Covers

Left: Proboscis monkey (Nasalis larvatus) ©Ikki Matsuda

This photo shows a female proboscis monkey (Nasalis larvatus) with an infant resting in a mangrove tree (Sonneratia caseolaris), taken in the Lower Kinabatangan, Sabah, Malaysia. The infant, just after birth, is covered with black fur all over its body. Over a period of about 2 years, the fur gradually changes to a colour similar to that of the adult, and finally the black colour of the face skin changes to the same colour as the adult, as the monkey becomes a juvenile. With the help of local governments and universities, Matsuda has been conducting long-term ecological studies of proboscis monkeys in the riverside forest (Sukau) and mangrove forests (Abai) in the Lower Kinabatangan since 2005. The proboscis monkey is a member of the Afro-Eurasian monkey subfamily Colobinae, and is unique to Borneo. It is a foregut fermenter and has a natural diet generally dominated by leaves, fruits (mostly unripe), and seeds. They are large, sexually dimorphic and arboreal colobines living in social groups that typically consist of a single adult male and multiple females, although mixed-sex groups occasionally contain several adult males; there are also all-male groups and sometimes solitary males. They are categorized as ‘Endangered’ under the IUCN Red List and listed under Appendix I of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) (Ikki Matsuda).

Upper right: Black and gold howler monkey (Alouatta caraya) ©Isadora Alves de Lima

Black and gold howler monkeys (Fig. 3) are South American atelids found in forests of the Cerrado, Pampa, Pantanal, Chaco, and Caatinga in Brazil, Argentina, Paraguay, and Bolivia. They are characterized by marked sexual dimorphism. All infants are born with a blonde pelage that starts to darken in young males and reaches full black at adulthood. Females continue blonde throughout their lives or turn light brown as they age. Black and gold howlers live in social groups of 2 to around 20 individuals, often led by a single dominant adult male. The bulk of their diet is composed of leaves and fruit, complemented with flowers, stems, seeds, and bark. Howler monkeys play an important role in the structuring and regeneration of their forested habitat via seed dispersal. A highly flexible diet helps them to adapt to disturbed and anthropogenic habitat patches. Urbanization causes habitat loss and fragmentation and increases the risk of interaction with humans. The presence of howler monkey groups in city squares is uncommon anywhere in the species range. Under these circumstances, howlers may supplement their diet with food from people, exposing them to the risk of contagion from infectious agents of human diseases. They can also be hit by cars, electrocuted in power lines, and chased by people and domestic dogs. This photo was taken in September 2022 in an urban square in Manoel Viana, state of Rio Grande do Sul, Brazil. The group consists of an adult male (not shown in the picture), an adult female, two subadult males, a juvenile male, a juvenile female (also not shown), and an infant male (Isadora Alves de Lima).

Lower right: Mountain Gorilla (Gorilla beringei beringei) ©Martha M. Robbins

Mountain gorillas (Fig. 4) live in cohesive social groups, typically consisting of one or more adult males (silverbacks), adult females, and immatures of all ages. A typical day for mountain gorillas consists of alternating periods of feeding and resting. During rest sessions, such as pictured here, members of the group are often in close spatial proximity. Adults may groom each other or simply rest near one another, while infants and juveniles play. The photo was taken when I was visiting a PhD student working in the Virunga volcanoes in 2009. The photo is of Cantsbee’s group, monitored by the Dian Fossey Gorilla Fund. Cantsbee, the silverback, was born in 1978, into one of the original groups habituated by Dian Fossey. Cantsbee was a young, subordinate silverback in a multimale group when I conducted my PhD research in the early 1990s. Eventually, he came to be the alpha male of a very large group and he sired many offspring (Martha M. Robbins).

