Contagious Yawning from Human to Domestic Dogs: Is It Possible? What Are The Implications?

Yawning is a phenomenon that occurs not only in human but also in other animals such as mammals, fishes, amphibians, reptiles and birds (Heusner, 1946; Baenninger, 1987; Gallup et al., 2009). There are many proposed reasons and functions as to what elicit yawning behavior in an individual but little is known about the role of contagious yawning and how animals can catch yawns from other species. Even though yawning is widespread in the animal kingdom, contagious yawning has only been reported in humans, chimpanzees (Pan troglodytes), stumptail macaques (Macaca arctoides) and recently in domestic dogs (Canis familiaris) (Provine, 1986; Platek et al., 2003; Anderson et al., 2004; Paukner & Anderson 2006; Joly-Mascheroni et al., 2008; Harr et al., 2008). In addition, studies have shown that there is a positive correlation in the susceptibility of contagious yawning with empathy and theory of mind (Platek et al., 2003; Preston & de Waal, 2002), and that emotional closeness and relatedness between an individual is key to eliciting contagious yawning in human (Norscia & Palagi, 2011).

Contagious yawning has been reported in humans, chimpanzees, stumptail macaques and  domestic dogs.

There have been many suggestions on the roles of contagious yawning, especially in primates. Some literatures hypothesized that contagious yawning in primates plays potential roles in communication, social interaction, empathy and self-awareness (Deputte, 1994; Daquin et al., 2001; Platek et al., 2003; Gallese et al., 2004; Platek et al. 2005) while others thinks that it is a stereotyped action behavior and an innate releasing mechanism (Provine, 1986). In addition, Platek et al. (2003) showed a positive correlation in the susceptibility to contagious yawning with self-face recognition and theory of mind stories while children with autism spectrum disorder showed an absence in contagious yawning (Senju et al., 2007) suggests that contagious yawning may be related to empathy (Preston & de Waal, 2002). A recent study on yawn contagion in human shows that related individuals (r ≥ 0.25) were the ones that are more susceptible to contagious yawning, and concludes that emotional closeness between an individual is key to contagious yawning in human as opposed to other variable such as sex or country of origin (Norscia & Palagi, 2011).

Although yawning is widespread in the animal kingdom, contagious yawning has only been reported in humans (Provine, 1986; Platek et al., 2003), chimpanzees (Anderson et al., 2004), stumptail macaques (Paukner & Anderson 2006) and domestic dogs (Joly-Mascheroni et al., 2008; Harr et al., 2008). Contagious yawning from human to domestic dogs  is interesting because it could further elucidate if empathy was inadvertently selected for in domestic dogs as they evolve side by side with modern humans. If yawns can indeed be passed from human to domestic dogs, we can posit that domestic dogs are capable of empathy. Further experiment on contagious yawning from the owner (human) to domestic dogs could also elucidate whether yawns are more susceptible based on emotional closeness as per Norscia & Palagi's (2011) research, albeit their subjects are all humans.

Neonatal macaque imitation the expression of a researcher.

Gallese et al. (2004) contended to the fact that mirror neurons play an integral part on the theory of mind and empathy. Later experiment by Iacoboni et al. (2005) posits that mirror neurons are involved in understanding the intention of others. By using an FMRI, human subjects were exposed to 3 types of stimuli on 24 second video clips. These stimuli show grasping hand action without a context (Action), context-only (Context), and grasping hand with and without context (Intention). In the Action stimuli, a hand was shown grasping a cup in the absence of context and an objectless background. Two types of grasping actions were used: either precision grasping (hand grasping the cup handle) or whole-hand grasping (hand grasping the cup body). The Context stimuli showed three dimensional objects such as a teapot, a mug or a cookie just before or just after having tea to elicit a drinking or cleaning context. For the Intention stimuli, the subjects were presented with both grasping actions in both drinking and cleaning context. When presented with the Intention stimuli, there is a significant signal increase in the premotor cortex; the posterior part of the inferior frontal gyrus and the adjacent sector of the ventral premotor cortex where hand actions are represented. The authors argue that the premotor mirror neuron areas are involved in understanding the intention of others, evident from a spike of signal in the FMRI when humans were exposed to Intention stimuli in the experiment.

Other experiments have shown that in pigtailed macaques, Macaca nemestrina, mirror neurons are also found in the inferior frontal gyrus (the F5 region). This region responded when the macaques make an active movements and also when they observe an experimenter making meaningful movements. (di Pellegrino et al., 1992; Gallese et al., 1996; Rizzolatti & Craighero, 2004; Hickok, 2009).

