Also, dog owners frequently describe how smart their cold-nosed friends are, how they know the words for large numbers of toys and other objects, and how they understand and sometimes obey numerous commands. (Good dog!) However, while there have been many studies investigating the linguistic abilities of primates, cetaceans, parrots and certain other species, there has been surprising little formal research into the verbal comprehension of dogs. Dogs have been tested for their understanding of specific words and commands, but there has been an absence of research into whether they can understand and distinguish the constituent parts of complex sentences that refer both to objects (e.g., “ball,” “stick” or “newspaper”) and to actions (e.g., “fetch,” “roll over,” or “point”).

Until recently, that is.

Chasing Down Linguistic Meaning

First, in 2011, John Pilley and Alliston Reid published a paper in Behavioural Processes detailing a variety of word comprehension tests that they had given to Chaser, a rock star border collie famous for knowing the names of over 1,000 objects.

In one of these experiments, Pilley and Reid tested whether Chaser could independently understand the meanings of verbs and nouns. In this test, Chaser was asked to respond appropriately when three different commands (take, paw, and nose) were randomly associated with three different stuffed cloth toys (Lips, a toy resembling human lips; ABC, a cloth cube with those letters written on its side; and Lamb, a stuffed lamb) in 14 independent trials using a double-blind procedure. Chaser was familiar with the commands, but none of the three toys had ever been paired with any of the commands prior to the experiment.

The three toys were lined up on a soft pad in front of a one-meter high cloth barrier. During the trials, neither Chaser nor the experimenter could see each other, as the experimenter knelt on one side of the barrier, with Chaser hanging out with the toys on the other side. The experimenter, who had been given a toy and command combination generated with a random number table, gave Chaser his instructions, while a confederate sat to the side where she could see Chaser perform and signal to the experimenter with a hand wave when the trial was over. Here’s a picture of the setup, taken before the experimenter retreated to the other side of the barrier to commence the trial (note that the confederate’s legs are visible to the right of the picture):

The tests were videotaped with sound recording, with three independent raters (not the experimenter or the confederate) scoring whether Chaser chose the correct toy and performed the correct command. Each rater first watched the videotape with the sound turned off (so he/she wouldn’t know which instructions had been given to Chaser), and recorded which command was actually executed towards which toy. After rating all 14 trials, the rater then watched each trial again with the sound turned on in order to assess whether Chaser’s behavior accurately matched the instructions given by the experimenter.

How did Chaser do? Perfectly.

There was absolutely no disagreement among the raters – each judged Chaser to be 100% accurate across the 14 trials, performing the correct command to the correct toy as instructed. As Pilley and Reid put it:

These results clearly support the conclusion that Chaser understood reference – that the verbal noun of an object referred to a particular object with distinct physical features independent of actions directed toward that object.

Comprehending Sentences

Then, earlier this month, Daniel Ramos and Cesar Ades of the University of São Paulo published a study in PLoS One that extended the Chaser research.

In their study, Ramos and Ades tested Sofia, a female mongrel dog, on two-item requests over a two year period, starting when she was a two-month old puppy. The testing consisted of eight progressive phases, during which Sofia first learned some basic vocabulary and then gradually faced increasingly complex tests of her comprehension abilities. The specific phases were as follows:

1. Learn the names for four objects (ball, key, bottle and stick) and two requests (point or fetch).
2. When presented with two objects, approach the correct object on request, or perform the correct action upon request.
3. Perform object and action requests in sequence – that is, first approach the proper object after being given an initial “object request” and then, after being given an “action request,” perform the correct action on the object.
4. Perform single multi-part requests – that is, after being given a compound request (e.g., ball fetch, ball point, key fetch, key point, bottle fetch and stick point), approach the correct object and perform the correct action.
5. To eliminate the possibility of inadvertent cues from the experimenter, perform the same tests as in phase 4 but with the following control variations: (1) experimenter wearing sun-glasses, (2) experimenter with mouth covered by a cloth band, (3) research assistant absent from the room, (4) unfamiliar person as experimenter, (5) testing in an unfamiliar room, (6) test objects scattered, distant from one another, and (7) new objects of the same category (new balls, keys, etc.) offered.
6. Perform reversed multi-part requests – that is, in response to compound requests in which the word order has been switched from object-action to action-object (e.g., fetch ball, point ball, fetch key, point key, fetch bottle and point stick), approach the correct object and perform the correct action just as in phase 4.
7. Perform multi-part requests with a new, previously-untested object, a teddy bear.
8. Perform multi-part requests with new combination object-action pairs (stick fetch and bottle point) that had not been used at all during prior training or tests.

And how did Sofia do? Well, she wasn’t perfect like Chaser, but she was pretty impressive. Her success rate was significantly above chance in all phases except for the final one, in which she had only 3 out of 10 correct responses for both the stick fetch and the bottle point requests. Notwithstanding this one area of underperformance, Ramos and Ades concluded:

Our results suggest that dogs share with “linguistic” animals the capacity to encode in memory at least two heterogeneous items of information to be used in subsequent directed performance, a capacity which, although far from being “an infinite use of finite means” as human grammars are, may have comparative relevance as a forerunner to syntactical functioning.

Now, I know what you are saying. Yes, your dog can do that too. I’m aware that she consistently beats you and your friends at poker, and I’ve seen the video where she plays charades while riding around your house on a Roomba.

You see, that’s actually the issue. Dogs are incredibly good at picking up human signals, which is why carefully-designed experiments are important in ruling out the “Clever Hans” effect (named after a horse who, more than a century ago, amazed crowds with his apparent mathematic abilities, but who was ultimately found to be picking up on involuntary body language cues from his trainer).

By eliminating visual contact between Chaser, Sofia and the experimenters and by adding controls such as having unfamiliar persons issue requests and moving around the objects, the researchers ensured that the dogs had to rely exclusively on words rather than on inadvertent human signals or other contextual clues. By changing the size, shape and color of the requested objects and introducing a new object (the teddy bear), the researchers were able to test whether Sofia was able to generalize and apply concepts to new objects in the same category. By reversing word order and thereby changing the acoustics of compound requests, the researchers were able to rule out the possibility that Sofia was performing based on memorizing the sound properties of requests rather than actually understanding the individual words comprising the requests.

