Maternal Infant Monitoring in a Free-ranging Group of Japanese Macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

In nonhuman primates, females with infants visually monitor their infants from a distance to detect and consequently avoid potential threats to their infants. We recorded maternal visual monitoring of infants (infant monitoring) ages 7–18 wk in a free-ranging, provisioned group of Japanese macaques (Macaca fuscata). The infant monitoring rate declined as a function of infants’ ages in weeks and increased when the infants were beyond their mother’s reach, indicating that infant monitoring reflects the vulnerability of infants. Females with infants increased infant monitoring when their infants were handled by other group members but not when their infants moved alone. This suggests that intragroup threats (harassment/mishandling or kidnapping) have a relatively stronger influence on infant monitoring than external threats (predation or infanticide) under the condition of this study. Infant monitoring of middle-/low-ranking females was more frequent than that of high-ranking females when their infants were handled by other individuals. This may reflect greater intragroup threats to infants of middle-/low-ranking females; however, further study is needed to confirm this. During important activities (feeding or grooming), the infant monitoring rate was lower than that during other activities (resting or self-directed behavior). However, even during important activities, females with infants increased infant monitoring when infants were handled. This indicates that females with infants face a trade-off between infant monitoring and other important activities, and even if females have to reduce the time spent on important activities, they increase infant monitoring when their infants face greater potential intragroup threats.     

Positional behavior of free-ranging Japanese macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

Positional behavior was quantitatively studied in identified free-ranging Japanese macaques (Macaca fuscata). Five male and 11 female adults were observed in a forested mountain habitat. Data were analyzed for proportion of bout distance, number and time of each locomotion and postural type. Japanese macaques are semiterrestrial, and mainly walk and run quadrupedally. This supports the notion that Macaca are generally quadrupeds. Sex differences in positional behavior were found in the preference of substrate and types of positional behavior. Males and females tend to be terrestrial and arboreal, respectively. Males leap more frequently and longer in distance than do females when they are feeding in trees. These sex differences are considered to be related to differences in morphology, food choice, social activity, and the nursing of infants. Frequencies of leaping and the distance covered by leaping in Japanese macaques are more than those of long-tailed macaques which are arboreal quadrupeds. However, Japanese macaques leap shorter distances at a time than do long-tailed macaques, which indicates that body size may be related to leaping distance more than the frequency of leaping and the distance covered by leaping. Japanese macaques are not as specialized for terrestrial locomotion as pig-tailed macaques. They use both terrestrial and arboreal supports, and are considered to be semi-terrestrial quadrupeds, somewhere between the arboreal long-tailed macaque and the terrestrial pig-tailed macaque. Electronic Publication     

Social Structure Affects Initiations of Group Movements but Not Recruitment Success in Japanese Macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

Research on collective movements has often focused on the sociodemographic parameters explaining the success of some individuals as leaders or initiators of collective movements. Several of these studies have shown the influence of social structure, through kinship and affiliative relationships, on the organization of collective movements. However, these studies have been conducted on semi-free-ranging groups of macaques that were not faced with a natural environment and its constraints. In the socially intolerant rhesus macaque (Macaca mulatta) the success of an initiator correlates with its hierarchical rank, the most dominant individuals being the most successful. We investigated the collective movements of another socially intolerant macaque species, Japanese macaques, in the wild, to assess whether the social structure was still a determinant factor under natural conditions. In line with previous studies of macaques, we found that social structure drove the organization of collective movements. More dominant individuals initiated more collective movements. However, dominance did not affect the success of an initiation, i.e., the number of individuals joining. In addition, kinship strongly constrained the associations observed in females during collective movements. These results reflect the social structure of Japanese macaques, in which strong power asymmetry and kinship relationships constrain the majority of interactions between individuals within the group. Moreover, these results are similar to those observed in semi-free-ranging rhesus macaques and support the hypothesis of an effect of social determinants on collective movements of primates even under natural conditions.     

