Born This Way? Gender-Based Toy Preferences in Primates

Last week, British parents who had hidden their child’s gender from the world finally revealed that their five year old, now ready to enter school, is a boy. While the parents had hoped to raise their son Sasha in a gender-neutral way (“Stereotypes seem fundamentally stupid. Why would you want to slot people into boxes?”), their approach raised eyebrows and controversy. Were they creating an environment where their child could find his own gender identity, free from crippling societal expectations, or were they conducting a bizarre and possibly harmful experiment on a family member?

Putting aside the issue of whether the parents acted appropriately, the story raises fascinating questions about gender-specific traits and preferences. To what degree are gender differences innate and biological, and to what extent do they arise out of societal modeling and environment?

Some (including Sasha’s parents) may see gender preferences as being primarily influenced by human social pressures, but there are indications of biological influences as well. For example, girls with a particular genetic condition that exposes them to high prenatal levels of androgen often show “masculine” toy preferences, even when their parents strongly encourage them to play with female-typical toys. Given the intertwining impacts of nature and nurture in human societies, can we learn anything from our animal relatives who grow up free from human societal norms?

In this post, I’d like to take a look at two recent studies that examine differing male and female toy preferences in primates.

Male Monkeys Prefer Trucks

First, in 2009 a research team led by Janice Hassett of the Yerkes National Primate Center at Emory University reported on experiments in which they the researchers to see whether rhesus monkeys (Macaca mulatta) would exhibit gender-specific toy preferences similar to those of human children.

In humans, studies have shown that boys gravitate strongly to stereotypically “masculine” toys such as trucks and other vehicles, while girls are less rigid, spending relatively equal amounts of time playing with boy-favored toys and with more traditionally “feminine” toys such as dolls. One hypothesis put forward to explain this difference has been that boys face greater societal discouragement when they play with “girl toys” than girls do in the reverse situation. The researchers figured that by looking at rhesus monkeys, who don’t face comparable social pressures to conform to gender roles, they might be able to illuminate biological influences on toy selection as well.

Of course I'm not playing; you gave me a Raggedy-Ann. Pass me that truck. Now. (photo credit: J.M.Garg, Wikipedia)

In their study, the researchers compared how 34 rhesus monkeys living in a single troop interacted with human toys categorized as either masculine or feminine. The “masculine” set consisted of wheeled toys preferred by human boys (e.g., a wagon, a truck, a car, and a construction vehicle); the “feminine” set was comprised of plush toys comparable to stuffed animals and dolls (e.g., a Raggedy-Ann™ doll, a koala bear hand puppet, an armadillo, a teddy bear, and a turtle). Individual monkeys were released into an outdoor area containing one wheeled toy and one plush toy, with the researchers taping all interactions using separate cameras for each toy, identifying all specific behaviors, and statistically analyzing the results.

The results closely paralleled those found in human children. As with human boys, male rhesus monkeys clearly preferred wheeled toys over plush toys, interacting significantly more frequently and for long durations with the wheeled toys. Also mirroring human behavior, female rhesus monkeys were less specialized, playing with both plush and wheeled toys and not exhibiting significant preferences for one type over the other. Here’s a chart illustrating the similar gender preferences of humans and rhesus monkeys (the information regarding human preferences comes from a 1992 study by Sheri Berenbaum and Melissa Hines):

The researchers noted that these similarities show that distinct male and female toy preferences can arise in the absence of socialization pressures and hypothesized that “there are hormonally organized preferences for specific activities that shape preference for toys that facilitate these activities.”

Barbie Really Is a Stick Figure

Next, in a brief paper published in 2010, Sonya Kahlenberg of Bates College and Richard Wrangham of Harvard University presented the first evidence of wild male and female primates, chimpanzees (Pan troglodytes) in the Kanyawara chimpanzee community of Kibale National Park, Uganda, interacting differently with play objects.

Over a 14 year period, Kahlenberg and Wrangham observed that juvenile Kanyawara chimpanzees tended to carry sticks in a manner suggestive of rudimentary doll play and that the behavior was more common in females than in males. Juvenile chimps, particularly females, would carry around small sticks for hours at time while they engaged in other daily activities such as eating, climbing, sleeping, resting and walking. While the same chimps used sticks as tools for specific purposes, the researchers were unable to discern any practical reason for the stick-carrying. The following chart shows the degree to which female chimps were more likely to engage the in stick carrying behavior:

Age and sex differences in the rate of stick-carrying in chimpanzees. Females: circles, solid line. Males: triangles, dashed line.

The researchers hypothesized that “sex differences in stick-carrying are related to a greater female interest in infant care, with stick-carrying being a form of play-mothering (i.e. carrying sticks like mother chimpanzees carrying infants).” In support of this proposition, they pointed to several factors. First, they never observed stick carrying by any female who had already given birth; that is, stick-carrying ceased with motherhood. Also, the chimps regularly carried sticks into day nests where they “were sometimes seen to play casually with the stick in a manner that evoked maternal play.” Finally, nurturing behavior towards objects like sticks had previously been reported in captive chimps and documented on a couple of occasions in the wild.

Also, the researchers suggested a social rather than biological basis for the behavior. Because regular stick-carrying hasn’t been reported in other wild chimpanzee communities, they proposed that that young Kanyawara chimpanzees may be learning the behavior from each other as a way of practicing for adult roles – a form of social tradition passed between juveniles previously described only in humans. Kahlenberg and Wrangham conclude by noting that:

Our findings suggest that a similar sex difference could have occurred in the human and pre-human lineage at least since our common ancestry with chimpanzees, well before direct socialization became an important influence.

So there you have it. One rhesus monkey study positing a biological and hormonal basis for gender-specific play, and another chimpanzee study emphasizing social learning… At least for now, the threads of nature and nurture impacting gender roles seem difficult to disentangle for non-humans, just as they are for us.

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ResearchBlogging.orgHassett, J., Siebert, E., & Wallen, K. (2008). Sex differences in rhesus monkey toy preferences parallel those of children Hormones and Behavior, 54 (3), 359-364 DOI: 10.1016/j.yhbeh.2008.03.008.

Berenbaum, S., & Hines, M. (1992). EARLY ANDROGENS ARE RELATED TO CHILDHOOD SEX-TYPED TOY PREFERENCES Psychological Science, 3 (3), 203-206 DOI: 10.1111/j.1467-9280.1992.tb00028.x.

Kahlenberg, S., & Wrangham, R. (2010). Sex differences in chimpanzees’ use of sticks as play objects resemble those of children Current Biology, 20 (24) DOI: 10.1016/j.cub.2010.11.024.

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Peace on Earth, Good Will towards Baboons (and Humans)

In the middle of the 1980s, a catastrophic event shattered the lives of a troop of olive baboons (Papio anubis) living in the Masai Mara Reserve in Kenya. While the troop ultimately survived the experience, it emerged as a fundamentally transformed society with new cultural traditions. This is its story.

The troop, known as the Forest Troop, was initially very much like other olive baboon troops – that is to say, an extremely hierarchical and aggressive society, fraught with battles for dominance and bullying of subordinates. While a female will remain with her birth troop for life and automatically inherit her mother’s social ranking, a male reaching adolescence must set off on his own to find a new troop and then jockey with other males for position on the social ladder. The stakes are high, as baboon society is polygamous and dominant males enjoy the best access to mating and food resources.

And so it was. The Forest Troop lived in the woods and slept in trees about a kilometer from the open-air garbage pit of a nearby tourist lodge. Over time, many of its most aggressive males got into the habit of traveling to the garbage pit at dawn in order to scavenge for food, fighting for scraps with the males of a neighboring troop.

