We have analyzed the ranging patterns of the Mimikire group (M group) of chimpanzees in the Mahale Mountains National Park, Tanzania. During 16 years, the chimpanzees moved over a total area of 25.2 or 27.4 km2, as estimated by the grid-cell or minimum convex polygon (MCP) methods, respectively. Annually, the M group used an average of 18.4 km2, or approximately 70 %, of the total home-range area. The chimpanzees had used 80 % of their total home range after 5 years and 95 % after 11 years. M group chimpanzees were observed more than half of the time in areas that composed only 15 % of their total home range. Thus, they typically moved over limited areas, visiting other parts of their range only occasionally. On average, the chimpanzees used 7.6 km2 (in MCP) per month. Mean monthly range size was smallest at the end of the rainy season and largest at the end of the dry season, but there was much variability from year to year. The chimpanzees used many of the same areas every year when Saba
comorensis fruits were abundant between August and January. In contrast, the chimpanzees used several different areas of their range in June. Here range overlap between years was relatively small. Over the 16 years of the study we found that the M group reduced their use of the northern part of their range and increased their frequency of visits to the eastern mountainous side of their home range. Changes in home-range size correlated positively with the number of adult females but not with the number of adult males. This finding does not support a prediction of the male-defended territory model proposed for some East African chimpanzee unit-groups.
Chronic weight loss in marmosets is often associated with wasting marmoset syndrome (WMS), an important disease that occurs in callitrichid colonies around the world. Even though its etiology is very difficult to determine, particular variables, such as weight loss, diarrhea and alopecia, associated or not with infestation in the pancreatic ducts with Trichospirura leptossoma (Nematoda: Thelazioidea), seem to be linked with the syndrome. This study investigated the histopathology of the lungs, duodenum, liver, gallbladder, extrahepatic bile ducts and pancreatic ducts of six common marmosets (Callithrix jacchus) suffering from severe non-diarrheic weight loss. Three individuals died naturally and the other three were euthanized. Microscopic findings showed the presence of adult flukes (Platynosomum) in the liver. These flukes, which provoke common infection in cats, were also observed inside the gallbladder as well as in the intra and extrahepatic bile ducts in common marmosets. Portal fibrosis was observed in two animals, which developed chronic fibrosing hepatopathy (biliary pattern, grade 3). The disease progresses without diarrhea and without pancreatic lesions or infestation. With the progression, the animals presented with ascending cholangitis, cholestasis and portal fibrosis, sometimes culminating in secondary biliary cirrhosis. Therefore, this infirmity, associated with chronic weight loss in common marmosets, could be another etiological factor linked with WMS.
Cebus flavius is a recently rediscovered species and a candidate for the 25 most endangered primate species list. It was hypothesized that the distribution of C. flavius was limited to the Atlantic Forest, while the occurrence of C. libidinosus in the Rio Grande do Norte (RN) Caatinga was inferred, given its occurrence in neighboring states. As a result of a survey in ten areas of the RN Caatinga, this paper reports on four Cebus populations, including the first occurrence of C. flavius in the Caatinga, and an expansion of the northwestern limits of distribution for the species. This C. flavius population may be a rare example of a process of geographic distribution retraction, and is probably the most endangered population of this species. New areas of occurrence of C. libidinosus are also described. Tool use sites were observed in association with reports of the presence of both capuchin species.
The white bald uakari (Cacajao calvus calvus) is among the least studied of the Amazonian primates and is found exclusively in remote areas of the central Amazon. The geographic distribution of this subspecies is still uncertain, and information on current threats and its conservation status is sparse. In this paper, we identify new locations of occurrence and propose range expansion of the Cacajao calvus calvus. Between 2008 and 2010, six field expeditions were undertaken in the middle Solimões region to search for the subspecies and to conduct interviews with local residents regarding its presence. The presence of the white bald uakari was confirmed in the lower courses of the Juruá and lower Jutaí rivers, in addition to areas inside the Mamirauá Reserve, where its presence was expected. Results indicate an expansion and new limits on the geographic range of the subspecies, including its detection in areas in which it had not previously been reported and its exclusion from areas where white bald uakaris were assumed to occur. The new information provided by this study and the remaining shortcomings regarding the distribution of the calvus group point to the urgent need for further research on the geographic distribution and habitat use of this group, especially along the lower courses of the Juruá and Jutaí rivers, which remain little explored.
We show that, in 1862, Richard Burton collected the type specimen of Pan troglodytes vellerosus not on Mount Cameroon, as has been generally assumed, but in Gabon. Therefore, P. t. vellerosus is not the correct name for the chimpanzee population of western Cameroon and southern Nigeria, if that population is taxonomically distinct. As First Reviser, we choose the name Pan troglodytes ellioti for this population of chimpanzees, based on Anthropopithecus
ellioti named by Matschie [Matschie P (1914) Neue Affen aus Mittelafrika. Sitzungsber Ges Naturforsch Freunde Berlin 1914:323–342] from a specimen in the Humboldt Museum, Berlin, collected in Bascho (=Basho), Cameroon, and given to the museum in 1905.
A detailed understanding of the range of the golden-mantle tamarin, Saguinus tripartitus (Milne Edwards, 1878), in Amazonian Peru and Ecuador is of particular relevance, not only because it is poorly known but also because it was on the basis of its supposed sympatry with the saddleback tamarin (S. fuscicollis lagonotus) that Thorington (Am J Primatol 15:367-371, 1988) argued that it is a distinct species rather than a saddleback tamarin subspecies, as was believed by Hershkovitz (Living new world monkeys, vol I. The University of Chicago Press, Chicago, 1977). A number of surveys have been carried out since 1988 in the supposed range of S. tripartitus, in both Ecuador and Peru. Here we summarize and discuss these issues and provide a new suggestion for the geographic range of this species; that is, between the ríos Napo and Curaray in Peru and extending east into Ecuador. We also review current evidence for the distributions of Spix's black-mantle tamarin (S. nigricollis nigricollis), Graells' black-mantle tamarin (S. n. graellsi), and the saddleback tamarin (S. fuscicollis lagonotus), which are also poorly known, and examine the evidence regarding sympatry between them. We conclude that despite the existence of a number of specimens with collecting localities that indicate overlap in their geographic ranges, the fact that the four tamarins are [corrected] of similar size and undoubtedly very similar in their feeding habits militates strongly against the occurrence of sympatry among them.
