Discrimination of macaques by macaques: the case of Sulawesi species

A series of work by the first author have demonstrated that many macaque species show a visual preference for the pictures of their own species when the monkeys actively press a lever to see the pictures. We expanded this study to Sulawesi macaques kept as a pet by local people with slight modification. All seven species of Sulawesi macaques were passively exposed to a variety of colored slides of Sulawesi macaques. The experimenter recorded the duration of visual fixation onto the pictures. Male monkeys of all the seven species clearly watched the pictures of their own species for longer duration than those of the other species. Such visual preference suggested that the seven Sulawesi macaques discriminate each other species and, thus, they may not be integrated into fewer number of species. This visual preference may work to prevent overall intergradation of the Sulawesi macaques who sometimes have hybrid zones only in limited areas. This preference was in general weaker in female monkeys. In one species,Macaca ochreata, females actively avoided to see the pictures of conspecifics. These results may be related to how female monkeys interact with other individuals.     

Development of visual preference for closely related species by infant and juvenile macaques with restricted social experience

Japanese and rhesus monkeys aged between 9 months old and 5 yrs old pressed a lever to see a variety of pictures of seven macaque species. These monkeys had various restricted social experience: namely, either reared by humans with conspecific or heterospecific peers, or cross-fostered between these two species. Rhesus monkeys tended to prefer seeing rhesus monkeys best among the pictures of the seven species without regard to their age or social experience. Japanese monkeys having restricted experience also liked to see rhesus monkeys better than Japanese monkeys, but not the best among the seven species. In a previous study, mother-reared infants of Japanese monkeys preferred seeing pictures of their own species over those of rhesus monkeys. These results suggest a dissociation of the determinants of this basic social preference: rhesus monkeys prefer to see their own species by nature while Japanese monkeys may learn to prefer their own species.     

Responses to urinary stimuli in pigtailed (Macaca nemestrina) and stumptailed (Macaca arctoides) macaques

Responses to different urine samples were studied in pigtailed (M. nemestrina) and stumptailed (M. arctoides) macaques. Both species exhibited more interest towards urine samples from their own species than neutral stimuli. Responses towards urine samples from other macaque species did not significantly differ from those towards neutral stimuli. In stumptailed macaques, no differential interest was observed between urine samples from a known (the adult male of the group) and an unknown adult male conspecific.     

Role of some physical characteristics in species recognition by pigtail monkeys

Three adult pigtail monkeys pressed a lever to see pictures of pigtail and Japanese monkeys with a variety of physical features being removed. The features included head, tail, body, background, and color. The duration and the interval of exposure of these visual stimuli were dependent upon subjects' responding. Preferences for those pictures were evaluated by the ratio of lever-pressing duration to interval of lever-pressing. Two of the subjects showed a consistent preference to see pictures of pigtail monkeys over those of Japanese monkeys. Though this preference tended to maintain when these physical features were removed, it became relatively weak when head and head + tail were removed. These results suggest that pigtail macaques may discriminate species based not on a single characteristics but on some combination of features, and that head may be relatively important than the other features.     

The stumptail macaques of China

The stumptail macaque species Macaca thibetana and Macaca arctoides replace one another from north to south in subtropical and tropical China. These species differ in external and cranial characters. Neonatal pelage color is pale grayish-brown in M. thibetana and whitish in M. arctoides. In adults, ventral pelage is whitish in M. thibetana and brown in M. arctoides. The forehead and cheeks are thickly furred in adult M. thibetana and bald in M. arctoides. Facial skin color typically is sexually dimorphic in M. thibetana—buffy in males and reddish in females—and monomorphic in M. arctoides—reddish in both sexes. Head and body length, weight, relative tail length, and relative ear length all tend to average greater in M. thibetana than in M. arctoides. Skull length, rostral-postrostral ratio, and relative canine length in males average greater in M. thibetana. than in M. arctoides; relative zygomatic breadth and relative bimalar breadth average greater in M. arctoides than in M. thibetana. Reproductive anatomy in both sexes is strikingly divergent in these two species. Although these species are adapted to different climatic zones, many aspects of their natural history are generally similar, as far as is now known. One apparent behavioral difference is that M. thibetana usually sleeps in caves or rocky crevices, while M. arctoides usually sleeps in trees.     