In a study by Platek et al. (2005), the authors found that the posterior cingulate and precuneus were activated during contagious yawning. These two regions are associated with the theory of mind and empathy. In another study from the same year, Schürmann et al. (2005) found that the superior temporal sulcus was the area that gets activated during contagious yawning. The superior temporal sulcus region is involved in the perception of eye gaze of others and are crucial in determining where others’ emotion are being directed through eye gaze (Campbell et al., 1990). Thus, neuroimaging results from Platek et al. (2005) and Schürmann et al. (2005) contradict each other in isolating the region of the brain that is activated during contagious yawning.

Two studies on contagious yawning from human to domestic dogs were published by Joly-Mascheroni et al. (2008) and Harr et al. (2008) in the same year. Joly-Mascheroni et al. (2008) were the first to demonstrate that human yawns are contagious to domestic dogs and that human yawns would elicit a yawning response from a non-primate species (domestic dog). In this ingenious experiment, Joly-Mascheroni et al. (2008) had 29 domestic dogs observed human yawning and making control mouth movements (not yawns). Out of the 29 domestic dogs, 21 of them yawned after observing a human yawning but none when exposed to control mouth movements (the control in the study). The experiment yielded impressive result, where 72% of the domestic dogs yawned when exposed to a human yawning. This is a higher rate than contagious yawning between humans (45% – 60%) (Provine, 1986; Platek et al., 2003) and from human to chimpanzee (33%) (Anderson et al., 2004). Joly-Mascheroni et al. (2008) posit from this experiment that domestic dogs possess a rudimentary empathic capability and that it helps in moderating human-dog interaction and communication.

A later study by Harr et al. (2008) in the same year also investigated whether human yawns are contagious to domestic dogs but used a different method than that of Joly-Mascheroni et al. (2008). Harr et al. (2008) used 15 domestic dogs in their experiment; the domestic dogs were shown video clips of humans and domestic dogs displaying yawns and open mouth expressions (not yawns) to determine whether these two social stimuli would elicit yawning in these domestic dogs. Their results show that the domestic dogs yawned on both stimuli (yawn and open mouth expressions) with no significant difference as determined by paired t test. Citing methodological difference than that of Joly-Mascheroni et al. (2008), Harr et al. (2008) posit that their results were due to using video clips instead of using live human models. They also conclude that it is possible that domestic dogs, like humans, attended differently to video stimuli than that of a live model.

Järveläinen et al. (2001) showed that in humans, there is a stronger reactivity time in the mirror neuron system when viewing live motor act than that of an artificially presented act. It is possible that domestic dogs also pay less attention to an artificially presented act than that of a live motor act. Understanding the umwelt of domestic dogs is important when using them as experimental subjects and to answer species-specific questions. Domestic dogs are excellent at reading human communicative and visual cues (Joly-Mascheroni et al., 2008) but maybe only so on live model and not video clips as evident from Harr et al. (2008) experiment. Thus, experiment on contagious yawning from human to domestic dogs should considering using only live models and not video clips.

P/S - Sorry if I made you yawn ;)

References

Anderson, J. R., Myowa-Yamakoshi, M., & Matsuzawa, T. (2004). Contagious yawning in chimpanzees. Proc. R. Soc. B, 271(Suppl. 6), S468–S470.

Baenninger, R. (1987). Some comparative aspects of yawning in Betta splendens, Homo sapiens, Panthera leo, and Papio sphinx. J. Comp. Psychol. 101, 349–354.

Campbell, R., Heywood, C.A., Cowey, A., Regard, M., & Landis, T. (1990). Sensitivity to eye gaze in prosopagnosic patients and monkeys with superior temporal sulcus ablation. Neuropsychologia, 28(11), 1123-1142.

Daquin, G., Micallef, J. & Blin, O. (2001). Yawning. Sleep Med. Rev. 5, 299–312.

Deputte, B. L. (1994) Ethological study of yawning in primates. 1. Quantitative analysis and study of causation in 2 species of Old World monkeys (Cercocebus albigena and Macaca fascicularis). Ethology, 98, 221–245.

di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., & Rizzolatti, G. (1992). Understanding motor events: A neurophysiological study. Experimental Brain Research, 91, 176–180.

Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain, 119, 593–609.

Gallese, V., Keysers, C., & Rizzolati, G. (2004). A unifying view of the basis of social cognition. Cognitive Sciences, 8(9), 396-403.

Gallup, A. C., Miller, M. L. & Clark, A. B. (2009). Yawning and thermoregulation in budgerigars, Melopsittacus undulates. Animal Behaviour, 77, 109e113.