Then, in 1983, disaster struck. Spoiled meat that had been discarded in the garbage pit caused a fatal epidemic of bovine tuberculosis. Every single Forest Troop male who had foraged for food at the pit – 46% of the troop’s adult males – died in the outbreak. The remainder of the devastated troop, comprised solely of females and less aggressive males, survived.

In the wake of the outbreak, researchers who had been observing the Forest Troop noticed a dramatic reduction in certain types of aggressive behavior within the troop, not a particularly surprising observation given the loss of all of the most aggressive males in the troop. However, because the researchers wanted to focus on an intact troop that hadn’t experienced social disruption, they turned their attention away from the Forest Troop and shifted their efforts to studying a nearby troop that hadn’t been impacted by the outbreak.

A number of years later, though, the researchers returned to the Forest Troop and noticed something fascinating – even though there had been a complete changeover in the troop’s adult males, the troop’s less aggressive behavioral features had persisted. That is, a new generation of baboons in the Forest Troop appeared to be carrying on what amounted to a cultural tradition of lessened baboon aggression.

Geez, another housewarming party?! That Forest Troop has GOT to be some sort of a cult or something. (photo: Philippe_Boissel)

In order to analyze the changed behavior more rigorously, the researchers engaged in what’s known as a “focal sampling” process. They systematically recorded the social behavior of individual Forest Troop baboons from 1993 through 1996, and then compared those observations to two other data sets that served as controls – pre-outbreak observations they had made of the Forest Troop from 1979 to 1982, and mid-1990s observations of a different olive baboon troop.

What they found bore out their initial impressions. In particular, the new generation of Forest Troop baboons displayed patterns of dominance and aggression behavior that created less stress for low-ranking males. While the overall number of incidents involving aggression and dominance behavior was comparable to that seen in the control cases, the mix was different. Forest Troop confrontations were now significantly more likely to involve closely-ranked males, as opposed to the control group behavior pattern in which very high ranking males tended to pick on the lowest-ranking ones. This is notable, as confrontations between baboons with large power disparities typically reflect harassment rather than true competition and can be particularly stressful to the lower-ranking subordinates. Moreover, in the post-epidemic Forest Troop, males acted less aggressively towards females, engaged in more social grooming with females, sat in closer proximity to other baboons, and were more likely to have adult females, infants, adolescents, and juveniles as neighbors. Finally, the researchers found that subordinate baboons in the kinder and gentler Forest Troop had much lower levels of glucocorticoids, adrenal hormones secreted in response to stress, than did subordinates in the control groups.

C’mon, Dad, faster! Bumbo and Uncle Phil are waaaay ahead of us!

The researchers next considered how the peaceful new social traditions of the Forest Troop were being passed on to new males joining the troop: were troop members teaching the newcomers to be less aggressive, were new arrivals learning through observation or because they had more opportunities for friendly interactions, or was self-selection causing less aggressive males to gravitate toward this more peaceful troop? The researchers found that new males acted with typical aggression upon arriving at Forest Troop and were greeted with the usual belligerence from other males, but that the Forest Troop females were now uncharacteristically welcoming to the new arrivals, grooming them and otherwise treating them as established residents. Because the females didn’t seem to be engaged in active teaching behavior (they showed the same friendly behavior to even the most aggressive of the newcomers), the researchers concluded that the peaceful Forest Troop cultural traditions were most likely being passed on as newcomers observed more positive interactions with females and had more opportunities to relate non-aggressively themselves.

So, out of ashes of death, a baboon troop forged a new culture and found a way to maintain its peaceful traditions, passing them along to new generations. Makes one think….

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ResearchBlogging.orgSapolsky, R., & Share, L. (2004). A Pacific Culture among Wild Baboons: Its Emergence and Transmission PLoS Biology, 2 (4) DOI: 10.1371/journal.pbio.0020106.

It’s Not That Funny, the Chimp Is Just Being Polite

“Ha ha ha,” politely hoots the chimpanzee, not exactly rolling on the floor. He’s not laughing spontaneously or for very long, but he does want to encourage his playmate to keep up the antics.

Continuing on in the spirit of last week’s post on the rodenty laughter of tickled rats, today’s post features a recent study on social laughing in chimpanzees.

As we all know quite well from experience, human laughter is a many-faceted thing. Sure, we sometimes laugh spontaneously and joyously (this is known as Duchenne laughter), but we also use our laughter as a multipurpose social tool, enabling us to establish rapport with social partners, to announce that we are nonthreatening and open to further communication, to alleviate tension and break barriers when meeting an unfamiliar face, and even to exclude others by demonstrating scorn or derision. In short, laughter sends a wide range of communicative signals, and our mastery over its many varieties lies close to the core of what’s sometimes referred to as emotional intelligence – the sophisticated way in which we assess, understand and navigate social situations.

Well, do any other animals manage their laughter for social reasons, or is nonhuman laughter inevitably spontaneous and reactive, like the high-pitched chirping of tickled rats? (Not that this would be a bad thing, just ask the rats….)

Marina Davila-Ross and her co-researchers from the University of Portsmouth decided to test some chimpanzees to find out. They studied 59 male and female chimpanzees of all ages living in four separate colonies at the Chimfunshi sanctuary in Zambia – two smaller colonies that had formed within the past five years, and two larger ones that had been together at least 14 years. In general, the chimps in the colonies that had been together longer belonged to more established families and had grown up with more opportunities to play with others in a familiar social environment.

Did you see the look on Mr. Mookimbo’s face when he bit into the “cake”? (photo credit: David Eppstein)

First, the researchers videotaped almost 500 one-on-one play sessions, documenting what the chimps did and when they laughed. The researchers recorded spontaneous laughter as well as laugh replications (laughter that followed within five seconds after a playmate’s laughter), and further noted whether the laugh replications occurred during the first second (rapid laugh replication) or within the next four seconds (delayed laugh replication).

The research team soon discovered that the chimps’ spontaneous laughter was substantially different than their laugh replications: the laugh replications were much shorter, consisting of significantly fewer calls per laugh series. Among other things, the researchers also found that:

  • Chimps in the more recently-formed colonies replicated the laughter of their playmates more frequently than did the chimps in longer-established colonies, even though the aggregate amount of all laughter in each of the colonies was relatively comparable.
  • Infants generally engaged only in spontaneous laughter, with little or no laugh replication.
  • Play bouts lasted significantly longer when they were accompanied by laugh replications than when they weren’t.
  • Laugh replications peaked at two discrete points, first at about .7 to .8 seconds after the initial laugh, and then again between 2 and 3 seconds after the initial laugh.

Next, the researchers tried to verify whether laugh replications were specifically triggered by a playmate’s laughter, and not just coincidentally associated with it. They combed through their previously-recorded video footage and, for specific chimps and their playmates, found matching play scenes that generally lined up very closely in terms of specific behaviors (chasing, tickling, grabbing, wrestling, gnawing, hitting, jumping, game playing, etc.), but that differed in one important respect – in one scene, the chimp’s playmate engaged in a potentially-triggering bout of laughter; in the other scene, it did not. When the researchers reviewed these paired scenes, they found that a chimp was significantly more likely to laugh in those scenes in which the other chimp laughed first, suggesting strongly that replicated laughter really was triggered by the playmate’s laughter as opposed to any other aspect of the chimps’ play behavior.