Reappraisal of <Emphasis Type="Italic">Macaca speciosa subfossilis</Emphasis> from the Late Pleistocene of Northern Vietnam Based on the Analysis of Cranial Anatomy

Jouffroy (Bulletin du Muséum National d'Histoire Naturelle. Série 2 31:209–216, 1959) described Macaca speciosa subfossilis on the basis of her study of the external anatomy of a nearly complete cranium (PV F1; Muséum national d’Histoire naturelle, Paris) found in the Late Pleistocene cave deposits, Thung-Lang, northern Vietnam. Whereas Jouffroy (Bulletin du Muséum National d'Histoire Naturelle. Série 2 31:209–216, 1959) considered it to belong to an ancestor of Macaca arctoides or M. thibetana, Fooden (Journal of Human Evolution 19:607–686, 1990) reexamined the facial anatomy and assigned it to the extant species M. arctoides. We used computed tomography images to reevaluate the phylogenetic position of Macaca speciosa subfossilis by comparing the external and internal features of PV F1 with those of the crania of the extant macaque species. PV F1 shows a lower degree of preorbital concavity than Macaca arctoides, M. assamensis, and M. thibetana, but shares an anteriorly directed malar as seen in the crania of the two former species. The size of the molars of PV F1 falls within a range such that the cranium may be assigned to any of the five species of Macaca arctoides, M. assamensis, M. thibetana, M. mulatta, and M. nemestrina. An analysis of the internal structure of the cranium reveals that only PV F1 and the cranium of Macaca arctoides have a pear-shaped nasal cavity expanding laterally at both the anterior and posterior regions. Such a feature is probably a derived condition in the macaque lineage, suggesting a close relationship between Macaca speciosa subfossilis and M. arctoides. This finding supports the paleobiological scenario that the members of the lineage of Macaca arctoides diverged from the other members of Asian macaques and became distributed in northern Vietnam as early as the Late Pleistocene.     

Morphometric analysis ofMacaca arctoides andM. thibetana in relation to other macaque species

As a first step in reviewing the classification of the two stump-tailed macaque species,Macaca arctoides andM. thibetana, as compared with other species of the genusMacaca, 72 linear dental and cranial variables of 11 macaque species were examined by morphometric analyses. The results indicate that the two stump-tailed species are the largest of the macaques and although rather similar overall, they exhibit significant differences in the pattern of variation in most of the five skull regions as shown by Principal Components and Canonical Variate Analyses. Euclidean Distances based on Canonical Variate scores indicate that the females ofM. arctoides andM. thibetana are more widely separated than eight other pairs of macaque species, and that the separations of the respective males are greater than those of three other pairs of species. These findings are consistent withFooden's classification of the stump-tailed macaques as two separate species (Fooden, 1976;Fooden et al., 1985). The present results suggest, as other researchers have proposed on the basis of external features, biochemistry and genetics, that the two stump-tailed macaque species andM. assamensis are closely related. The results also tentatively imply associations withM. fuscata andM. sylvanus but these require further study. The findings have implications for the assessment of the various Chinese Pleistocene macaque fossils.     

Genetic polymorphism of alpha-1-antitrypsin in macaque species

Thirty-two phenotypes of alpha-1-antitrypsin (al-AT) controlled by 18 codominant alleles of PI_mac locus were identified by isoelectric focusing in 1.121 macaques of nine species. In terms of al-AT polymorphism macaque species vary markedly from nearly monomorphic (Macaca mulatta, M. arctoides) to highly polymorphic (M. nemestrina, M. fascicularis). Only 4 of 18 PI_mac alleles are common for two or more macaque species, the rest of the alleles are species-specific.     