Birth-season variation in Japanese macaques,<Emphasis Type="Italic"> Macaca fuscata</Emphasis>

Japanese macaques, Macaca fuscata, exhibit an annual reproductive cycle that apparently is maintained intrinsically. Translocation of nine troops to new latitudes within the northern hemisphere has had minimal effect on the timing of birth seasonality in these troops; translocation of one troop to the southern hemisphere has resulted in a 6-month forward displacement of birth seasonality in this troop. Limited available evidence indicates that, in the latitudinal zone between Toimisaki (31°22′N) and Kinkazan (38°17′N), mean birth date in in-situ troops becomes earlier as latitude of troop localities increases; the same relationship between mean birth date and latitude apparently does not apply to in-situ troops south and north of the Toimisaki–Kinkazan latitudinal zone. Within the Toimisaki–Kinkazan latitudinal zone, earlier mean birth dates at higher latitudes may permit infants to achieve an adequate level of development before the earlier onset of poor winter food conditions. South of the Toimisaki–Kinkazan latitudinal zone, winters are relatively mild and may be less of a factor in infant survival; north of this zone, poor winter food conditions persist so long that earlier infant births may be maladaptive. Electronic Publication     

Subcutaneous malignant mast cell tumor in a Japanese macaque (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

The histopathological, immunohistochemical, and ultrastructural morphologic characteristics of a tumor in the subcutaneous tissue of the chest of a 19-year-old female Japanese macaque were investigated. Consequently, the mass was diagnosed as a malignant mast cell tumor (MCT). Tumors were present in both mammary gland portions of the anterior thorax. Both tumors showed the same histopathological findings. The tumor tissue was defined by the presence of delicate connective tissue, and the tumor cells grew in a cord-like or cobblestone pattern. The tumor cell cytoplasm was very clear. The nuclei were relatively uniform and the cells showed a low nucleus-cytoplasm ratio. The cytoplasmic granules stained blue with Alcian blue and eosinophils had infiltrated into the tumor tissue. Furthermore, immunohistochemical analysis revealed that the tumor cell membrane was positive for the anti-c-kit antibody. In ultrastructural morphologic analyses, all tumor cells showed a rich cytoplasm and, occasionally, granules wrapped in a limiting membrane of high electron density. The tumor cells had metastasized to the axillary lymph nodes, the kidney, and the peritoneum. Based on these results, the mass was diagnosed as a malignant MCT originating from the subcutaneous tissue of the chest. Since cases of MCTs in macaques are very rare, this report presents important new knowledge of neoplastic lesions in this species.     

Factors influencing mutual gaze in captive female Japanese monkeys (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

Mutual gaze occurs when two animals simultaneously look at each other, and therefore signals reciprocal visual attention. We studied the occurrence of mutual gaze among adult female Japanese monkeys (Macaca fuscata) housed at the Central Park Zoo in New York City (USA). We found that the frequency of mutual gaze varied according to one aspect of social context (proximity), and that monkeys’ age-rank was negatively correlated with the frequency of mutual gaze. The behavioral contexts in which mutual gaze was observed did not include aggression, and social rank did not predict frequency of mutual gaze. Mutual gaze therefore varies according to some aspects of social context and is generally predicted by factors that influence other social behaviors (e.g., age).     

Testing for Links Between Female Urine Odor and Male Sexual Behaviors in Japanese Macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

Urine is involved in sexual communication in New World monkeys and lemurs, but most studies of the role of olfaction in sexual communication in Old World monkeys have focused on vaginal secretions rather than urine. We investigated whether female urine promotes male sexual behaviors (approaches and inspections of genital area) in Japanese macaques (Macaca fuscata). We used a sequential presentation paradigm in behavioral experiments, presenting unfamiliar female urine and control cotton swabs to males living in a social group with cycling females. We tested whether males (N = 3) showed more processing behaviors (licking, sniffing, tasting) toward female urine (22 stimuli per male from prefertile, fertile, and postfertile phases, based on urinary estrone and progesterone conjugate profiles) than control odor (8 stimuli per male). We then compared male sexual behaviors toward resident females pre- and post-exposure to stimuli and in relation to the females’ reproductive status (perifertile, nonfertile, and pregnancy periods, based on fecal estrone and progesterone conjugate profiles). We found that males showed significantly more processing behaviors toward urine stimuli than to controls but that male behavior did not vary across urine samples from prefertile, fertile, and postfertile phases. Exposure to unfamiliar female urine stimuli did not modulate male approaches to and inspections of resident females at any stage of the female reproductive cycle. Although our study is limited by its small sample size, the results suggest that female urine contains compounds that males detect, but we found no evidence that female urine is related to male sexual behaviors.     