Well, one thing’s for sure, they’re not going to trust us with *next year’s* holiday decorations… (photo credit: Christa Saayman)

Based on their findings, the researchers concluded that chimps laugh in response to the laughter of their playmates, that this laughter differs in acoustic form and timing from their spontaneous laughter, and that the purpose of their non-spontaneous laughter appears to be to prolong social play, promoting group cohesion and perhaps providing the chimps with important social advantages.

In support of these conclusions, the researchers also observed that the lack of laughter replication in infant chimps suggests that socially managed laughter is a skill that chimps learn as they mature. Further, they hypothesized that the chimps in the newer colonies may have engaged in more replicated social laughter because they were living in a less predictable social environment and may have had a greater need to manage laughter in order to establish social cohesion.

So, next time you’re at a party with a group of laughing chimpanzees (don’t think I don’t know you, AnimalWise readers), listen very closely to the rising levels of laughter around you. While you might be tempted to believe that you’re hanging out with a particularly hilarious crowd, the truth may be that your fellow party goers are simply adept at using laughter as a social lubricant. Let the good times roll!

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ResearchBlogging.orgDavila-Ross, M., Allcock, B., Thomas, C., & Bard, K. (2011). Aping expressions? Chimpanzees produce distinct laugh types when responding to laughter of others. Emotion, 11 (5), 1013-1020 DOI: 10.1037/a0022594.

A Yawning Divide? Contagious Yawning and Empathy in Animals

A group of red-footed tortoises ran away (rather slowly) with the 2011 Ig Nobel Prize in physiology1, bringing to center stage the potential link between contagious yawning and empathy in animals. While the Ig Nobels are a tongue-in-cheek spoof of the Nobel Prizes, their purpose is not frivolous – they “honor achievements that first make people laugh, and then make them think. The prizes are intended to celebrate the unusual, honor the imaginative — and spur people’s interest in science, medicine, and technology.” Here’s the story of the tortoises’ claim to fame and what we know about contagious yawning in animals.

Tortoise yawning? I don’t think so!

It turns out that the underlying cause of contagious yawning has been something of a puzzle – why is it that when you see someone else yawn (or even hear a yawn or just think about yawning), you sometimes are overcome with the urge to yawn yourself? The most common hypotheses are that contagious yawning results either from empathy or from non-conscious social mimicry, the tendency to adopt a social partner’s postures, gestures and mannerisms. An alternative hypothesis, however, is that it may simply reflect a fixed action pattern, an innate or instinctual response to a stimulus (a triggering yawn).

No, really, go on - I'm listening... (photo: Peter Baumber)

And that’s where the red-footed tortoises lumber into the picture. Lead researcher Anna Wilkinson and her colleagues figured the tortoises would offer a good way of testing the fixed action pattern hypothesis, since they are known to yawn and respond to social stimuli, but are not believed to exhibit empathy or engage in non-conscious social mimicry.

The researchers worked very hard to induce contagious tortoise yawning, spending six months training one of them (Alexander, if you’re curious) to yawn whenever he saw a red square-shaped symbol, and then devising a series of tests to see whether six “observer” tortoises would yawn after seeing Alexander yawn. Initially, the observers were presented with three scenarios: one in which they watched Alexander giving one of his patented yawns, another in which they watched a non-yawning tortoise (Alexander?), and a third in which they simply viewed Alexander’s red square. A second experiment mirrored the first, except this time the observers watched Alexander yawn multiple times. Finally, they went to the movies, seeing clips of real tortoise yawns, fake yawns and an empty background.

And the results? Nothing, nada, zilch. The tortoises simply didn’t yawn more frequently after seeing another tortoise yawn; no contagious yawning whatsoever. This spectacular display of non-yawning in tortoises led the researchers to “suggest that contagious yawning is not simply the result of a fixed action pattern and releaser stimulus …. We suggest that contagious yawning may be controlled through social processes such as nonconscious mimicry or empathy….” Naturally, international acclaim ensued.

Apes and Monkeys and Dogs, Oh My!

So, which animals do demonstrate contagious yawning? Well, as with other cognitive realms, our views of contagious yawning have followed “AnimalWise’s Rule”: first we believed it to be an exclusively human behavior, then we observed it in chimpanzees, then we saw it in monkeys, next in dogs, now … hmm … Taste it, fur-face, I have opposable thumbs!  Ok, I lied, that’s not a real rule; I just made it up.

Here’s a run-down on what we actually know about contagious yawning in non-humans:

Chimpanzees

The phenomenon was first demonstrated in chimpanzees in 2004 when a research team led by James Anderson of the University of Stirling reported2 on a small study in which six adult female chimps watched video scenes of other chimps who were either yawning naturally or, alternatively, displaying open-mouthed facial expressions that weren’t yawns. Two of the observers (33%) yawned significantly more often in response to the yawn videos and none of them yawned more frequently in response to the open-mouth control videos, a response rate only slightly lower than that in humans watching comparable videos. In 2009, Matthew Campbell and colleagues from the Yerkes National Primate Research Center (YNPRC) expanded on these findings, reporting3 that, much like humans responding to on-screen yawns by Pixar characters, a group of 24 chimps yawned significantly more often after watching 3D computer animations of yawning chimps than after watching animations of chimps displaying non-yawn mouth movements. Finally, Matthew Campbell and Frans de Waal of the YNPRC reported4 this year on an experiment lending empirical support to the hypothesis that contagious yawning stems from empathy. Campbell and de Waal found that, consistent with studies showing that humans demonstrate greater empathy towards others they view as being similar, chimps yawned significantly more frequently in response to videos of familiar chimps yawning than they did to either videos of unfamiliar chimps yawning or videos of chimps (regardless of familiarity) who were at rest.

Monkeys

The first study supporting contagious yawning in non-ape primates was published5 in 2006 by University of Stirling researchers Annika Paukner and James Anderson, who had 22 stumptail macaques watch video clips of other macaques either yawning or making non-yawn facial movements. Although the macaques yawned significantly more in response to yawn tapes than to non-yawn tapes, the researchers noted that the macaques engaged in more self-directed scratching (a tension-relieving behavior) while watching the yawn tapes, making it difficult to differentiate between actual contagious yawning and the release of stress perhaps brought on by the yawn tapes. The case for non-hominid contagious yawning was bolstered in 2009, though, when Elisabetta Palagi of Pisa University and her colleagues published6 a study in which they recorded and reviewed over 3,200 baboon yawning displays (all occurring in the absence of stressful events or behavior). They not only found clear evidence of contagious yawning among adult baboons, but also discovered that females (but not males) tended to match the type of yawning display (baboons make different facial expressions when yawning) that had triggered their own yawn, and that the degree of contagiousness correlated with social closeness, thus supporting an empathy-basis for yawn contagion and anticipating the results of 2011 chimpanzee experiment described above.

Dogs

Lastly, in 2008 Ramiro Joly-Macheroni and colleagues from the University of London reported7 on an experimental first on multiple fronts: yawn contagion in a non-primate species and the first demonstration of possible contagious yawning across different species. In their study, 29 dogs observed an unfamiliar human either yawning or making non-yawning mouth movements, with 21 dogs yawning in response to the yawning human and not one yawning in response to the human who displayed the non-yawning control behavior.

Future Directions

I know that if the Internet were allowed to vote, researchers would spend much of their waking hours considering YouTube videos of impossibly cute kittens yawning, but I want to take this opportunity to call for a full and serious investigation into the concerning link between contagious duck wing flapping and odd French Canadian music:

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ResearchBlogging.org1Wilkinson, A., Sebanz, N., Mandl, I., & Huber, L. (2011). No evidence of contagious yawning in the red-footed tortoise Geochelone carbonaria. Current Zoology, 57(4), 477-484.