Wounding patterns in three species of captive macaques

The incidence of wounding in captive groups of rhesus (Macaca mulatta), pigtail (M. nemestrina), and stumptail (M. arctoides) macaques was studied for 21 months. Groups were monitored daily for evidence of wounding. Wounded animals were captured, treated by veterinary staff, and returned following recovery. Records were kept on the age, sex, and species of the recipient, along with the type and location of wound. In each species of macaque, adult males incurred the highest frequency of wounds and multiple wounds of any age-sex class. This contrasted with previously reported behavioral data indicating low frequencies of aggression received by adult males, especially contact aggression and bites. These discrepancies indicate wounding frequencies do not necessarily correspond with behavioral measures of aggression. Inhibition of aggression directed toward infants and the selective avoidance of bites directed to vital body regions were presented as possible mechanisms that modify intragroup aggression. Increased wounding in the birth season under captive conditions suggests that the pattern of increased wounding reported during the breeding season under freeranging conditions may reflect xenophobic responses to immigrating males, rather than direct male-male competition for estrous females.     

Baculum length and copulatory behavior in primates

The length of the baculum (os penis) was measured in 74 adult males representing 46 primate species. These data, and a review of previously published measurements, indicate that variation in baculum length among primates is related to taxonomic and behavioral differences. Thus, many New World monkeys have shorter bacula, relative to body weight, than Old World monkeys. The baculum is shorter in colobine monkeys than in cercopithecines. Among the great apes, reduction of the baculum is more pronounced in Pan and Gorilla than in Pongo. Very long bacula are found in some nocturnal prosimians (eg, Lorisidae) and also in Macaca arctoides. A comparison of baculum length relative to body weight was made in 34 species for which detailed information on copulatory behavi or was available. The presence of an elongated baculum was shown to correlate with copulatory patterns involving prolonged intromission and/or the maintenance of intromission during the postejaculatory interval (eg, Galago crassicaudatus, Loris tardigradus, M, arctoides). The evolutionary significance of these observations is discussed and it is suggeted that similar copulatory patterns may occur in species with elongated bacula (eg, Daubentonia, Perodicticus) for which behavioral data are lacking at present. The same hypothesis also applies to an extinct adapid primate which possessed a very large baculum.     

Non-seasonal breeding pattterns in stumptail macaques (Macaca arctoides)

This paper summarizes published reports of breeding patterns across the genusMacaca. Patterns range from strictly seasonal to non-seasonal. Data on sexual behavior and birth patterns are presented which confirm previous reports of non-seasonality forMacaca arctoides. In a captive colony, 63 births were recorded, and individuals were born during every month of the year. Heterosexual mounting activity was recorded over a two-year period and occurred during every month of that period. It is clear thatM. arctoides does not exhibit the seasonal cyclicity observed in some other macaque species.     

Experimental analysis of causal relationships between grooming behavior and inter-individual proximity in the stumptailed macaque (Macaca arctoides): a preliminary report

Some causal relationships between allogrooming, autogrooming, locomotion and close proximity in the behavior of one (adult female) Macaca arctoides while in the presence of another (adult male) monkey of the same species are reported. Allogrooming reduces the probability of walking away in the groomer, and thus increases the time spent close to the other monkey; autogrooming seems to have a similar effect. The duration of autogrooming is increased in a non-proportional manner by reduction of locomotion, but the duration of autogrooming seems to directly reduce the amount of locomotion. Up to a certain optimal value, the duration of autogrooming increases accordingly as the time spent close to the other monkey increases. The duration of allogrooming may be influenced in the same way as the duration of autogrooming.     