So, you were right all along – your dog really does understand you. The problem is everyone else.

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Pilley, J., & Reid, A. (2011). Border collie comprehends object names as verbal referents Behavioural Processes, 86 (2), 184-195 DOI: 10.1016/j.beproc.2010.11.007.

Ramos, D., & Ades, C. (2012). Two-Item Sentence Comprehension by a Dog (Canis familiaris) PLoS ONE, 7 (2) DOI: 10.1371/journal.pone.0029689.

Many social animals are able to solve problems and shortcut the costly process of trial and error learning by simply observing the behavior of their peers. While some have speculated that this type of observational learning is an adaptation for social living that may be unique to animals who live together in groups, a research team led by Anna Wilkinson of the University of Vienna wanted to see whether a decidedly non-social animal, the red-footed tortoise, could also learn by observing others. Wilkinson specifically hoped to test the hypothesis that social learning abilities may simply be a reflection of an animal’s general learning capacity, and that non-social animals may be able to learn by observing peer behavior in fundamentally the same way as they use other environmental stimuli to learn.

Finally – respect for my brains as well as my dashing good looks!

The red-footed tortoises were perfect subjects for this study. The natives of Central and South American forests are naturally solitary, receiving no parental care (once the eggs hatch, it’s every little tortoise for himself and herself!) and, unless presented with a mating opportunity, living apart from other tortoises.

For Wilkinson’s study, eight young (juvenile or sub-adult) tortoises – four randomly assigned to the “non-observer” condition and the other four assigned to the “observer” condition – participated in a series of trials in which they needed to navigate around an obstacle to achieve a food reward. All trials took place in a square arena in which a 40 cm high V-shaped fence separated the tortoise from the desired food:

First, the tortoises in the non-observer groups were each given 12 trials (one per day) in which they were allowed two minutes to solve the task. Between trials, the bark flooring in the arena was redistributed to prevent the tortoises from being able to latch onto any scent trails from prior trials.

Next, the observer group tortoises had their turn. Their trials were identical except that, before each test, they were able to observe a specially-trained tortoise who invariably detoured around the right side of the obstacle and ate the food prize.

The results were unambiguous. While none of the non-observer tortoises ever solved the puzzle (they went up to the fence by the food, but never figured out how to go around the obstacle), all of the observer tortoises succeeded at least twice, with two of them correctly navigating around the barrier on the first attempt.

In other words, the red-footed tortoises have another addition for their trophy room. Not only are they the first red-footed and hard-shelled recipients of the Ig Nobel Prize, they are also the first non-social reptile to display social learning skills, revealing that group living is not necessarily a prerequisite for social learning.

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Wilkinson, A., Kuenstner, K., Mueller, J., & Huber, L. (2010). Social learning in a non-social reptile (Geochelone carbonaria) Biology Letters, 6 (5), 614-616 DOI: 10.1098/rsbl.2010.0092.

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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Hassett, 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.

It’s far less common, though, to find relationships where non-humans participate on a more equal footing, where they appear to train us at least as much as we train them. (People who are owned by cats should feel free to rebut this statement in the comment section below.)

Today’s post features one such relationship, the partnership between humans and the greater honeyguide (Indicator indicator), a bird that lives in the trees of sub-Saharan Africa.

Honeyguides and humans have very complementary appetites. Honeyguides get most of their food from beehives, feasting on larvae and wax that they extract from honeycombs (yes, they actually eat and can digest the wax!). Of course humans, too, seek out beehives, although our interest lies more in the bees’ sweet honey, and we’re generally more than happy to leave the wax and grubs for others to enjoy.

The bee-related skills of humans and honeyguides are relatively complementary as well. Honeyguides can fly swiftly across large areas and are expert at locating bee colonies, but have difficulty in extricating the combs on their own. Humans move more slowly along the ground and aren’t so adept at finding colonies, but once we have one in our sights, we’re able to overcome bee defenses and dig the combs out, even when the bees have nested deep within rock crevices and other hard-to-reach locations.

Out of this opportunity for mutualistic benefit, honeyguides and humans have worked out an elaborate interspecies communication system that allows them to work in tandem with certain signals understood by both parties.  This partnership has been formally documented in a three year field study conducted in the dry bush country of northern Kenya, focusing on the interactions between honeyguides and the nomadic Boran people who populate the area.

Each partner knows how to get the other’s attention. To attract the birds, the Borans call them with a penetrating whistle (known in the Boran language as Fuulido) that can be heard over a distances of greater than a kilometer and that is made by blowing air into clasped fists, modified snail shells, or hollowed-out palm nuts. Comparably, hungry honeyguides flag down humans by flying up close, moving restlessly from perch to perch, and emitting a double-noted, persistent “tirr-tirr-tirr-tirr” call. (Side note: I’ve been practicing this at home, and it doesn’t seem to attract much other than odd stares and raised eyebrows.)

The joint food expedition commences when the honeyguide flies briefly out of sight and then returns to a nearby, conspicuously visible perch. When the human companion approaches this perch, the honeyguide takes off, displaying its white outer tail feathers, and flies to a new resting place a short distance away, calling loudly when it lands. The Boran partner then approaches the new perch and the bird flies off again, repeating the pattern. As the Borans work with the bird, they whistle and shout to keep the bird interested in guiding. (Again, this doesn’t seem to work too well at home.)

The researchers found that the honeyguides signal the path and distance to the bee colony in a variety of ways. First, they indicate the correct direction through their flight paths, traveling consistently in the direction of the nest and increasing their precision as they near the target. It appears that the know in advance where the nests are located, as the researchers observed the honeyguides briefly visiting nests before dawn, peering into the entrances while it was still dark and the bees were docile.

Also, the honeyguides vary their behavior depending on distance to the hive. For example, when the hive is relatively distant, the birds begin the process with a relatively long disappearance during their first flight; conversely, their first disappearance is briefer when the hive is relatively nearby. Further, the honeyguides stop more frequently and the legs between perches become shorter as they and their human followers approach the nest, especially during the last 200 meters. Finally, the honeyguides select increasingly lower perches as they close in on the colony.

