Crested Gibbons: Song Structure as Indication of Phylogenetic Relatedness

The genus Nomascus are one of the four genus that occurs in the Hylobatid family. Males have erect crown hair thus giving this genus its common name, crested gibbons. Crested gibbons are sexually dichromatic; males and females of the same species have different fur coloring and markings.The males tend to have black fur while females have orange to yellow fur. All species of Nomascus are either endangered or critically endangered. Like all gibbons, their trademark is their species-specific songs that they sing to communicate to each other. These songs, unlike those from song birds, are instinctual and are not learned (Thinh et al., 2011). Gibbons are the only monogamous ape.

Nomascus leucogenys mother and male offspring.

A new study, published this month on BMC Evolutionary Biology by Thinh et al. (2011) found that crested gibbons have species-specific song that can be used to differentiate the Nomascus species and also predict the phylogenetic relatedness of this genus. In this study, 6 Nomascus species were used as analysis: N. nasutus, N. concolor, N. leucogenys, N. siki, N. annamensis and N. gabriellae. The researchers used 92 out of 175 song recordings for acoustic analysis, analyzing 440 great calls (duets between males and females) and 447 male calls from 92 gibbon groups at 24 locations to confirm the relationship between song structure and phylogeny in Nomascus.

Video of Cao Vit gibbons (N. nasutus) singing. Notice the sexual dichromatism that occurs in males and females.

The researchers were able to tell the 6 Nomascus species apart by just listening to their song acoustics, albeit some with greater difficulties than others. N. nasutus and N. concolor could clearly be identified from their song acoustics. N. leucogenys, N. siki, N. annamensis and N. gabriellae on the other hand, have songs that are similar in structure but with minute differences. They also found a significant correlation between song structures and genetic similarity, which means that Nomascus species that are more closely related have similar song structures. This would account to N. leucogenys, N. siki, N. annamensis and N. gabriellae having same song structures but with minute differences in them because they are very closely related.

Map shows the distribution of all 7 Nomascus species. Illustration from ExtraWildlife.com

The authors also found that song similarities among species correspond to geographic location. They found a large difference in song structures between the most northern species and the most southern species, and a gradual difference when compared from the northernmost species to the southernmost species. This gradual difference in song structure, from the most northern species to the most southern species, supports the hypothesis that the genus originated from the north and successively migrated to the south. N. hainanus (omitted in the study) and N. nasutus are basal among crested gibbons (Nomascus). Together, these two species form a clade. N. concolor branched off first, then following by the rest of the Nomascus species; N. leucogenys, N. siki, N. annamensis and N. gabriellae. 

The cladogram of the genus Nomascus. Illustration from  Thinh et al. (2011).

Reference:
Thinh, V.N. Hallam, C. Roos, C. Hammerschmidt, K. 2011. Concordance between vocal and genetic diversity in crested gibbons. BMC Evolutionary Biology 11: 36 DOI: 10.1186/1471-2148-11-36

Apes Walking Upright: That's Just How They Roll (or Walk).

Orangutans, gorillas and chimpanzees do it. Bonobos seem to love doing it. Apparently gibbons do it really well. Indeed, bipedalism is not unique to humans and is quite common among apes. Apes are known to walk upright once in awhile, although bonobos seem to do it more frequently than other apes. Bipedalism is just one of the natural repertoire of ape locomotion.

(From left to right) Upright Apes Brigade: Gibbon, Orangutan, Gorilla, Chimpanzee and Bonobo. Click photo for larger image.

Upright Gorilla Goes Viral: 

Ambam the gorilla. Photo from Dailymail.

Currently going viral on the internet is a video of Ambam, a Western lowland gorilla (Gorilla gorilla gorilla) that was filmed walking upright in his enclosure. This 21 year-old, 485 lb. ape currently resides at Port Lympne wild animal park in Kent, England.

If you have not heard of Ambam or caught on to this internet sensation, you can read about him on :
Ambam, the swaggering silverback gorilla who walks around his pen on two legs (DailyMail)
Yes, he can walk. But just how close IS he to being human? (DailyMail)
Walk like a man: Gorilla strolls on hind legs (MSNBC).

It is not uncommon to see a gorilla walk upright but what's unique about Ambam is that he seems to walk upright quite frequently and good at it too. Bipedal locomotion is common in gorillas but they spend most of their time knuckle-walking. Ambam's upright gait and locomotion is definitely not an upright display to intimidate. Instead, it is most probably in response to curiosity and foraging in his enclosure. One of his keeper, Phil Ridges said:

"We think he might use it to get a height advantage to look over the wall when keepers come to feed him and standing up can also help him in looking for food generally in his enclosure as it gives him a better vantage point." Ridges added that Ambam could also carry more food if his hands were freed from walking and it also meant "he doesn't get his hands wet when it is raining."

