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.

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.

Cheek Pouches: Cercopithecines' Arsenal for Global Domination

Cheek pouches are bilateral sacs on the lower cheek wall where food moves between the oral cavity and pouches through a slit-like opening (Lambert & Whitham, 2001). Most of us are familiar with cheek pouches in rodents, such as chipmunks, squirrels and hamsters. The cheek pouch is also one of the most important and distinguishing physical characteristics of the cercopithecines.

The cheek pouches of a White-tailed Antelope Squirrel. Most of us are much more familiar with cheek pouches in rodents than in cercopithecines. Photo on Flickr by J.N. Stuart.

A subfamily of the Old World Monkeys, cercopithecines range from Asia to sub-Saharan Africa and as far north as Gibraltar. Baboons, mandrills and macaques are examples of cercopithecines. According to fossil records, cercopithecines and colobines split between 12.5 and 10 million years ago. This suggests that the cheek pouch probably evolved at least 10 million years ago (Lambert & Whitham, 2001). The cheek pouch is present in all members of the cercopithecines but not in the colobines. While the exact adaptive function of the cheek pouch is unknown, numerous behavioral studies have been done on different cercopithecines to understand what the cheek pouch is selected for.

A rhesus macaque storing its food inside its cheek pouches. Photo from Garlyn Zoo.

Reducing Intraspecific and Interspecies Competition: 
A study with red-tail monkeys (Cercopithecus ascanius) and grey-cheeked mangabeys (Lophocebus albigena) in the Kibale National Park, Uganda showed that they were significantly more likely to use their cheek pouches in the presence of their conspecific (the same species) (Lambert, 1998). A subsequent study by Lambert (2005) with red-tail monkeys and grey-cheeked mangabeys also shows that both species were more likely to use their cheek pouches in the presence of greater numbers of conspecific.

A study of blue monkeys (Cercopithecus mitis stuhlmanni) by Smith et al. (2008) in the Kakamega Forest, Kenya shows that individuals are more likely to use their cheek pouch when their nearest neighbor is higher ranking than them.

Lambert & Whitham (2001) observed a group of captive yellow baboons (Papio cynocephalus) at a zoo and found that cheek pouches are mostly used when there are intense competition with their conspecific during main feeding time. Higher ranking individuals are less likely to use their cheek pouches compared to lower ranking individuals. The authors posit that the cheek pouches is an anatomical solution to maximizing energetic input while mitigating competitive intraspecies and interspecies competition.

Red-tail monkeys, like the one above, are more likely to use their cheek pouches in the presence of their conspecific and more so when the number increases.

Predator Risk and Avoidance: 
Lambert's (2005) study also shows that both red-tail monkeys and grey-cheeked mangabeys retreated to the safety of dense vegetation to process foods that were stored inside their cheek pouches. Lambert posits that this is a predator avoidance strategy.

A study of polyspecific association between Campbell’s monkey (Cercopithecus campbelli), spot-nosed monkey (Cercopithecus petaurista), and Diana monkey (Cercopithecus diana) from Taï Forest, Côte d’Ivoire shows that cheek pouches might be used to mitigate interspecific competition (Buzzard, 2006). Diana monkeys are the most frugivorous (ate fruits) while spot-nosed monkeys are the least frugivorous. Campbell's monkeys are more frugivorous than spot-nosed monkeys but less frugivorous than Diana monkeys. By comparing the cheek pouch distension of all 3 species, Buzzard found that Campbell's monkeys have the most cheek pouch distension overall, but had more distended cheek pouch when not near the highly vigilant Diana monkeys. Buzzard posits that the cheek pouch of Campbell's monkeys were the most distended as a response to predator risk and avoidance. Without the warning calls of the highly vigilant Diana monkeys, Campbell's monkeys stuffed their cheek pouch with food and retreated to a safer environment before they process their food.

Smith et al. (2008) posits that blue monkeys were less vulnerable when emptying their cheek pouch than filling them, therefore supporting the hypothesis that cheek pouch is selected for predator avoidance and reducing exposure to aerial predation. These blue monkeys (and most arboreal primates) retrieve to an area with high-density foliage and closer to the trunk of the tree to reduce exposure to predators.

Blue monkeys are less vulnerable when processing food in high-density foliage.

Storing Food, Resource Distribution:
Lambert's (1998) study also showed that red-tail monkeys and grey-cheeked mangabeys were significantly more likely to use their cheek pouches when feeding in clumped and high-quality resources (such as fruits).