Harr, A.L., Gilbert, V.R. & Phillips, K.A. (2008). Do dogs (Canis familiaris) show contagious yawning? Animal Cognition, 12, 833-837.

Hickok, G. (2008). Eight Problems for the Mirror Neuron Theory of Action Understanding in Monkeys and Humans. Journal of Cognitive Neuroscience, 27(7), 1229-1243.

Iacoboni, M., Molnar-Szakacs, I., Gallese, V., Buccino, G., Mazziotta, J.C., & Rizzolatti, G. (2005). Grasping the Intentions of Others with One's Own Mirror Neuron System. PLoS Biology, 3(3), e79. doi:10.1371/journal.pbio.0030079.

Järveläinen, J., Schürmann, M., Avikainen, S., & Hari, R. (2001). Stronger reactivity of the human primary motor cortex during observation of live rather than video motor acts. Neuroreport, 12, 3493-3495.

Joly-Mascheroni R.M., Senju, A., & Shepherd, A.J. et al. (2008). Dogs Catch Human Yawns. Biology Letters, 4, 446-448.

Norscia, I. & Palagi, E. (2011). Yawn Contagion and Empathy in Homo sapiens. PLOS One, 6(12): e28472. doi:10.1371/journal.pone.0028472.

Paukner, A. & Anderson, J. R. (2006). Video-induced yawning in stumptail macaques (Macaca arctoides). Biology Letters 2, 36–38.

Platek, M.S., Critton, S.R., Myers, T.E. & Gallup, G.G. (2003). Contagious yawning: the role of self-awareness and mental state Attribution. Cognitive Brain Research 17, 223–227.

Platek, S.M., Mohamed, F.B., & Gallup, G.G. (2005). Contagious yawning and the brain. Brain Res Cogn Brain Res, 23, 448–452.

Preston, S. D. & de Waal, F. B. (2002). Empathy: Its ultimate and proximate bases. Behav. Brain Sci. 25, 1–20.

Provine, R.R. (1986). Yawning as a Stereotyped Action Pattern and Releasing Stimulus. Ethology, 72(2), 109-122.

Rizzolatti, G., & Craighero, L. (2004). The Mirror-Neuron System. Annu. Rev. Neurosci, 27, 169 92.

Schürmann, M., Hesse, M.D., Stephan, K.E., Saarela, M., Zilles, K., Hari, R., & Fink, G.R. (2005). Yearning to yawn: the neural basis of contagious yawning. Neuroimage, 24, 1260 1264.

Senju, A., Maeda, M., Kikuchi, Y., Hasegawa, T., Tojo, Y. & Osanai, H. (2007). Absence of contagious yawning in children with autism spectrum disorder. Biology Letters 3, 706 708.

Handedness in Humans and Geladas

I thought I’d share a paper I wrote from last semester’s Comparative Psychology class on handedness in humans and geladas. Debating if I should actually follow through with this preliminary report and do some data collection. There is a YouTube video that accompanies this paper, which will appear on the bottom of the page.

Handedness can be defined as the unequal distribution of fine motor skills between the left and right hands. Simply put, handedness is the preference to use left, right or both hands when performing tasks. Humans are mostly right-handed across cultures. Here, I compare handedness in humans (Homo sapiens) to handedness in geladas (Theropithecus gelada).

Right-handedness is predominant across cultures in humans. About 85% to 90% of humans report themselves as right-handers (10). In studies of great apes, comparative analysis indicates that chimpanzees and bonobos exhibit population-level preference in right-handedness while gorillas and orangutans do not exhibit population-level preference in handedness (10). However, right-handedness seems to be uniquely human as no other primate species has such a clear bias (1, 13 & 14). The objective of this preliminary study is to elucidate whether geladas exhibit preference in handedness.

A male gelada at The Bronx Zoo.

Geladas are Old World Monkeys and can be found in the high plateau of North Central Ethiopia and Eritrea (9 & 2). Geladas are sometimes referred to as “bleeding heart monkeys” due to the presence of a naked, pink patch of skin on the chest of males and females that looks like an hourglass (2). They exhibit sexual dimorphism; males have manes and are slightly larger than females. The maximum lifespan of a gelada is about 19 years in the wild (5) and well over 30 years in captivity (9). Geladas are gramnivores; they are unique among primates because grass is their main food source but is occasionally supplemented by seeds, roots, and bulbs (3).

There are many definitions of handedness. Here, I define handedness as the preference of left, right or either hand when performing tasks. In humans, those who have a preference for using their right hand are right-handed while those that prefer using their left hand are left-handed. Those that prefer to use either hand when performing tasks are ambidextrous.

