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.

Touching Death

The following guest post by Eric Michael Johnson is part of the Primate Diaries in Exile blog tour. You can follow other stops on this tour through his RSS feed or follow him on Twitter. If this is your first time visiting The Prancing Papio make sure to browse some of the other posts on the blog. Thanks. - EMJ

I had always been afraid of my grandfather and now I was staring at his pale, lifeless hand inches from my face. But the very same arthritic fingers I had seen him use countless times to push tobacco inside his pipe or the hard candies he loved into his toothless mouth now just looked wrong to me. They were alien and artificial. It was as if a sculptor had taken the man I knew and placed a life-sized replica in his coffin to fool us. I had to touch him. Later I would learn that this impulse wasn’t unique to that curious ten-year-old attending his first funeral.

In fact, no lesser a figure than the famous 17th-century English parliamentarian and diarist Samuel Pepys would be similarly tempted. After attending a public dissection at London’s Barber-Surgeons Hall one evening in 1663 he enticed his host to let him see the body alone, a sailor who had been hanged for robbery. Afterwards, in the flickering candlelight, Pepys wrote in his diary what I might have expressed myself if I’d had the vocabulary. “I did touch the body with my bare hand; it felt cold, but methought it was a very unpleasant sight.”

There is something intensely animal about our relationship with the dead. As an atheist I don’t feel particular reverence or awe at the site of a cadaver. It mostly just creeps me out. But even religious believers, those who should be comfortable with the idea that a dead body retains no trace of the person they once knew, also seem to have trouble letting go of what St. Paul called “confidence in the flesh.” In funerary observances around the world cadavers are regularly touched, kissed, washed, anointed with oils, bedaubed with ceremonial makeup, carted to sacred ground, entombed with their clothes or belongings, and generally treated in death as if their body were going on a different journey than miasmic decay.

However, as is often the case where human universals are concerned, looking to similar behaviors in other animals can be especially instructive. For example, a study that has just been released in the American Journal of Primatology has captured the most complete process to date of what could only be described as mourning behavior in nonhuman primates. Katherine Cronin and colleagues at the Max Planck Institute, Gonzaga University, and the Chimfunshi Wildlife Orphanage Trust in Zambia have documented a case where a chimpanzee mother faced what for most of us would be an unthinkable horror: the death of her child.








Video footage by Cronin et al. 2011.

The infant had been observed behaving sickly ever since birth when, on May 18, 2010, researchers saw the chimpanzee mother, Masya, carrying the dead body of her offspring. Masya continued to carry her lifeless child until the following day when observers were present to record what they saw next. The infant was placed in a clearing while Masya sat a short distance away staring at the motionless form. Researchers recorded over the next hour as the mother approached her offspring 23 times to place her hands on the child. 21 of these contacts were directed toward her offspring’s face or neck. At the end of this display Masya once again picked up her infant and carried her to the center of the social group about 20 meters away. When she laid her infant down the other group members, eight in total, proceeded to gently touch, stroke the dead infants belly, and groom it with straw. After about twenty minutes Masya retrieved the body and walked off. The next day Masya was observed on her own, she had let go of her dead child.

This is not the first time that primates have been observed to pay special attention to a deceased member of their group. In April last year similar behaviors were observed by a chimpanzee mother in Bossou, Guinea who ended up carrying her infant’s body for a total of 27 days. The mother, Jire, regularly groomed and slept next to her infant’s body and showed distress whenever they became separated. In 2000 a chimpanzee mother in the Mahale Mountains of Tanzania carried her infants body for nearly four months and individuals throughout the community were heard making distinctive vocalizations that the researchers had come to associate with fear and agitation. Other cases have been observed in the mountain gorillas of Rwanda, baboons of Ethiopia, macaques in Japan, and ring-tailed lemurs of Madagascar (see the timeline below).

There have also been notable examples of care being taken with the dead in African elephants and bottlenosed dolphins. In the case of the elephants, an ailing matriarch was observed to receive support from unrelated members of her group, behaviors that couldn’t be explained by either Hamilton’s theory of kin selection nor Trivers theory of reciprocal altruism. This concern with her body continued after death. Further study looked at how the group interacted with the bones of their former group mates and confirmed that the famous behaviors observed at elephant graveyards are intentional, individuals focused more intently on these remains than to other features of their environment. According to lead author Iain Douglass-Hamilton, these results challenge existing theories on where altruistic behavior ultimately comes from.