Lambert & Whitham (2001) posit that the cheek pouches is an anatomical solution to maximizing energetic input while mitigating competition over limited food resources.

Smith et al. (2008) posit that cheek pouches use could also reflect the differences in the distribution of food resources (such as leaf feeding sites). Cheek pouches can be used to maximize foraging on extremely competitive resources.

An olive baboon feeding on the fruit of a Sausage Tree (Kigelia) in Manyara, Tanzania. Notice that she is stuffing her cheek pouches with the fruit. Photo on Flickr by Kibuyu.

Overall, cheek pouches in cercopithecines are used for more than one function and most probably varied between different species. Whether it is for interspecies/intraspecies competition, predator risk and avoidance or resource distribution, cheek pouches provide an added advantage for survival and are probably the reason why they were selected.

References:
Buzzard, P. 2006. Rank and age related feeding strategy observed through field experiments in the Koshima group of Japanese macaques. Primates 47(4): 336-341. DOI: 10.1007/s10329-006-0188-6.

Lambert, J.E. 1998. A field investigation into the adaptive function of the cercopithecine cheek pouch. American Journal of Physical Anthropology 25(suppl): 145–146.

Lambert, J.E. 2005. Competition, predation, and the evolutionary significance of the cercopithecine cheek pouch: The case of Cercopithecus and Lophocebus. American Journal of Physical Anthropology 126(2): 183-192. DOI: 10.1002/ajpa.10440.

Lambert, J.E. Whitham, J.C. 2001. Cheek Pouch Use in Papio cynocephalus. Folia Primatologica 72(2): 89-91. DOI: 10.1159/000049928.

Smith, L.W. Link, A. Cords, M. 2008. Cheek Pouch Use, Predation Risk, and Feeding Competition in Blue Monkeys (Cercopithecus mitis stuhlmanni). American Journal of Physical Anthropology 137(3): 334-341. DOI: 10.1002/ajpa.20879.

Meet Kera, the long-tailed macaque

Earlier this week, I was lucky to catch this tweet from Stephen, executive director of Primarily Primate:

@MonkeysAndBirds (cont) Of the 25 macaques, about 10 of them have no names (only lab numbers tattooed across their chest, so we need good monkey names.

I tweeted Stephen and submitted a name. I was lucky that the name was actually picked! Meet #29209. Actually meet Kera. Kera is about 4 years old and judging from the pictures Stephen sent me, it looks like he really likes grapes!

I chose "Kera" because the word kera means monkey in Malay. Me and long-tailed macaques go a long way. Most don't know that it's these macaques that inspired me to be a primatologist when I was just a wee kid. Watching them groom each other peaked my interest in primates.

Anyways, not only did I named him, I actually sponsored him! For a small amount of $10.00 per month, you can sponsor one of these macaques as well. Here's a list of the macaques that now resides at Primarily Primates. Right now, 7 8 out of 25 macaques have been sponsored.

29203  Blondie
28743  Brownie
28764  B.B.
27735  Buzzbee
27756  Theo (Sponsored - Andy Cockrun)
29189  Gabriel
29192  Bojangles (Sponsored - Parker Lewis @FOA_Parker)
29196  Peanut
29212  Tonks (Sponsored - Priscilla Feral)
29177  Peg
29185  Teddy
29191  Don
29211  Shy Guy
29201  Shiva (Sponsored - @VeganinLA)
29202  Neville (Sponsored - Barbara @Gonepie)
29209  Kera (Sponsored - Raymond Ho @PrancingPapio)
29175  Rudy
29198  Lazarou
29199  Blaise (Sponsored)
29173  Edwin
29207  Monchou
29208  Milano
29184  Jupiter
29197  Lee (Sponsored - Lee Hall, @Animal_Law)

If you are interested in sponsoring one of these macaques (and I hope you do!), you can do so at Primarily Primate's website. Stephen told me that you can also email him with any questions at stephentello AT gmail.com.

For more about the macaques and the journey to the sanctuaries, read the article A Journey of 1,700 Miles, From Toxic Tests to Sanctuary. 

Female Rhesus macaques: Grooming, group size, and feeding priority

Michelle from Spider Monkey Tales has an interesting post about her poster: Grooming, group size, and feeding priority in female Rhesus macaques in Cayo Santiago, Puerto Rico. You can check her poster if you happen to be going to the 79th annual AAPA meeting in Albuquerque, New Mexico.