Platynosomum illiciens (Trematoda, Plagiorchida) is a trematode parasite reported in felids and falconiforms. It was identified in the gall bladder of eight captive neotropical necropsied primates from the National Primate Center (CENP), Ananindeua, State of Pará, Brazil. This is the first description of Platynosomum illiciens as a parasite of primates.
Cruz Lima’s saddle-back tamarin Saguinus fuscicollis cruzlimai Hershkovitz, 1966, was described from a painting by Eládio da Cruz Lima in his book Mammals of Amazonia,
Vol. 1, Primates (1945). The painting was of four saddle-back tamarins from the upper Rio Purus, one of them distinct and the inspiration for Hershkovitz to describe it as a new subspecies. Its exact provenance was unknown, however, and the specimen was lost. Surveys in the Purus National Forest in 2011 resulted in sightings of this tamarin along the north bank of the Rio Inauini, a left-bank tributary of the middle Purus, and also on the left bank of the Purus, north and south of the Rio Inauini. It is possible that it extends north as far as the Rio Pauini, and that S. f. primitivus Hershkovitz, 1977, occurs north of the Pauini as far the Rio Tapauá, both also left-bank tributaries of the Purus. Morphometric and molecular genetic analyses and the coloration of the pelage indicate that this tamarin differs from its neighbors sufficiently to be considered a full species. In his doctoral dissertation [2010, Taxonomy, Phylogeny and Distribution of Tamarins (Genus Saguinus Hoffmannsegg, 1807) Georg-August Universität, Göttingen], C. Matauschek found that saddle-back and black-mantle tamarins diverged from the tamarin lineage around 9.2 million years ago; time enough to warrant their classification in a distinct genus. Leontocebus Wagner, 1840, is the first name available. In this article we re-describe Cruz Lima’s saddle-back tamarin. We propose a neotype with a precise locality, and make it a full species in the genus Leontocebus.
This study presents reproductive parameter data gathered by direct observation over a 40-year period (1971-2011) of the provisioned free-ranging population of orangutans at Camp Leakey in Tanjung Puting National Park, Central Kalimantan, Indonesia. Age at first reproduction, interbirth interval (IBI), sex ratio at birth, and infant mortality for 19 female orangutans (11 first-generation wild-born ex-captive mothers and 8 second-generation mothers) are included in this analysis. Age at first reproduction among the first-generation mothers was similar to that among wild orangutans, while second-generation mothers had a significantly earlier age at first reproduction. IBIs were similar among first- and second-generation mothers and were significantly shorter than those recorded in studies of wild orangutan populations. There was an expected male-biased sex ratio at birth and a slightly higher than expected rate of infant mortality when compared to wild populations. Infant mortality was primarily seen among second-generation mothers who gave birth before the age of 12, and among first births of some first-generation mothers. These results lend support to the ecological energetics hypothesis, which predicts that increased diet quality leads to a faster rate of reproduction.
Natal emigration by male and female mantled howlers (Alouatta palliata), and subsequent immigration into breeding groups, is well documented for the free-ranging population on Hacienda La Pacifica, Costa Rica, but secondary transfer was considered rare (Glander in Int J Primatol 3:415-436, 1992). Population surveys in 1998 and 2006 caused us to question our assumptions and to re-evaluate our long-term data set from a post hoc perspective. We first identified all animals observed or captured as adults in more than one non-natal group anywhere in the population. We then systematically analyzed joining or leaving by adults in seven groups tracked for various times from 1975 to 2005 for patterns suggesting secondary transfer. Fourteen adults (nine females, five males) were found in two different non-natal groups as adults. In addition, one male and one female that became dominant and reproduced in their natal group later transferred to a second group, and one female was known to be a tertiary transfer. Data from the seven tracked social groups indicate that 35% of all the males and 29% of all the females were potential secondary transfers. In these groups, males leaving or joining was not associated with group size or absolute number of females. Females leaving or joining was not associated with group size or absolute number of males, but females left groups with more females and joined groups with fewer females. Both sexes left groups with unfavorable sex ratios for their sex and joined groups with sex ratios more favorable for their sex. Since a favorable sex ratio is associated with reproductive success in other howler populations, this suggests secondary transfer as a reproductive strategy. Other factors could also influence secondary transfer.
This paper presents the results of a demographic analysis of 22 years of data recorded on a colony of tufted capuchin monkeys (Cebus apella) in captivity at the CNR Primate Centre (Rome, Italy). Information is provided on reproduction, sex ratio, inter-birth interval (IBI), seasonality, and body weight. From 1984 to 2006, 46 live births were recorded. There were births in almost all months of the year, but a higher frequency was observed during spring and summer (71.1%). The sex ratio was 1:1 M:F for newborns and 1:1.06 M:F for surviving offspring. At birth, infants' average weight was 238.13 +/- 37.51 g, i.e. 250 +/- 56.79 g for males and 231 +/- 26.08 g for females. Age at first birth for females ranged from 4.9 to 7 years (n = 9), while males achieved first paternity between the ages of 5 and 9.2 years (n = 6). Only one pair of twins was recorded during this period. For females, the mean IBI was 17.88 +/- 1.84 months, when they reared infants, and 12.70 +/- 1.73 months, when they did not rear offspring. Infant mortality within the first 2 months was 28.3%.
