Sexual behavior of wild Barbary macaque males (Macaca sylvanus)

Recent assertions that the Barbary macaque (Macaca sylvanus) is a multiple-or serial-mounting species are incorrect. Data are presented from over 300 copulations observed among wild Moroccan Barbary macaques which establish empirically that males of this macaque species are single mounters. The average length of an ejaculatory copulation was 8.7 sec, with a range of 6 to 14 sec. Ejaculation occurred an average of 6.3 sec after mounting, with an average of nine pelvic thrusts per ejaculation. Males appeared capable of ejaculating twice within 16 min, and three consecutive times within 37 min. Characteristically, only one mount and ejaculation occurred during a sexual association between an estrous female and each of her consorting males. Schemes of macaque evolution which incorrectly classify Barbary macaques as a multiple-mounting species should be viewed cautiously.     

Maternal discrimination of offspring vocalizations in Barbary macaques (Macaca sylvanus)

The response of Barbary macaque (Macaca sylvanus) females to vocalizations of their offspring was studied in a semi-free ranging population. The results of both facal observations and playback experiments demonstrated that mothers preferentially turned to their offspring's vocalizations over those of other young, providing evidence that mothers are able to recognize their offspring by acoustic signals alone. We assume that they may use this ability to monitor their infants' activities.     

A propos du Cercopithecidae (Mammalia,primate) villafranchien de l'Ain Brimba,Tunisie

C. Arambourg has described a new genus and a new species of a cercopithecid Anomalopithecus bicuspidatus (1), from the Ain Brimba Villafranchian site (Tunisia). This form is based on heterogeneous material: the species holotype is an upper incisor of Hyaena striata praecursor ARAMBOURG (1), meanwhile the syntypes (M₂ and M³) belong to Macaca sylvanus cf. sylvanus.     

A new 2CTAB/PCI method improves DNA amplification success from faeces of Mediterranean (Barbary macaques) and tropical (lowland gorillas) primates

Animal genomic DNA extracts of sufficient quality to address questions about population biology or behavioural ecology can be obtained from faeces when adequate extraction procedures are used. The presence of PCR inhibitors in extract products appears generally the main factor limiting DNA amplification success. We compared DNA amplification success from faeces of a tropical primate (western lowland gorilla, Gorilla g. gorilla) and a Mediterranean primate (Barbary macaque, Macaca sylvanus) between a standardized extraction technique widely used in animals (QIAamp^® stool kit), a technique mainly used in plant species (CTAB) and a new protocol (2CTAB/PCI). Amplification success varied from 51% to 97%, the highest success being reached with the 2CTAB/PCI protocol in both species.     

Estrogen and Progestogen Correlates of the Structure of Female Copulation Calls in Semi-Free-Ranging Barbary Macaques (<Emphasis Type="BoldItalic">Macaca sylvanus</Emphasis>)

Females of many Old World primates produce conspicuous vocalizations in combination with copulations. Indirect evidence exists that in Barbary macaques (Macaca sylvanus), the structure of these copulation calls is related to changes in reproductive hormone levels. However, the structure of these calls does not vary significantly around the timing of ovulation when estrogen and progestogen levels show marked changes. We here aimed to clarify this paradox by investigating how the steroid hormones estrogen and progesterone are related to changes in the acoustic structure of copulation calls. We collected data on semi-free-ranging Barbary macaques in Gibraltar and at La Forêt des Singes in Rocamadour, France. We determined estrogen and progestogen concentrations from fecal samples and combined them with a fine-grained structural analysis of female copulation calls (N = 775 calls of 11 females). Our analysis indicates a time lag of 3 d between changes in fecal hormone levels, adjusted for the excretion lag time, and in the acoustic structure of copulation calls. Specifically, we found that estrogen increased the duration and frequency of the calls, whereas progestogen had an antagonistic effect. Importantly, however, variation in acoustic variables did not track short-term changes such as the peak in estrogen occurring around the timing of ovulation. Taken together, our results help to explain why female Barbary macaque copulation calls are related to changes in hormone levels but fail to indicate the fertile phase.     