2Anderson, J., Myowa-Yamakoshi, M., & Matsuzawa, T. (2004). Contagious yawning in chimpanzees Proceedings of the Royal Society B: Biological Sciences, 271 (Suppl_6) DOI: 10.1098/rsbl.2004.0224.

3Campbell, M., Carter, J., Proctor, D., Eisenberg, M., & de Waal, F. (2009). Computer animations stimulate contagious yawning in chimpanzees Proceedings of the Royal Society B: Biological Sciences, 276 (1676), 4255-4259 DOI: 10.1098/rspb.2009.1087.

4Campbell, M., & de Waal, F. (2011). Ingroup-Outgroup Bias in Contagious Yawning by Chimpanzees Supports Link to Empathy PLoS ONE, 6 (4) DOI: 10.1371/journal.pone.0018283.

5Paukner, A., & Anderson, J. (2006). Video-induced yawning in stumptail macaques (Macaca arctoides) Biology Letters, 2 (1), 36-38 DOI: 10.1098/rsbl.2005.0411.

6Palagi, E., Leone, A., Mancini, G., & Ferrari, P. (2009). Contagious yawning in gelada baboons as a possible expression of empathy Proceedings of the National Academy of Sciences, 106 (46), 19262-19267 DOI: 10.1073/pnas.0910891106.

7Joly-Mascheroni, R., Senju, A., & Shepherd, A. (2008). Dogs catch human yawns Biology Letters, 4 (5), 446-448 DOI: 10.1098/rsbl.2008.0333.

Analogical Reasoning in Animals

In today’s post, I’d like to explore some surprising recent findings about the abilities of animals in the area of analogical reasoning.

Reasoning by analogy is central to the way we think, enabling us to use familiar concepts to solve new problems. When a catastrophic event strikes Wall Street, economists inevitably point to analogous historical disruptions in their attempts to predict whether we’re facing long-term troubles or a quick recovery. When lawyers advocate on behalf of clients in new realms such as digital media, they often ground their arguments in principles that evolved centuries ago to protect real property interests. When scientists explain the motion of molecules and other phenomena that we cannot directly perceive, they frequently turn to concrete examples such as colliding billiard balls or streams of water.

On a more mundane level, analogical thinking underlies many of our idioms and permeates our everyday language. Think how lost you’d be if you were suddenly unable to understand phrases that explicitly or implicitly apply concepts from one context to events or actions in another. Conversations at work would confuse you (more than usual). Your boss’ suggestion that you take some time off to recharge your batteries would leave you scratching your head rather than looking for deals on tropical island vacations. You wouldn’t be able to follow political discussions (oh no!). You’d be the only one asking “oh my god, was it with guns or knives?” after hearing that one candidate outdueled another in a debate. You’d be the only one worrying about cannibalism after learning that the people were hungry for new leadership. You’d find sports to be newly upsetting, as you’d literally go into mourning after learning of your favorite team’s fatal missteps. (Ok, I take that back – nothing has changed here, especially for Boston Red Sox fans.)

Relational Matching Tests

One of the most common tests used to assess an individual’s ability to solve analogy problems is known as relational matching-to-sample or RMTS. In its classic form, RMTS involves first showing the subject a sample set consisting of two or more objects that are either identical (for example, two circles) or nonidentical (for example, a square and a circle). Sets containing identical objects are sometimes referred to as reflecting the “identity relation” and those containing nonidentical objects are said to reflect the “nonidentity relation.” Next the subject is shown two comparison sets containing novel objects, one embodying the identity relation (e.g., two triangles) and the other the nonidentity relation (e.g., a rectangle and a triangle). To succeed, the subject must choose the comparison set that matches the relationship demonstrated by sample set. For instance, the correct choice for a subject shown two circles in the sample would be the comparison set containing the two triangles, whereas the correct choice for the subject initially shown the square and the circle would be the comparison set containing the rectangle and the triangle.

RMTS is particularly well suited for testing the abilities of non-human animals, as it poses an analogy problem in a strictly visual manner, not relying in any way on linguistic skills. In essence, success requires the subject to not only make a “first order comparison” between same and different, but also to make a “second order comparison” by applying this underlying distinction to a novel environment. Many researchers consider this ability to lie at heart of analogical reasoning.

A “Profound Disparity”?

Until recently, studies have suggested that humans and a select few great apes stand far apart from all other animals in terms of analogical reasoning abilities. While many animals can successfully distinguish between same and different shapes or colors, they tend to struggle when it comes to making second order comparisons of the sort required by RMTS tasks. Since only humans and some chimpanzees, gorillas and orangutans have performed well at RMTS testing, researchers have proposed that a “profound disparity” exists between the analogical reasoning capacity of hominids and other animals.

For example, several studies have shown that some baboons and pigeons can learn to pass RMTS tests if they involve large-sample and comparison sets (e.g., comparisons involving 4 x 4 grids of 16 all identical and 16 all different objects), but that their performance rapidly deteriorates as the size of the grid decreases as well as when the distance between the objects in the grid increases. According to researchers, one reason why animals do better with larger sample sets may be that there’s a greater amount of variation or “entropy” between non-analogous grids in larger sample and comparison sets, which makes the task of distinguishing between potential answers easier.

Notwithstanding these prior findings, however, two studies published in the last few months now pose a challenge to the “profound disparity” concept, suggesting that a suitable testing environment can showcase robust analogical reasoning skills in non-apes.

Clever Capuchins

In the first study, which was published in PLoS ONE in August 2011, researchers led by Valentina Truppa and Elisabetta Visalberghi of the National Research Council in Rome, Italy, found that New World tufted capuchin monkeys (Cebus apella) were capable of solving RMTS tasks involving sample and comparison sets involving sets of as few as two objects.

What are all of those freaking squiggles in that diagram above my head? (image credit: Charlesjsharp)

The research team studied five capuchin monkeys, testing them over and over again on RMTS tasks involving varying numbers of icons. While the specific tests varied, the general approach was to start by giving the monkeys trials involving a relatively small pool of different icons and, only if and when a monkey achieved proficiency (as measured by percentages of correct answers) over the course of thousands of trials, to introduce novel icons for comparison. Also, in one of the experiments, if the monkey did not ultimately reach the proficiency threshold on a two-icon comparison test, “entropy” was increased and the monkey was given an easier four-icon test.

Ultimately, after a total of 21,888 trials (yes, that’s correct!) one of the five capuchins, Roberta, proved to be a real overachiever. As the researchers put it:

The current study demonstrates the acquisition of abstract concepts based on second-order relations by one capuchin monkey, Roberta. She was first successful with four-item stimuli and then with two-item stimuli, the latter being the most difficult condition previously thought to be mastered only by apes. Since her performance was robust across different types of stimuli and well above that of the other subjects, we can argue that relational analogies are very difficult for capuchins, but under specific circumstances not impossible.

Way to go, Roberta!

Bright Baboons

In a second study, published on September 20, 2011, in Psychological Science, a research team headed by Joël Fagot of the Centre National de la Recherche Scientifique at the Université de Provence reported that guinea baboons (Papio papio) can learn to perform surprisingly well at RMTS tasks … and then retain this ability over a 12-month period. In this study, 29 baboons with no language training and little or no experience with relational matching tests participated in various RMTS experiments involving geometric shape comparisons.