In the present study, we recorded all births, immigrations, deaths, and emigrations for a population of ring-tailed lemurs at Berenty Reserve, Madagascar, between September 1989 and August 1999. In September 1989, three troops (C, B, and T) inhabited the study area of 14.2 ha. During the 10-year period, eight troop divisions, six evictions of females, and three troop takeovers of ranges by other troops occurred in and around the study area. Consequently, in August 1999, the number of troops in the same area increased to six (CX, C1, C2A, C2B, T1, and T2). The number of lemurs aged > 1 year increased from 63 to 82, which resulted from 204 births, 58 immigrations, 125 deaths, and 118 emigrations. Of the 204 newborn lemurs during the study period, 103 died, 44 emigrated outside the study area, and 57 remained within the study area. The total number of lemurs that emigrated from natal troops was 69 (54 males and 15 females). Natal males left their troops around the age of 3. Non-natal males changed troops after a tenure varying from 1 to 7 years. Survival curves showed a fall in survival rates of both sexes to < 0.5 between the ages of 2 and 3. For females, the survival rate gradually decreased to < 0.2 at the age of 9. On the other hand, due to emigration, the survival rate of males could not be determined after the age of 5 yr. Since some males attained high-rank at the age of 6 - 10 yr, the prime age for male ring-tailed lemurs is thought to be around 7 - 10 yr. Ring-tailed lemurs are essentially female philopatric, because all cases of females leaving natal troops resulted from troop divisions or forced evictions. Such social changes may have resulted from competition among females. All cases of troop divisions or evictions occurred in larger troops consisting of >or=20 lemurs, and only a few females could rejoin their troops. When males joined such a female-group, a new troop was formed. Although promoted by an increase in population, frequent emigrations of females from original troops are the characteristics of ring-tailed lemurs at Berenty.
We present two new records for the vulnerable dwarf marmoset, Callibella humilis. The first record, based on observed and photographed individuals, is from a campinarana area on the left (west) bank of the Rio Madeirinha, a left (west)-bank tributary of the Rio Roosevelt in the state of Amazonas, municipality of Novo Aripuanã and extends the distribution of the species ~270 km southwards, to the left (west) bank of the rio Roosevelt. The second record is based on an individual collected from the mouth of the Rio Roosevelt, at less than 10 km from the type locality of Mico marcai. This indicates that the species occurs sympatrically with M. marcai and probably Mico melanurus. We also present the first sonogram analysis of its long call structure, which shows some similarities, in the note duration and frequency, with Cebuella pygmaea and Mico argentatus.
The second-to-fourth digit ratio (2D:4D) is a putative biomarker for prenatal androgen effects, which has been widely employed to study androgenic-programming effects on shaping sex-linked traits and behaviours in humans. This approach is now increasingly applied to non-human species. Heritability studies of 2D:4D in both humans and zebra finches indicate substantial genetic contributions to the expression of this trait. This study examines the heritability of 2D:4D in rhesus macaques, based on the resemblance of mother-infant dyads, to see how these compare with human values. Results suggest that familial resemblance in 2D:4D is also strong in rhesus monkeys. Heritability estimates were within the range of estimates from human studies. These preliminary results suggest that the strength of heritability of 2D:4D may generalize across taxa.
We analysed the reproductive parameters of free-ranging female orangutans at Sepilok Orangutan Rehabilitation Centre (SORC) on Borneo Island, Sabah, Malaysia. Fourteen adult females produced 28 offspring in total between 1967 and 2004. The average censored interbirth interval (IBI) (i.e. offspring was still alive when mother produced a next offspring) was 6 years. This was shorter than censored IBIs reported in the wild but similar to IBIs reported for those in captivity. The nonparametric survival analysis (Kaplan-Meier method) revealed a significantly shorter IBI at SORC compared with wild orangutans in Tanjung Putting. The infant (0-3 years) mortality rate at SORC of 57% was much higher than rates reported both in the wild and captivity. The birth sex-ratio was significantly biassed toward females: 24 of the 27 sex-identified infants were females. The average age at first reproduction was 11.6 years, which is younger than the age in the wild and in captivity. The high infant mortality rate might be caused by human rearing and increased transmission of disease due to frequent proximal encounters with conspecifics around the feeding platforms (FPs). This young age of first reproduction could be because of the uncertainty regarding estimated ages of the female orangutans at SORC. It may also be affected by association with other conspecifics around FPs, which increased the number of encounters of the females with males compared with the number of encounters that would take place in the wild. Provision of FPs, which improves the nutritional condition of the females, caused the shorter IBI. The female-biassed birth sex-ratio can be explained by the Trivers and Willard hypothesis. The female-biassed sex ratio could be caused by the mothers being in poor health, parasite prevalence and/or high social stress (but not food scarcity) due to the frequent encounters with conspecifics around FPs.
In contrast to other papionin monkeys, hamadryas baboons are characterized by female-biased dispersal. Given that hamadryas females do not disperse voluntarily, one mechanism for female transfer between bands is thought to be abductions during aggressive intergroup conflict. To date, however, no successful abductions have been witnessed. We describe three abduction events at the Filoha field site in Ethiopia, two interband and one intraband, in which the abductors successfully separated a female from her leader male for several minutes or hours. In each case, the original leader male located the abductor and retrieved the female, even if it involved entering the social sphere of another band. These observations suggest that a hamadryas leader male will risk injury and loss of additional females in his attempt to retrieve a female from an abductor unless the abductor has openly challenged the leader for possession of his female and physically defeated him.