Cranio-Mandibular Biometrics and Skull Maturation of Macaca sylvanus L., 1758

We report on the biometrics of cranial and dental features in 42 Macaca sylvanus specimens from various museums across Europe. Age classes were determined following dental criteria. Standard biometric landmarks were used to take 17 measurements on the cranium and five on the mandible. The permanent cheek dentition (except the whole C₁/C¹–P₃/P³ complex) was also recorded with four measurements for each molar tooth (three for the P₄/P⁴). Skull measurements show strong sexual dimorphism for characters tied to the mandibular and muzzle/facial portions. The unusual molar dimorphism of M. sylvanus is an unexpected result, because the Cercopithecoid molar pattern is often considered as generally conservative and not very dimorphic. A significant difference between M. sylvanus and other macaques also regards the absolute narrowing of the molar distal loph. This difference may result from a retained plesiomorphic condition, perhaps correlated with the less specialized and tougher diet maintained by M. sylvanus. A multivariate comparison for cranial (both sexual and ontogenetic) difference in M. sylvanus suggests that the full maturation of the male skull shape is delayed longer than what would be expected according to the most restrictive dental criteria adopted here for subadult/adult discrimination. The clustering results, indeed, indicate that significant phenetic differences persist between most of the male crania which are far advanced in their latest dental steps and those of the “fully developed adults”. Outcomes of final growth such as those observed in M. sylvanus suggest that polymorphic maturational patterns can mislead the assessment for a true adult skull shape.     

Differences in Activity Budgets and Diet Between Semiprovisioned and Wild‐Feeding Groups of the Endangered Barbary Macaque (Macaca sylvanus) in the Central High Atlas Mountains,Morocco

The Barbary macaque, Macaca sylvanus is a very adaptable primate species occupying a wide range of habitats in Morocco and Algeria. Several groups of this endangered macaque can be found in tourist sites, where they are affected by the presence of visitors providing food to them. We compare the activity budgets and the diet of semiprovisioned and wild‐feeding groups of Barbary macaques in the central High Atlas Mountains of Morocco from February to August 2008. We used instantaneous scan sampling at 15‐min intervals. The behaviors included in the activity budget were feeding, moving, foraging, resting, and aggressive display. Food items were grouped into seven categories. We found no differences between the two groups in the daily percentages of records attributed to feeding. The semiprovisioned group spent significantly more time engaged in resting and aggressive behavior, and foraged and moved significantly less than the wild‐feeding group. There was no significant difference between the two groups in time spent eating leaves, fruits, or roots and bark. The semiprovisioned group, however, spent significantly less time per day feeding on herbs, seeds, and acorns than the wild‐feeding group. Human food accounted for 26% of the daily feeding records for the semiprovisioned group and 1% for the wild‐feeding group. Our findings agree with previous studies and indicate that in the tourist site, where food is highly clumped, macaques decreased foraging time yet showed higher levels of contest competition. Our results support the common claim that the diet of the Barbary macaque is highly flexible, differing among its varied habitats. Conservation efforts for the Barbary macaques should take into account the changes in behavior that human‐modified environments may cause.     

G-banding in the barbary macaque (Macaca sylvanus, Linnaeus, 1758) of Morocco

G-banding was performed on the lymphocytes of six barbary macaques (Macaca sylvanus). Four chromosomes appear to have polymorphic variants: number 1, number 4, number 16, and the “marker” chromosome, number 9. These polymorphic forms differe from the G-banding reported for Macaca mulatta, Macaca fascicularis, and Macaca arctoides. It may be that evolutionary relationships among various macaque species can be ascertained by using such chromosomal polymorphisms.     