All this RMTS stuff gives me a headache (image: Animal Globe)

The first experiment consisted of classic RMTS trials, each involving a sample set made up of pairs of identical or nonidentical geometric shapes, and two comparison sets with new geometric shapes, with only one of the comparison sets matching the relationship demonstrated by the sample set. At first, the testing pairs were selected randomly from among 10 geometric shapes, but once a baboon had achieved an accuracy level of 80% or better in three consecutive sessions of 100 trials, new geometric shapes were introduced up to a maximum of 90 shapes by the end of the experiment. Six of the 29 baboons were able to make it to the 80% threshold level, and five were ultimately able to proceed through testing until they reached all 90 shapes.

The second experiment included changes designed to make the challenge more difficult: the geometric shapes were moved further apart and, perhaps more significantly, in half of the tests the “incorrect” comparison pair, rather than containing all new geometric shapes, actually contained one of the shapes from the sample pair. In other words, even though this comparison pair was incorrect from the standpoint of analogy testing, it contained a shape that was directly linked to the sample set, potentially confusing the baboon if it was focused on the similarity of the shapes rather than the conceptual relationship between the shapes.

In spite of the enhanced degree of difficulty, all five of the baboons who participated – the same baboons who had been successful in the first experiment – performed at above chance levels throughout the second experiment (although, not surprisingly, their performance tailed off somewhat in the trials where the incorrect response shared a shape with the sample set).

Finally, the research team retested the five successful baboons in accordance with the first experiment methodology after a one-year lapse during which the baboons had no practice at RMTS tasks. All five baboons reached the 80% success level far more quickly than they had the first time around, providing strong evidence that they had been able to retain their relational matching skills over this one-year period.

As with the capuchin monkeys, the baboons were not naturals at these tests – they went through thousands upon thousands of trials and only gradually acquired their relational-matching skills. Once again, though, the research strongly suggests that there is not a bright line “profound disparity” between the capabilities of hominids and those of other animals, and that other animals can demonstrate the cognitive foundation necessary for abstract analogical reasoning.

So, as in other areas, the more we explore the abilities of animals, the more we find that we have been wrong about what we thought were cognitive barriers. As we become more adept at designing experiments that are patiently conducted and thoughtfully tailored to the skills and natural adaptations of the specific animals we are studying (rather than the skills and adaptations of college undergraduates), we should continue to see the breakdown of additional barriers.

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ResearchBlogging.orgTruppa, V., Piano Mortari, E., Garofoli, D., Privitera, S., & Visalberghi, E. (2011). Same/Different Concept Learning by Capuchin Monkeys in Matching-to-Sample Tasks PLoS ONE, 6 (8) DOI: 10.1371/journal.pone.0023809

Fagot, J., & Thompson, R. (2011). Generalized Relational Matching by Guinea Baboons (Papio papio) in Two-by-Two-Item Analogy Problems Psychological Science, 22 (10), 1304-1309 DOI: 10.1177/0956797611422916

Grief in Animals

I’ve been thinking about grief lately. It can be so overpowering – the dull ache of emptiness, the stabbing pain of loss, and the prism of sadness that transforms the bright colors of everyday life into a harsh and alien landscape. Consumed by grief, we are alone; yet somehow our solitary suffering can end up strengthening the bonds we have with others we know and love.

I’ve also been thinking about grief in animals, and what we know about it. When our cat Puggsley died, our younger Siamese, Moose, felt the full impact of the loss. The two had always been close, perhaps tied together by their mutual skepticism over Wednesday, our third cat and official people-pleaser. Moose and Puggsley were constant companions, playmates, napping buddies, and a rather frightening pair of mischief makers. When Puggsley became old and frail, he would curl up stiffly by the fireplace, and Moose would bed down near him. At the very end, Moose was right there, tenderly licking Puggsley as he was overcome by a seizure. And after he was gone, she mourned – she was lost without her friend, and had little appetite or energy for weeks. She never bedded down by the fireplace again. How do I know this was grief? Well, it was obvious; I just know.

Puggsley and Moose

But what do we really know about grief in animals – that is, in a scientific sense? Not particularly much, it turns out.

We are (mostly) beyond the era in which animals were considered thoughtless automatons, incapable of feeling pain and other emotions. Still, there have been relatively few formal studies of how animals experience grief.

In a way, this isn’t so surprising. For one, opportunities to systematically observe grieving behavior in the wild are rare and, if you think about it, it’s difficult to design ethical studies intended to cause social animals to grieve in captive settings. Also, what specifically do you test for and how do you quantify and evaluate an inherently subjective experience like grief? It’s tough enough to evaluate this sort of thing in humans, who can respond to questionnaires and use language to express their emotions….

As a result, most the scientific literature about grief in animals is anecdotal or observational in nature, and in many of these accounts it’s clear that otherwise objective researchers have struggled to come up with scientific ways of reporting what, in the end, are their own reactions, what they just know.

Although the record is sparse everywhere, there have been some recent papers on grief in primates. Brian Switek, who writes the Laelaps blog for Wired Magazine, has written a terrific piece on this research in his “What Death Means to Primates” posting (I strongly encourage you to check out Laelaps; it’s one of the best blogs out there on paleontology, evolution, and the history of science).

As Brian recounts in detail, studies have documented chimpanzee and other primate mothers who have continued to carry dead infants, sometimes for weeks and even to the point of mummification. In one of the studies1, researchers described two chimpanzee mothers (Jire and Vuavua) in Bossou, Guinea, who carried their dead babies (aged 1.2 years old and 2.6 years old, respectively) after they had died in a respiratory epidemic, grooming them regularly, chasing away flies, and carrying them during all travel. The researchers pondered:

An obvious and fascinating question concerns the extent to which Jire and Vuavua “understood” that their offspring were dead. In many ways they treated the corpses as live infants, particularly in the initial phase following death. Nevertheless they may well have been aware that the bodies were inanimate, consequently adopting carrying techniques never normally employed with healthy young (although mothers of handicapped young have also been known to respond appropriately).

In another study2, James Anderson, Alasdair Gillies and Louise Lock reported on the peaceful death of an older chimpanzee, Pansy, who lived in a safari park. They videotaped the reactions of Pansy’s companions and observed a number of behaviors that they found to be comparable to human bereavement. The degree to which the researchers sought out human counterparts to the chimps’ behavior is evident from the following description in their paper:

During Pansy’s final days the others were quiet and attentive to her, and they altered their nesting arrangements (respect, care, anticipatory grief). When Pansy died they appeared to test for signs of life by closely inspecting her mouth and manipulating her limbs (test for pulse or breath). Shortly afterwards, the adult male attacked the dead female, possibly attempting to rouse her (attempted resuscitation); attacks may also have expressed anger or frustration (denial, feelings of anger towards the deceased). The adult daughter remained near the mother’s corpse throughout the night (night-time vigil), while Blossom groomed Chippy for an extraordinary amount of time (consolation, social support). All three chimpanzees changed posture frequently during the night (disturbed sleep). They removed straw from Pansy’s body the next morning (cleaning the body). For weeks post-death, the survivors remained lethargic and quiet, and they ate less than normal (grief, mourning). They avoided sleeping on the deathbed platform for several days (leaving objects or places associated with the deceased untouched).

With this focus, it’s not surprising that they concluded by proposing that “chimpanzees’ awareness of death has been underestimated.”