Upon arrival at the destination, the honeyguides perch close to the nest and emits an “indication call.” The researchers describe the scene as follows:

This call differs from the previous guiding call in that it has a softer tone, with longer intervals between successive notes. There is also a diminished response, if any at all, to whistling and shouting by humans. After a few indication calls, the bird remains silent. When approached by the searching gatherer, it flies to another perch close by, sometimes after circling around the nest. The resulting flight path finally reveals the location of the colony to the gatherer. If the honey collector does not (or pretends not to) detect the nest, the bird gives up after a while. It may then leave the area either silently or start a guiding session to another colony. In the latter case, it switches from the indication call to the guiding call and resumes a fairly direct flight pattern. Once the human team members find the nest, it becomes their turn to go to work and hold up their part of the bargain. After using smoky fires to reduce the bees’ aggression, the Boran honey gatherers use tools or their hands to remove the honey comb, and then break off pieces to be shared with their honeyguide partners.

To sum things up, here’s a great BBC video (featuring David Attenborough!) that describes the bird-human partnership and shows the honeyguides in action:

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Isack, H., & Reyer, H. (1989). Honeyguides and Honey Gatherers: Interspecific Communication in a Symbiotic Relationship Science, 243 (4896), 1343-1346 DOI: 10.1126/science.243.4896.1343.

Word of our mammal-centric coverage seems to have reached the small, oval ears of the always-influential parrot lobby, though, as just last week the journal Behavioural Processes published a study describing social yawning in budgerigars (Melopsittacus undulatus), the small Australian parrot often referred to as the parakeet. This study provides the first support for contagious yawning in a non-mammal, and even ups the ante by documenting what may be the first instance of contagious stretching, another stereotyped behavior that may play a social role for certain animals. Some may say that the paper’s timing is an utter coincidence and that only someone with delusions of grandeur would believe that it was even remotely linked to the AnimalWise post. We, speaking in our usual royal manner, prefer to think otherwise.

Fascinating, simply fascinating...

Michael Miller, Andrew Gallup and other researchers from the University of the Binghamton conducted an observational study of yawning and stretching in a group of approximately 20 adult male and female budgerigars living together in an aviary as an established flock. Over a period of about a year and a half, the research team video recorded the flock on 23 separate occasions. The recording sessions, each of which lasted 90 minutes, were conducted at varying times of the day, and the researchers took a number of precautions (such as ignoring the first 15 minutes of each tape) to ensure that the flock’s behavior was as natural and undisturbed as possible. Trained reviewers then systematically reviewed all of the tapes, recording the time and occurrence of each yawn and stretch, and categorizing each stretch by whether the bird extended one or both legs.

The researchers’ hypothesis was that, if yawning and stretching were spreading contagiously among the birds, the behaviors would occur in nonrandom “clumps” – that is, rather than being evenly dispersed throughout the recording sessions, multiple yawns (or multiple stretches of the same type) would take place in closely-spaced bouts and then be followed by a long interval until a new priming behavior triggered another bout. Further, they predicted that, although there might be might be overall tendencies tied to particular times of the day (for example, the budgerigars might, on average, yawn more frequently during evening sessions), if the yawning and stretching really were being triggered contagiously, then specific clumping patterns would not repeat themselves when multiple same-time-of-day sessions were compared.

To test their hypotheses, the researchers performed detailed, session-by-session analyses of each type of behavior. For example, they tallied how frequently each behavior occurred, measured the time between adjacent stretches and yawns, and sorted the adjacent pairs into different “bins” depending on the length of the interval. They also analyzed each session for clumping by breaking it down into a large number of short (20 to 30 second) intervals, which allowed them to identify “runs” of consecutive intervals that either did, or did not, contain the behavior in question. Finally, they statistically analyzed their data in a variety of ways to identify patterns and associations.

And the results?

Both yawning and stretching behaviors were indeed clustered within trials, and the period between adjacent yawns and stretches was “strongly biased toward very short (< 20 sec) and very long (> 300 sec) intervals,” especially for the yawns. Also, as hypothesized, despite the clustering for both behaviors, “neither behavior routinely occurred at specific times from the start of a session across multiple recordings at the same time of day. This suggests that the clumping of these behaviors was due to social influences, and not to underlying physiological effects as a result of similar circadian patterns.”

The research team summarized its findings and suggested directions for future investigation as follows:

The observational results presented here suggest that yawning and stretching are at least mildly contagious in budgerigars under semi-natural flock-living conditions. In line with each behavior’s presumed physiological function, contagious yawning and stretching may ultimately coordinate mental state and a group’s collective movements, but future research needs to test these predictions.

So, kudos to the budgerigars! Parrots everywhere can take pride in these findings, which point to previously-unknown areas of avian social signaling and coordination, and which may open up new avenues for studying collective behavior.

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Miller, M., Gallup, A., Vogel, A., Vicario, S., & Clark, A. (2011). Evidence for contagious behaviors in budgerigars (Melopsittacus undulatus): An observational study of yawning and stretching Behavioural Processes DOI: 10.1016/j.beproc.2011.12.012.

“Liebster” is a German word meaning dearest, beloved or favorite, and the Liebster Award is sort of a chain letter among bloggers that’s intended to showcase exceptional up-and-coming blogs (typically, those with 200 or fewer followers). Now, there’s no evaluation committee or formal award process for the Liebster, but in a way it’s even nicer – it’s recognition that a peer has noticed and appreciated your hard work.

I want to thank Mary very much for the recognition. Please check out her blog, which – with good reason – has already received the Liebster Award. Mary writes engagingly about biology, psychology, neuroscience, ecology, and all flavors of animal behavior. She earned her PhD from Brown University, where she researched bat echolocation and bullfrog chorusing (admit it, you’re jealous!). While you’re there, be sure to watch the video she’s posted about Li’l Drac, the adorable baby bat; you’ll be adopting your very own fruit bat before long.

Now, the rules for the Liebster Award are:

1. Show thanks to the blogger who gave you the award by linking back to them.
2. Reveal your top five picks and let them know by leaving a comment on their blog.
3. Post the award on your blog.
4. Bask in the love from some of the most supportive people on the internet—other writers and artists.
5. And best of all – have fun and spread the karma.