Orangutans have the longest immature period and inter-birth interval of all ape species. This may be explained by a slow life history, the need to develop skills or by their relatively solitary lifestyle, which prevents a mother from associating with two offspring. This study of wild immature orangutans at the Ketambe Research Station, Indonesia, describes, with partly cross-sectional, partly longitudinal data, their development to independence. The study subjects ranged from 1 to 11 years of age. Data on their activity budget, diet, mother-offspring proximity and maintenance of proximity, association with conspecifics and play behavior were collected. The results indicate that immature orangutans can provide for their own food and transport, and therefore were independent of direct maternal care, at an age of possibly 3 but more clearly 6 years. This is similar to chimpanzees, and refutes the slow life history hypothesis. Immature orangutans remain within their mother's vicinity until the age of 8 years, indicating a dependence on indirect maternal care, and this coincides with the period during which the mother does not produce another offspring. A female orangutan seems unable to associate with an older immature while caring for a new infant. This is consistent with the solitary-lifestyle hypothesis and corroborates the results obtained with the Sumatran orangutan population at Suaq Balimbing. However, why an immature depends indirectly on its mother for such a long period remains unclear. It is possible that it needs to develop ecological or social skills or needs the protection of its mother. Unfortunately, no data were available to distinguish between these possibilities.
In previous studies we demonstrated that brown and black lemurs (Eulemur fulvus and E. macaco) showed self-control abilities under a reverse-reward contingency. They were able to significantly select the smaller quantity of food to be rewarded with the larger one and to generalize this ability when presented with two rewards that differed in quality. In the present study, previously trained subjects had to choose between graphic representations of two different quantities of food under the reverse-reward contingency. Three out of four subjects learned to associate a graphic representation of the reward with the corresponding quantity. Only one subject consistently selected the representation of the smaller quantity to be rewarded with the larger quantity of food and therefore showed abstraction as well as relative numerousness skills. Indeed, she was able to discriminate between representations of different quantities and to ordinate them. We discuss how primates mentally represent food quantities and how self-control is involved in foraging strategies.
We examined the relationship between fruit abundance and chimpanzee (Pan troglodytes) party size by comparing data from four study sites: the Kalinzu Forest Reserve, Uganda, the Djinji Camp and Guga Camp in the Ndoki Forest, Congo, and Kahuzi-Biega National Park, Democratic Republic of Congo. Although the difference in the fruit abundance between the sites was responsible for the difference in the party size between the sites, the seasonal changes in fruit abundance did not explain the changes in the party size in each study site. Across the four study sites, there were significant correlations of the mean and minimum of monthly party size with the mean of monthly fruiting-tree density, and a significant correlation of the maximum of monthly party sizes with the minimum of monthly fruiting-tree density. We proposed a hypothesis that (1) the monthly fruit abundance affects the monthly party size in the sites where the fruit availability is as low as to limit the party size during a major part of a year, while (2) the party size does not increase with the increase in the monthly fruit abundance, but is affected by other social factors, in the sites where the minimum of monthly fruit abundance is high enough for chimpanzees to form parties of an adequate size.
The present study aimed to gather baseline information about chimpanzee nesting and density in Lagoas de Cufada Natural Park (LCNP), in Guinea-Bissau. Old and narrow trails were followed to estimate chimpanzee density through marked-nest counts and to test the effect of canopy closure (woodland savannah, forest with a sparse canopy, and forest with a dense canopy) on nest distribution. Chimpanzee abundance was estimated at 0.79 nest builders/km(2), the lowest among the areas of Guinea-Bissau with currently studied chimpanzee populations. Our data suggest that sub-humid forest with a dense canopy accounts for significantly higher chimpanzee nest abundance (1.50 nests/km of trail) than sub-humid forest with a sparse canopy (0.49 nests/km of trail) or woodland savannah (0.30 nests/km of trail). Dense-canopy forests play an important role in chimpanzee nesting in the patchy and highly humanized landscape of LCNP. The tree species most frequently used for nesting are Dialium guineense (46 %) and Elaeis guineensis (28 %). E. guineensis contain nests built higher in the canopy, while D. guineense contain nests built at lower heights. Nests observed during baseline sampling and replications suggest seasonal variations in the tree species used for nest building.
We report information on population density, group size, and habitat preferences of primates along the lower Río Urubamba and in the Río Urubamba-Río Tambo interfluvium, in central-eastern Peruvian Amazonia, an area that has been little explored with regard to its primate fauna. During 425 km of transect walks in October-November 2008 and April-May 2009 totally 174 groups of nine primate species were encountered, the most common being Callicebus brunneus (45 groups), Saguinus imperator (41 groups), and Aotus nigriceps (26 groups). Group sizes were smallest for A. nigriceps and C. brunneus (mean of 2.8 and 2.9, respectively) and largest for Saimiri boliviensis (mean 15.6). Population densities were lowest for Lagothrix cana (3.3 individuals/km(2)) and highest for A. nigriceps (31.1 individuals/km(2)). Groups of C. brunneus, S. imperator, S. boliviensis, Cebus albifrons, and Cebus apella were most frequently (83 % of sightings) encountered in semi-dense or in open primary forest that included stands of bamboo (Guadua sarcocarpa) or where bamboo was a very common species.
Previous studies on Japanese macaque (Macaca fuscata) densities suggest that both total annual food abundance and the quality of fallback foods in the winter bottleneck period affects density. We reviewed data on the seasonal changes in home range size to explain how both factors affect density. In general, home range was large in summer or autumn and small in spring or winter, indicating that density is determined by the home range size in the seasons before winter. The main foods in these seasons are fruits and seeds. If these foods are not abundant, macaques need to range over a larger area, thus decreasing density. Macaques survive the winter by depending on the fat deposited before winter through eating these high-quality foods. If the food condition in winter is severe and the amount of required fat deposition is large, macaques need a larger home range before winter, and thus density becomes lower.