Also, more anecdotally, many were moved by the apparent grief captured in this poignant National Geographic photo of chimpanzees at a rehabilitation center peering at the lifeless body of Dorothy, their long-time companion, being taken to her burial:

Chimpanzee burial (National Geographic, photo: Monica Szczupider)

There has also been some research into the behavior of elephants towards the dead and dying. In one study3, Iain Douglas-Hamilton, Shivani Bhalla, George Wittemyer and Fritz Vollrath reported on the death of Eleanor, a matriarch elephant in the Samburu National Reserve in Kenya. They were able to use GPS technology to track the movements of elephants in Eleanor’s family and in other families as they reacted to her collapse and subsequent death. The researchers found that Eleanor was visited frequently by both related and unrelated elephants, concluding:

Combined with earlier work and the data of other scientists it leads to the conclusion that elephants have a generalized response to suffering and death of conspecifics and that this is not restricted to kin. It is an example of how elephants and humans may share emotions, such as compassion, and have an awareness and interest about death.

Grace visiting Eleanor's body (photo: Douglas-Hamilton, et al)

In another paper4, Karen McComb, Lucy Baker and Cynthia Moss described experiments in which they assessed elephants’ strong interest in and sometimes dramatic reactions to elephant bones and tusks. After systematically presenting elephants in Amboseli National Park in Kenya with different combinations of elephant and other animal skulls, ivory and pieces of wood, the researchers found that the elephants were significantly more interested in elephant skulls and tusks than they were in the skulls of other animals or in the wood, but that they did not demonstrate a special affinity to the skulls or ivory of deceased relatives. The following video provides a nice glimpse into the way in which elephants seem to be fascinated by elephant bones and tusks:

Several reports have also documented cetaceans reacting with apparent grief. In one report5, for example, Mark Simmonds described an incident in which two male orcas appeared to grieve over the death of a female orca thought to be their mother. For years, the two males had spent all their time swimming with this female. After her death, the males were seen swimming together but apart from all other orcas for a day or two, repeatedly visiting the places that their mother had passed in her last few days. In another instance, Robin Baird of the Cascadia Research Collective reported seeing two orcas, a mother and adult son, swimming with a dead calf in the Puget Sound, with the mother balancing the calf on her rostrum or carrying it on top of her head and occasionally lifting it out of the water, and both adults diving deep to recover the baby when it began sinking.

Dolphin and calf (Tethys Research)

Scientists at the Tethys Research Institute related a similar occurrence off the coast of Greece, where a mother bottlenose dolphin was seen interacting with a dead newborn calf. Their description vividly underscores the difficulties in evaluating these sorts of situations from a scientific perspective:

Whilst researchers must avoid being driven by their own feelings and make arbitrary interpretations, in this case it was quite clear that the mother was mourning. She seemed to be unable to accept the death, and was behaving as if there was any hope of rescuing her calf. She lifted the little corpse above the surface, in an apparent late attempt to let the calf breath. She also pushed the calf underwater, perhaps hoping that the baby could dive again. These behaviours were repeated over and over again, and sometimes frantically, during two days of observation.

The mother did never separate from her calf. From the boat, researchers and volunteers could hear heartbreaking cries while she touched her offspring with the rostrum and pectoral fins. Witnessing such desperate behaviour was a shocking experience for those on board the research boat.

Finally, Marc Bekoff (he of the Yellow Snow fame) has written an eloquent article that includes many additional anecdotes regarding animal grief in his Psychology Today column.

Ultimately, there is much we will never be able to understand regarding how animals experience the world. We can trace commonalities between human and other animal brain structures and neural pathways associated with emotional experiences, and we can try to add more systematic observations to our collection of behavioral anecdotes, but in some fundamental ways the animal mind (and, for that matter, the mind of other humans) will always be cloaked in private experience, inaccessible to us. Moreover, as some of the accounts in this post have illustrated, our attempts at understanding animal emotions are inevitably colored by our own human experiences. We can know human grief, but how can we understand what it means to experience chimp grief, or elephant grief, or orca grief?

Nevertheless, just because we cannot fully comprehend what we see in other animals, that does not mean that grief in animals does not exist or that animals cannot lead rich emotional lives. Indeed, what we do see is a pattern that makes it increasing clear that death can impact other animals profoundly.

How do I know this? Just ask Moose, Puggsley or Wednesday – I just know.

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ResearchBlogging.org1Biro, D., Humle, T., Koops, K., Sousa, C., Hayashi, M., & Matsuzawa, T. (2010). Chimpanzee mothers at Bossou, Guinea carry the mummified remains of their dead infants Current Biology, 20 (8) DOI: 10.1016/j.cub.2010.02.031.

2Anderson, J., Gillies, A., & Lock, L. (2010). Pan thanatology Current Biology, 20 (8) DOI: 10.1016/j.cub.2010.02.010.

3Douglas-Hamilton, I., Bhalla, S., Wittemyer, G., & Vollrath, F. (2006). Behavioural reactions of elephants towards a dying and deceased matriarch Applied Animal Behaviour Science, 100 (1-2), 87-102 DOI: 10.1016/j.applanim.2006.04.014.

4McComb, K., Baker, L., & Moss, C. (2006). African elephants show high levels of interest in the skulls and ivory of their own species Biology Letters, 2 (1), 26-28 DOI: 10.1098/rsbl.2005.0400.

5Simmonds, M. (2006). Into the brains of whales Applied Animal Behaviour Science, 100 (1-2), 103-116 DOI: 10.1016/j.applanim.2006.04.015.

Multi-Modal Monkey Memory

Recognizing someone you know is actually not a simple cognitive task – it requires you interpret the information you’re currently receiving through your senses, and then link back to a previously-formed conceptual representation you have of the individual in question. It’s especially difficult if you are acting cross-modally, for example matching someone’s voice to a photograph or vice versa.

Oh yeah, I remember him. He's the one with the high squeaky voice, isn't he? (photo credit: Joe Kegley)

Recently, two separate studies have shown that rhesus macaque monkeys (Macaca mulatta) are quite up to this challenge, reflecting that they possess a considerable degree of social memory and engage in complex conceptual thinking about other individuals.

French Pictures

In the first study1, published earlier this year in Proceedings of the National Academy of Sciences, a French research team headed by Julian Sliwa of the University of Lyon confirmed that rhesus macaques are able to spontaneously match the faces of known macaques and humans to their voices.

In their experiments, the research team gave six macaques a large number of tests in which they played short voice samples of known individuals (coos and grunts for other macaques, short French sentences and phrases for humans) and then measured how long the macaques spontaneously looked at cropped photographs of two known faces, only one of which matched the voice they had heard. The researchers statistically analyzed whether the macaques spent more time looking at specific photos after hearing the matching voice than they did after hearing a different voice, and found that the macaques did indeed stare significantly longer at a photo – whether of another macaque or a human – if the matching voice had been played first.

In reviewing individual performance, the researchers observed that five of six of the macaques displayed this effect overall, and that a greater number were better at recognizing photos that matched human voices than ones matching the voices of fellow macaques (the researchers noted that they were surprised at this finding, but pointed out that perhaps the explanation was that there were more useful auditory cues in the human speech samples than there were in the monkey coo vocalizations). Finally, the researchers found that five of the six monkeys showed preferences for specific faces, spending an especially long time looking at matching” photos of certain individuals – often a “neighbor” monkey or the researcher who was their main caregiver.

The researchers concluded that rhesus macaques can recognize individuals, linking together abbreviated visual and auditory perceptual cues (small, two-dimensional photos and short sound samples) to spontaneously identify other macaques and socially-relevant humans, and even to reflect the preference biases they have towards specific individuals.

At the Movies

The second study2, published last week in PLOS ONE, extended the findings to show that rhesus macaques can also recognize photos of other macaques whom they had seen during video clips, an additional challenge because specific features can be harder to identify in dynamic movies than in still images.