Without further ado, here are my five nominees:

• Endless Forms Most Beautiful: Kimberly Gerson captures and expresses the wonders she sees in the natural world vividly and with grace. Be sure to read about Romeo the wolf and what Kimberly would like you to do if she gets eaten by a polar bear.
• Inkfish: Elizabeth Preston, the editor of MUSE, the award-winning children’s science magazine, stretches out her tentacles to bring you entertaining accounts of offbeat and fascinating new research studies relating to biology, psychology, evolution, physics, economics, and everything in between. Inkfish is playful and fun, but always accurate and true to the underlying science.
• Puff the Mutant Dragon: Mutant Dragon breathes fire and writes exquisitely. The blog wraps together biology, biochemistry and history and toasts them into a delectable treat. If history was never your thing and you’ve always avoided chemical equations, I especially invite you to dig in – I think you just may find that you’ve found a new favorite cuisine!
• Popperfont: David Ng, a molecular geneticist and member of the faculty at the University of British Columbia, has created Popperfont, an eclectic mix of scientific trivia, quotations, graphics, comics, stories and other assorted gems. Stop by Popperfont whenever you’re in the mood for some science fun and fascination.
• Empirical Zeal: Aatish Bhatia, a Rutgers University grad student, shares his excitement regarding breakthroughs in diverse areas of science, including evolutionary biology, genetics, neuroscience and physics. Empirical Zeal is what great science blogging is all about: wonderful writing that makes technical topics understandable, accessible and exciting. Visit Empirical Zeal and you’ll see what I mean.

So thanks again to Mary, and I hope you enjoy the five nominee blogs as much as I do!

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

An experienced female knows this well, and plays the game accordingly. When she goes into heat – or oestrus – and attracts male suitors through chemicals in her urine, she gives impressive senior bulls the green light by holding her tail high, walking with an exaggerated gait, and exchanging affectionate trunk caresses. Lower-ranking young males don’t fare so well. She actively avoids them and, to the extent they aren’t chased off by her favored partner, she’ll often spurn their advances by running away. (Little known fact: female African elephants can typically outrun male ones.)

It’s not so easy for a young female entering oestrus for the first time. She sometimes runs from the larger musth males, who can weigh more than twice as much as her, and not infrequently ends up consorting with a series of younger, lesser males. This can lead to unfortunate results, especially when you consider that an elephant pregnancy lasts 22 months.

Now, though, there’s evidence that experienced females may help their younger relatives in sorting through the confusing tangle of elephant sexual dynamics. These helpful older elephants – sisters, aunts, mothers, and matriarchs – appear to simulate oestrus in order to show their innocent family members how to act, enabling them to avoid the pitfalls of poor mating choices.

If I said you had a beautiful trunk, would you hold it against me? (photo: WildlifeDirect, Dzanga Forest Elephants)

After hearing anecdotal accounts of this behavior, a team led by Lucy Bates of the University of St. Andrews decided to dig deeper by taking advantage of an invaluable resource – a comprehensive multi-decade database cataloging the daily life activities of 2,200 Amboseli elephants compiled by Cynthia Moss, Joyce Poole, and other researchers as part of the Amboseli Elephant Research Project (AERP).

Bates and her colleagues systematically combed through 28 years of detailed AERP records and located all occasions on which an observer had concluded that an identifiable elephant was in oestrus (based on postural and behavioral changes in females, interactions with males, etc.). In total, they found descriptions of 999 oestrus events, slightly less than 10% of which (98 events) recorded two or more members of the same elephant family displaying simultaneous oestrus behavior.

Next, the researchers cross-referenced these accounts with AERP demographic records to find any that must have been “false” oestrus events, which they defined as oestrus-like behavior by a female who was either already pregnant, in a state of lactation-induced infertility, or senescent (which they deemed to be the case if she was over 50 years old, had not given birth to any calves during the prior five years, and had no subsequent calves).

They discovered that, while false oestrus behavior was relatively rare (occurring only 19 times and representing only about 2% of all recorded oestrus events), its timing was fascinating. Very often, it occurred just when a young relative was coming into oestrus for the first time.

Even though simultaneous oestrus behavior had been recorded less than 10% of the time, over half of the false oestrus events (10/19) clearly occurred at the same time as the true oestrus of a young female family member who had never given birth. Further, subsequent birth records confirmed that on four additional occasions a false oestrus event occurred during the month that a young relative conceived her first calf (that is, the young female must have been in oestrus at the time, even though it wasn’t specifically called out in the AERP database). Finally, one of the false oestrus events occurred simultaneously with the genuine oestrus of a female relative who had given birth before. Thus, the large majority of the false oestrus events – 15 of 19 – coincided with true oestrus events, in most cases, the first oestrus of a young relative. (Moreover, note that the balance of the false oestrus events could also have coincided with true ones if, as in the four cases described above, the true oestrus event simply had not been observed or recorded in the AERP database.)

The researchers then examined various hypotheses that might explain the false oestrus behavior:

• That false oestrus merely results from hormonal changes and has no functional purpose;
• That it somehow induces sexual receptivity in the simulating female, thereby increasing her own chances of successfully reproducing;
• That it indirectly benefits the simulating female by providing a young family member with increased access to suitable males (this type of indirect benefit is known as an inclusive fitness benefit); or
• That it indirectly benefits the simulating female by encouraging a confused younger relative to engage in more suitable oestrus behavior (another potential example of inclusive fitness).

They quickly rejected the all but the final hypothesis. For one, hormonal changes couldn’t adequately explain either the observed patterns (false oestrus occurred in both pregnant and non-pregnant females, as well as during all stages of pregnancy) or the higher-than-expected coincidence of false oestrus with the genuine oestrus events of inexperienced relatives. Second, it was clear that the simulating elephants weren’t improving their own reproductive success: in 14 of 19 cases the simulating the female was already pregnant, and in four others she was senescent. Third, AERP records revealed that false oestrus behavior had no impact on the number of available males, the relative percentage of males who were in musth, or the amount of sexual activity engaged in by inexperienced female.

Ultimately, the researchers concluded that:

Further data is required to confirm or reject the hypothesis that this behaviour functions to teach the young, naïve females, but we suggest that it remains the only viable possibility based on the current analyses.

In particular, they noted that additional research and data collection was necessary to explain the instances in which false oestrus didn’t appear to coincide with an inexperienced relative’s oestrus as well as to support the notion that inexperienced females were able to correct substandard mating behavior after they were shown what to do by their older relatives.

In the meantime, though, you’d be well advised to stay away from those frivolous young guys and find yourself a dashing older bull who knows his way around the herd.