Composition of the landscape matrix of surrounding forest fragments is thought to be critically important to the survival of arboreal primates because it offers structures that help the animals move between fragments and other foraging sites. However, little is known about the composition of the matrix used by these animals. The aim of this study was to quantitatively assess the importance of the landscape matrix and its effects on primate abundance, using black howler monkeys (Alouatta pigra) living in a landscape fragmented by the expansion of agriculture and pastures for livestock in southeastern Mexico. In 2008, a complete census of the monkeys was carried out across the 2000-ha landscape matrix, and for every site where we observed monkeys, we recorded canopy height, tree basal area, food-source abundance, and distance to the nearest fragment. A total of 244 howler monkeys, distributed among 48 groups (including six solitary males) were counted in the matrix. Mean troop size was 5.6 ± 2.8 individuals, and the mode was three individuals. The highest number of troops and greatest howler monkey abundance were recorded in the isolated trees, the eucalyptus plantation, and orchards. A generalized linear model revealed that monkey abundance tended to be higher in matrix elements with higher canopy height, greater food availability, and closest to rainforest fragments. These results suggest that it is necessary to take into account the many elements of the landscape when drawing up conservation and habitat management plans, particularly in order to establish connectivity among the fragments and elements of the matrix with native trees.
Primates acquire knowledge about relationships of third parties and group structure by monitoring their conspecifics. We show that Barbary macaques (Macaca sylvanus) utter specific vocalizations while monitoring interactions of other group members. As they did not direct other behaviours to the interacting group members, we provisionally termed these vocalizations 'vocal comments'. We investigated the acoustic properties of these comments and the social contexts in which they occurred. Most adult males and females of two studied groups produced low-amplitude calls when observing close contact interactions of other group members. The acoustic features of these calls varied with characteristics of the commented situation. Our results suggest that such calls might not be directed towards the agents of the commented situation, but towards other group members. The vocal comments may signal the caller's awareness of the observed interaction and possibly attract the attention of others to the situation.
Malagasy primates of the genus Hapalemur are exceptional in their exhibition of specialisations allowing for a folivorous diet despite their small body size. Members of this group are well known for their preference for specific parts of woody bamboo, the primary food resource throughout much of their range. The southern gentle lemur (H.
meridionalis), however, inhabits littoral forests that contain little or no woody bamboo. Similar to its closely related congener, the Alaotran gentle lemur (H. alaotrensis), the question is raised as to how these lemurs subsist in this ecological context. The aim of this study was to gain an initial understanding of the ecological niche of the southern gentle lemur in the threatened ecosystem of the littoral forest of southeastern Madagascar. Lemurs were habituated and observed over a 3-month period during the austral winter, allowing for collection of both continuous and instantaneous focal data on their feeding ecology. Preferred food species were identified and collected, and biochemical analyses determined macronutrient and secondary compound values for consumed food items. The diet of the southern gentle lemur was found to be of low nutritional quality, as evaluated through the low protein-to-fibre ratio, especially when compared with other folivores. This lemur is also unique in spending a majority of its time grazing on terrestrial grasses (family Poaceae) during the resource-poor winter months. Our data indicate that Hapalemur spp. possess a behavioural flexibility, and possibly, digestive abilities, higher than previously thought for an animal of its small body size.
This study identifies populations currently classified as Allen's galago (Galago alleni) at ten locations in Gabon, Cameroon and Bioko Island. Morphological diversity was evident both within and between populations. Attention to the loud calls revealed three distinct vocal profiles which are consistent within biogeographical regions. This work is based on the Recognition Concept of Species which refers to a Specific Mate Recognition System. Galagos rely less on visual signals than diurnal primates and recognise each other principally by means of auditory and olfactory signals. Galagos possess repertoires of loud calls relating to contact and alarm which are thought to be species-specific. Other studies of nocturnal prosimians (galagos, tarsiers) have demonstrated that the unique loud call repertoires are reliable indicators of species boundaries; whereas characters such as body size and pelage coloration are highly variable, even within populations. The vocal data in this study provide evidence of at least three acoustic forms of galago within the Allen's group which are predicted to represent three distinct species: the Allen's form on Bioko Island and south-west Cameroon, the Gabon form in southern Cameroon and northern Gabon and the Makandé form in Gabon south of the Ogooué river. Some populations may be vulnerable to extinction due to limited distributions and habitat destruction.
This preliminary study characterizes the ultrasonic vocalizations produced by Philippine tarsiers, Tarsius syrichta. Data were collected at the Philippine Tarsier Foundation Sanctuary in Corella, Bohol, Philippines, from July through October 2010. Recordings were made on a Wildlife Acoustics Ultrasonic Song Meter 2 BAT from 29 wild, free-living adult resident T. syrichta (23 females and six males). A total of 10,309 USVs were recorded. These vocalizations fell into three main categories: chirps, twitters, and whistles. Chirps were the most frequent, followed by twitters and whistles. Whereas chirps and twitters were emitted by both male and female Philippine tarsiers, whistles were only emitted by adult males. Given that vocalizations reported in this study were exclusively recorded during capture and handling, it is very likely that these vocalizations function as distress calls. However, as the long whistle was only given by adult males who were captured at the same time as the female or the group's infant, the function of the long whistle might be slightly different than the function of the other relatively lower-frequency USVs.
The capacity of nonhuman primates to actively modify the acoustic structure of existing sounds or vocalizations in their repertoire appears limited. Several studies have reported population or community differences in the acoustical structure of nonhuman primate long distance calls and have suggested vocal learning as a mechanism for explaining such variation. In addition, recent studies on great apes have indicated that there are repertoire differences between populations. Some populations have sounds in their repertoire that others have not. These differences have also been suggested to be the result of vocal learning. On yet another level great apes can, after extensive human training, also learn some species atypical vocalizations. Here we show a new aspect of great ape vocal learning by providing data that an orangutan has spontaneously (without any training) acquired a human whistle and can modulate the duration and number of whistles to copy a human model. This might indicate that the learning capacities of great apes in the auditory domain might be more flexible than hitherto assumed.