Upper left: gray woolly monkey (Lagtothrix lagotricha cana) ©Thiago Cavalcante

Gray woolly monkeys are large-bodied, opportunistic frugivorous primates that occur in the Amazon forests of Brazil, Peru, and Bolivia. They live in multi-male, multi-female groups of up to ca. 40 individuals. This taxon provides invaluable seed-dispersal services and its disappearance from tropical forests can alter long-term forest dynamics that maintains above-ground biomass and carbon stocks. This photograph of an adult individual vocalizing was taken in July 2016 in a forest fragment in the municipality of Cacoal (Rondônia state, Brazil), during a study on gray woolly monkeys’ social dynamics. Woolly monkey social structure is typically described as characterized by male philopatry, with females usually leaving their natal groups. Their diet is mainly composed of fruit (up to 80%), and complemented with leaves, flowers, arthropods, and even small vertebrates. Intragroup feeding competition, especially over fruit, is an important modulator of their social dynamics. To sustain such large groups and highly frugivorous diets, their home ranges can reach up to more than 1000 ha. However, this monitored population had probably the smallest home range recorded for woolly monkeys (less than 100 ha). In such small, isolated habitats, feeding competition can be expected to occur at a high frequency due to the exploitation of patchily distributed and seasonally scarce high-quality food resources, as shown by the research carried out in the area. Rondônia has one of the highest deforestation rates of all states of the Brazilian Amazonia. Unfortunately, this population is increasingly facing serious threats from habitat loss, free-roaming domestic dogs, hunting, and forest fires. (Thiago Cavalcante). 

Upper right: Borneo orangutan (Pongo pygmaeus) ©Tomoko Kanamori

The Danum Valley Conservation Area, located in Sabah, Malaysia, is the oldest primary forest in Borneo and is strictly protected. The forest vegetation in the area is lowland mixed dipterocarp forest, in which a phenomenon known as 'mast fruiting' occurs, when many tree species bear fruit at the same time once every 2–10 years. A Japanese team has been conducting long-term ecological research on wild orangutans in the Danum Valley since 2004. Researchers are still working on topics such as how foraging behavior, population density, and reproduction change depending on the mast fruiting season, DNA paternity testing, and stable isotope analysis, etc. In 2022, 63 orangutans were identified, of which 17 settled individuals are continuously being monitored. One of these is the orangutan in this photo. This adult male Borneo orangutan was photographed in 2017 at Danum Valley. His name is SON and at the time he was estimated to be around 30 years old. When male orangutans reach maturity, large folds on both cheeks called “flanges” develop on the most dominant ones. SON has slightly thin flanges. He began to appear within our survey area in 2016 and was still observed in 2019. SON is not fearful of people and sometimes leaves the forest to roam around the village. Due to the pandemic, there was a period when researchers could not visit the survey area. However, since the survey was resumed in July 2022, he has been spotted occasionally. The photograph was taken when SON was eating fruit of Area catechu. (Tomoko Kanamori). 

Lower: Baboon (Papio ursinus griseipes) ©Lee Bennett 

This is one of the male baboons from the Floodplain troop of Gorongosa National Park, Mozambique. This photo was taken where the Muzicadzi River in the park makes a sharp turn before joining the Sungue River. It is a popular crossing point for many animals but all of them are aware of the crocodiles that lurk just below the surface of the water. The whole troop had crossed earlier and this male was one of the “tail enders” and, like all of the baboons that had crossed before him, he put all of his energy into the leap. It is interesting to note that despite the water being only about 10 cm deep, which can be deduced by looking at the water level on the yellow-billed storks’ legs, and that the riverbed is sand and not soft mud, the baboon still committed totally to his jump. He did not hesitate at all when he got close to the water; he made a short run and jumped, landing well clear of the water. Some of the young baboons hesitated before jumping, and only did so after seeing other troop members cross successfully, and when their feet got wet when landing they accelerated and looked startled (Lee Bennett & Susana Carvalho). 