Approximate location of Broca's area and Wernicke's area. Photo from Wikipedia.

Handedness is due to the lateralization (asymmetry) of the brain hemispheres. Those that are right-handed have a more dominant left hemisphere, while those that are left-handed have a more dominant right hemisphere. In most humans, the left hemisphere of the brain is more dominant. The left brain hemisphere is also involved in language and is where Broca’s area and Wernicke’s area are located. Broca’s area is involved in speech production while Wernicke’s area is involved in language comprehension.

Right-handed preference is deep-seated in hominid evolution. Analysis of stone tools from Lower Pleistocene sites in Koobi Fora, Kenya and Middle Pleistocene sites in Ambrona, Spain showed that there is a consistent pattern of tools being produced by right-handed Homo habilis and Homo erectus (15). Preference for right-handedness may have existed as early as 1.4 to 1.9 million years ago, and might hint that the hominid brain had lateralized and was well on its way to becoming more specialized for different functions (15). Analysis of scratch patterns in incisors and canines from archaic humans (Sima de los Huesos in Atapuerca, Spain) and European Neandertals (Sima de los Huesos in Atapuerca, Spain and Vindija, Croatia) also showed that there was a persistent pattern of right handedness (6 & 7).

The prevalence of right-handedness in humans has a linear correlation with left hemisphere dominance (12). Since the left brain hemisphere plays an important role in language, brain lateralization leads to right-handedness. Thus, the prevalence of right-handedness in humans is a byproduct of human language.

The left-handed Ned Flanders from The Simpsons. Photo from SF Weekly.

The subjects for this study are from a captive population of geladas at The Bronx Zoo (Wildlife Conservation Society). There were 7 individuals present during the observations and all were male. Observations were done on two separate days between 12 P.M. and 3 P.M. The geladas were recorded using a video camera, and the recordings were later analyzed.

Geladas spend a significant amount of their time foraging (8). Site studies show that geladas spend 35.7% to 81.6% of their time foraging (8). There is a positive correlation between altitude and time spent foraging; more energy is burnt at higher altitudes, therefore more time is spent foraging (11).

A male gelada foraging with both hands.

My observations showed that geladas use either hand while foraging. They use either their left or right hands to pick up bunches of grass to eat. As my observation progressed, I became concerned that their repetitive motion of picking up grass and putting it in their mouths was not a sufficiently varied behavior to indicate handedness. Therefore, I also observed the geladas grooming.

A female gelada grooming herself.

There are two types of grooming in geladas: autogrooming (self grooming) and allogrooming (social grooming). Grooming is not only important for hygienic reasons but also important for strengthening social bonds (4). A study by Dunbar suggests that the major reason for grooming is the satisfaction of physical contact between the groomer and the individual being groomed (4).

From my observations, allogrooming starts with the individual being groomed initiating eye contact with the groomer. Then, the individual lies down and presents the area that needs to be groomed. Sometimes, a groomer simply approaches the individual they want to groom and starts grooming them. My observations showed that there is also no preference for which hand is used by geladas during grooming. The geladas used either hand for both autogrooming and allogrooming. The decision to use their left or right hand seemed to be determined by the area of the body that needed grooming.

From my observations, it seems that the geladas use either hand for foraging and grooming. The geladas at The Bronx Zoo seem to exhibit ambidexterity because they have no preference for their left or right hand, unlike humans who are predominantly right-handed.

Handedness is correlated with brain hemisphere dominance. For most humans, the left brain hemisphere is dominant and is also involved in language. Thus, the prevalence of right-handedness is a byproduct of human language. None of the geladas I observed at The Bronx Zoo exhibited preference for handedness. This is probably due to the fact that geladas do not have language; therefore, their left brain hemisphere is not dominant and does not lead to right-handedness. Besides foraging and grooming, more behavioral repertoire should be used in future analysis to further elucidate the preference in gelada handedness.









 References

 1. Cashmore, L., Uomini, N., & Chapelain, A. (2008). The evolution of handedness in humans and great apes. Journal of Anthropological Sciences, 86, 7-35.

 2. Dunbar, R.I.M., &; Dunbar, P. (1975). Contributions to Primatology: Social Dynamics of Gelada Baboons (Vol. 6). Basel, Switzerland: S. Karger AG.

 3. Dunbar, R.I.M. (1984). Reproductive Decisions. Princeton, New Jersey: Princeton University Press.

 4. Dunbar, R.I.M. (2008). The social role of touch in humans and primates: Behavioural function and neurobiological mechanisms. Neuroscience and Biobehavioral Reviews, 34(2), 260-268.

