 50 to 97 individuals, for 18 months in the Tangkoko-DuaSudara Nature Reserve, North Sulawesi. They spent 59% of the day moving and procuring food, especially fruits, and 41% of the day resting and socializing. Their diet is composed of more than 145 species of fruit (66% of observed feeding bouts), vegetative material (2.5%), invertebrates (31.5%), and occasional vertebrate prey. Group differences were more pronounced than seasonal or diurnal differences. Specifically, the largest group moved farther during the day, moved at a faster and more uniform rate, ate less fruit, rested more, and socialized less than the smaller groups did. The largest group had the largest home range, but it included less primary forest and more disturbed habitat than the ranges of smaller groups. There are individual differences in activity budgets of adult males and females in time spent moving, resting, feeding, and socializing that may reflect differences in reproductive strategies of males versus females. The behavior of large juveniles is more similar to that of adults than to that of small juveniles. Daily movements and use of home range are correlated with diet. Macaques moved shorter distances as the proportion of time spent feeding on fruit increased, and the top four dietary items accounted for most of the variance in entry into hectare blocks of home range.     

Female ovarian cycle phase affects the timing of male sexual activity in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar

Although all macaques have a multimale multifemale mating system, the degree of promiscuity shown by the Barbary macaque is considered to be extreme in terms of both mating frequency and number of mating partners. How mating activity is distributed throughout the female menstrual cycle and whether or not copulations are concentrated around the fertile phase as in other members of the genus is, however, not known. To examine this, we collected data on rates of copulation throughout 29 ovarian cycles from 13 free-ranging females of the Gibraltar Barbary macaque population and related them to the time of ovulation and the female fertile phase as determined from fecal hormone analysis. In addition, patterns of male inspection of females and time spent in consortship, both indicators of female attractivity, were also analyzed. The results indicate that both mating behavior and female attractivity vary predictably with ovarian cycle stage. Rates of copulation were found to increase toward the time of ovulation, with a distinct peak of ejaculatory (but not non-ejaculatory) copulations occurring in the fertile phase. Additionally, we show that frequency of inspection of females by males and time spent in consortship were also highest during the fertile phase and that ejaculatory copulations and male pericopulatory behaviors were significantly correlated with levels of female sex hormones. Our findings indicate that the Barbary macaque shows a mating pattern during the cycle similar to that described for other members of the genus. More importantly, however, our study provides clear evidence that despite an extreme degree of promiscuity Barbary macaque males concentrate their reproductive effort to the fertile phase, implying that they are able to discern this period and that thus timing of ovulation is not concealed from them. Estrogen-related cues appear to be involved in the process of recognition of female reproductive status by males, but the exact nature of these cues and how male Barbary macaques use them remains to be clarified.     

Visitor Perceptions of Captive,Endangered Barbary Macaques (Macaca sylvanus) Used as Photo Props in Jemaa El Fna Square,Marrakech, Morocco

ABSTRACT

Visitors to Jemaa El Fna Square can pay to have their photograph taken with Barbary macaques. Our aim was to characterize visitors’ perceptions of such photo props, enabling demand-reducing interventions to be targeted appropriately and destination managers to maintain or enhance the visitor experience. Visitors to Jemaa El Fna (n = 513) were surveyed using a 25-item questionnaire including closed and open questions. Most visitors (88%) neither intended to use macaque photo props nor did; 7% either intended to or did use photo props; while 5% both used photo props and had intended to do so. Moroccans were more likely than foreigners to use macaque photo props or intend to do so. Among international visitors, those who had their photo taken or intended to were younger, with a lower level of education and lower income than those who neither had their photo taken nor intended to. Visitors who did not use photo props pitied the animals’ treatment, disapproved of captivity or exploitation, had concerns over hygiene or safety, and disliked trader harassment. Visitors who did use photo props valued novelty and contact with the animal, although half of them also described negative experiences including trader harassment and animal mistreatment. While 16% felt the presence of macaques makes Marrakech lively and interesting, 40% recognized risks to health and safety, and 57% thought Marrakech would be a better place without macaque photo props. Although 66% agreed the practice should be illegal, 80% were unaware that it is illegal. Only 25% correctly identified the Barbary macaque as endangered. Macaque photo props undermine current conservation objectives and legislation, contribute to Disneyfication of macaques, and may threaten the image of the destination; however, their appeal to a minority of visitors indicates a desire to interact with animals, which visitor education might divert toward more responsible tourism.     

No Short‐Term Contingency Between Grooming and Food Tolerance in Barbary Macaques (Macaca sylvanus)

The exchange of services such as allo‐grooming, allo‐preening, food tolerance and agonistic support has been observed in a range of species. Two proximate mechanisms have been proposed to explain the exchanges of services in animals. First, an animal can give a service to a partner depending on how the partner behaved towards it in the recent past. This mechanism is usually tested by examining the within‐dyad temporal relation between events given and received over short time periods. Second, the partner choice mechanism assumes that animals give favours towards specific partners but not others, by comparing how each partner behaved towards them over longer time frames. As such, the partner choice mechanism does not make specific predictions on a temporal contingency between services received and given over short time frames. While there is evidence for a long‐term positive correlation between services exchanged in animals, results for short‐term contingencies between services given and received are mixed. Our study investigated the exchange of grooming for food tolerance in a partially provisioned group of Barbary macaques, by analysing the short‐term contingency between these events. Tolerance over food was compared immediately after grooming and in control condition, using food of different shareability. We found no evidence that grooming increases food tolerance or decrease aggression around food in the short term. Food tolerance was affected by the shareability of the food and the sex of the partners. The exchanges of grooming and food tolerance in non‐human primates may be little affected by recent single events. We suggest that long‐term exchanges between services given and received and social partner choice may play a more important role in explaining social interactions than short‐term contingent events.     