“The conclusion must be that elephants are interested in the sick, dying or dead elephants irrespective of genetic relationship,” he said. “There seems to be a generalized response to elephants in distress, rather than help or interest only being restricted to close kin.”

In a similar way to what primatologist Frans de Waal has documented in chimpanzees, the individuals appear to experience empathy with those who are sick or dead. But does this mean that nonhuman animals have a concept of death? According to Katherine Cronin in the case of the chimpanzee Masya the behaviors are certainly suggestive of this.

“These behaviors would supply tactile and visual information about the current state of the body,” she said. The mother was intently observing her infant, her eyes rarely straying from the body as it lay in the sun. Likewise, as she was touching her baby’s face or neck, could note the absence of breath or lack of blood circulation warming her tiny frame. “Conceivably, this information could be remembered the next time she encountered the same set of cues,” Cronin said. In this way, the implications of death could be learned by chimpanzees.

At the Sanaga-Yong Chimpanzee Rescue Center, chimpanzees look on as Dorothy--a beloved female felled in her late 40s by heart failure--is borne to her burial. Image: National Geographic / Monica Szczupider

Our desire to touch the dead, to adorn them in their Sunday best and wish them a final farewell, is the human process of gathering similar information. It is a way to reconcile our deep familiarity with the body of our loved ones with the realization that what they may once have been is no more. I’m not even certain that we have a concept of death beyond what we can tell from directly comparing what is different between the living and the dead. I certainly didn’t as a ten-year-old child shuffling past my grandfather’s coffin. In my desire to touch his cold hand I may have been fulfilling a need that many animals experience when confronted with their own realization of death. Whether it’s a chimpanzee mother carrying her dead infant on her back, or what the New York Times reported of the woman from Plainfield, New Jersey who “talked to her dead infant as though it was alive” as she rode the crowded rail car home, the effect may be to ease our minds towards acceptance. For regardless of where we started in life, we all end up in the same place. Death is the great unifier and as we reach out to touch the dead, we are ultimately connecting with everyone else who is struggling to let go.

Reference:

Katherine A. Cronin, Edwin J.C. van Leeuwen, Innocent Chitalu Mulenga, Mark D. Bodamer (2011). "Behavioral response of a chimpanzee mother toward her dead infant," American Journal of Primatology, Article first published online: January 21, 2011. DOI: 10.1002/ajp.20927

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

"Home for Oliver"

"Home for Oliver" is an inspiring project by Andy Cockrum. Here in his own words:

I want to create a web series about the life of Oliver the chimpanzee and efforts to build him a new living area at a Texas sanctuary. My hope is that the series will document, promote and inspire the building of new habitats for Oliver and other captive chimpanzees and monkeys who are cast-offs from the pet trade, entertainment and biomedical research industries ... Today, Oliver lives at the sanctuary with another chimpanzee named Raisin. While the sanctuary is continuing to create larger grass-bottomed habitats for all of its chimpanzees, in a tough economy, they have not been able to raise funding to build a new, larger, grass habitat for Oliver, who also has special needs due to blindness and advanced age.

I am looking to raise a total of $4600.00, which should allow me to produce two to three webcasts per month for six months. Those webcasts will feature animal stories, expert interviews and the sanctuary's efforts toward building Oliver a new living area. Additionally, I may travel to other U.S. sanctuaries to conduct documentary research into the best type and size of habitat to build, and ways to utilize green building techniques.

Please note: 

My hope is to create this web series as the first step towards the goal of giving Oliver a new and more natural living area. The money I am seeking will go toward producing these webcasts and will not directly support the construction of Oliver’s new home, which could cost between $30,000 and $170,000. Those who would like to directly support the renovations at the sanctuary can do so through their web site, www.primarilyprimates.org.