In this study, researchers led by Ikuma Adachi of the Yerkes National Primate Research Center began by training five macaques to watch brief silent video clips of familiar individuals before identifying which of five randomly placed photos represented the individual in the video. At first the macaques were allowed to continue to look at the last frame of the video before having to choose the correct photo, but in a second phase of the experiment the screen went black after the video was played, and the monkeys had to choose the correct photo after a time lag.

In each case the macaques became proficient at the task, even performing well after seeing videos taken from a novel perspective that was substantially different than the view in the training videos. Thus, their performance suggested that they were able to recognize specific features of known individuals as they appeared in dynamically-changing scenes in a range of videos, and then extract that information to identify those individuals later on in still images.

Next, the researchers repeated the testing, but this time they tweaked the conditions by playing a brief vocalization right after showing the last frame of the some of the videos – either a vocalization of the macaque in the video (the “congruent condition”) or of a different macaque (the “incongruent condition”). Only two of the macaques participated in this testing, as apparently the other three weren’t comfortable with working in the sound isolation booth necessary for this phase.

The researchers found that the macaques, who had never been trained to use vocalizations to guide their test responses, continued to be good at choosing the “correct” photo, but that when they made errors, they were statistically more likely than chance to pick the image of the vocalizing monkey, rather than the one in the video.

In other words, hearing the vocalizations systematically biased the macaques’ choice behavior, indicating that the voices may have activated visual representations of the vocalizing monkeys that occasionally superseded the impact of what had been seen in the video. Again, the macaques were demonstrating how they processed the information they used to recognize information cross-modally.

So, clearly “see no evil” is linked to “hear no evil” – perhaps we’ll see how “speak no evil” fits into the picture in a later post.

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ResearchBlogging.org

1Sliwa J, Duhamel JR, Pascalis O, & Wirth S (2011). Spontaneous voice-face identity matching by rhesus monkeys for familiar conspecifics and humans. Proceedings of the National Academy of Sciences of the United States of America, 108 (4), 1735-40 PMID: 21220340.

2Adachi, I., & Hampton, R. (2011). Rhesus Monkeys See Who They Hear: Spontaneous Cross-Modal Memory for Familiar Conspecifics PLoS ONE, 6 (8) DOI: 10.1371/journal.pone.0023345.

Pantomiming Primates

When considering language abilities in non-human animals, it pays to keep in mind that spoken words are not the only path to sophisticated communication. For example, while great apes like chimpanzees and orangutans may be limited in their ability to adapt their vocalizations to human speech, they are able to control their hand movements very well, and can engage in extremely expressive and effective gesturing behavior.

In a thought-provoking study first published online last year and now appearing in the August 23, 2011 issue of Biology Letters1, two Canadian researchers, Anne Russon of Glendon College and Kristin Andrews of York University, reported on their extensive review of data regarding instances in which orangutans in Borneo have used “pantomime” to communicate with their target audiences.

What part of "give me more food" don't you understand? (photo credit: Tom Low)

Russon and Andrews mined 20 years’ data that had been collected during systematic observational studies on the behavior of ex-captive orangutans as they underwent rehabilitation and were living free or semi-free lives in the forest. After reviewing original field notes and videos covering over 7,000 hours of observation, they identified 18 salient pantomime cases (14 addressed to humans and four to other orangutans) in which orangutans physically acted out messages in order to communicate specific goals.

In most of the cases, the orangutans used pantomime to provide additional or better information after an initial attempt at communication had failed – for example, by being more specific about an action, item or tool requested; by offering better tools for a requested task after a previous tool had been ignored; by pretending to be unable to perform a task after a request for help had been ignored; or by clarifying friendly intent after non-aggressive approaches had been refused.

A few specific examples will help to illustrate how the orangutans used pantomime to achieve specific communication goals:

  • An adolescent female named Siti, who had partially opened and eaten a coconut, handed it to a technician who in turn handed it back to her, gesturing to her that she should finish the job. She proceeded to briefly, weakly and ineffectively poke at the coconut (very much in contrast to her prior behavior), before handing it back to the technician. When he again refused to help her, she used a palm petiole (stalk) to chop at the coconut repeatedly, as one would with a machete. Russon and Andrews described their interpretation of the incident in the data supplement to their paper:

After [the technician’s] first refusal she faked inability to do the job herself; after the second refusal she elaborated her request by acting out what she wanted done, specifying what tool and target to use and how to use the tool.  She acted out the actions she wanted of her partner, which included a skill that was not in her own repertoire (machete use).  Given the complex conjunction of conditions and the specificity of her request, Siti’s pantomime must have been invented on the spot even if she was familiar with all constituent elements.

Fortunately, you can see this incident for yourself, as there’s a video of Siti and the coconut – enjoy!

  • After a three year old female named Kikan had hurt her foot on a sharp stone, a research assistant removed the stone and dripped latex from the stem of a fig leaf on the wound to help make it heal faster. After that, Kikan (who had previously not been particularly friendly with the assistant, hitting or trying to bite her when she passed by) approached the assistant in a friendly manner on a number of occasions, holding up her wounded foot for the assistant to see. On one specific occasion, Kikan picked up a leaf, pulled the assistant’s hand until she paid attention, and then acted out the leaf treatment the assistant had given to the foot. (This is not only interesting for its communication content, but it could be an indication of episodic-like memory (mental time travel), a topic that Felicity Muth recently discussed in some detail in two Scientific American blog posts, here and here).
  • An adult female named Unyuk played with forest assistant who pretended to give her a haircut with a Swiss Army Knife. While they played she noticed a backpack, an item regularly stolen by orangutans in hopes of finding food. Unyuk made no immediate move for the pack – instead she continued to act out her role in the haircutting game, grabbing the hair on top of her head and inviting the assistant to continue playing as she gradually moved sidewise and closer to the pack. Once she had a free path, she lunged and made a grab for the unattended pack. (This was one of seven pantomimes that the researchers labeled as deceptive, where the actor feigned an inability, an interest or an intent in order to obtain help, distract, or express friendly intent and facilitate reconciliation.)

Russon and Andrews believe that some of the pantomime cases contain attributes of natural language:

including compositionality (large meaningful units are composed of smaller meaningful units…), systematicity (the actions and entities pantomimed are meaningfully rearranged following predictable patterns…) and productivity (…unique creations of the moment). Thus, orangutans can communicate content with propositional structure and have the kind of cognitive capacities with constituent structure typically associated with linguistic capacities.

Although spontaneous pantomiming appears to be fairly rare among orangutans (again, a total of 18 examples were unearthed from 20 years’ of data), the underlying data came from studies that were not focused on communication, and the researchers believe that other studies may have missed similar pantomiming to the extent that they focused on the functional aspects of gestures rather than the significance of pantomime as a medium for communication.

In any event, the study offers an eye-opening lesson in how sophisticated – to the point of being linguistic – non-verbal communication can be. If nothing else, we should not be too overconfident if we ever have a chance to play charades against a team of orangutans.

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1Russon, A., & Andrews, K. (2010). Orangutan pantomime: elaborating the message Biology Letters, 7 (4), 627-630 DOI: 10.1098/rsbl.2010.0564.

On the Branch of a Tree, Not at the Top of a Ladder

Every so often, it’s good to see something clearly illustrating that it’s not all about us, that evolution doesn’t simply progress its way up a ladder, climbing ever higher until it reaches humans on the top rung.

Genetic comparisons offer one such clear illustration.