Fibrinopeptides A and B of Japanese monkey (Macaca fuscata) and patas monkey (Erythrocebus patas): their amino acid sequences, restricted mutations, and a molecular phylogeny for macaques, guenons, and baboons

Amino acid sequences of fibrinopeptides A and B from the macaque, Macaca fuscata (Japanese monkey) and the guenon, Erythrocebus patas (patas monkey) were established. Fibrinopeptides A of the monkeys had a sequence identical with those of baboons: Ala-Asp-Thr-Gly-Glu-Gly-Asp-Phe-Leu-Ala-Glu-Gly-Gly-Gly-Val-Arg. Fibrinopeptides B were 9-residue, "short," peptides with the sequences Asn-Glu-Glu-Ser-Leu-Phe-Ser-Gly-Arg for M. fuscata and Asn-Glu-Glu-Val-Leu-Phe-Gly-Gly-Arg for E. patas. The sequence of the B peptide of M. fuscata differed from that of a close-related species, M. mulatta (rhesus monkey), at a single site, Leu (M.f.)----Pro (M.m.). A single replacement between the B peptides of E. patas and Cercocebus aethiops (green monkey), Val (E.p.)----Gly (C.a.), was detected. A phylogenic relationship of macaques, guenons, and baboons, named Cercopithecinae (Old World monkey), was deduced from the sequence data. A selective rather than random amino acid replacement was observed in the B peptides of these Old World monkeys, suggesting a restricted mutation of their fibrinopeptides during primate evolution.     

Vocal communication of tonkean macaques in confined environments

Vocal recordings of one semi-free-ranging group and one captive group of Tonkean macaques (Macaca tonkeana) were used to establish the vocal repertoire of the species. Only the alpha male of the groups uttered a very distinctive loud call. Localization variants of coo calls were found. Alarm calls given by this species were acoustically similar to those by Japanese, rhesus, and long-tailed macaques (M. fuscata, M. mulatta, andM. fascicularis). Adult females uttered a specific variant of vocalizations during sexual morphological changes. The repertoire of agonistic vocalizations was more variable than that of any other macaque species investigated. These characteristics were discussed with reference to previous studies on vocalizations of macaque species.     

Cranial adaptation to a high attrition diet in Japanese macaques

Primates with diets that require greater occlusal forces to process exhibit anteroposteriorly shorter, vertically deeper faces, more anteriorly placed masseter attachment areas, and broader, taller mandibular corpora compared to closely related species/populations. Japanese macaques (Macaca fuscata)eat different, perhaps mechanically tougher to process, foods than other macaques do. Accordingly, they should exhibit structural features of the skull related to dissipating great occlusal loads. To test this hypothesis I compared cranial variables amongst wild-caught, adult female skulls (n = 85) of M. fuscataand three other macaque species (M. mulatta, M. fascicularis,and M. nemestrina)and applied least-squares and reduced-major-axis regression analysis and principal components analysis (PCA) to 17 cranial variables reflecting facial, vault, and mandibular dimensions. When scaled for size, the Japanese macaque has a vertically deeper and anteroposteriorly shorter face,a broader but not taller mandibular corpus, and a more anteriorly placed masseter muscle than the other three macaques do. The first PCA axis isolates variation due to a suite of characters related to mechanical efficiency in dissipating occlusal loads (vertically deep face and broad corpus) and differentiates the Japanese macaques from the other species. This, coupled with reported dietary differences among species, suggests that Japanese macaques are selected for dissipating greater occlusal loads than other macaques are. The presence of a narrow mandible relative to cranial breadth and a hyperrobust mandibular corpus width suggests that axial torsion is a significant influence in the masticatory regime of M. fuscata.The lack of an increase in corpus height indicates that parasagittal bending is not as significant an influence. Geographic and climatic influences cannot account for the patterns of variation between M. fuscataand the other macaques.     