Left: ring-tailed lemurs (Lemur catta) ©Shinichiro Ichino

An adult female carries three newborn infants, in Berenty Reserve, southern Madagascar. This is not a mother and triplets. Instead, the adult female is carrying her own infant and those of her two sisters. Moreover, she appears to nurse them (allonursing). The ring-tailed lemur is characterized by strict seasonal breeding, with gestation occurring during the dry season and lactation in the wet season. In Berenty, most females give birth annually around September. Troop members have a strong interest in newborn infants and frequently try to approach the mother and lick the infant. Infants sometimes move onto other group members through physical contacts, especially among close kin. In most cases the infant returns to its mother after a short time, but sometimes the transfer continues for more than a day. This adult female (ME-899401♀) belonged to troop C1 when the photo was taken in September 2006. Starting around 2004, there was tension among females in the troop, and this female and her sisters (ME-899499♀ and ME-899402♀) were evicted from the troop after some intense aggression by other females. Subsequently, the three sisters successfully rejoined the troop, and were dominant over other females by September 2006. The female and her sisters are likely to have shared strong bonds. In 1981, Dr. Naoki Koyama started observing individually identified ring-tailed lemurs in Berenty, and long-term studies by him and his coworkers have been going on since then. (Dr. Shinichiro Ichino). 

Upper right: bearded capuchin monkeys (Sapajus libidinosus) ©Luca Antonio Marino

An adult male (“Mansinho”) with a palm nut kernel in his mouth; he has just cracked open the nut using a round-shaped, heavy stone as a hammer to pound the nut on a log anvil. The young male Coco is watching closely while Mansinho extracts remaining kernels from inside the shell. This photograph was taken by Luca Antonio Marino in October 2014 in Fazenda Boa Vista (FBV), in the state of Piauí, Brazil. At that time, Mansinho was a subordinate male in his group. He was previously the alpha male, but a change in status occurred in 2010 after a male takeover fight which resulted in him being severely injured and losing his left foot. In 2015 the group split, and since then he has been the alpha male of the smaller group. The bearded capuchins in FBV have been studied since 2003 by Dr. Patrícia Izar (University of São Paulo, Brazil), Dr. Elisabetta Visalberghi (ISTC, CNR, Italy), and Dr. Dorothy Fragaszy (University of Georgia, Athens, GA, USA), coordinators of the EthoCebus project. This long-term research revolutionized our understanding of conditions for tool use and traditional inheritance processes in nonhuman primates. Challenging the view that capuchins have no understanding of properties of objects, naturalistic observation and field experiments demonstrated that capuchins in FBV perceive the affordances of tool materials and tasks, such as weight and friability of stones and resistance of nuts, and are capable of at least short-term planning when selecting stones and adjusting their body movements and force for nuts of different resistance. These skills develop through a long process (ca. 5 years) of individual practice, socially influenced by the activity and artifacts of skilled group members that attract sustained attention of unskilled youngsters. Unfortunately, these amazing monkeys and their traditions along with the traditions of the local human communities that have coexisted for millennia are now at risk due to expanding, intensive agriculture in the region. It is our duty as primatologists to raise awareness about the impact of human activities on the environment and fight for the survival of other species. (Dr. Patrícia Izar). 

Lower right: stump-tailed macaques (Macaca arctoides) © Aru Toyoda

The stump-tailed macaque (or bear macaque) is the most distinctive species in genus Macaca in terms of reproductive anatomy and reproductive behaviors. This species is widely distributed in continental Southeast Asia including northeastern India, southern China, Myanmar, Laos, Thailand, Vietnam, Cambodia, and the northwest tip of West Malaysia on the Malay Peninsula. As the Japanese name implies (benigao in Japanese means rosy-faced in English), both males and females have red faces. The color of the dorsal pelage is usually reddish-brown, but some individuals in southern populations have a blackish pelage. The blackish population used to be classified as a different subspecies (M. arctoides melanota). Unusually for this genus, infants are born with a completely different pelage color from adults; it is whitish or pale-golden, turning darker as the infant matures. Whitish infants play an important role as a catalyst for various social interactions. Adults show interest in white infants and frequently touch their genitals. This behavior, described as “Touch Baby’s Genitals,” can trigger social interactions with the mother as she carries the infant or relieve tension between adults in an aggressive context. These are examples of “agonistic buffering.” The photograph shows a family of wild stump-tailed macaques—a mother feeding her infant and older siblings welcoming their new brother. An older daughter sitting next to her mother touches her younger brother’s genitals. As the mother always pays attention to her infant, the young daughter may be looking for opportunities to interact with her mother through touching the infant. The photograph was taken in October 2020 at Khao Krapuk Khao Taomor Non-hunting Area, Phetchaburi province, Thailand. There were known to be 22 individuals in this population when it was first studied in 1988. Currently, it has at least 391 individuals, divided into five groups, recorded by A. Toyoda in 2017. This population has been studied since 2015 by A. Toyoda, under the supervision of Prof. Dr. Tamaki Maruhashi. (Dr. Aru Toyoda). 