For example, now that we’ve fully sequenced the human and chimpanzee genomes, we can take a close look at the different paths our genes have travelled during the six or seven million years since we parted ways from a common ancestor. In that time, humans and chimpanzees have plainly diverged quite a bit — on the one hand, humans have learned to walk on two legs, experienced dramatic growth in brain size, and now excel at speech, language and a whole host of cognitive functions; on the other hand, although chimpanzees are clearly intelligent primates, they still retain many of the physical and behavioral characteristics that they had millions of years ago.

Obviously, then, our genes have undergone the greater process of Darwinian natural selection … right?

Wrong.

The Human-Chimpanzee Genome Comparison

Do you think those humans are ever going to evolve like us? (photo credit: Delphine Bruyere)

A team of researchers led by Margaret Bakewell and Jianzhi Zhang of the University of Michigan1 decided to systematically compare the human and chimpanzee genomes to find out which species’ lineage has undergone more positive Darwinian selection over time. In essence, they lined up the two genomes to identify where they differed, and then used the DNA of the rhesus macaque, which shares an older ancestor with each of us, to figure out whether differences were due to changes in the human or in the chimpanzee DNA.

Moreover, since some DNA changes have no impact on protein production, the team was able to use statistical methods to look at the changes that do impact protein production and identify which of these were positive in the sense that they conferred a survival or reproductive advantage. (Without getting into the mathematical details, genes where a disproportionate number of the DNA changes do impact protein production are the ones where positive selection is taking place.)

In all, the researchers scanned nearly 14,000 genes (greater than 50% of the genes in the primate genome), and carefully controlled for relatively quality differences in the available genomic sequences. Using their most conservative data, they identified 154 genes that were under positive selection in the human lineage and 233 in the chimpanzee lineage. In other words, chimpanzees have 51% more positively-selected genes than humans have.

The research team summed up these findings:

[I]n sharp contrast to common belief, there were more adaptive genetic changes during chimp evolution than during human evolution. Without doubt, we tend to notice and study human-specific phenotypes more than chimp-specific phenotypes, which may have resulted in the prevailing anthropocentric view on human origins.

Interestingly, the types of genes undergoing positive change are not particularly correlated to the areas where we have seen the greatest physical divergence, such as brain size. Rather, as the below charts indicate, the areas of positive selection are widely distributed through biological processes, molecular functions and tissue groups (in the charts, PSG stands for “positively selected gene”) :

What Explains the Greater Positive Selection in Chimps?

The researchers believe that the principal explanation for the findings is that, for most of the time that humans and chimpanzees have evolved separately, the average population size of chimps was 3-5 times as large as that of humans. This is significant, as population genetic theories predict that positive selection is less effective in smaller populations (i.e., in a small group there are simply fewer opportunities for the occurrence of beneficial mutations with survival and/or reproductive advantages).

Now, there are a few caveats to this story. For one, this type of comparison does not necessarily capture recent or ongoing changes that are not yet “fixed” in the genome, so recent positive changes to the human genome may have gone undetected. Also, while this analysis adds up the relative number of genes undergoing positive change, it does not take into account the fact that some changes may be more important than others, as a change to a single gene can sometimes have a dramatic impact. Also, the study focuses on changes to genes that impact the proteins that they produce, but not the way in which those genes are expressed (e.g., whether and when the genes are turned on or off), and gene expression can account for very significant differences between species.

Nevertheless, even with these caveats, this study is an eye-opener.

From a human perspective, we naturally see our distinguishing characteristics as critically important, and often assume that they reflect something special from an evolutionary standpoint. When we look closely, though, we sometimes find that our views are far more subjective than objective. From a broader perspective, we have been just a single species with (for most of our history) a relatively small population, and have accordingly undergone a correspondingly slower rate of natural selection.

Makes one wonder whether the chimps, with all of those positive genetic changes, could have evolved a way for handling debt ceilings and political consensus. Now that would be an adaptation that would come in handy these days!

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1Bakewell, M., Shi, P., & Zhang, J. (2007). More genes underwent positive selection in chimpanzee evolution than in human evolution Proceedings of the National Academy of Sciences, 104 (18), 7489-7494 DOI: 10.1073/pnas.0701705104

Chimps Don’t Ape Humans – Develop Tools Independently

The more we learn about the capabilities of animals, the less it seems we can claim as uniquely our own. Now it appears that we may even have to share our treasured Flintstones cartoons, as we have learned that we aren’t the only species to have enjoyed an ancient Stone Age history.

Chimp eating nuts and thinking about upcoming Chimpanzee Iron Age

A few years ago, archeologists led by Julio Mercader of the University of Calgary discovered that chimpanzees in West Africa were using stone tools to crack nuts thousands of years ago, before humans had begun engaging in agriculture in the area. The research team, exploring sites located in the Ivory Coast’s Taï National Park, found stone “hammers” that were 4,300 years old and that had all the hallmarks of chimpanzee tools, rather than human ones. Science 2.01 described the tool findings as follows:

The stone hammers that the team discovered, essentially irregularly shaped rocks about the size of cantaloupes – with distinctive patterns of wear – were used to crack the shells of nuts. The research demonstrates conclusively that the artifacts couldn’t have been the result of natural erosion or used by humans. The stones are too large for humans to use easily and they also have the starch residue from several nuts known to be staples in the chimpanzee diet, but not the human diet.

The research team elaborated further in the paper it published in the Proceedings of the National Academy of Sciences2:

This discovery speaks of true prehistoric great ape behavior that predates the onset of agriculture in this part of Africa. The chimpanzee assemblages are contemporaneous with the local Later Stone Age; thus, they represent a parallel “Chimpanzee Stone Age”….

The systematic archaeological study of prehistoric chimpanzee cultures suggests that the “Chimpanzee Stone Age” started at least 4,300 years ago, that nut-cracking behavior in the Taï forest has been transmitted over the course of >200 generations, and that chimpanzee material culture has a long prehistory whose deep roots are only beginning to be uncovered. These findings substantiate the contribution of rainforest archaeology to human evolutionary studies in areas other than the classical savanna-woodlands of East and Southern Africa and add support to fossil discoveries from these other regions indicative of an ancient chimpanzee past.

I love it: the Chimpanzee Stone Age! Also, it’s amazing that this tool use tradition has been passed down over 200 generations, and is still in use today.  Here’s a nice BBC video clip that shows today’s generation of chimps using the same sort of tools to expertly crack open nuts.

Archeology3, the official publication of the Archeological Institute of America, haled Mercader’s research as one of the “Top 10 Discoveries” of 2007, noting that:

The discovery shows that stone tool use is not a behavior that chimpanzees learned recently by watching the farmers who live in the area, as some skeptics believe. Mercader thinks that humans and chimpanzees may have inherited stone tool use from an ancestral species of ape that lived as long as 14 million years ago.

At this point, Mercader’s views on the origins of tool use are still open to debate and further research. The fact, though, that there can even be such a discussion about tool use, a capability once thought to so uniquely identify the human species, illuminates how much thinking we have had to do recently about the common characteristics we share with other animals. Interesting stuff.

We’ll keep you posted as the story unfolds, and let you know as soon as they discover the first prehistoric chimpanzee satellite TV dishes and computer operating systems.

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1Science 2.0, “Hammer Using Chimps Make Us Wonder Where They Learned It,” February 13, 2007.

2Mercader, J., Barton, H., Gillespie, J., Harris, J., Kuhn, S., Tyler, R., & Boesch, C. (2007). 4,300-Year-old chimpanzee sites and the origins of percussive stone technology Proceedings of the National Academy of Sciences, 104 (9), 3043-3048 DOI: 10.1073/pnas.0607909104.

3Archeology, “Ancient Chimpanzee Tool Use,” Volume 61, Number 1, January/February 2008.

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