This study describes video-task acquisition in two nonhuman primate species. The subjects were seven rhesus monkeys (Macaca mulatta) and seven chimpanzees (Pan troglodytes). All subjects were trained to manipulate a joystick which controlled a cursor displayed on a computer monitor. Two criterion levels were used: one based on conceptual knowledge of the task and one based on motor performance. Chimpanzees and rhesus monkeys attained criterion in a comparable number of trials using a conceptually based criterion. However, using a criterion based on motor performance, chimpanzees reached criterion significantly faster than rhesus monkeys. Analysis of error patterns and latency indicated that the rhesus monkeys had a larger asymmetry in response bias and were significantly slower in responding than the chimpanzees. The results are discussed in terms of the relation between object manipulation skills and video-task acquisition.
Sportive lemurs constitute a highly diverse endemic lemur family (24 species) for which many biogeographic boundaries are not yet clarified. Based on recent phylogeographic models, this study aims to determine the importance of two large rivers (the Antainambalana and Rantanabe) in northeastern Madagascar as species barriers for Lepilemur seali. The Antainambalana River was previously assumed to act as the southern border of its distribution. A total of 1,038 bp of the mtDNA of four individuals stemming from two adjacent inter-river systems south of the Antainambalana River was sequenced and compared to sequences of 22 described Lepilemur species. The phylogenetic reconstruction did not find support for either of the two rivers as species barrier for Lepilemur, as all captured individuals clustered closely with and therefore belonged to L. seali. However, a previously published sequence of an individual from a site south of our study sites belongs to a separate species. The southern boundary of L. seali must therefore be one of two large rivers further south of our study sites. The results suggest that L. seali may possess a relatively large altitudinal range that enabled this species to migrate around the headwaters of the Antainambalana and Rantanabe Rivers. Previous phylogeographic models need to be refined in order to incorporate these findings, and more species-specific altitudinal range data are urgently needed in order to fully understand the biogeographic patterns of lemurs on Madagascar.
We presented two chimpanzees with a task in which they were required to pull each end of a rope simultaneously to drag blocks supporting food into reach. The chimpanzees did not succeed in initial tests. They did not immediately understand the necessity for cooperation, and they did not adjust their behavior to work with the partner. However, the frequency of success gradually increased as the number of sessions increased and the task was varied. They began to look at the partner frequently, wait if the partner was not holding the rope, and pull the rope in synchrony with the partner. However, they did not use interactive behaviors or eye contact to synchronize their behavior. One chimpanzee was then paired with a human partner in the same situation. After initial failures, the chimpanzee began to solicit the human partner for cooperation: looking up at his face, vocalizing, and taking the partner's hand. When this chimpanzee was again paired with the chimpanzee partner, no soliciting behavior was observed. Thus, the chimpanzees could learn to coordinate their behavior through trial and error. Communicative behavior emerged during the task, but the communication differed according to the identity of the partner.
This is the first report of foot preference during locomotion in Old World monkeys. Foot preferences during the quadrupedal walking action and the bipedal shifting action of a naturalistic group of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Zhouzhi National Nature Reserve in the Qinling Mountains of China were investigated. Twelve of 21 individuals tested on quadrupedal action and all 21 individuals tested on bipedal action exhibited a significant foot preference. Both significant right- and left-footed preferences were observed; sex affected neither direction nor strength of foot preference in both actions. The finding that 61.90% of focal R. roxellana showed a right-foot preference, both in quadrupedal action based on the footed index and in bipedal action based on the z-score, is in partial agreement with the postural origin hypothesis on footedness. Foot preference was significantly stronger in bipedal action than in quadrupedal action, supporting the view that posture could be a crucial factor influencing foot preference as well as hand preference in this species.
Limestone hill habitats pose unique challenges to langurs. One of the characteristics of this habitat is its cliffs, which account for about 10-20% of the total area. We have never observed langurs falling from the cliffs during our 10-year field study. Five patterns of locomotion were exhibited by the white-headed langur: (1) arboreal ascent and descent, (2) arboreal quadupedalism, (3) terrestrial quadrupadelism, (4) moving on cliffs and (5) leaping on cliffs. Locomotor patterns varied according to the substrate, but terrestrial quadrupedalism accounted for more than 50% of locomotion time. Moving on cliffs and leaping on cliffs may be modes of locomotion unique to the white-headed langur, at least in terms of frequency. White-headed langurs have an intermembral index of 76 and, compared to langurs with a similar intermembral index, are more terrestrial. Further analysis indicates that greater terrestrialism may be the result of adaptation to their limestone habitat. Interestingly, white-headed langurs select caves on the cliff as their sleeping sites, and they exhibit special behaviors for exiting and entering the cave very early in the morning and late in the evening.
We describe and document with digital images an adult female baboon (Papio anubis) from the Kibale National Park, Uganda, who was missing all but the basal part of her upper jaw and nose, i.e., no premaxilla and very little of the maxilla and nasal bones. She appeared otherwise healthy, well integrated into a social group, and apparently reproducing, based on the fact that she was grooming a juvenile who suckled from her and that she appeared to be pregnant. Her extreme deformity raises numerous questions and demonstrates the highly adaptable capabilities of wild baboons.
It has been argued for nearly two decades that lemurs' low basal metabolic rate (BMR) by comparison to other primates is an adaptation to Madagascar's unpredictable climate. However, data from two recently published studies show that it is not just lemurs, but all strepsirrhines (the Suborder to which lemurs belong), that have low metabolic rates by comparison to other primates. Therefore, the better comparison to substantiate the argument is one with other strepsirrhines, not with all other primates. Data from the two studies do not allow the conclusion that lemurs' BMR is lower than that of other strepsirrhines.