Ethnoprimatology: Human-Macaque Interaction In Sulawesi

Ethnoprimatology is defined as the approach that draws from primate socioecology, ethnoecology/environmental anthropology, and conservation biology. This approach enable us to see the multifaceted interaction between humans and nonhuman primates in a dynamic ecosystem. It seems to be something I would like to do and learn more. What's a better way to incorporate the fundamentals of cultural anthropology and biological anthropology.

An ethnoprimatology paper by Riley and Priston (2010) on the American Journal of Primatology, Macaques in farms and folklore: exploring the human-nonhuman primate interface in Sulawesi, Indonesia (free abstract) explores the complex interaction between macaques and humans through overlapping resource use and cultural perceptions of macaques. If you do not have access to the paper, I can send you a copy of the pdf.

Macaca tonkeana, one of the endemic macaque species of Sulawesi. Photo from Wikipedia.

There are six species of macaques endemic to the island of Sulawesi. Macaca nigra, Macaca nigrescens, Macaca maura, Macaca tonkeana, Macaca hecki and Macaca ochreata. Despite constant crop raiding by macaques, farmers in Sulawesi show considerable tolerance to this behavior. This tolerance can be explained by a positive reinforcement in the farmer's local culture, folklore and religion. Two types of farming subsistence exists in Sulawesi: dryland crops and wet-rice agriculture.

Macaca nigra, one of the endemic macaque species of Sulawesi. Photo from Wikipedia.

Most dryland crops farmers are Muslim. They abstain from killing and/or eating these macaques (which Balinese Hindus would have no problem doing) as it is considered haram. In the Lindu highlands, the macaques are considered kin by the To Lindu people. In Buton, certain places in the forest are considered sacred, thus these places are protected by the locals. Macaques and other animals benefits from this protection, making these pockets of forest their refuge.

Macaques Like To Keep Their Conversations Short

Formosan macaques. Photo from Wikipedia.

Macaques, like humans, seem to prefer conversing in short calls (or using short words) rather than lengthy vocalizations. In humans, we use the words "the", "a" and "of" often and they do not take long to say. The calls used often by macaques (greetings, grunts and coos) are also short.

The relationship between the length of a word and how often we use it can be explained by the "law of brevity", which states that the words we use very often are very short and the words we use very rarely are long, said Dr. Stuart Semple from Roehampton University, UK.

The vocal repertoire of the Formosan macaques (Macaca cyclopsis) conforms to the law of brevity, indicating a commonality in the basic structure of communications in humans and non-human primates. The article by Semple et al. (2010), Efficiency of coding in macaque vocal communication is published on Biology Letters (free pdf)

Read more on BBC News: Monkeys keep chatter 'short and sweet'.

Japanese Macaques Floss Teeth

Earlier this year, I blogged about long-tailed macaques (Macaca fascularis) in Thailand using human hair as dental floss to clean their teeth. This behavior gives us an insight to culture transfer as mothers were observed teaching their infants how to floss repeatedly.

In Kyoto, Japan, a Japanese macaque (Macaca fuscata) name Chonpe was observed flossing her teeth using her own hair. She perfected not one, but three flossing techniques.

Lead author Jean-Baptiste Leca told Discovery News that dental flossing could have been a fortuitous yet "accidental byproduct of grooming." Leca, a post-doctoral fellow at Kyoto University's Primate Research Institute, explained that "Japanese macaques sometimes bite into hair or pull it through their mouths to remove external parasites." The hair might have become stuck in Chonpe's teeth, and as she drew the hairs out, "she may have noticed the presence of food remains attached to them". "The immediate reward of licking the food remains off the hair may have encouraged her to repeat the behavior for the same effect in the future," he added.

Chonpe is a middle ranking female with no children. Her only close kin is her mother and her sibling, therefore diffusion of knowledge is somewhat limited to her only sibling. She was observed flossing her teeth about four years ago and had only recently seen this behavior spread among Chonpe's troop. Chonpe was also observed her rolling small stones in her hand while attempting to remove a spine stuck in her palm, so she might be particular an innovative individual, the researchers added.

Chonpe flossing her teeth. Photo by Jean-Baptiste Lena on Discovery News.

Read about the article from Discovery News, Tidy Monkey Flosses Teeth and The first case of dental flossing by a Japanese macaque (Macaca fuscata): implications for the determinants of behavioral innovation and the constraints on social transmission on the journal Primates.