2021

Snow monkeys (Macaca fuscata) in the snow. Photo by Toshio Hagiwara.

These are Japanese monkeys in Jigokudani, Shiga Heights, in Nagano prefecture. This photograph was taken by Toshio Hagiwara, for which he received the Grand Prize in Nature’s Best Photography Windland Smith Rice International Award in 2006. The award is presented by The Smithsonian’s National Museum of Natural History. The photo is of a young adult female, 6–7 years old, with her infant, and was taken on January 12, 2005. Mr. Hagiwara is currently the General Director of the Jigokudani Yaen-Koen, Wild Snow Monkey Park. Japanese monkeys, often called snow monkeys, of Jigokudani developed hot-spring bathing behavior soon after provisioning began in 1962. This behavior continues to attract attention from people outside of Japan and the foreign media, but without a proper understanding of the origin of the behavior. This is mainly due to the lack of academic literature written on the topic in English. However, the journal Primates has been publishing scientific papers on this unique behavior since 1965: see the most current one by Takeshita et al. (2018). In addition to hot-spring bathing, long-term studies of Japanese monkeys in various places have revealed the culturally transmitted behaviors or social customs that are unique to each of the wild groups. Koshima monkeys are known for sweet-potato washing. Awajishima monkeys form extra-large clusters, Arashiyama monkeys engage in stone-handling, Yakushima monkeys (Macaca fuscata yakui) embrace in a unique way, and so forth. Field studies of Japanese monkeys started in 1948.

The long-term research over 7 decades has brought new findings and provides firm foundations for conservation efforts. Many people do not realize that in many countries many wild monkeys are killed because they are considered pests. In Japan, this happens to about 15,000 individuals per year on average. The Primate Research Institute (PRI) of Kyoto University has started setting up monkey colonies for breeding in the financial support from National BioResource Project (NBRP) of the Japanese government in 2002. The use of wild individuals directly for invasive experimental purposes is prohibited. The NBRP contributes toward conservation of the regional groups as well. The pair of monkeys in the photo actually belong to a group that was transferred from Jigokudani to the PRI. They became members of a troop for producing the next generation of captive-born monkeys for various kinds of experimental use. There are hundreds species of living primates depending on which classification is used: 447 by Japan Monkey Centre in 2018 and 512 species of 79 genera by IUCN in 2019 Humans and nonhuman primates have to coexist not only in Japan but also in other host countries across the world. We are still on the way to find the best solutions for peaceful coexistence. To that aim, we will continue scientific studies of nonhuman primates in parallel with efforts to improve captive animal welfare and conservation in the wild.

Tetsuro Matsuzawa, Immediate-Past Editor-in-Chief

2020

Chimpanzee (Pan troglodytes) in Bossou, Guinea, Photo by Anup Shah and Fiona Rogers.

A young male chimpanzee, Peley, performs a form of tool use called ‘‘algae scooping’’. He uses a stick to collect algae floating on a pond. This unique tool use behavior was first found in Bossou in 1995. I have been studying the Bossou chimpanzee community since 1986. Peley was born in April 1998. The mother, Pama, was about 31 years old at the time, and had two other offspring:, a 5-year-old son named Poni, born on February 4, 1993, and an 11-year-old daughter named Pili, born in early 1987. Pili had already given the birth to her own son, Pokuru, in August 1996–Pokuru was thus Pama s 1.5-year-old grandson. At the time of Pokuru’s birth, the young mother Pili was only 9 years old. It is very rare for wild chimpanzees to give birth at such an early age. However, we have so far observed four different cases of 9-year-olds giving birth at Bossou. This might be due to the nutrition-rich diet of Bossou chimpanzees who consume various human agricultural products. Let me tell you the story after Peley s birth. Poni, his older brother, died in November 2003, at the age of 10 years during a flu-like epidemic that ravaged the Bossou community.