 5. Falk, D. (2000). Primate Diversity. New York and London: W.W. Norton & Company.

 6. Frayer, W.D., Fiore, I., Lalueza-Fox, C., Radovčić J., & Bondioli, L. (2010). Right handed Neandertals: Vindija and beyond. Journal of Anthropological Sciences, 88, 113-127.

 7. Frayer, W.D., Lozano, M., de Castro, J.M.B., Carbonell, E., Arsuaga, J.L., Radovčić J., Fiore, I., & Bondioli, L. (2011). Laterality: Asymmetries of Body, Brain and Cognition, doi:10.1080/1357650X.2010.529451

 8. Gron, KJ. (2008, September 3). Primate Factsheets: Gelada baboon (Theropithecus gelada) Taxonomy, Morphology, & Ecology. Retrieved May 11, 2011, from www.pin.primate.wisc.edu/factsheets/entry/gelada_baboon

 9. Hiller, C. (2000). "Theropithecus gelada" (On-line), Animal Diversity Web. Retrieved May 11, 2011, from www.animaldiversity.ummz.umich.edu/site/accounts/information/Theropithecus_ gelada.html

10. Hopkins, W.D. (2006). Comparative and Familial Analysis of Handedness in Great Apes. Psychology Bulletin, 132(4), 538–559.

 11. Iwamoto, T., & Dunbar, R.I.M. (1983). Thermoregulation, Habitat Quality and The Behavioural Ecology of Gelada Baboons. Journal of Animal Ecology, 52, 257-366.

12. Knecht, S., Dräger, B., Deppe, M., Bobe, L., Lohmann, H., Flöel, A., Ringelstein, E.-B., & Henningsen, H. (2000). Handedness and hemispheric language dominance in healthy humans. Brain, 123 (12), 2512-2518

13. McGrew, W.C., & Marchant, L.F. (1997). On the other hand: Current issues in and meta-analysis of the behavioral laterality of hand function in nonhuman primates. American Journal of Physical Anthropology, 104(25), 201-232.

 14. Steele, J. & Uomini, N. (2009). Can the Archaeology of Manual Specialization Tell Us Anything About Language Evolution? A Survey of the State of Play. Cambridge Archaeological Journal, 19, 97-110.

15. Toth, N. (1985). Archaeological Evidence for Preferential Right-Handedness in The Lower And Middle Pleistocene, and Its Possible Implications. Journal of Human Evolution, 14(6,) 607-614.

Rise of the Planet of the Apes

This trailer makes me wish it's August already! If you don't know what it is, it's the prequel to Planet of the Apes. The movie adaptation was first made in 1968 with a remake in 2001. I expect to not see mistakes that were made in previous Planet of the Apes movies, among some of them, non-human apes were portrayed walking upright with a human gait. All the non-human apes in this movie will be CGI so I expect the designers to have done their homework. Though one seem to wonder, did these non-human apes (from the movie) evolved a bipedal gait just like those of human? What do you think?

Are you as excited as I am about this movie? I am interested to see how this movie portray the ethnics and "consequences" of primate testing in labs. I think I might Netflix the previous movies before I watch this one in August.

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

These primates are busy!

I realized I have not updated my blog for almost a month now, so first and foremost, apologies to my avid readers. I know I have left you high and dry without any post! Since my last post, I have started volunteering at Prospect Park Zoo. The zoo has a special place in my heart (especially the hamadryas baboons) because it is there that I did my research for my Honors Thesis. I never thought I would enjoy working with kids but they DO ask the darndest things. Of all the kids that had asked me questions or talked to me, one really stood out. The kid asked if I know who Steve Irwin is and that he (the kid) enjoys his (Irwin's) work. Can you believe it? The kid even recited how primates are different than other mammals. I think he's gonna grow up to be me. I'm cereal.

Have you seen the new ASP website? It's quite spiffy. I actually contributed some photos to the site ... can you spot them?

The annual Monkey Day is fast approaching. Celebrated annually on December 14th, Monkey Day not only celebrates the simian that lend its name to the festival, it also celebrates anything primate (prosimians, monkeys and apes). Over at Serious Monkey Business, Ashlee is starting a Monkey Day Blog Carnival. If you are interested in contributing to the carnival, please contact her.

A friend of mine started a new blog, The Primate Chronicles. Kayley is a graduate student at University of Calgary and does her fieldwork in Belize. Check it out.