A new species of fossil Mus (Rodentia, Muridae) from the Indian Himalaya: Evolutionary and phylogenetic implications

A new species of fossil Mus (Rodentia, Mammalia) is reported from the Late Pleistocene fluvio-lacustrine deposits of the Kumaun sector of Indian Himalaya. The fossiliferous horizon, medium-coarse grained sand lenses embedded in the massive carbonaceous mud, is exposed at locality Dulam and is Late Pleistocene (ca. 30 ka) in age. A new species, Mus dulamensis n. sp., is proposed. Characterized by strongly distorted and moderately elongated M¹ (about 170% of M² length) with prominent conules in front of the t₂, higher magnitude of stephanodonty (between the t₁ and t₄ and between the t₃ and t₆), moderately reduced M³ (about 56% of M² length) and stronger connection between the cusps, this species is distinct from all other species of the genus and is included in the “booduga group”. I suggest that M. dulamensis n. sp. is comparatively more derived than M. auctor, M. flynni, M. jacobsi and Mus sp. and it may have given rise to M. booduga or M. dunni. It is further suggested that presently living M. booduga and M. dunni are more specialized than Mus dulamensis n. sp.     

Rank relations among sisters in semi-free-ranging Barbary macaques (Macaca sylvanus)

Although semi-free-ranging Barbary macaque females are able to outrank older females from lower-ranking matrilines (matrilineal rank acquisition), they do not systematically outrank their older sisters, as is known to be the case for semi-free-ranging rhesus monkeys (Macaca mulatta) and Japanese macaques (Macaca fuscata). We test the hypothesis that differences in the support received by younger sisters against their older sisters and against older lower-ranking females might account for this interspecific difference. Thirty-one sister dyads, members of a group of 109 Barbary macaques living at La Montagne des Singes, France, were observed during 16 months. The results indicate that (1) all females were dominant to their younger sisters, and the latter were never observed to challenge their older sisters; (2) younger sisters received as much kin support against their older sisters as against older lower-ranking females; (3) only very young females received support from their kin against their older sisters; (4) younger sisters received much more support from nonkin females against lower-ranking females than against their older sisters; and (5) Barbary macaque females appear to be supported against their older sisters less frequently than rhesus macaque females are. We conclude that the lack of nonkin support is the main factor accounting for the failure of younger sisters to outrank their older sisters in Barbary macaques. Initially this might result from kin support not being sufficient to induce younger sisters to challenge and to solicit support against their older sisters.     

Intergroup variation in stable isotope ratios reflects anthropogenic impact on the Barbary macaques (Macaca sylvanus) of Gibraltar

Interactions with humans impact many aspects of behavior and ecology in nonhuman primates. Because of the complexities of the human–nonhuman primate interface, methods are needed to quantify the effects of anthropogenic interactions, including their intensity and differential impacts between nonhuman primate groups. Stable isotopes can be used to quickly and economically assess intergroup dietary variation, and provide a framework for the development of specific hypotheses about anthropogenic impact. This study uses stable carbon and nitrogen isotope analysis to examine intraspecific variation in diet between five groups of Barbary macaques, Macaca sylvanus, in the Upper Rock Nature Reserve, Gibraltar. Analysis of hair from 135 macaques showed significant differences in δ¹³C and δ¹⁵N values between a group with minimal tourist contact and groups that were main tourist attractions. Because we observed no overt physiological or substantial behavioral differences between the groups, feeding ecology is the most likely cause of any differences in stable isotope ratios. Haphazard provisioning by tourists and Gibraltarians is a likely source of dietary variation between groups. Stable isotope analysis and observational data facilitate a deeper understanding of the feeding ecology of the Barbary macaques relevant to the role of an anthropogenic ecology for the species.     

Fossil Macaca remains from RDB quarry (Villafranca d'Asti, Italy): new data and overview

Mentioned in faunal lists since the late 1960s, Macaca remains from Villafranca d'Asti (early Villafranchian, Italy) were never described in detail. If some doubts were reported in the past about the related stratigraphic position, at present, partly thanks to the original acquisition labels, there is enough information to place these finds within the updated stratigraphic and biochronologic framework of the Villafranca d'Asti area.The reported sample consists of upper dentition and postcranial bones. By size and morphology all these remains are clearly Cercopithecinae, comparable with the extant Macaca sylvanus and mostly distinguishable from Mesopithecus, Dolichopithecus and Paradolichopithecus. The dental remains in particular give us the opportunity to discuss an inferred European size trend from smallest Pliocene macaques up to the larger living species M. sylvanus. Although Pliocene localities in western Europe have yielded so far only scanty Macaca finds, our data (even if preliminary) refute a major overall size difference between the extant Barbary macaque and the related fossil remains.     