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Bates, L., Handford, R., Lee, P., Njiraini, N., Poole, J., Sayialel, K., Sayialel, S., Moss, C., & Byrne, R. (2010). Why Do African Elephants (Loxodonta africana) Simulate Oestrus? An Analysis of Longitudinal Data PLoS ONE, 5 (4) DOI: 10.1371/journal.pone.0010052.

Because of this, I’m an absolute sucker for all of those YouTube videos of cats curling up with mice, horses who befriend sheep, elephants and dogs who are inseparable, and the like. You know the ones I mean.

Many times, though, these are artificial pairings that spring up after we humans have altered the environment, habituating or even confining the animals with one another. While these human-influenced relationships can be incredibly heartwarming, it somehow seems even more magical when animals forge connections across species boundaries in the wild, in their native habitats and without any human intervention.

With that background, I’d like to introduce a paper published last year in the journal Aquatic Mammals¹, which reports on two separate playful and – as you’ll see – uplifting encounters between bottlenose dolphins (Tursiops truncatus) and humpback whales (Megaptera novaeangliae).

The first took place on a January afternoon off the northwest coast of Kauai, when a group of eight bottlenose dolphins met up with a pair of humpback whales. Two of the dolphins – apparently adults – approached one of the whales, first appearing to surf the pressure wave created by the whale’s head as it swam, and later taking turns lying perpendicularly across the whale’s rostrum when it surfaced to breathe. Then, while one of the dolphins lay balanced over the end of its rostrum, the whale stopped and slowly lifted the dolphin high into the air. The dolphin maintained an arched position and made no effort to escape, allowing the whale to continue lifting until it was nearly vertical in the water, at which point the dolphin slid down the whale’s rostrum, dove into the water, and porpoised back to its fellow dolphins.

Here’s a color photo of the dolphin just about to go whale-sliding:

Look Ma, No Hands! (photo credit: L. Mazzuca)

And here’s a black and white series of shots that captures the full adventure sequence:

The second encounter also occurred on a January afternoon, this time off the northwest coast of Maui, when an adult female bottlenose dolphin swam up to a mother humpback whale and her calf. After diving underwater, the dolphin and mother whale resurfaced with the dolphin resting across the mother whale’s rostrum. The mother then proceeded to lift the dolphin a total of six times over 8.5 minutes, with the dolphin either lying on her stomach or right side during the lifts, which varied in length from four to 45 seconds. Again, the dolphin made no attempt to escape and held her position in such a way as to facilitate the whale’s lifting.

Here’s a sequence of photos showing this second duo demonstrating the proper technique for lifting a relaxed-looking dolphin:

The authors of the Aquatic Mammals paper considered alternate explanations for these interactions, including whether they represented an aggressive whale response to an antagonistic dolphin approach, whether the whales were demonstrating concern regarding perceived distress in the dolphins, or whether the cetaceans were simply playing together. They found the first two hypotheses to be unlikely – among other things, the interactions were too cooperative and relaxed in pace to be aggressive, and the dolphins were in good health and showed no evidence of distress. In the end, while the authors didn’t rule out the possibility that maternal instinct was involved in the whales’ lifting behavior, they concluded that the best explanation was that these were simply instances of interspecies play between the bottlenose dolphins and humpback whales.

Further, these bouts of play between dolphins and whales may not be all that uncommon, as back within the friendly confines of YouTube I was able to locate a video documenting another episode in which a bottlenose dolphin went for a ride on the rostrum of a humpback whale:

…

Play may serve a number of important purposes – for example, it may provide an avenue for intelligent, social animals like dolphins and whales to experiment with their surroundings, hone their physical skills and learn how to interact collaboratively with others. But aside from any practical evolutionary significance, I like to think of these encounters as illustrating how animals can, on occasion, take a few minutes away from the serious business of survival to share some pure joy and wonder with a fellow being, even a fellow being of a different species.

So, all of this is comforting. If dolphins and whales (and other animals who form interspecies bonds) can find a way to communicate playfulness with each other and to share experiences without any kind of a common language, perhaps we humans can do a bit better ourselves. Maybe some of the divides we see today – political discord, religious conflict, international posturing, cultural and racial inequities – aren’t so unbridgeable after all. Perhaps all we need to do is to remember an uplifting dolphin story or two.

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¹Deakos, M., Branstetter, B., Mazzuca, L., Fertl, D., & Mobley, J. (2010). Two Unusual Interactions Between a Bottlenose Dolphin (Tursiops truncatus) and a Humpback Whale (Megaptera novaeangliae) in Hawaiian Waters Aquatic Mammals, 36 (2), 121-128 DOI: 10.1578/AM.36.2.2010.121.

As reported in a paper published online last week in Behavioural Processes,¹ the caretakers decided that it was time solve the mystery. First, they hung a small plastic envelope filled with food near the name tag and watched to see what the dingoes would do. The dingoes were having none of that, however – as long as observers were around, the dingoes studiously ignored both the name tag and the envelope of food. Since the direct approach clearly wouldn’t work, the staff resorted to sneakiness, rigging up a video camera and then leaving the dingoes to their own devices.

Success! When the staff returned to the enclosure, they found that the food was gone and, more importantly, that the videotape reflected perhaps the first documented instance of tool use by a member of the Canid family. As described in the Behavioural Processes paper:

Big deal, Lassie; when Timmy fell down *my* well, I hoisted him out using a system of pulleys. (Sterling at Dingo Discovery and Research Centre, photo by Dingo Lyn)

[A]fter several unsuccessful attempts at jumping for the envelope, Sterling “solved” the task by first moving and then jumping up onto a trestle table (1.2 m × 0.6 m × 0.73 m) which allowed him to gain the additional height necessary to reach the food item. To move the table, Sterling clamped his mouth onto the strut between the legs of the table. He then walked backwards, dragging the table approximately 2 m, until it appeared that either his back leg or tail touched the enclosure mesh. He then jumped onto the table, but as he was still at least a body-length away from the envelope, he had to span the gap between the table and the enclosure mesh by propping his front paws onto the mesh gradually moving them towards the envelope. At full stretch, he reached the envelope on his second attempt.