Habitat, diet and leaf chemistry are compared between Japanese and Barbary macaques to reveal the similarities and differences in dietary adaptations of temperate primates living at the eastern and western extremes of the genus Macaca. Tree species diversity and proportion of fleshy-fruited species are much higher in Japan than in North Africa. Both species spend considerable annual feeding time on leaves. Japanese macaques prefer fruits and seeds over leaves, and Barbary macaques prefer seeds. These characteristics are adaptive in temperate regions where fruit availability varies considerably with season, since animals can survive during the lean period by relying on leaf and other vegetative foods. The two species are different with respect to the higher consumption of herbs by Barbary macaques, and the leaves consumed contain high condensed and hydrolysable tannin for Barbary but not for Japanese macaques. Barbary macaques supplement less diverse tree foods with herbs. Because of the low species diversity and high tannin content of the dominant tree species, Barbary macaques may have developed the capacity to cope with tannin. This supports the idea that digestion of leaves is indispensable to survive in temperate regions where fruit and seed foods are not available for a prolonged period during each year.
Four cases of coprophagy and two cases of fecal inspection were identified during the 1142 h of observing wild bonobos at Wamba in the Luo Scientific Reserve in the Democratic Republic of the Congo. At least 5 females in the study group practiced coprophagy and/or fecal inspection. According to our daily behavioral observations, boredom and stress, insufficient roughage, and the search for essential nutrients could not explain the coprophagy. Several episodes observed in this study indicated that bonobos might have sought and ingested certain valuable food items, such as hard Dialium seeds, in feces during relatively lean seasons. Although coprophagy occurred only rarely among wild bonobos, this practice appeared to represent a possibly adaptive feeding strategy during periods of food scarcity rather than a behavioral abnormality.
Coprophagy occurred during major periods of feeding on fruits of Dialium spp. (Caesalpiniaceae) in a group of orphaned chimpanzees released in Conkouati Douli National Park, Republic of Congo. Since stress, boredom or food scarcity could not explain coprophagy according to our daily behavioral and veterinary control observations, we suggest that Dialium seeds were the item of interest in the feces. Two types of Dialium seeds were commonly found in the feces after chimpanzees swallowed the mesocarp and whole seeds together. These seeds were either whole and hard or whole/broken and soft imbibed. A mechanical and/or chemical effect of the gut passage may enable the chimpanzees to chew and ingest the seeds, thus providing nutritional intake.
Myanmarpithecus yarshensis is an amphipithecid primate from the middle Eocene Pondaung Formation in Myanmar. It was previously known based on maxillary fragments with P(4)-M(3) and mandibular fragments with C-P(3) and M(2-3). This study reports new materials for the genus, including a humeral head fragment, a lingual fragment of the right M(2), a lingual fragment of the right M(3), and a left I(1). These new materials were collected from approximately the same point, and likely belonged to the same individual. The upper molar morphology and size of the new materials show similarity to those of the type specimen, indicating that the new materials can be assigned to M. yarshensis. The humeral head is the first postcranial element that is associated with dental materials for amphipithecids. The morphological similarity between the previously reported larger humerus and this specimen confirms the assignment of the former specimen to Amphipithecidae and suggests common locomotor adaptations in the family. The upper central incisor is large relative to the molar fragments, but is within the variation among extant platyrrhines. The tooth is spatulate-shaped and high crowned, and lacks the mesial process, indicating similarity to I(1) of haplorhines and clear differences from that of adapoids. It has been suggested that amphipithecids, including Myanmarpithecus, have affinities with notharctine adapoids, but the morphology of I(1) does not support the notharctine hypothesis of the Amphipithecidae.
Chiang Muan is the first Miocene fossil site in Southeast Asia, from which large-bodied Miocene hominoids have been discovered (Kunimatsu et al., Primate Res 16:299, 2000a). In this article, we describe a hominoid lower molar (CMu15-5'01) recovered from the Upper Lignite Member of Chiang Muan. The age of Chiang Muan is estimated to be latest Middle or earliest Late Miocene (around 11 Ma), based on the mammalian fauna.
Temperate forests are characterized by pronounced climatic and phenological seasonality. Primates inhabiting such environments experience prolonged resource scarcity and low ambient temperatures in winter and are expected to adjust time allocation and foraging behavior so as to maintain their energy balance. We analyzed the activity scheduling of a group of Yunnan snub-nosed monkeys (Rhinopithecus bieti) based on data collected over 20 months in the high-altitude (>3000 m) Samage Forest, Baimaxueshan Nature Reserve, PRC. The forest consists of evergreen conifers and oaks and deciduous broadleaf trees. The diet varied seasonally, with young leaves preferentially exploited in spring and fruits in summer. The monkeys subsisted on readily available fallback resources (mainly lichens) in winter [Grueter et al. in (Am J Phys Anthropol 140:700-715, 2009)]. We predicted that this switch to a relatively low-quality diet would prompt an increase in feeding effort and decrease in moving effort. We found that the monkeys spent significantly more time feeding in winter than in the other seasons. The monthly time devoted to feeding was also negatively correlated with temperature and positively with percentage of lichens in the diet. Time spent on moving did not vary among seasons or with temperature, but day-journey length was found to be longer on hotter days. Time spent resting was lower in winter and under colder conditions and was also negatively correlated with time spent feeding, indicating that resting time is converted into feeding time during times of ecological stress. These results indicate a strong effect of seasonality on time allocation patterns, constraints on inactivity phases, and the prevalence of an energy-conserving foraging strategy in winter, when costs of thermoregulation were high and the availability of preferred food was low.