Reciprocation and interchange of grooming,agonistic support,feeding tolerance,and aggression in semi‐free‐ranging Barbary macaques

Evidence from a range of primate species indicates that grooming can be exchanged either for itself or for other rank‐related “commodities,” such as agonistic support, feeding tolerance, or reduced aggression. Patterns of exchange behavior have been found to vary considerably between species, and understanding the causes of this variation is central to the study of the evolution of primate social systems. It is, therefore, essential that exchange behavior is examined in a wide range of species and settings. This article is the first to explore the reciprocation and interchange of grooming in the Barbary macaque (Macaca sylvanus). We collected focal data on semi‐free‐ranging adult female Barbary macaques at Trentham Monkey Forest, England, and analyzed dyadic data using Generalized Linear Mixed Models. We found evidence for the reciprocal exchange of grooming and for the interchange of grooming for agonistic support and tolerance while feeding. There was no evidence that grooming was traded for a reduction in aggression; indeed, we found a positive relationship between aggression given and grooming received. This may reflect the “extortion” of grooming from subordinates by dominant animals. These results will facilitate comparative analyses of exchange behavior by adding to the current database a new species, characterized by a different social style from those macaque species previously investigated. Am. J. Primatol. 73:1127–1133, 2011. © 2011 Wiley Periodicals, Inc.     

Ecology,demography, and population genetics of barbary macaques in Algeria

Over a 9-year period from 1982 to 1990 ecological and demographic data were collected on two genetic isolates of Barbary macaques (Macaca sylvanus) in Algeria, from the deciduous oak-forest of Akfadou and from the evergreen cedar-oak forest of the National Park Djurdjura. Macaques at Djurdjura profit from more suitable ecological conditions and have a higher rate of population increase as well as a higher male migration rate than those at Akfadou. Genetic data, gained from 23 genetic markers (blood proteins), proved to be highly influenced by the demographic structure of the groups. The macaque populations of Akfadou and Djurdjura have become genetically differentiated. Group fission, coupled with founder effect (genetic drift) and kin-structured (matrilineal) separation, resulted in a priori genetic diversity between one newly-established group and its parent group.     

Habitat distribution and habitat preference in Barbary macaques (Macaca sylvanus)

Barbary macaques (Macaca sylvanus,L.) occur at varying densities in a number of different habitat types in Morocco and Algeria. Taub (1977) has argued that the abundance of the species in cedar forests of the Moyen Atlas, Morocco, is an indication of a habitat preference. A reexamination of available data on the distribution and abundance of Barbary macaques suggests that monkey numbers reflect the distribution of habitat size rather than habitat types. Differences between populations relative to habitat types can be seen only between forest and scrub localities. Human factors are considered more important in determining the present status of this eclectic feeder. The modern distribution of the Barbary macaque is inadequate evidence for a habitat preference.     

Comparative odontometrical analysis of the first lower molar in <Emphasis Type="Italic">Microtus (Terricola) multiplex</Emphasis> (Arvicolinae,Rodentia) from western Alps

The morphology of the first lower molar (M₁) of Microtus (Terricola) multiplex (Fatio, 1905) was compared amongst 15 populations from the Alps (Switzerland, Italy, France). M. multiplex orientalis from Trentino Alto Adige is close to the nominative subspecies M. multiplex multiplex from Ticino characterised by a great size, a not tilted pitymyan rhombus and an important development of the anterior part of the M₁. M. multiplex druentius from Ubaye mainly differs from the nominative subspecies by a smaller tooth size. Populations from Valle d’Aosta and Piemonte show on the whole a morphology intermediate between M. m. multiplex and M. m. druentius subspecies, however, the pitymyan rhombus is more tilted and the development of the anterior part more reduced in populations from Eastern and Central Piemonte. The Western populations (from Trièvès, Vercors, Royans and Chambaran) belonging to the subspecies M. m. niethammeri are the most differentiated with a small or median size of the M1, a reduced development of the anterior part and a very tilted pitymyan rhombus, particularly in the population from Chambaran. The populations from Matheysine and Grésivaudan are morphologically a link between M. m. druentius and M. m. niethammeri subspecies.     