Frequency of aggressive behavior and a case of mortal attack in wildMacaca sylvanus in the Middle Atlas region (Morocco)

We observed a mortal attack against an adult female in a wild population ofMacaca sylvanus in the Middle Atlas Cedar forest ecosystem near the town of Azrou, Morocco. This species is generally believed to be the least aggressive in the whole GenusMacaca. We investigated the possible factors responsible for such an extreme case of increased aggression such as: 1) density of population, 2) availability of food rescues, 3) male competition for females. During a twelve month behavioral observation, we compared the hourly agesex class aggression frequency in the population where the mortal attack occurred with another macaque population living in different ecological conditions relative to density, food distribution and distance from human settlements. The pattern of age-sex seasonal distribution of aggression shows that, in the Middle Atlas, the adult female is the age-sex class most involved in aggressions and especially during food shortage and when resources are patchily distributed, as in the case were the mortal attack occurred.     

Brief communication: Self‐suckling in Barbary macaque (Macaca sylvanus) mothers before and after the death of their infant

We report here self‐suckling in four wild female Barbary macaques (Macaca sylvanus), living in two troops (i.e. “Flat face” and “Large” troop) in the middle‐Atlas Mountains, Morocco. The four females lost their infants due to predation or for unknown causes. Self‐suckling was observed before and after the infants died in the four females living in the “Flat face” troop. When the infants were still alive, self‐suckling was of short duration and it was probably a method to improve milk flow when the infant switched from one nipple to the other. After the infants died, self‐suckling lasted significantly longer and the females were apparently drinking their own milk. Self‐suckling was never observed among the four lactating females in the “Large” troop (including one monkey who lost her infant) and it could thus represent a cultural difference. Moreover, self‐suckling after the death of an infant may be explained by the energetic and immunological benefits that a monkey may gain from drinking their own milk. Finally, self‐suckling may have a stress‐releasing effect on the mothers who have lost their infants. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Activity patterns of Asiatic black bears (Ursus thibetanus) in the Central Mountains of Taiwan

Shifts in activity patterns and time budgets in response to environmental variables may yield insights into key factors affecting animal life histories. Activity data on wild Asiatic black bears Ursus thibetanus are limited, and non-existent in tropical portions of their geographic range. During November 1998–November 2000, we monitored the activity (active vs. inactive) of bears within a national park in the tropics of central Taiwan. On the basis of 4630 readings from motion-sensitive transmitters obtained in 24-h monitoring sessions, bears were active 54–57% of the time over the course of the year. However, bears were more active during summer (60±15% sd ) and fall (60±15%) than in spring (47±13%). They were active mainly during daylight hours in spring and summer, and also during fall when acorns, a principal fall food, were scarce. However, extensive nocturnal activity occurred in fall when acorns were abundant. Increased nocturnal activity in fall is consistent with studies of the related American black bear Ursus americanus , and suggests that this behavior is not necessarily driven by preparation for winter denning or because of disturbance by hunters (as posited in previous studies), as bears in our study did not den (except parturient females) and were not hunted or otherwise disturbed by people.     

Diet composition of the endangered giant water bug Lethocerus deyrolli (Hemiptera: Belostomatidae) in the rice fields of Japan: Which is the most important prey item among frogs,fish, and aquatic insects?

The food habits of the endangered giant water bug, Lethocerus deyrolli, were studied in the rice fields of Nose, in the north of Osaka Prefecture, Japan. Field observations revealed that frogs were the most important prey item. Frogs represented 86.4% and 78.6% in the diet of L. deyrolli in spring and summer, respectively. Among seven species of three families (Hylidae, Rhacophoridae, and Ranidae) exploited by L. deyrolli, the most important food item was adult Hyla japonica in spring and juvenile Rana nigromaculta in summer. Fish and aquatic arthropods were not considered important foods for L. deyrolli. The frog‐dependent food habits indicate that the recovery and conservation of frogs should be prioritized to protect L. deyrolli from extinction.     

Dietary diversity of an ecological and macronutritional generalist primate in a harsh high‐latitude habitat,the Taihangshan macaque (Macaca mulatta tcheliensis)

Recent advances in niche theory have stressed the importance of understanding dietary generalism at multiple levels, including the range of habitat and foods exploited by a species, foods exploited within populations, and patterns of nutrient intake. Here we apply this framework to examine the dietary strategy of the Macaca mulatta, a primate species that is second only to humans in their breadth of geographical distribution, and occupy diverse ecological habitats from cold temperate to tropical latitudes. A recent study showed that the Taihangshan subspecies ( M. mulatta tcheliensis) in China, which is found at the northern latitudinal limit of the species range, respond to ecologically constrained interannual variation in the macronutrient ratios of the spring diet in a way that theory predicts should be associated with ecological generalism. Here we further extend this study, examining the relationships between seasonal variation in food availability and the patterns of food selection across a full year. We found that, despite the ecological and macronutritional generalism of the species, Taihangshan macaques subsist on a relatively small range of foods (57 different foods, spread across 8 categories comprising seeds, fruits, buds, flowers, leaves, herbs, young bark, and twigs), but face considerable seasonal variation in the combinations available. In spring and summer, when seeds were scarce, leaves accounted for 60.3 ± 13.8% of their diet (dry matter [DM] %), and herbs contributed 31.7 ± 22.2%. However, in autumn and winter, when seeds were abundant, they contributed 68.5 ± 22.7% of the diet while herbs accounted for 18.9 ± 12.9% on a DM. Although young bark and twigs were available in all seasons, the macaques only fed on them in winter. We present comparative data from the literature on the diets of M. mulatta and other Macaca species, to interpret this pattern of resource use within the framework of multilevel niche theory.