About my involvement with the sanctuary:

I have volunteered my production and post-production services to the Primarily Primates animal sanctuary for several years now, having filmed, produced and edited over 50 videos for the sanctuary. These can be found in the “videos” section of the sanctuary’s web site at www.primarilyprimates.org.

Thank you!

Andy Cockrum

So, if you can, please help the chap out by backing his project. Click on the banner above for more information (it will redirect you to the project's website where you can donate and watch web series).

Oliver in his earlier days.

Born around 1958 in the Republic of Congo (then Zaire), Oliver was "acquired" at about 2 years old by trainer Frank and Janet Berger. Perhaps the most peculiar behavior exhibited by Oliver was habitually walking upright (instead of walking on his knuckle like most chimpanzees do). However, due to old age and arthritis, Oliver no longer walks upright (he is 52 this year!) and had reverted to walking on his knuckles like his fellow chimps. 

Human and chimpanzee genome. M indicated Mitochondrial DNA. Illustration from Wikipedia.

Some of you might know Oliver as the "humanzee", thought to be an intermediate form of humans and chimpanzees due to Oliver's habitually bipedal gait and supposedly having 47 chromosomes (humans have 46 chromosomes and chimpanzees have 48 chromosomes). A paper by Ely et al. (1998) disproved that Oliver has 47 chromosomes. They found that Oliver, in fact, display 48 chromosomes (as expected of chimpanzees) and displayed a high sequence homology to the Central African variety of chimpanzees (Pan troglodytes troglodytes).


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: 10.1002/(SICI)1096-8644(199803)105:3<395::AID-AJPA8>3.0.CO;2-Q

Happy New Year Y'all. Dolphins Smarter Than Chimps?

Happy New Year to all my readers, humans and non-humans alike (I've caught my cat reading my blog more than twice). Sorry for not posting this few days but I've been sick since New Year. Suffice to say, 2010 didn't really start on a good note for me.

Apparently 2010 did not start on a good note with my fellow primate, the chimpanzees, either. Lori Marino, a zoologist at Emory University in Atlanta, Georgia claim that the second most intelligent creature after humans are dolphins, not chimpanzees as many researchers believed. Diana Reiss, a psychology professor from Hunter College (CUNY) in New York City found that bottlenose dolphins can recognize themselves in front of the mirror and learn rudimentary symbol-based language. Both Marino and Reiss will present their findings at a conference in San Diego, California, next month. These findings have tremendous implications on human-dolphin interactions, specifically the use of dolphins for entertainment in marine parks.

Sad chimpanzee is sad because he is no longer the second smartest after humans.

Read the article Scientists say dolphins should be treated as 'non-human persons' from Times Online. I wonder if both had any papers that will be published soon about this topic. I've only found Marino & Reiss (2001) Mirror self-recognition in the bottlenose dolphin: A case of cognitive convergence and Marino (2002) Convergence of Complex Cognitive Abilities in Cetaceans and Primates. Why is this story being published in 2010, almost 8 years since the papers were published? Something is fishy here (no puns intended because dolphins are in fact mammals, not fish).

Chimps Observed Using Tools To Cut Food Into Smaller Pieces

From BBC News, chimps from the Nimba Mountains of Guinea, Africa were observed using tools to chop up and reduce food into smaller bite-sized pieces.

Kathelijne Koops and William McGrew of the Leverhulme Centre for Human Evolutionary Studies, University of Cambridge (UK) with Tetsuro Matsuzawa from Kyoto University, Inundate (Japan) observed this behavior and published it on Primates. They found that these chimps use tools to process Treculia fruits, a large volley ball-shaped fruit that is hard and fibrous.

Abstract:

Wild chimpanzees (Pan troglodytes) are renowned for their use of tools in activities ranging from foraging to social interactions. Different populations across Africa vary in their tool use repertoires, giving rise to cultural variation. We report a new type of percussive technology in food processing by chimpanzees in the Nimba Mountains, Guinea: Treculia fracturing. Chimpanzees appear to use stone and wooden “cleavers” as tools, as well as stone outcrop “anvils” as substrate to fracture the large and fibrous fruits of Treculia africana, a rare but prized food source. This newly described form of percussive technology is distinctive, as the apparent aim is not to extract an embedded food item, as is the case in nut cracking, baobab smashing, or pestle pounding, but rather to reduce a large food item to manageably sized pieces. Furthermore, these preliminary data provide the first evidence of chimpanzees using two types of percussive technology for the same purpose.