It seems that the penchant for bipedalism runs deep in Ambam's family. His father, sister and half-sister (same father) prefer to walk upright and stand the same way as Ambam.

Ambam standing upright. Photo from Dailymail.

Is this a novel behavior in response to being in captivity? Is his skeletal and muscular structure (and in some sense his father, sister and half-sister) different than other gorillas? I think it would be interesting to see a behavioral study and an ethogram on Ambam's choice of locomotion. What are the percentage (or time spent) of him walking upright compared to knuckle-walking. Will his offspring be a fan of bipedality as well?

The Other Upright Ape:
While Ambam seem to prefer walking upright once in awhile, there is another ape that came before him who is a habitual biped. This ape is a chimpanzee named Oliver.

Oliver was a media (and science) sensation in the 60s and 70s for his preferred upright locomotion, having 47 chromosomes and a less prognathic face compared to other chimpanzees. Humans have 46 chromosomes while chimpanzees have 48 chromosomes. It was thought that Oliver is a "missing link" between chimpanzees and humans, thus nicknamed the "humanzee". While Oliver is not the missing link (Ely et al.,1998), he is truly a habitual biped.

The 52 year-old Oliver currently resides at Primarily Primates, a sanctuary in San Antonio, Texas. Below is a really good video of Oliver from his early years to his retirement. Seeing what happened to Oliver, I hope that they will not parade Ambam around like a freak of nature.

UPDATE: Oliver passed away on June 2nd 2012 at Primarily Primates. Read more here.

Reference:
Ely, J.J. Leland, M. Martino, M. Swett, W. Moore, C.M. 1998. Technical note: Chromosomal and mtDNA analysis of Oliver. American Journal of Physical Anthropology 105(3) 395-403. DOI: http://www3.interscience.wiley.com/journal/28165/abstract?CRETRY=1&SRETRY=0

Interspecies grooming at The Bronx Zoo

Interspecies grooming between Bonnet macaques (Macaca radiata) and Gray langur (Semnopithecus entellus thersites) at Kalakkad and Mundanthurai Tiger Reserve, India. Photo from TrekNature by Gopi.

Interspecies grooming is not unheard of and does occur naturally. While grooming can be dyadic and triadic (or even more), it can also be one-directional. Since grooming is central to primate sociality, there are reported instances of grooming between two different species of primates or even between a primate and non-primate. Grooming has many functions: hygiene, social bonding and even gaining favor.


I found this video yesterday (above) on Youtube by thekingchivas. I could not believe my eyes with what the camera caught. It shows a Malayan tapir (Tapirus indicus) being groomed by a White-cheeked gibbon (Nomascus leucogenys). After doing a Google search, I realize that this is not an isolated incident. Apparently The Bronx Zoo is also aware of this behavior and had posted its own video, which seems to be a separate incident from the one caught by thekingchivas.


I'm not going to definitively say that the tapir will not reciprocate in this grooming but chances are highly unlikely. I wonder what makes these gibbons (there were two females in the exhibit, The Bronx Zoo currently has a mated pair) groom their fellow exhibit-mate. While this might not be an altruistic exchange, we can view it as a mutual symbiotic relationship. Neither animal had its fitness reduced, so it is not altruism. Instead, both individuals benefit from this interaction so it is symbiotic.

The gibbons meticulously groom the tapir to remove insects, which in turns become a tasty snack for these gibbons. The tapir on the other hand, benefits by having pesky insects removed off its body. Is it significant that both animals are female? Is this behavior natural? There are recorded accounts of interspecies grooming between primates and non-primates, so it is quite likely.

A macaque grooming a goat on the streets of Chilkur, India. An example of mutual symbiosis between a primate and a non-primate. Photo by Libran Lover from A Lover's Journal.

A langur grooming a pig in Jaipur, India. Somehow nature managed to put two animals that I have polar opposite feelings together (one I love, the other I hate). Another example of mutual symbiosis between a primate and a non-primate. Photo by Christa Kate Hyland from Laddus and Langis.