Call for submissions: The next edition of Four Stone Hearth will be hosted by Archive Fire on December 8th. If you have wrote or saw interesting Anthropology posts around the web, please send it to ambientdisorder at gmail dot com. Afarensis, current host of the blog carnival, needs hosts for future editions. If you are interested, please email Afarensis, afarensis1 at sbcglobal dot net.

All over the blogosphere and Twitter-land, Anthropological primates are choosing sides. Are you "Team Jacob" or "Team Edward"? Errr .... I mean, are you "for" or "against" removing the word "science" from  American Anthropological Association (AAA)'s mission statement. The controversy with removing the word "science" from mission statement even reached CNN. Some of the interesting blog posts on this subject matter includes:

• Why anthropology is ‘true’ even if it is not ‘science’ and Ethnography as a solution to #AAAfail by Savage Minds.
• Anthropology, Science, and Public Understanding by Neuroanthropology.
• What is a generous interpretation of the AAA mission statement change? by Context and Variation.
• Removing science from anthropology: Parallels with medicine by Respectful Insolence.
• No Science, Please. We're Anthropologists by Psychology Today.
• American Anthropological Association's Long-Range Plan, a rebuttal to the brouhaha.

What's your stand? I don't really have a strong reaction to this, probably because I am not an AAA member. I understand the initial shock of disbelieve or just a general WTF to the decision. But seriously, are they just fishing for publicity? Those damn non-science Anthropologist!

Last but not least, to my Jewish readers, Happy Hanukkah. Chag Sameach!

Wordless Wednesday

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.

Ape behavior inside the exhibit and holding area

An insightful paper published by Ross et al. (2010), compares zoo-living ape behavior inside their holding and exhibit areas in Lincoln Park Zoo, an accredited member of Association for Zoos and Aquarium (AZA). Zoo animals usually have at least two areas where they are housed (excluding some aquatic animals): the holding area and the exhibit area. During visiting hours and at night, zoo animals are housed in their exhibit area. In the morning, before the zoo opens, they move into the holding area to receive husbandry care and their morning food ration.

The gorilla exhibit area in Lincoln Park Zoo. Photo from Things You Should Do.

One of the chimpanzee from the study, Kipper (now deceased), from Lincoln Park Zoo interacting with a child. Photo by Chicago Tribute.

Holding and exhibit areas differ in size, design and functionality. A study by Ross and Lukas on 11 AZA-accredited zoos shows that holding areas are usually about 40 times smaller than exhibit areas (Ross et al., 2010). At the Lincoln Park Zoo, the holding area is about 9.3% of the size of the exhibit area (for both gorillas and chimpanzees). Whereas the exhibit area is designed for the complexity and to mimic the natural environment of its animal inhabitant, the holding area is usually designed for simplicity and functionality to meet husbandry needs.

Seven gorillas (2 males, 5 females; N = 7) and seven chimpanzees (3 males, 4 females; N = 7) were observed in this study. I should point out that the authors of the study is by no means criticizing Lincoln Park Zoo. It is an informal observation of behavioral changes for these animals in different environment. The result of the study shows that:

Gorillas
Inside the holding area - Increased locomotion and affiliative behavior. Also showed increased rates of aggression, self-directed behavior (subject touches, manipulates or examines the body, skin, or hair) and solitary play. Were in close proximity with each other.

Inside the exhibit area - Increased feeding and foraging behavior and also sexual behavior.

Chimpanzees
Inside the holding area - Increased aggression. Increased rate of scratching and self directed behavior (subject touches, manipulates or examines the body, skin, or hair). Were in close proximity with each other.

Inside the exhibit area - Increased feeding and foraging behavior.

Schematic representation of a typical holding area suite for an individual chimpanzee or gorilla social group at the Regenstein Center for African Apes. Shaded areas indicate animal enclosures; noncolored areas are sections of human activity (caretakers and data collectors). (Ross et al., 2010)

Both gorillas and chimpanzees showed increased aggression accompanied with self directed behavior when inside holding area. Increase in aggression can sometimes be attributed to overcrowding and self directed behavior generally means that an animal is nervous. Being constrained in a smaller space increases the chance of mixed-sex and mixed-dominance encounters thus resulting in agonistic and submissive observations. When inside exhibit areas, both apes exhibited an increase in feeding and foraging behavior. This presumably is due to their feeding and foraging habit in the exhibit area. If I remember correctly, one of the major breakthrough in exhibiting apes (and most animals) is to encourage foraging behavior throughout the day. It is no surprise that these apes exhibit these behaviors.