We lost five chimpanzees in total: two old ladies, two infants and Poni. Pili, Peley’s big sister, disappeared with her son sometime between late 2000 and early 2001 (it is likely that they emigrated from their natal Bossou community to a neighboring one). Thus, years later, at the time this photo was taken in December 2010, Pama had only one son remaining at Bossou, Peley. He always accompanied her everywhere. Then, one day in September 2013, Pama, Peley and Tua, the former alpha male of the community, suddenly disappeared. The final witness saw the three chimpanzees in the forest of Seringbara, the destination of a ‘‘green corridor’’ connecting Bossou and the Nimba Mountains. We were puzzled why the two big males and the adult female decided to depart, but their loss made a huge impact on the continued survival of the Bossou community. Once the chimpanzees of Bossou are gone, their unique culture will be gone too. 

2019 

The new cover of Primates features a young male chimpanzee named Jeje walking along a human trail toward the observers. Photo taken by Anup Shah and Fiona Rogers in Bossou, Guinea. I have been studying the Bossou chimpanzee community since 1986. Jeje was born in December 1997. The mother Jire, who was about 40 years old at the time, had another elder female child, named Juru. Juru was born on November 19, 1993, and disappeared in December 2001, at the age of 8 years. It is common for wild chimpanzees to disappear (likely emigrate from their natal community to a neighboring one) once they enter puberty. Years later, at the time this photo was taken in December 2010, Jire had three offspring: Jeje (14 years old) and two other dependent youngsters, Joya (6 years old) and Jodoamon (1 year old). Joya was born at 14h00m on September 2nd 2004. It is rare for researchers to have the opportunity to directly observe a birth among wild chimpanzees. Jodoamon was an infant female born on November 18, 2010. Jeje had just become the alpha male of the community. (written by Tetsuro Matsuzawa). 

2018

The new cover of Primates features a young female chimpanzee named Joya using a pair of stones as a tool to crack open an oil-palm Nut. Photo taken by Anup Shah and Fiona Rogers in Bossou, Guinea. She was born on September 2nd, 2004, and this event occurred in December 2010, when she was 6 years and 3 months old. The chimpanzees of Bossou use a pair of stones as a hammer and anvil to crack open the hard shell of the oil-palm nut to get at the soft, edible part within, the kernel. This is a cultural behavior unique to this community and is transmitted socially from one generation to the next. The chimpanzees acquire the skill at around 4-5 years old. The learning process involved is called "Education by Master-apprenticeship" (Matsuzawa et al., 2001). 

2017

The new cover of Primates features an infant male chimpanzee named Flanle wearing a leaf hat. Photo taken by Anup Shah and Fiona Rogers in Bossou, Guinea. Flanle was born September 14, 2007, and the episode occurred at the age of 3 years and 3 months. The hat was made from palm leaves and was used by local people as a cushion for the head when carrying heavy objects. It was discarded by a villager who had carried a heavy oil-palm bunch. No adult chimpanzees paid attention to the discarded leaf hat, but the infant chimpanzee found it and put it on his head immediately. This is an example of delayed imitation of human behavior by a chimpanzee. The mother was using stones to crack open oil-palm nuts. When the infant came near his mother, she tried to make Flanle stop playing with the hat, but he ran away. 

2016

The new cover of Primates features an infant male chimpanzee named Flanle wearing a leaf hat. Photo taken by Anup Shah and Fiona Rogers in Bossou, Guinea. Flanle was born September 14, 2007, and the episode occurred at the age of 3 years and 3 months. The hat was made from palm leaves and was used by local people as a cushion for the head when carrying heavy objects. It was discarded by a villager who had carried a heavy oil-palm bunch. No adult chimpanzees paid attention to the discarded leaf hat, but the infant chimpanzee found it and put it on his head immediately. This is an example of delayed imitation of human behavior by a chimpanzee.