The range of both Malayan tapirs and White-cheeked gibbons does not overlap. Malayan tapirs occur in Malaysia, Indonesia, Thailand and Myanmar while White-cheeked gibbons are found in Vietnam, Laos and the Yunnan province of China. Therefore, interspecies grooming between Malayan tapir and White-cheeked gibbon is probably a novel behavior that cannot be observed in the wild.

Map shows the current and historic range of Malayan tapir, as of 2003. Notice that Malayan tapirs do not occur in Vietnam, Laos nor China (Yunnan province) where White-cheek gibbons occur. Illustration by Sasha Kopf from Wikipedia.

New Gibbon Species Discovered

A new gibbon species have been discovered by researchers, led by Christian Roos, from the German Primate Center (Deutschen Primatenzentrums) and was published on Vietnamese Journal of Primatology. The northern buffed-cheeked gibbons (Nomascus annamensis) live in the rainforests of Annamite Mountains, situated around Vietnam, Laos and Cambodia. The northern buffed-cheeked gibbons were once thought to be the yellow-cheeked gibbons (Nomascus gabriellae) but vocalization and genetic research prove that both are distinct species.

The northern buffed-cheeked gibbon males (left) have a black pelt that shimmers silver in sunlight. The chest is brownish in color and the cheeks are deep orange-golden. The crest is very prominent in males. Females (right) are orange-beige in color and lack the characteristic crest. Photo by Tilo Nadler, Endangered Primate Rescue Center, Vietnam.

"The discovery of a new species of ape is a minor sensation", Christian Roos warns. All crested gibbons (genus Nomascus) are either endangered or critically endangered with Hainan black crested gibbons (Nomascus nasutus hainanus) the most critically endangered, totaling to only 20 individuals. The sharp decline of Hylobatids can be contributed to illegal hunting and loss of habitat. “Knowledge of their biology and exact distributions is essential for effectively protecting the animals. Only if we know where which species is found and how many individuals there are can we start with serious conservation actions", Roos adds.

Comparison between the northern buffed-cheeked gibbon male (left) and the yellow-cheeked gibbon male (right). Photo of the yellow-cheeked gibbon from The Gibbon Network.

Comparison between the northern buffed-cheeked gibbon female (left) and the yellow-cheeked gibbon female (right). Photo of the yellow-cheeked gibbon from The Gibbon Network.

Gibbons are mostly monogamous, pair-bonding primates that are strongly territorial. These vocal displays or songs, usually a duet between a mated pair and sometimes their offspring, can be heard from as far as 1km away. Gibbon songs are territorial displays, perhaps if a gibbon can hear another gibbon sing then it is  encroaching a mated pair territory. Oh, in case you are wondering, gibbons do not have tails (they are apes).

For more about this discovery:
New ape species uncovered in Asia on Mongabay.com
New gibbon species discovered in Indochina on Informationsdienst Wissenschaft

Thinh, VN. Mootnick, AR. Thanh, VN. Nadler, T. Roos, C. A new species of crested gibbon, from the central Annamite mountain range. Vietnamese Journal of Primatology 1(4), 2010, 1-12.

P/S - Anyone able to find Thinh et al. (2010) publication online or the Vietnamese Journal of Primatology is not available online?

So Adowable

A baby white-handed gibbon was born at Vienna's Schoenbrunn Zoo to father Robert (aged 11) and mother Sipura (aged 21) on Sept 23rd. The baby was dubbed "ET" by the Vienna media after the famous Hollywood blockbuster alien although the zoo does not have an official name for the baby yet. Isn't he adorable? I can't stop saying "awwwwww".

 "ET" snuggling with his mother. Photo from Austrian Times.

White-handed gibbons or Lar gibbons (Hylobates lar), are listed as near threatened in the International Union for Conservation of Nature (IUCN) Red List. The Philadelphia Zoo has white-handed gibbons in their PECO Primate Reserve. Awwwwww ........

Two Rare Primates From China and Vietnam Given a Second Chance

Two new protected areas were designated in China and Vietnam recently to protect two of the world's most endangered primates by Fauna and Flora International (FFI). The Tonkin snub nosed monkey (Rhinopithecus avunculus), found only in Vietnam, numbers about only 200 individuals in the wild while the eastern black crested gibbon or cao vit gibbon (Nomascus nasutus), second most endangered primate in the world, numbers only just 110 individuals. Both species are listed as "critically endangered" in the International Union for Conservation of Nature (IUCN) Red List. The Tonkin snub nosed monkeys were thought to be extinct until a small population was rediscovered in the early 1980s.

Read more about the Tonkin snub nosed monkeys, cao vit gibbons and the new nature reserves from Wildlife Extra.