While this account of Sterling’s actions may sound impressive, it’s even more striking when seen on video:

…

Bradley Smith of the University of South Australia and his colleagues noted in their paper that Sterling’s behavior appeared to be spontaneous – he had never been trained or encouraged to position the table in order to reach food (or name tags) – but they cautioned that they had to rely on information provided by the sanctuary’s staff regarding Sterling’s (lack of) relevant training in the past.

No problem, just bring me a socket wrench, a crow bar and three sticks of gum... (Sterling at Dingo Discovery and Research Centre, photo by Dingo Lyn)

Sterling, for his part, was no one-hit wonder. According to sanctuary staff, from an early age Sterling was adept at manipulating his environment to serve his purposes. For example, during one breeding season he used his front paws to roll a barrel to a wall, jumped up on the barrel, scrambled over the wall, and approached a female dingo in another area of the sanctuary. Also, the staff and research team later videotaped separate occasions in which Sterling used his mouth to drag a plastic dog kennel to differing locations around his enclosure, allowing him to stand on the kennel and peer over walls into neighboring dingo enclosures.

Thus, while the researchers couldn’t exclude the possibility that Sterling’s problem-solving abilities were the result of observational learning or that they had somehow been reinforced when he was younger, they rightly recognized that he appeared to be engaging in “high order behaviour” in using tools within his environment to solve complex problems. (Indeed, on the face of it, Sterling’s problem-solving is quite very reminiscent of Kandula the elephant’s insightful use of a box within his yard to solve an out-of-reach food challenge.)

So, now that you know what canines are capable of, please feel free to ask your dog Barkley when he’s going to get around to assembling that futon you bought at Ikea. No more excuses.

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¹Smith, B., Appleby, R., & Litchfield, C. (2011). Spontaneous tool-use: An observation of a dingo (Canis dingo) using a table to access an out-of-reach food reward Behavioural Processes DOI: 10.1016/j.beproc.2011.11.004.

²As we’ve noted in previous posts (see, for example, the post on the poison rat and the tuskfish tool post), scientific authorities have defined the concept of “tool use” in various ways. In the Beck and Shumaker treatise discussed in the poison rat post, the authors describe a couple of anecdotal instances that may qualify as canid tool use under their broad definition, including an account of a wolf mother who used meat as a “baiting” and “enticing” tool to distract her young pup. Fox, M. (1971). Possible Examples of High-Order Behavior in Wolves Journal of Mammalogy, 52 (3) DOI: 10.2307/1378613.

Are there any parallels in the animal world, any similarly gifted nonhuman mathematicians that have innovated with the concept of zero?

The answer seems to be yes: Alex, the male African Grey Parrot of book and movie fame (Alex & Me), may go down in history as the parrot equivalent of Albert Einstein, revolutionizing parrot mathematics with his insight into concepts of nothingness.

How many crackers do I see? None! (image: The Alex Foundation)

It was in late 2003, early 2004 that Alex appears to have had his great breakthrough regarding the mathematical usefulness of zero-like concepts. At that time, Irene Pepperberg and Jesse Gordon of Brandeis University, who had been working with Alex over an extended period on a variety of cognitive and communicative studies, decided to conduct some experiments to explore the extent of his numerical competence.

Alex already was adept at tests requiring him to identify numbers of objects – he knew the English words for one through six, and could provide accurate verbal responses to questions about, for instance, how many green blocks were included in a mixed array of blue, red and green blocks and balls. Pepperberg and Gordon now wanted to see whether Alex really understood the numbers he was providing and could grasp the interchangeability of numerical questions.

To do so, they flipped things around: rather than asking Alex to provide the number of objects in particular groupings as he had in prior experiments, they went in the other direction by asking him to indicate which object groups were associated with a particular number. That is, they presented Alex with a tray of objects of various materials, colors and shapes (for example, six green plastic spoons, four yellow tops and three orange wooden sticks), and asked him questions such as “What color six?” and “What toy four?” Alex’s task was to look at the objects on the tray and then respond correctly (in this case, with “green” based on the six green spoons and “top” based on the four yellow tops).

(I know, this all sounds a bit like Jeopardy: “Please be sure to phrase your answer in the form of a question…”)

Perhaps not surprisingly, Alex aced the test, responding correctly to this new battery of questions over 80% of the time. More significant, though, is how Alex – apparently bored with the questioning – spontaneously extended the scope of the experiment:

On the 10th trial within the first dozen, Alex was asked “What color 3?” to a set of two, three, and six objects. He replied “five”; the questioner asked him twice more and each time he replied “five.” The questioner, not attending to the tray, finally said “OK, Alex, tell me, what color 5?” Alex immediately responded “none.”

Now, Alex had previously been trained to use the word “none” in a different context – comparing objects for similarity or difference (for example, to respond to a question about which of two identically-sized objects was bigger) – but he had never been taught to use “none” to describe a quantity that was not present. Fascinated, Pepperberg and Gordon randomly interspersed six more “none trials” into the ongoing experiment. It turned out that Alex’s response was no fluke – he gave the correct “none” response in five out of six of these trials, an accuracy rate of 83.3%.

Here’s a brief video in which Pepperberg describes the experiment and Alex’s unexpected use of the “none” concept:

…

Thus, it appears that Alex spontaneously used “none” in a zero-like manner to label a null set and designate an absence of objects. As the researchers summarized it, “the notion of none, even if already associated with absence of similarity and difference (and lack of size difference), is abstract and relies on violation of an expectation of presence; that Alex transferred the notion from other domains to quantity, without training or prompting by humans, was unexpected.”

While Alex’s use of “none” may not be as full and robust as the true zero concept that we use today, it nonetheless (no pun intended) is quite impressive. Moreover, Alex’s insight may prove to be quite practical, with the parrot concept of “none” providing helpful guidance as we attempt to answer some of the more pressing questions of our time, including:

• How many neutrinos are able to travel faster than the speed of light?
• How much deep fried batter-covered butter on a stick should you attempt to eat at one sitting (or ever)?
• How many people are surprised at the fact that dinosaurs went extinct after hearing the Barney the Dinosaur “I Love You” theme song?

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Pepperberg, I., & Gordon, J. (2005). Number Comprehension by a Grey Parrot (Psittacus erithacus), Including a Zero-Like Concept. Journal of Comparative Psychology, 119 (2), 197-209 DOI: 10.1037/0735-7036.119.2.197.