Grandmothers Taking Care Of Their Granddaughters: Japanese Macaques

Japanese researchers observed two separate cases of grandmothers taking care of their granddaughters. The catch is, these grandmothers are free-ranging Japanese macaques (Macaca fuscata) and the researchers think that this is the first observed behavior in nonhuman primates that would support the "Grandmother Hypothesis". The Grandmother Hypothesis posits that female's post reproductive lifespan is reflected by the reproductive success of her offspring and the survival of her grandchildren.

According to the paper published on Primates, Nakamichi et al  (2009) observed that these grandmothers, without dependent offspring, were observed taking care of their granddaughters and even suckling them. The first case was a 24 year-old grandmother who provided essential care to her 2 month-old granddaughter after her mother temporarily disappeared from the group (the author cited unknown reason for her disappearance). The second case was a 23 year-old grandmother who suckled her 14 month-old granddaughter after her mother gave birth to a younger sibling. In summary, these behavioral data indicate that healthy grandmothers without dependent offspring could contribute to the survival of their grandchildren thus supporting the Grandmother Hypothesis.

The grandmother (GM1) is retrieving her granddaughter (GD1) (a), and GD1 is holding GM1’s nipple in her mouth (b) during the period of the mother’s (M1) temporary disappearance (21 July 2008). GM1 is grooming M1 who is nursing GD1 on the first day when M1 returned to the group (28 July 2008) (c). Photo from Nakamichi et al. (2009)

Read more about the article, Old grandmothers provide essential care to their young granddaughters in a free-ranging group of Japanese monkeys (Macaca fuscata) on Primates. Also, BBC ran a story about this article, Grandmother monkeys care for baby.

"To our knowledge, there have been no reported cases in which, instead of a mother, a grandmother without dependant offspring has continuously provided essential care for the survival of her dependant grandchild, which is in accordance with the grandmother hypothesis," Dr Nakamichi and colleagues write in the journal Primates. BBC Earth News, 2009.

References:

Nakamichi, M. Onishi, K. Yamada, K. 2009. Old grandmothers provide essential care to their young granddaughters in a free-ranging group of Japanese monkeys (Macaca fuscata). Primates Retrieved November 24, 2009, from http://www.springerlink.com/content/a30977860p50wt76/ doi: 10.1007/s10329-009-0177-7.

Walker, M. 2009. Grandmother monkeys care for baby. BBC Earth News Retrieved November 24, 2009, from http://news.bbc.co.uk/earth/hi/earth_news/newsid_8370000/8370743.stm.

Homosexuality: Was Darwin Wrong On Sexual Selection?

The article "The effeminate sheep and other problems with Darwinian sexual selection" by Jonah Lehrer was published in the June/July 2006 issue of SEED magazine. It's been circulating around the internet this past week after news broke that a high school teacher from Piasa, Illinois was suspended for giving his students this article to read as an optional class discussion. Soon, a Facebook group was created by students from Southwestern High School in support of their beloved teacher, Dan DeLong. The author of the article, Jonah Lehrer, also showed his support on his blog The Frontal Cortex. DeLong had since been given his job back after he publicly apologize for handing out an age inappropriate article. This whole outburst just screams homophobia to me. It is a disgrace to the country's education system because a thought provoking and queer-friendly curriculum resulted in someone being suspended. I bet none of the parents would even complain if their kids were given an article explaining the extinction of dinosaurs were due to them being late to Noah's ark.

Dinosaurs, Left Behind. Illustration from CartoonStock.

Anyway, back to the article. Joan Roughgarden, a Biology professor from Stanford University thinks that Darwin got it wrong about sexual selection. She also thinks that sexual theory is still stuck in the 19th century.

 Joan Roughgarden's book Evolution's Rainbow.

Two female bonobos having sex. Bonobos are fully bisexual, they don't really care which gender they are having sex with.

Sexual selection cannot explain homosexuality in over 450 different vertebrate species, said Roughgarden. Homosexuality, long thought to be deviant and serves no purpose biologically, is actually normal and a necessary fact of life.. Her book, Evolution's Rainbow, is an attack on Darwin's theory of sexual selection citing that the pervasiveness of homosexuality in the animal kingdom is actually adaptive and had not been weeded out by natural selection. She also said that homosexuality is a necessary side effect for getting along: a necessary feature of advanced animal communities that require communal bonds to function.

 Gay mallards Anas platyrhynchos. Photo from Wikipedia.