Do chimpanzees (Pan troglodytes) use cleavers and anvils to fracture Treculia africana fruits? Preliminary data on a new form of percussive technology (free abstract).

Wild Chimps Know What Fire Is ... Kinda, Part II (Link to Jill Pruetz's Paper)

The paper by Jill Pruetz and Thomas LaDuke about Fongoli chimps and their conceptualization of fire is out on the American Journal of Physical Anthropology. As promised, here is the link to the paper, Brief communication: Reaction to fire by savanna chimpanzees (Pan troglodytes verus) at Fongoli, Senegal: Conceptualization of "fire behavior" and the case for a chimpanzee model (only free abstract).

Read the previous post, Wild Chimps Know What Fire Is ... Kinda.

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.

Wild Chimps Know What Fire Is ... Kinda.

Jill Pruetz, an ISU associate professor of anthropology, has been studying savanna chimpanzees at her Fongoli research site in Senegal since 2001. Her new study documents how the chimps understand the fire they encounter in the region. Photo by Bob Elbert, ISU News Service.

A new study by Iowa State University anthropologist Jill Pruetz suggests that savanna chimps (Fongoli chimps) in Senegal have a near human understanding of wildfire and would alter their behaviors in anticipation of the wildfire's movement. Along with Thomas LaDuke, an associate professor of biological sciences at East Stroudsburg University in Pennsylvania, they co-authored the paper, which will be published in the American Journal of Physical Anthropology, 2010 edition. (I will post another blog post with link to the paper once it's published).

According to Pruetz and LaDuke, humans must accomplish three cognitive stages to truly control fire. First, they must have a conceptualization of what fire is and understand its behavior. Second, they must have the ability to control fire, including the containment and manipulation of the fire. Third, they must have the ability to start a fire. The Fongoli chimps seem to have mastered the first stage, according to Pruetz. However, she does not anticipate the chimps to start fire anytime soon due to the constrains of their flexibility.

Read the rest of the article from Iowa State University here.

Chimps Mourn The Death Of Their Own

A picture is worth a thousand words. So, I'm gonna just let the photo do most of the talking. Ever since this photo was published it has gone viral everywhere. Read about this news story at National Geographic and an in depth explanation of the photo here.

This photo is not surprising because it is well documented that chimpanzees mourn the death of their own. I guess the reason why it went viral is because the sheer volume of individuals mourning the death of this female chimpanzee. It looks almost human-like and behaviors that are human-like tend to evoke empathy in humans.

Chimpanzees: Ask And You Shall Receive

A new study published by Shinya Yamamoto, Tatyana Humle and Masayuki Tanaka on PLoS ONE found that chimpanzees willing to help one another. All they have to do is ask.

Ask and you shall receive. Video from NewScientist.

Using two tool-use scenarios (a stick tool-use and a straw tool-use), both chimpanzees were placed in adjacent booths with non-corresponding tools. The chimpanzee in a stick tool-use scenario was given a straw while the chimpanzee in a straw tool-use was given a stick. Successful use of tool resulted in a reward, a carton of juice. A spontaneous tool transfer was observed between paired chimpanzees, mostly following the request of the recipient. Even though reciprocity was not always observed, the chimpanzees continue to assist their partners as long as their partner requested help.

The authors argues that these results further prove the evidence for altruistic behavior in chimpanzees without direct personal gain or immediate reciprocation. These results also highlight the importance of "request" as a cause for prosocial behavior in chimpanzees, between kins or non-kins and also interaction between dominant and non-dominant individuals.

When compared to humans, chimpanzees do not perform acts of voluntary altruism. Unlike humans,  chimpanzees do not necessarily act altruistically by just observing another chimpanzee struggle to achieve its goal. Chimpanzees cannot accurately understand others' desires in the absence of communicative signals such as a request.

Further reading on NewScientist.