Chimpanzee subjects in a single enclosure in a holding area suite, during a period of free access (following training and research protocols). Photograph was taken from the central caretaker area. (Ross et al., 2010)

These apes reacted differently when inside their holding area than in their exhibit area because they are exposed to different sensory. Apart from the difference in size and complexity, these two areas also differ in the degree of human interaction, cross-species presence, environmental factors and time spent between these two areas. An understanding of these differences and motivational factors is important in promoting optimized environments for captive apes. The authors encourage that zoos would consider species-specific functional, physical and social preferences when designing enclosures for apes regardless of frequency of use.

Reference:
Ross, S. Wagner, K. Schapiro, S. Hau, J. 2010. Ape behavior in two alternating environments: comparing exhibit and short-term holding areas. American Journal of Primatology 72: 951–959. doi: 10.1002/ajp.20857

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?

Wordless Wednesday

Life Is Good: Baby Gorilla Relaxing In Human-Like Pose

Yewande relaxing in human-like pose. Photo from Telegraph.

This photo was taken at Calgary Zoo, Canada by zoo visitor Nancy Chow. The baby lowland gorilla, a six month old female name Yewande, decided to "chillax" after playing with her favorite pink blanket. Struck by Yewande's pose, Chow took this picture. "When I took this shot I love it right away because the baby gorilla was so adorable, Yewande looks so human-like. It is easy to see how closely we are related to these great apes, Yewande's pose could be any one of us taking a well-earned break. Except I don't think I could do that with my feet", said Chow. Read more on Telegraph: Baby gorilla pictured 'relaxing' in human-like pose.

What a great photo. Thanks to my friend Kambiz for pointing it out that it's blog-worthy. This photo also reminds me of what Dr. Frans de Waal said, "Contrary to general belief, humans imitate apes more than the reverse". So, is this baby gorilla relaxing in human-like pose or are humans relaxing in ape-like pose?

First Molars And Life History In Living African And Asian Apes

Another interesting paper on teeth, specifically the eruption of the first molar (M1), by Jay Kelley and Gary Schwartz from The Institute of Human Origins, Arizona State University (ASU) Since the emergence of M1 correlates with many life history attributes in extant primates, data from this paper can be used to compare the life history among extant primates and also extinct apes and hominins.

"Knowing the age when the first molar appears in the mouths of most primates allows researchers to predict a host of life history attributes, such as gestation length, age at sexual maturity, birth spacing and overall lifespan," said Schwartz. "Humans are unique among primates because our life histories are so slow and thus our molars emerge relatively late. Given that apes are our closest living relatives, understanding the broader context of when the characteristic slower development of humans evolved is of great interest."

"Like annual growth rings inside trees, the cells that produce teeth (both the enamel and underlying dentine) leave behind a trace of their presence, not as annual markers, but as growth lines that appear every day," said Kelley. By slicing the teeth in half, he and Schwartz were able to examine these incremental growth lines in ape individuals that died as their first molars were just erupting into their mouths. "Because teeth preserve this phenomenal internal chronometer, we were able to count up how many days it took the first molars to form," said Schwartz. "In apes and monkeys, first molars start forming very close to the time of birth. As the first molars were still erupting in our specimens, development was incomplete and the final growth line was laid down on the day those animals died. Therefore, by counting backwards from the final growth line to the day of birth, we determined their age at death and thus the age at which that molar was erupting." Using this novel approach, the two scientists were able to mark the age of the gorilla's first molar emergence at 3.8 years, nearly identical to that of a wild chimpanzee's. The orangutan's age at first molar emergence was surprisingly much later, at 4.6 years, which falls closer to the age of approximately 6 years in modern humans.

Read the article, Molars provide insight into evolution of apes, humans by ASU and Dental development and life history in living African and Asian apes from PNAS.

Global Warming Threatens Folivory Primates

Black and white colobus monkey, one of the folivory species threaten by global warming.

A paper by Korstjens et al. (2009) suggests that even an annual temperature rise of 2°C would threaten folivory primates because these species would be forced to spend more time resting than foraging for food. This paper, Resting time as an ecological constraint on primate biogeography, was published online on Animal Behaviour. Here's the abstract:

Time constraints can limit an animal's potential to survive in a given habitat and the maximum size of its group. Many studies have, therefore, investigated the ecological correlates of time allocated to travelling, foraging and vigilance. However, animals spend more time inactive than active, and understanding the determinants of this resting time may provide new insights into the habitat-specific time-budgeting problems that animals face. We analysed the environmental constraints that determine the minimum amount of daytime an average primate has to spend resting, using data from a wide range of ecologically different species. However, total resting time consists of two components: enforced resting time (imposed on the animal by ecological constraints) and free resting time (the time available for allocation to ecologically functional activities). We show that the ecologically important enforced resting time is determined by diet and annual temperature as well as by temperature variation. Our tests of the biological significance of this relationship show that enforced resting time distinguishes between locations that are suitable or unsuitable for particular genera. We show that an annual temperature increase of 2–4 °C would greatly increase enforced resting time, leading to serious time-budgeting problems for many species. The effect of changes to enforced resting time on the biogeographical distribution of species is especially strong for folivorous primates. This study shows that resting time is an important component of animal behaviour that can help us understand extinction risk and geographical distribution of taxa.

Read more about this paper on PhysOrg.com, African leaf-eating monkeys are 'likely to be wiped out' by climate change.

Meat May Be The Reason Why Humans Live Longer Than Apes

 Meat, that's what for dinner.

Ever wonder why humans outlive apes? The answer might be because we eat a lot of meat. Genes evolved in humans to adjust to a meat-rich diet helps fight diseases associated with aging such as cancer, heart disease and dementia. Not to mention, the expansion of brain size in the genus Homo is also attributed to an increase in meat diet. Check out the MSNBC article "Meat may be the reason humans outlive apes" and the paper "Evolution of the human lifespan and diseases of aging: Roles of infection, inflammation, and nutrition" by Caleb Finch on PNAS.

Can I See Your Fingers Please?

That is what University of Liverpool's Emma Nelson probably would have said if she were to meet our hominan ancestors in person. Known to hold true in anthropoids (humans, apes and monkeys), the index (second digit) to ring (fourth digit) fingers ratio or 2D:4D is an indication of how much an individual were exposed to androgen (such as testosterone) in the womb. The more androgen you are exposed to, the longer the ring fingers are (and the shorter the index fingers are compared to the index fingers).

Photo of a human's left hand. From left to right: thumb, index, middle, ring and little finger. Photo modified from Wikipedia.

Nelson et al. believe that a high ratio (longer index finger, shorter ring finger) suggests monogamy (or pair-bonded) while a low ratio (shorter index finger, longer ring finger) suggests polygamy (or non pair-bonded). Simply put, individuals with high androgen level is likely to be non pair-bonded and the telltale sign is in the index and ring fingers. Also, some controversial studies had suggested that both men and women who receive high levels of androgen in the womb are more likely to be stronger, faster, and more sexually competitive.

Nelson and her researchers recently looked at the fossils of two Neandertals and one Australopithecus afarensis with complete index and ring fingers to determine their 2D:4D. They found that Neandertals had long ring fingers, suggesting that they were polygamous just like modern day primates that live in groups. A. afarensis on the other hand, had long index fingers. Nelson is puzzled by this discovery. "These were small creatures that probably lived in groups and were being eaten by predators. How do you keep from mating with different members of the group?", she said.

Indeed it does not make sense for A. afarensis to be monogamous if they live in groups. Notice that Nelson et al. only used one A. afarensis fossil to get the 2D:4D. Perhaps it is not their fault that only one A. afarensis specimen had complete index and ring fingers but such are the dilemma of using fossil specimens to generalize a whole species.The result might just be a statistical outlier. However, I can't speculate the result or the implications but anyone that are familiar with statistical data knows that a small sample size leads to a higher sampling error. Also what would a 2D:4D = 1 (same index and ring finger length) be?

Interesting enough, John Hawks at John Hawk's Weblog mentioned the correlation of 2D:4D with male homosexuality (Robinson and Manning, 2000). I would know about this. In fact, my 2D:4D is indeed low.  Robinson and Manning predicted right! Maybe ...

I do find both Nelson et al. and Robinson and Manning (2000) research interesting but I would like to stress that the results are mere predictors and correlations. Take it with a grain of salt. Don't go measuring 2D:4D of your future spouse, boyfriend or girlfriend and accuse them of not being monogamous or a homosexual.

Emma Nelson and her team presented their research at this year's Society for Vertebrate Paleontology meeting held in Bristol, United Kingdom. Read more about Emma Nelson's research.

References:

Reilly M. 2009. Human Ancestors Conflicted on Monogamy. Discovery News. Retrieved September 25, 2009, from http://dsc.discovery.com/news/2009/09/24/human-monogamy.html

Robinson SJ. Manning JT. 2000. The ratio of 2nd to 4th digit length and male homosexuality. Evolution and Human Behavior 21(5): 333-345. [doi:10.1016/S1090-5138(00)00052-0]

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?"