Barbary macaques, like other non-human primates living in highly seasonal temperate environments, display high monthly variations in their diet. In addition, their diet changes according to the habitat type they colonize and to the degree of habitat degradation due to resource exploitation by local people, in particular through pastoralism. We studied the time-budget adjustments of wild Barbary macaques in three cedar-oak forests impacted by different intensities of grazing pressure from goats and sheep. We examined how diet variations influenced the time monkeys spent in their activities and their day range lengths (i.e. their energy costs). At three studied sites, diet composition and time budgets showed marked seasonal variations. Diet composition had a strong influence on monkeys' time budget. In the forest where pastoralism was the highest, diet included a greater proportion of underground resources, shrub fruit and acorns, which led to an increase in the time spent foraging and moving, as well as an important increase in day range lengths. Energy costs were therefore higher in a degraded environment than in a suitable habitat. The monkeys living in forests subjected to pastoralism took advantage of increased day lengths to spend more time searching for food. However, in the forest with the highest pastoralism pressure, although monkeys spent more time foraging, they spent less time feeding than monkeys at the other sites. In addition, they appeared to have reached the limits of the available time they could devote to these activities, as their diurnal resting time was at its lowest level over several months. Temperature variations did not appear to modify monkeys' time budgets. In the least favourable habitat, saving time from resting activity allowed monkeys to maintain a relatively high level of social activity, partly linked to rearing constraints.
We examined growth changes in concentrations of plasma insulin-like growth factor-1 (IGF-1) and testosterone, and somatometric parameters in two captive male agile gibbons from birth to about 4 years of age, to examine the evolution of growth patterns in primates. Plasma IGF-1 concentrations in agile gibbons generally increased with age with values ranging from 200 to 1100 ng/ml. The growth profiles in plasma IGF-1 in the gibbons were similar to those reported for chimpanzees. The highest concentrations of plasma testosterone (230 and 296 ng/dl) were observed within the first 0.3 years from birth, then the concentrations rapidly decreased and fluctuated below 100 ng/dl. Continuously higher IGF-1 concentrations were observed after 2.6 and 3.5 years of age. The profiles of plasma testosterone in these gibbons also resembled those of other primates including humans. However, their plasma testosterone levels in both neonate and adult stages (60 ng/dl) were lower than those reported for macaques and chimpanzees of respective stages. The obtained growth profiles of plasma IGF-1 and testosterone suggest that the adolescent phase starts around 2.6 or 3.5 years of age in male agile gibbons. The growth trend in many morphological parameters including body weight showed a linear increase without a significant growth spurt at approximately the onset of puberty. Head length and first digit length had reached a plateau during the study period. Brachial index, which indicates the relative length of forearm to upper arm, significantly increased gradually through the growth period. This result indicates that forearm becomes relatively longer than the upper arm with growth, which may be an evolutionary adaptation for brachiation.
Male mating tactics vary extensively in many primates. Some variation occurs because adolescent males often are sexually active but cannot invest heavily in mating effort because of their limited ability to compete directly with adults and because they are still investing in growth; consequently, most of their mating attempts may be surreptitious and/or with females whose fecundity is low. Chimpanzees (Pan trogolodytes) have a complex mating system: most copulations occur between estrous females with full sexual swelling and multiple males in group settings where the potential for sperm competition is high, but males sometimes mate-guard females, and sometimes male-female pairs mate exclusively with each other while avoiding other males during "consortships." Among other factors, dominance ranks, coalition formation, and variation in male-female association influence male mating and reproductive success. Mating effort increases from adolescence into prime adulthood. At Gombe and Mahale, adolescent males copulated more with nulliparous than with parous females, and mostly when females were unlikely to be ovulating, partly because of low adult male interest in nulliparous females and partly because of aggression from or avoidance of adult males. Adolescents thus had low probabilities of siring infants. However, adolescents are known to have gained some paternity at Gombe and in other populations, and their mating behavior deserves more study. I present data on mating by adolescent males in an unusually large chimpanzee community at Ngogo, Kibale National Park, Uganda. Adolescents at Ngogo also copulated more with nulliparous than parous females and mostly copulated outside of periovulatory periods. Also, they directed less aggression at estrous females than did adult males. However, they gained lower shares of copulations than reported for Gombe and Mahale, regardless of female parity, and received more aggression from adult males. These differences might partly reflect the influence of variation in the number of males per community on male mating tactics.
The present study examined grooming relationships of adolescent females in a free-ranging group of Japanese macaques (Macaca fuscata) at Katsuyama. To assess whether the loss of the mother influenced the grooming relationships of adolescent females (5-7 years old), we compared the time spent in grooming interactions and the number of grooming partners among the following three groups: 6 adolescent orphans with sisters, 9 adolescent orphans without sisters, and 11 adolescent non-orphans with surviving mothers. In Japanese macaques, grooming most frequently occurs between mothers and their daughters. Therefore, it is expected that if the mother is lost, orphans will devote less time to grooming interactions than non-orphans. However, the time spent in overall grooming interactions did not differ among the three groups. While non-orphans maintained grooming relationships with their mothers, orphans acquired alternative grooming relationships with other group members. Orphans adopted two kinds of tactics to compensate for the loss of the mother. First, adolescent orphans with sisters developed more affiliative grooming relationships with their sisters than non-orphans with sisters. Secondly, adolescent orphans without sisters spent more time in grooming interactions with same-aged females and non-related adult females. Moreover, regarding grooming interactions with same-aged females and non-related adult females, orphans without sisters had a larger number of grooming partners than non-orphans. These results indicate that adolescent females have enough flexibility to develop their grooming network after the loss of their mothers, and that the lack of mother and sisters might accelerate socialization of adolescent females and enable them to be integrated in reciprocal adult grooming relationships.