An example of this in the primate societies are the Japanese macaques (Macaca fuscata).

Japanese macaques, an old world primate, illustrate this principle perfectly. Macaque society revolves around females, who form intricate dominance hierarchies within a given group. Males are transient. To help maintain the necessary social networks, female macaques engage in rampant lesbianism. These friendly copulations, which can last up to four days, form the bedrock of macaque society, preventing unnecessary violence and aggression. Females that sleep together will even defend each other from the unwanted advances of male macaques. In fact, behavioral scientist Paul Vasey has found that females will choose to mate with another female, as opposed to a horny male, 92.5% of the time. While this lesbianism probably decreases reproductive success for macaques in the short term, in the long run it is clearly beneficial for the species, since it fosters social stability. “Same-sex sexuality is just another way of maintaining physical intimacy,” Roughgarden says. “It’s like grooming, except we have lots of pleasure neurons in our genitals. When animals exhibit homosexual behavior, they are just using their genitals for a socially significant purpose.”

Read more about Jonah Lehrer's "The effeminate sheep and other problems with Darwinian sexual selection" here.

"And Tango Makes Three". A storybook based on the real story of Silo and Roy, two gay chinstrap penguins from Central Park.

I think homosexuality in primates is an interesting yet often times a taboo topic. There should be more studies on the effect of homosexuality in primate societies. Are there differences and similarities between primate and human societies when it comes to homosexuality? I also think its about time to regard homosexuality as adaptive as opposed to maladaptive and start coming up with research to see how societies benefit from homosexuality. We already have the "Grandmother Hypothesis" so what about the "Gay, Lesbian and Transgender Family Member Hypothesis"?

Actor Rosario Dawson and her gay uncle, Frank. Poster from PFLAG.

What struck a cord for me was Roughgarden's explanation of homosexuality, “Same-sex sexuality is just another way of maintaining physical intimacy ... It’s like grooming, except we have lots of pleasure neurons in our genitals. When animals exhibit homosexual behavior, they are just using their genitals for a socially significant purpose".

Reference:

Lehrer, J. 2006. The effeminate sheep and other problems with Darwinian sexual selection. SEED Retrieved November 3, 2009, from http://seedmagazine.com/content/article/the_gay_animal_kingdom/

Self-Suckling in Barbary Macaques Before and After Infant's Death

Self-suckling is a rare behavior that occurs among Barbary macaques (Macaca sylvanus) and might have been a learned behavior. Dr. Bonaventura Majolo and his PhD. student Richard McFarland noticed this behavior while studying Barbary macaques in the middle-Atlas mountains of Morocco (2009). They published their findings, "Brief communication: Self-suckling in Barbary macaque (Macaca sylvanus) mothers before and after the death of their infant" on American Journal of Physical Anthropology last July.

Dr. Majolo and his student observed eight females with infants from two troops; "Flat face" and "Large". They found that four mothers from "Flat face" troop self-suckle themselves for a brief moment when their infant is still alive, possibly to improve milk flow when the infant change from one nipple to the other. All four of these females lost their infant due to predation or some unknown cause. They then observed these females self-suckling in bouts up to two minutes. Self-suckling was never observed between four females in "Large" troop before and after the death of an infant (only one monkey lost its infant in this troop).

Barbary macaque females from "Flat face" troop. Photo from BBC.

Majolo and McFarland think that self-suckling in Barbary macaque is cultural although they don't know why such behavior exists. It might be a response to make up for the energy they had invested in producing milk, help relieve engorged breasts, to help boost the females' immune system or even an emotional response to losing an infant.

"In humans and other species, breast-feeding reduces the stress through the release of prolactin. It is therefore possible that the self-suckling functions to reduce the stress generated by the loss of the infant ... It is interesting that we observed self-suckling in just one troop and not the other. This may indicate that self-suckling is a sort of cultural behavior. We will have to wait to see if self-suckling is consistently displayed by females in the same troop and not in the others", said Dr. Majolo.

References:

Majolo, B. McFarland, R. 2009. Brief communication: Self-suckling in Barbary macaque (Macaca sylvanus) mothers before and after the death of their infant. American Journal of Physical Anthropology 140(2): 381-383. [10.1002/ajpa.21125]

Walker, M. 2009. Grieving monkeys drink own milk. BBC. Retrieved October 5, 2009, from http://news.bbc.co.uk/earth/hi/earth_news/newsid_8287000/8287774.stm