Reference:
Yamamoto, S. Humle, T. Masayuki, T. 2009. Chimpanzees Help Each Other upon Request. PLoS ONE 4(10): e7416. [doi:10.1371/journal.pone.0007416]

Even Howler Monkeys Think Veganism Is Whack (Sorry PETA)

Alright fine. Maybe these black and gold howler monkeys are not Whitney Houston and they don't think veganism is whack but new observation had shown that these howler monkeys actually raid chicken coop (or bird nests) for eggs. Yes, for food not to paint Easter eggs.

Male (left) and female (right) black and gold howler monkey . Flickr photo from lemai13

Thought to be exclusively folivores, the black and gold howler monkeys (Alouatta caraya) feed mainly on leaves, fruits and other parts of the plants such as flowers and bark. However, the population of black and gold howler monkeys in the forest of Rio Grande do Sul, Brazil had been observed eating eggs. "Alouatta is the most studied New World primate genus in the wild and there is not a single observation of intentional ingestion of animal matter in the literature", said primatologist Dr. Julio Bicca-Marques.

In 2005 Ms Helissandra Prates, a student of Dr Bicca-Marques, observed two juvenile black and gold howler monkeys (Alouatta caraya) licking the interior of a dove's nest at Estancia Casa Branca, a 2 ha orchard forest in Alegrete. The nest contained a broken egg shell. She later found evidence of egg remains in howler monkey dung collected from the orchard floor.

Then in 2007, Ms Muhle, another of Dr Bicca-Marques's students, witnessed howler monkeys eating birds' eggs at a separate woodland site at Beco Xavier. Over an eight month period, she recorded 19 separate instances of egg predation by a group of five individuals. All these later cases involved chicken eggs, which the monkeys stole from a chicken coop. While all five monkeys were seen to enter and investigate the coop, most of the eggs were actually eaten by a single subadult male.

-  Walker M. 2009. Monkeys 'reject vegetarianism'. BBC.

The evolution of egg-eating is localized in this population, leading researchers to think that it is a response to environmental conditions. There is a high density of howler monkeys living in a habitat with low food sources. Bicca-Marques et al. think that eggs act as a surrogate supplementary source of protein because of the low food diversity. The shift from folivory to omnivory reflects the flexibility of the black and gold howler monkey's diet. Watch the video of a black and gold howler monkey raiding a chicken coop.

Dr Julio Bicca-Marques and her colleagues from the Primatology Research Group published their findings in the International Journal of Primatology. The paper, "Habitat Impoverishment and Egg Predation by Alouatta caraya" is available in .pdf form through SpringerLink for free.

A quick Google search reveals that local zoos feed their black and gold howler monkeys meat and eggs such as Connecticut's Beardsley Zoo. Interesting. Coincidence?

This finding reminds me of the dietary shift and exploitation of new food sources in chimpanzees. We know that Gombe chimpanzees (Pan troglodytes schweinfurthii) prey on red colobus monkeys (Colobus badius tephrosceles) (Stanford et al., 2005) while savanna chimpanzees (Pan troglodytes verus) from Fongoli hunt lesser bushbabies (Galago senegalensis) using spear-like tool (Pruetz and Bertolani, 2007). Will we see more published paper about dietary shift and exploitation of new food sources? I guess it would have to be a trend as these primates lose more and more of their food sources and habitat. Perhaps those with a flexible diet will better adapt to their changing environment and ecology.

Sorry PETA. It seems that omnivory is in and veganism is out.

References:

Bicca-Marques JC. Muhle CB. Prates HM. De Oliveira SG. Calegaro-Marques C. 2009.
Habitat Impoverishment and Egg Predation by Alouatta caraya. International Journal of Primatology 30 (5):743-748. [doi:10.1007/s10764-009-9373-y]

Pruetz JD. Bertolani P. 2007.Savanna Chimpanzees, Pan troglodytes verus, Hunt with Tool. Current Biology 17(5): 412-417. [doi:10.1016/j.cub.2006.12.042]

Stanford CB. Wallis J. Matama H. Goodall J. 2005. Patterns of predation by chimpanzees on red colobus monkeys in gombe national park, 1982-1991. American Journal of Physical Anthropology 94 (2): 213-228. [doi:10.1002/ajpa.1330940206]

Walker M. 2009. Monkeys 'reject vegetarianism'. BBC. Retrieved September 30, 2009, from http://news.bbc.co.uk/earth/hi/earth_news/newsid_8270000/8270801.stm

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?"