Copulatory behavior in relation to anatomical characteristics of three macaques

Anatomy of copulatory organs and patterns of copulatory behavior were studied in three species of Macaca. The copulatory behavior of the rhesus monkey (M. mulatta) and crab-eating macaque (M. fascicularis) were similar. Mounting time was longer in stump-tailed macaque (M. arctoides) (48 seconds) than in the rhesus monkey or crab-eating macaque (8.5 seconds). Species differences were correlated with anatomical differences in the female and male reproductive organs. In the stump-tailed macaque the male has a relatively long penis, and the female has an elaborate vestibular colliculus in the vestibule. Both rhesus and crab-eating macaques have a short penis, and the female has no vestibular colliculus. Under scanning electron microscope, cone-like projections (3–4 mm) were observed on the surface of the glans and corpus penis of M. arctoides. In M. fascicularis shorter projections (0.05–0.1 mm) were observed on the glans penis but not the corpus penis.     

Birth and breeding cyclicity in an outdoor living stumptail macaque (Macaca arctoides) group

Birth records were examined for a group of 56 Stumptail macaques that lived in an half-acre outdoor enclosure from 1971 to 1974. Approximate conception times for 33 offspring were calculated and two graphs, one for births and the other one for fertile matings were constructed. Although births occurred throughout the year, 48.5% or these took place between June and September with a peak in July and August (39.4%). Two secondary peaks, one between February and April (27.3%) and the other in November (12.1%) were noted. Fertile matings also took place throughout the year but 56.6% were concentrated between January and June with a peak in January and February (30.3%). A secondary peak was observed for September (12.1%). The data show that no discrete seasonality in matings and births is present forMacaca arctoides but that an unusual pattern consisting of three peaks throughout the year, for births, may be typical of the species. The data are compared with data on the taxonomically close Japanese macaque and a striking dissimilarity is found. While thefuscata macaque has discrete breeding seasonality, thearctoides macaque breeds and gives birth throughout the year and its pattern is more similar to that of the distantly related Crab-eating macaque. This work was supported by grants from Behavioral Sciences Foundation and by NSF-#GB-42235.     

Evolution of genes involved in the unusual genitals of the bear macaque,Macaca arctoides

Genital divergence is thought to contribute to reproductive barriers by establishing a “lock‐and‐key" mechanism for reproductive compatibility. One such example, Macaca arctoides, the bear macaque, has compensatory changes in both male and female genital morphology as compared to close relatives. M. arctoides also has a complex evolutionary history, having extensive introgression between the fascicularis and sinica macaque species groups. Here, phylogenetic relationships were analyzed via whole‐genome sequences from five species, including M. arctoides, and two species each from the putative parental species groups. This analysis revealed ~3x more genomic regions supported placement in the sinica species group as compared to the fascicularis species group. Additionally, introgression analysis of the M. arctoides genome revealed it is a mosaic of recent polymorphisms shared with both species groups. To examine the evolution of their unique genital morphology further, the prevalence of candidate genes involved in genital morphology was compared against genome‐wide outliers in various population genetic metrics of diversity, divergence, introgression, and selection, while accounting for background variation in recombination rate. This analysis identified 67 outlier genes, including several genes that influence baculum morphology in mice, which were of interest since the bear macaque has the longest primate baculum. The mean of four of the seven population genetic metrics was statistically different in the candidate genes as compared to the rest of the genome, suggesting that genes involved in genital morphology have increased divergence and decreased diversity beyond expectations. These results highlight specific genes that may have played a role in shaping the unique genital morphology in the bear macaque.     

How laboratory-raised Japanese monkeys (Macaca fuscata) perceive rotated photographs of monkeys: Evidence for an inversion effect in face perception

Five laboratory-raised Japanese monkeys (Macaca fuscata) were presented various types of photographs of Japanese and rhesus monkeys (Macaca mulatta) in upright, horizontal, and inverted orientations in a sensory-reinforcement experiment. The ratio of the duration of potential viewing time for the photographs which the subjects controlled to the interval between subject-controlled presentations of them (the D/I score) was used as a measure of preference for the photographs. When inverted photographs were presented, the D/I scores were lower than for upright photographs. The difference in D/I scores between photographs of the two species, which indicated discriminability between them, also diminished when the photographs were inverted. The results obtained suggest an inversion effect in face perception in macaque monkeys.