Male (left) and female (right) cao vit gibbons. Photo from Fauna and Flora International.

The Tonkin snub nosed monkey. Photo from Fauna and Flora International.

When Is A Monkey Really A Monkey?

A little boy pressed his nose on the glass where a Western Lowland Gorilla is interacting with the zoo-goers. He turns around to his parents with a big smile. “Oh look, the monkey wants to kiss you”, said his mother.

At the lemur exhibit, a girl asks her parents what those black and white primates were. Her dad picks her up and said, “It’s a monkey, sweetie … let’s go”.

A pair of gibbons gracefully swings around in their exhibit. Excited, a group of kindergarteners cheered as these gibbons maneuver around its habitat with great agility. “These monkeys are so active”, said the teacher.

If this sounds familiar to you then you are not alone. I spent a great deal of time near primate exhibits mainly because I love to observe their behaviors. I also enjoy watching interaction between humans and primates. However, there are times when I just can’t control myself and felt compelled to walk over to these people and explain to them that the word “monkey” is not a general term for primates (politely, of course). It shocks me that most of the time people do not read the information panel at the exhibit (aren’t zoo trips for educational purposes?). So when is a monkey really a monkey?

Monkey is a colloquial term for any cercopithecoids (Old World monkey) and platyrrhines (New World monkey). Monkeys are not hominoids (apes) or prosimians. One of the most distinctive characteristic that differentiate monkeys and apes is the presence of a tail in monkeys. Gibbons, siamangs, orangutans, gorilla, chimpanzees and bonobos are apes because they do not have a tail.

Gorillas do not have tails, so they are not monkeys but apes.

Differentiating monkeys and prosimians are a little tricky; all prosimians have grooming claws (toilet claws) but it is generally not visible within zoo exhibits. Prosimians include lemurs, lorises, galagos, aye-ayes and tarsiers.

A ring-tailed lemur is a prosimian. Although it has a tail, it also have grooming claws so lemurs are not monkeys.

A hamadryas baboon is technically a monkey because it has a tail but has no grooming claws.

The Barbary Macaque, Macaca sylvanus, was formerly named Barbary Ape due to the absence of a tail (to be more precise, they have a vestigial tail that looks like a stump). However, we know now that it is more closely related to macaques than to apes so its name was changed to correctly reflect what they are.

A Barbary Ape (notice the lack of tail). Flickr photo from Gerald Davison.

This brings us back to the question, “when is a monkey really a monkey’? The most straightforward answer would be “when it has a tail but doesn’t have grooming claws”. However, the most convenient answer usually lies in front of you … on the information panel.

Flickr photo taken by tim ellis at the Twycross Zoo, England.
The sign reads "Who are you calling a monkey?"

Mirror Mirror On The Wall, Who Is That Other Gibbon?

Gibbons (lesser apes) have no use for mirrors, studies had shown (Suddendorf and Collier-Baker, 2008). They are not able to recognize themselves in front of a mirror. Typical human children starts to recognize themselves in front of the mirror around two-years-old. Mirror self recognition or visual self recognition is not unique to humans, it was only documented in great apes (chimpanzees, bonobos, orangutans and gorillas). Humans and great apes are different than other primates because they can recognize themselves in front of a mirror. Self recognition in front of a mirror enable them to see areas of the body where they cannot see directly. Self recognition probably evolved in the common ancestors of great apes around 18 million years ago.

Primate phylogeny. The ability of mirror self awareness probably evolved around 18 million years ago with great apes (chimpanzees, bonobos, orangutans and gorillas) common ancestors Image from www. mun.ca

A gibbon seems to be interested in itself, but none tried to get at icing on their own faces (Image: Emma Collier-Baker) Photo from www.newscientist.com

The gibbons sometimes tried to reach around the mirror to get at the ape on the other side (Image: Emma Collier-Baker) Photo from www.newscientist.com

Read more about "The evolution of primate visual self-recognition: evidence of absence in lesser apes" by Suddendorf and Collier-Baker, 2008 (full article) (abstract).

"King of the swingers has no use for mirrors" by Ewen Callaway on Newscientist.com

Citation:
Suddendorf T. Collier-Baker E. 2008. The evolution of primate visual self-recognition: evidence of absence in lesser apes. Proceedings of the Royal Society B (doi: 10.1098/rspb.2008.1754 ) http://rspb.royalsocietypublishing.org/content/early/2009/02/21/rspb.2008.1754.full