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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Davila-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.

Panksepp, who had been studying play behavior in young human children as well as 50-kHz ultrasonic chirping noises made by juvenile rats during rough-and-tumble play, had just put two and two together: “I had the ‘insight’ (perhaps delusion) that our 50 kHz chirping response in playing rats might have some ancestral relationship to human laughter.”¹

The rest has been history, and today Panksepp is undoubtedly the world’s foremost authority on rodent tickling:

…

As they progressed with their research, Panksepp and his colleagues found that many of their rats seemed irresistibly drawn to tickling, chasing after the ticklers and making substantially more play chirps while being tickled than during any other behavior. But the researchers weren’t content with anecdotal observations, and over the course of several years and a number of experiments, they systematically documented a dozen separate lines of evidence suggesting that the rats’ tickle chirping corresponded behaviorally to playful laughter in young human children.²

No, I went "chirp, chirp, chirp." If I'd been laughing, it would have been "chirp, chirp, chirp."

They compiled data establishing, among other things, that certain areas of the body are particularly ticklish (the nape of the neck, for you do-it-yourselfers), that the most playful rats tend to be the most ticklish, that rats can become conditioned to chirp simply in anticipation of being tickled, that tickle response rates decline after adolescence, that young rats preferentially spend time with older ones who chirp more frequently, that the tickle response appears to generate social bonding, that chirping decreases in the presence of negative stimuli (such as the scent of a cat), that rats will run mazes and press levers to get tickled, etc. Based on their research and observations, Panksepp and his fellow researchers hypothesized that rats, when being tickled or engaging in other playful activities, experience social joy that they vocalize through 50 kHz chirping, a primordial form of laughter that is evolutionarily related to joyful social laughter in young human children.

Does it look like my name is Elmo?

It’s safe to say that the neuroscientific community did not exactly rush to embrace this hypothesis. Behavioral neuroscience can be a particularly conservative and skeptical field, one that has traditionally been extremely wary of any theorizing about emotions controlling neural processes or behavior in animals. Since subjective experiences cannot, after all, be measured directly, it has been considered far more appropriate to those functional brain activities and processes that can be scanned and measured objectively, and to simply deny or ignore the possibility that animals experience complex emotional states such as joy, at least in the context of scientific research. As Panksepp put it:

Of course, it was hard to publish this kind of work, and it was ironic that the publication of our initial manuscript was impeded by prominent emotion researchers, some of whom take pains to deny that we can ever know whether animals have any emotional feelings.³

Hahaha, we've had our little fun now, haven't we? If you tickle me again, I'll pee in your coffee.

Fortunately, time and scientific progress have been on Panksepp’s side. We have identified an increasing number of common underlying structures and processes (homologies) in the brains of humans and other mammals and, as brain scanning technologies have become more sophisticated, we have gained greater insight into neural activities triggered in connection with particular emotional experiences. While the ability to cognitively “get a joke” may depend on our incredibly advanced human neocortex, we now believe that much of the foundational brain circuitry relating to laughter, mirth, social joy, social play and emotional processing lies deep within subcortical regions, where our brains are much more similar to those of other animals.

At this point, Panksepp and his colleagues recognize that they have not definitively proven their hypothesis, but their view is essentially that they have made a reasonable case that fits their data and that hasn’t been disproved:

Until someone can offer us some data that falsifies our hypothesis, we believe our theoretical approach better reveals the true nature of the underlying processes than any intellectual scheme that simply constrains itself simply to the accurate description of the environmental and neural control of behavioral acts.⁴

Even acknowledging the understandable caution of neuroscientists and the obvious difficulty in drawing scientific conclusions about the subjective experiences of animals, it does seem entirely plausible (and not overly surprising) that social animals such as rats would enjoy playful romping and tickling, and that they might vocalize their pleasure in a way that was somewhat akin to basic human laughter. In fact, we hope and fully expect that, as our knowledge of comparative brain structure and function grows over time, we will see more and more studies that show clear linkages between the minds and brains of humans and other animals.

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¹Panksepp, J. (2007). Neuroevolutionary sources of laughter and social joy: Modeling primal human laughter in laboratory rats Behavioural Brain Research, 182 (2), 231-244 DOI: 10.1016/j.bbr.2007.02.015.

²Panksepp, J., & Burgdorf, J. (2003) “Laughing” rats and the evolutionary antecedents of human joy?. Physiology & Behavior, 79(3), 533-547. DOI: Panksepp, J., & Burgdorf, J. (2003). “Laughing” rats and the evolutionary antecedents of human joy? Physiology & Behavior, 79 (3), 533-547 DOI: 10.1016/S0031-9384(03)00159-8.

³Panksepp & Burgdorf (2003).

⁴Panksepp (2007).

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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¹Wilkinson, 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.

That’s right, you’re a bottlenose dolphin, and you’re curious. Curious not because you’re going to do anything about it, but simply because you want to be sure that you haven’t missed out on anything. You want knowledge for knowledge’s sake, however painful it might be.

Humans often need to know certain things, even when finding out opens the doors to an unpleasant discovery. After the worker receives a raise, he can’t help poking around to see whether his coworker received a larger increase. After the shopper buys a large flat screen TV, she keeps looking at advertising circulars to see whether she paid too much. While our curiosity sometimes serves a clear purpose (perhaps that raise can still be renegotiated, maybe that TV can be returned), we often persist in our quest for potentially negative information even when it is too late to change anything, even after the raise has been formally accepted and the TV can no longer be returned. Research on human-decision-making suggests that we act this way because we find the uncertainty of “not knowing” to be uncomfortable. Finding out even the most-unpleasant truths can relieve us from ruminating obsessively over our suspicions, enable us to make sense of our missed opportunities, assist us in coming to terms with our past decisions, and ultimately allow us to regulate our moods in a healthy fashion.

But dolphins? The actions of nonhuman animals are not typically described in these terms. Rather, we find utilitarian explanations – a tangible benefit to compensate the animal for the energy and risk of exploration, a way in which the animal’s curiosity will improve its fitness or survival chances.