Contagious Yawning in Chimpanzees

Animation of chimpanzee yawning from Emory University. Illustration from BBC News.

I'm sure we are all familiar with this scenario: Someone yawns and we would "catch" it or vice versa. This is the phenomenon of contagious yawning.

A new paper from The Proceedings of The Royal Society "Computer animations stimulate contagious yawning in chimpanzees" suggests that the phenomenon of contagious yawning and empathic response to animation occurs in chimpanzees. Computer animations of yawning chimpanzees (see illustration above) can be use to stimulate contagious yawning in chimpanzees. Previous researches have documented contagious yawning in chimpanzees through video-recorded footage.

Dr. Matthew Campbell, lead author of the paper from Emory University's Yerkes National Primate Research Center said that they would also like to learn more about behaviors that are related to empathy such as consolation (when an individual does something nice to the victim of aggression). They want to know if individuals that are good contagious yawners are also good consolers. Understanding how chimpanzees empathize and imitate animations can help us understand how we, as human beings, empathize and imitate animations as well, said Dr. Campbell.

Jane Goodall's New Book, "Hope for Animals and Their World: How Endangered Species Are Being Rescued from the Brink"

Jane Goodall's new book, Hope for Animals and Their World: How Endangered Species Are Being Rescued from the Brink.

I was at The Union Square Barnes and Nobles yesterday evening for Jane Goodall's book signing. She, along with Thane Maynard (Cincinnati Zoo director) and Gail Hudson (author of Harvest of Hope), was there to give a brief talk and sign her new book Hope for Animals and Their World: How Endangered Species Are Being Rescued from the Brink. I have yet to read the book but a chance to meet her in person (even for 1 minute) was exciting for me. I must admit that I was kinda shaking (again, with excitement) when I told her she's a great inspiration though she just looked at me slowly and smiled. She's pretty much the Whitney Houston of primatology, so she needs her diva moment. I will write more about the book once I am done with it.


I'm sure most people associate Jane Goodall with chimpanzees and primatology, but did you know that along with Dian Fossey (studied mountain gorillas) and Biruté Galdikas (studies orangutan), they are referred to as "Leakey's Angels"? Yes, Leakey as in Louis Leakey, the famous archaeologist who worked at Olduvai Gorge and discovered Oldowan tools.

The Fongoli Chimps of Senegal

A Fongoli chimp. Photo by Frans Lanting, National Geographic.

I just stumbled upon this on Twitter (Thanks to DarwinMonkey). It's a National Geographic page about the Senegalese Fongoli chimps, named after the Fongoli stream that runs through the chimpanzee's range. There are videos showing these chimps using tools fishing for termites, hunting a bushbaby and taking baths. Mary Roach's field note-like article "Almost Human" offers readers an insight to what the daily life of a chimpanzee is like (the Fongoli chimps are savanna-woodlands chimp), the concept of "ecological intelligence" and innovative tool use by the Fongoli chimps that were suppose to be unique to humans.

Read about "Almost Human" on National Geographic.

Homo floresiensis Walked Out of Africa

Skull of LB1 (Homo floresiensis, or the hobbit). Photo from Science Museum

New analysis by a team led by Australian National University doctoral student Debbie Argue showed that Homo floresiensis, nicknamed hobbits, were early hominin and walked out of Africa to Flores. Their findings supports the argument that Homo floresiensis had a unique wrist anatomy that originated from a lineage that lived long before the common ancestor of Homo sapiens and Neanderthals.

With Mike Moorwood from University of Wollongong and Thomas Sutikna from Indonesian Center for Archaeology, Debbie Argue compared 60 skulls and skeletal features from two individual hobbits to those of hominins, chimpanzees and gorillas using cladistic analysis. The result shows that Homo floresiensis "probably took one of two evolutionary paths from Africa to Flores. One began 1.66 million years ago, the other 1.9 million years ago".