Grandmothers care for orphans in a provisioned troop of Japanese macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

This study reports cases in which grandmothers and other closely related adult females cared for orphans in the Arashiyama E-troop, a provisioned troop of Japanese macaques (Macaca fuscata). I observed the behavioral patterns of three orphans (aged 1, 2, and 3 years, respectively). The grandmothers cared for two orphans, while three other closely related adult females cared for the rest of the orphans whose grandmothers were absent. These observations differ from those of previous studies that reported that grandmothers were indifferent towards orphans. This intraspecific variation may be attributed to the demographic conditions of the troop in this study, which had only a few related nulliparous adult females, as a result of artificial birth control. In this group, adult females showed decreased fecundity and an increased interbirth interval as they received birth control treatment; thus, in the absence of their own dependent infants, these females may have invested time in the care of related orphans. Although caregiving by grandmothers is believed to be rare or insignificant in primates, this study suggests that grandmothers and other closely related adult females play an important role for orphans in troops with few related adult females.     

Temporal Variation in Adult Affiliation Patterns in Wild Taiwanese Macaques (<Emphasis Type="Italic">Macaca cyclopis</Emphasis>)

We studied temporal variation in affiliative behavior among adults in 2 multimale groups of wild Taiwanese macaques from 2 different populations: one in Southern Taiwan, and one in Northern Taiwan. Although the study areas differed dramatically in their elevation, average temperatures, and rainfall patterns, both populations displayed marked similarities. Analyses of grooming and proximity showed that only male-female affiliative patterns had significant temporal variation. The males and females of both populations had the highest frequencies of grooming and proximity in a mating context. Outside of the mating season, male-female affiliation rates dropped dramatically. In contrast, female-female and male-male affiliation patterns showed no significant temporal variation.     

Twinning frequency of Japanese Macaques (<Emphasis Type=Italic>Macaca fuscata</Emphasis>) at Takasakiyama

In a wild-living, artificially provisioned population of Japanese macaques at Takasakiyama in southern Japan, nine sets of twins were recorded from 12,392 known deliveries over a 56-year study period. Recorded twinning frequency was 0.073%. During the first 28-year period, artificial food was given until macaques were satiated and population size increased rapidly. In the second 28-year period, provisioned food was restricted to about half of the former period’s calorific content. Seven sets of twins were born in the first period and two sets in the second. Twining frequency in the two periods was 0.137 and 0.027%, respectively. In comparing studies of other Catarrhine primate samples, we hypothesize that twinning frequency is influenced by living conditions, and we suggest that living conditions should be carefully evaluated in studies of twinning frequency.     

Postglacial population expansion of Japanese macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>) inferred from mitochondrial DNA phylogeography

We investigated the diversity and phylogeography of mitochondrial DNA (mtDNA) in Japanese macaques (Macaca fuscata), an endemic species in Japan that has the northernmost distribution of any non-human primate species. DNA samples from 135 localities representing the entire range of this species were compared. A total of 53 unique haplotypes were observed for the 412-bp partial mtDNA control region sequence, with length variation distinguishing the two subspecies. Clustering analyses suggested two putative major haplogroups, of which one was geographically distributed in eastern Japan and the other in western Japan. The populations in the east showed lower mtDNA diversity than those in the west. Phylogeographical relationships of haplotypes depicted with minimum spanning network suggested differences in population structure. Population expansion was significant for the eastern but not the western population, suggesting establishment of the ancestral population was relatively long ago in the west and recent in the east. Based on fossil evidence and past climate and vegetation changes, we inferred that the postulated population expansion may have taken place after the last glacial period (after 15,000 years ago). Mitochondrial DNA showed contrasting results in both variability and phylogenetic status of local populations to those of previous studies using protein variations, particularly for populations in the periphery of the range, with special inference on habitat change during the glacial period in response to cold adaptation. Electronic supplementary material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