A comparative study of adult facial morphology and its ontogeny in the fossil macaque Macaca majori from Capo Figari, Sardinia, Italy

This study examines the morphology of the face in the fossil macaque Macaca majori from Capo Figari (north-eastern Sardinia, Italy) in a comparative ontogenetic context. Thus, a fairly complete face from an adult representative of this fossil species is compared with 3 extant macaque species: Macaca sylvanus (of which species it is questioned whether it is a subspecies, M. sylvanus majori), Macaca mulatta and Macaca fascicularis. Additional incomplete subadult and adult specimens are also examined in order to compare their facial ontogeny with that of the same living species. The comparisons are based on facial landmark data and are undertaken using geometric morphometric methods. These studies indicate that the adult facial morphology and ontogeny of face size and shape in M. majori share much in common with extant macaque species. However, the adult M. majori face displays some unique morphological features, in particular with regard to lateral flaring and relative size of the zygomatic roots. From the study of a limited sample of fossils there is an indication that this flaring arises during postnatal growth, and in consequence the ontogeny of the face of this fossil species may be different from that of M. sylvanus and the other macaque species included in this analysis. From these studies, we conclude that M. majori shows differences in adult facial morphology and possibly in ontogeny from M. sylvanus compatible with a specific rather than subspecific distinction.     

Intergroup interactions in wild Barbary macaques (Macaca sylvanus), Ghomaran Rif mountains,Morocco

Data are presented on intergroup interactions between six groups of Macaca sylvanus in the Ghomaran region of the Moroccan Rif mountains. Intergroup encounters (0.026/observation hour) were defined as two groups being near each other (< 150 m). Encounters were further classified into: 1) neutral (indeterminate) encounters, in which very little intergroup interaction took place, with the exception of male monitoring (N = 7); 2) approach-retreat encounters with intergroup displacement, in which, without any overt agonism, members of one group slowly approached another and caused it to retreat (N = 3); and 3) agonistic encounters with intergroup displacement (N = 3). These results are compared to the only other study of intergroup interactions in wild Barbary macaques, and it is concluded that 1) observations of intergroup unification and/or coordination of movement in Barbary macaques (“herding”) probably resulted from observer error, or if these phenomena do occur, they are rare throughout the range of this species; 2) approximately half of all intergroup encounters in both studies resulted in intergroup displacement and/or intergroup agonism, evidence of intergroup competition; and 3) current data on intergroup interactions in Barbary macaques conform to the predictions of Wrangham's model of mutually competitive female-bonded, multimale groups.     

<Emphasis Type="Italic">Macaca munzala</Emphasis>: A New Species from Western Arunachal Pradesh,Northeastern India<Superscript>*</Superscript>

Macaca, comprising 20 well-characterized species, represents the largest and one of the most ecologically and socially diverse of all the nonhuman primate genera. We report the discovery of a macaque that is new to science from the high altitudes of western Arunachal Pradesh, a biodiversity-rich state in northeastern India. We propose the scientific name Macaca munzala and the vernacular name Arunachal macaque for the species. It shares morphological characteristics independently with the Assamese macaque (Macaca assamensis) and with the Tibetan macaque M. thibetana; like them, it appears to belong to the sinica species-group of the genus. However, the species is distinctive in relative tail length, which is intermediate between those of Tibetan and Western Assamese macaques, the subspecies with which it is sympatric. It is also unique in its altitudinal distribution, occurring largely at altitudes between 2000 and 3500 m. We provide a morphological characterization of the species, report preliminary data on its field biology and discuss possible taxonomic identity in relation to the other closely-related species of Macaca.^*This paper is dedicated to Dr. A. J. T. Johnsingh for his immense contributions to the study and conservation of India’s wildlife and for being an inspiration to a whole generation of students.