Read more here: Hobbits Walked Out of Africa

Humans Evolved From Tree Climbers

A research from Duke University by Daniel Schmitt, associate professor of evolutionary anthropology, and Tracy Kivell, a post-doctoral research associate, shows that human evolved from tree climbing ancestors, not from knuckle-walkers. Schmitt and Kivell examined and compared the wrist bones of humans and African apes. Their research, "Independent evolution of knuckle-walking in African apes shows that humans did not evolve from a knuckle-walking ancestor", was published in the Proceedings of the National Academy of Sciences on August 10th, 2009.

They also found that knuckle walking evolved at least two different times; gorillas fundamentally knuckle walk differently than chimpanzees and bonobos.

Kivell and Schmitt think this suggests independent evolution of knuckle-walking behavior in the two African ape lineages.

Some scientists point to features in the human anatomy as our own vestiges of a knuckle-walking ancestry. One notable example is the fusion a two wrist bones that could provide us extra stability, a feature we share with gorillas, chimps and bonobos.

But some lemurs have that feature too, and they do a variety of different movements in the trees but do not knuckle-walk, Kivell said.

Altogether, the evidence leans against the idea that our own bipedalism evolved from a knuckle-walking ancestor, the pair wrote. "Instead, our data support the opposite notion, that features of the hand and wrist found in the human fossil record that have traditionally been treated as indicators of knuckle-walking behavior in general are in fact evidence of arboreality."

In other words, a long-ago ancestor species that spent its time in the trees moved to the ground and began walking upright.

There are no fossils from the time of this transition, which likely occurred about seven million years ago, Kivell and Schmitt said. But none of the later fossils considered to be on the direct human line were knuckle-walkers.

Read more on Science Daily: Bipedal Humans Came Down From The Trees, Not Up From The Ground

New Study Suggests That Humans are More Closely Related to Orangutans, Not Chimps

Sorry, been traveling here and there lately so don't really have time to post blog updates. Found this interesting article on EurekAlert!

A new study suggests that humans share a common ancestor with orangutans, not chimpanzees according to shared physical characteristics.

Comparing physical characteristics instead of DNA, researchers Jeffrey H. Schwartz and John Grehan found that humans shared 28 unique physical characteristics with orangutans, share only two features with chimpanzees and seven with gorillas. Humans share seven characteristics with all three apes (chimpanzees, gorillas, and orangutans). Gorillas and chimpanzees shared 11 unique characteristics.

Schwartz and Grehan proposed to have a new "grouping" or classification for humans, orangutans and last common ancestor call "dental hominoids" because they all share similar thick-enameled dental.

Read more about this study at EurekAlert! Humans related to orangutans, not chimps, says new Pitt, Buffalo Museum of Science study.

Great Apes LOL Like Human Too

A baby orangutan being tickled. Photo from Discovery News.

We're not the only species that are capable of laughing according to new study. Great apes are able to laugh like humans too, and they do it frequenty. This finding suggests that the last common ancestor of humans and apes also laughed around 10 to 16 million years ago. The ability to laugh subsequently evolved among apes and human, resulting in distinctive ways of laughing among them.

"Orangutans produce a short laugh series of noisy calls. Gorillas, chimps and bonobos produce longer laugh series and the calls are produced more rapidly" said project leader Marina Davila Ross, a primatologist from University of Portsmouth. With partners Michael Owren and Elke Zimmermann, Davila Ross recorded over 800 recordings of 22 juvenile and infant apes, and also three human babies laughing as they were tickled in their palms, feet, necks and armpits.

Presented in the latest edition of Current Biology, the study shows that human laughter is most similar to that of chimpanzees and bonobos, followed by gorillas and orangutans. Human laughter is least similar to those of siamangs, a lesser ape. "These results coincide with the genetic topology of great apes and humans," said Davila Ross. She doesn't rule out if apes or monkeys have a sense of humor but said that "it is difficult to find a method to accurately test it".

Read the rest of the article from Discovery News: Chimps, Other Apes Laugh Like People.

I wonder what function does laughing serve in primates.