Molecular cloning of protamine-2 and expression with aging in Japanese monkey (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

In order to isolate genes relating spermatogenesis with postnatal development and aging, we have attempted to obtain genes showing differences in expression in testis of Japanese monkeys (Macaca fuscata) by means of differential display PCR, and we have cloned, sequenced and characterized protamine-2 (PRM2) of Japanese monkey. The predicted open reading frame encoded a protein of 103 amino acid residues, most of which are common to those of other mammals. Northern analysis revealed that the PRM2 gene is expressed at adult and aged stages, but not at the juvenile stage. In situ hybridization revealed that the PRM2 gene is expressed mainly in late spermatids and its expressional potential is decreased from adult to aged stages. It suggests that PRM2 in spermiogenesis is mediated by the age of the animal.     

<Emphasis Type="Italic">Ty</Emphasis>1<Emphasis Type="Italic">/copia</Emphasis>- and <Emphasis Type="Italic">Ty</Emphasis>3<Emphasis Type="Italic">/gypsy</Emphasis>-like DNA sequences in <Emphasis Type="Italic">Helianthus </Emphasis>species

Two repeated DNA sequences isolated from a partial genomic DNA library of Helianthus annuus, p HaS13 and p HaS211, were shown to represent portions of the int gene of a Ty3 /gypsy retroelement and of the RNase-Hgene of a Ty1 /copia retroelement, respectively. Southern blotting patterns obtained by hybridizing the two probes to BglII- or DraI-digested genomic DNA from different Helianthus species showed p HaS13 and p HaS211 were parts of dispersed repeats at least 8 and 7 kb in length, respectively, that were conserved in all species studied. Comparable hybridization patterns were obtained in all species with p HaS13. By contrast, the patterns obtained by hybridizing p HaS211 clearly differentiated annual species from perennials. The frequencies of p HaS13- and p HaS211-related sequences in different species were 4.3x10(4)-1.3x10(5) copies and 9.9x10(2)-8.1x10(3) copies per picogram of DNA, respectively. The frequency of p HaS13-related sequences varied widely within annual species, while no significant difference was observed among perennial species. Conversely, the frequency variation of p HaS211-related sequences was as large within annual species as within perennials. Sequences of both families were found to be dispersed along the length of all chromosomes in all species studied. However, Ty3 /gypsy-like sequences were localized preferentially at the centromeric regions, whereas Ty1/ copia-like sequences were less represented or absent around the centromeres and plentiful at the chromosome ends. These findings suggest that the two sequence families played a role in Helianthusgenome evolution and species divergence, evolved independently in the same genomic backgrounds and in annual or perennial species, and acquired different possible functions in the host genomes.     

New combinations and typifications in <Emphasis Type="Italic">Bistorta</Emphasis>, <Emphasis Type="Italic">Persicaria</Emphasis>, <Emphasis Type="Italic">Polygonum,</Emphasis> and <Emphasis Type="Italic">Rumex</Emphasis> (Polygonaceae)

New combinations are proposed in anticipation of the Polygonaceae treatment in the forthcoming volume of Intermountain Flora: Polygonum kelloggii var. esotericum, P. kelloggii var. watsonii , Rumex densiflorus var. pycnanthus , R. salicifolius var. utahensis, and R. occidentalis var. tomentellus. Typifications are proposed to facilitate ongoing studies in Polygonaceae and to maintain current usage.     

Technological Response of Wild Macaques (<Emphasis Type="Italic">Macaca fascicularis</Emphasis>) to Anthropogenic Change

Anthropogenic disturbances have a detrimental impact on the natural world; the vast expansion of palm oil monocultures is one of the most significant agricultural influences. Primates worldwide consequently have been affected by the loss of their natural ecosystems. Long-tailed macaques (Macaca fascilularis) in Southern Thailand have, however, learned to exploit oil palm nuts using stone tools. Using camera traps, we captured the stone tool behavior of one macaque group in Ao Phang-Nga National Park. Line transects placed throughout an abandoned oil palm plantation confirmed a high abundance of nut cracking sites. Long-tailed macaques previously have been observed using stone tools to harvest shellfish along the coasts of Thailand and Myanmar. The novel nut processing behavior indicates the successful transfer of existing lithic technology to a new food source. Such behavioral plasticity has been suggested to underlie cultural behavior in animals, suggesting that long-tailed macaques have potential to exhibit cultural tendencies. The use of tools to process oil palm nuts across multiple primate species allows direct comparisons between stone tool using nonhuman primates living in anthropogenic environments.     

Pedogamy in <Emphasis Type="Italic">Neidium</Emphasis> (<Emphasis Type="Italic">Bacillariophyceae</Emphasis>)

Single (unpaired) vegetative cells of freshwater pennate diatom Neidium cf. ampliatum differentiated into gametangia and produced a single zygote (auxospore) via a pedogamic process. The gametic nuclei fused after auxospore expansion had begun. The auxospore expanded in parallel to the apical axis of the gametangium.     

<Emphasis Type="Italic">Entamoeba histolytica</Emphasis> and <Emphasis Type="Italic">E. dispar</Emphasis> infections in captive macaques (<Emphasis Type="Italic">Macaca fascicularis</Emphasis>) in the Philippines

Entamoeba histolytica is a protozoan parasite that infects man and animals. This parasite has a global distribution and the disease it causes is usually characterized by diarrhea. In order to detect the parasite, it is necessary to differentiate it from Entamoeba dispar. E. dispar appears morphologically similar to E. histolytica but does not cause disease and tissue invasion. This study reports on the prevalence of E. histolytica and E. dispar among captive macaques in a primate facility in the Philippines. PCR was used to correctly identify both Entamoeba species. Indirect fluorescent antibody test (IFAT) was also performed to determine the seroprevalence of amebiasis in the captive macaques. Based on PCR targeting of the peroxiredoxin gene, of the 96 stool samples collected, 23 (24%) contained E. histolytica while 32 (33%) contained E. dispar. IFAT revealed 26 (27%) serum samples positive for antibodies against E. histolytica. Sequence analysis of the 18S rRNA gene showed that the 23 E. histolytica isolates were identical to human E. histolytica isolates deposited in the GenBank and not Entamoeba nuttalli as found in macaques in other recent reports. The Philippines is a major exporter of monkeys for biomedical research purposes, so screening animals before transporting them to other locations lessens the risk of spreading zoonoses to a wider area. This is the first report of the molecular detection of E. histolytica and E. dispar among macaques in the Philippines. This study complements the limited information available on the animal hosts of E. histolytica in the Philippines.     

Floral development and systematic position of <Emphasis Type="Italic">Arillastrum</Emphasis>, <Emphasis Type="Italic">Allosyncarpia</Emphasis>, <Emphasis Type="Italic">Stockwellia</Emphasis> and <Emphasis Type="Italic">Eucalyptopsis</Emphasis> (Myrtaceae)

We have investigated the floral ontogeny of Arillastrum, Allosyncarpia, Stockwellia and Eucalyptopsis (of the eucalypt group, Myrtaceae) using scanning electron microscopy and light microscopy. Several critical characters for establishing relationships between these genera and to the eucalypts have been determined. The absence of compound petaline primordia in Arillastrum, Allosyncarpia, Stockwellia and Eucalyptopsis excludes these taxa from the eucalypt clade. Post-anthesis circumscissile abscission of the hypanthium above the ovary in Stockwellia, Eucalyptopsis and Allosyncarpia is evidence that these three taxa form a monophyletic group; undifferentiated perianth parts and elongated fusiform buds are characters that unite Stockwellia and Eucalyptopsis as sister taxa. No floral characters clearly associate Arillastrum with either the eucalypt clade or the clade of Stockwellia, Eucalyptopsis and Allosyncarpia.We gratefully acknowledge Clyde Dunlop and Bob Harwood (Northern Territory Herbarium) for collecting specimens of Allosyncarpia, and Bruce Gray (Atherton) for collecting specimens of Stockwellia. The Australian National Herbarium (CANB) kindly lent herbarium specimens of Eucalyptopsis for examination. This research was supported by a University of Melbourne Research Development Grant to Andrew Drinnan.