OMG, do you see what the Snorkersons are having for dinner?! (image credit: Peter Asprey)

Recently, though, a research team from Israel reported in the Journal of Economic Psychology on a clever experiment indicating that bottlenose dolphins (Tursiops truncatus) are much like humans in seeking knowledge for knowledge’s sake. The researchers studied a group of eight bottlenose dolphins at a “commercial sea enclosure” as they were fed over a seven-month period. The dolphins were fed meals of varying size five times a day, with all dolphins eating at the same time. The dolphins were fed from three separate rafts, with each dolphin assigned one of the rafts and summoned to the proper feeding location with a specific sound signal. During the study period, the researchers observed a total 1,250 dolphin feedings and made special note whenever a dolphin went to over to another raft to explore what other dolphins were being fed.

One of the researchers’ hypotheses was that, to the extent the dolphins sought out knowledge for knowledge’s sake (described in the paper as “Non-Instrumental Curiosity”), they would increase this behavior once their basic survival needs had been satisfied. The researchers were assisted in exploring this hypothesis by two factors: first, about halfway through the study, the dolphins were put on a diet, receiving approximately 15% less food per day on average for the remainder of the testing period, and second, during the latter portion of the experiment the dolphins’ sexual interactions increased markedly due to higher water temperatures and seasonal changes. (Note to self: watch out for pods of horny dolphins as the impacts of global warming become more severe.)

The researchers found that, over the course of the experiment, dolphins visited other feeding rafts 26% of the time (325 of 1,250 feedings). All dolphins visited other rafts, but the percentage of visits ranged from 11.3% to 37.9%, indicating individual differences in curiosity among dolphins. Because the dolphins managed to obtain food scraps on only three occasions (i.e., less than 1% of the time), the research team concluded that it wasn’t likely that the dolphins were using their explorations as a foraging strategy. Moreover, the researchers statistically analyzed the explorations and did not find correlations between the visiting behavior and the dolphins’ known social structure (that is, associations between mothers and calves, adolescent males and females, etc.). In short, there were no obvious benefits to the dolphins’ behavior, and the results supported the premise that they were visiting other feeding rafts out of Non-Instrumental Curiosity.

Hrmph... Next time let's put the researchers on a diet, and see how it impacts *their* behavior (image credit: Laaude at fr.wikipedia)

In addition, the researchers found that dolphins were significantly more likely to visit other rafts when they received larger meals, and that their overall curiosity level was much lower during the phase of the experiment when they were on a diet (they visited other rafts only 13% of the time when on a diet, compared to 38% of the time during the non-dieting phase). Further, during the dolphins’ more sexually active phase, they significantly decreased their exploratory behavior — they visited other rafts only 12% of the time during this phase, compared to 43% during the period when they were less sexually active. (Note though that, because there was a substantial overlap between the dieting and sexually active phases, it wasn’t really possible to separately tease out the relative impacts of these two factors.)

The researchers summarized their results as follows:

In this manuscript, we show that bottlenose dolphins as well, sometimes seek to increase their knowledge concerning food allocated to other dolphins in the group, even though such knowledge could not increase self-food availability. This search increases when own feed is augmented, and decreases when sexually engaged (a competing basic need to food and curiosity), suggesting that knowledge for knowledge’s sake emerges particularly when the organisms’ basic needs (e.g., food) have been satisfied, allowing higher-level psychological needs to emerge.

It seems to me that another way to look at Non-Instrumental Curiosity is that it may be an indication that dolphins are sensitive to inequity and that they possess a sense of fairness, and that it would be interesting to see further research into related cognitive realms, such as their capacity for altruism, empathy and self-awareness. While that may be the subject of future experiments and later AnimalWise posts, for now I’m kind of curious – where did you get all of that tasty looking mackerel?

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Shani, Y., Cepicka, M., & Shashar, N. (2011). Keeping up with the Joneses: Dolphins’ search knowledge for knowledge’s sake Journal of Economic Psychology, 32 (3), 418-424 DOI: 10.1016/j.joep.2011.02.014.

Through what’s known as mental time travel, or MTT, you can move backwards and forwards through time – visiting the past when you remember a specific event you’ve already experienced, and then zipping forward to the future as you use this memory to predict, plan for and shape events that are yet to come.

Mental time travel is no mean feat: it implicates sophisticated cognitive processes and is thought to form the foundation for advanced forms of consciousness such as self-awareness and the ability to attribute independent thought, desires and intentions to others (an ability sometimes referred to as “theory of mind”).

So, can other animals engage in mental time travel? Perhaps not surprisingly, this has been a controversial topic, and many have argued that we humans are the only ones able to mentally flit about the fourth dimension, leaving all other animals stuck in the here and now. Although this may be partly attributable to our anthropocentric world view¹, the language barrier between humans and other animals also poses a real problem, as it’s difficult to design MTT experiments that don’t involve interviews, since the best time travel evidence may consist of the voyager’s personal and subjective reports of the experience. Accordingly, solid evidence for MTT in other animals has been limited, and much of the evidence that does exist consists of anecdotal accounts and a small number of experiments involving great apes and western scrub-jays.

In a paper² published in the October 14, 2011, issue of Behavioral Ecology, though, a research team led by Corina Logan of the Department of Experimental Psychology at the University of Cambridge proposed an intriguing new avenue for further research, one that might significantly expand the number of species that may be tested for MTT abilities. More specifically, Logan and her colleagues identified a specialized strategy among birds – army ant bivouac checking – that may provide conditions in the wild that could favor the development of mental time travel in a variety of species.

If I go back in time and shoot my grandmother, does that mean I’ll never be born?? (White Whiskered Puffbird, credit Glenn M. Duggan FZS)

While many tropical rain forest birds earn an opportunistic living by gobbling up insects and other small invertebrates flushed out of hiding by army ants on food raids, a subset go a step further – after raids by a specific army ant species (Eciton burchellii), these birds follow the ants back to their temporary nests (known as a bivouacs) in the evening, and then return to check on the bivouacs the next morning before the ants raid again. To date, twenty one different “bivouac-checking” bird species have been identified.

Tracking army ant bivouacs is more complicated than one might think. As the ants raise their young, they cycle through two distinct phases: one (approximately 20-day) phase during which they remain in a set location, conducting most of their raids at the beginning and end of the phase and relatively few during the middle two weeks; and a second (approximately 14-day) nomadic phase, during which they move their bivouac on a daily basis and conduct raids almost every day.

Aren’t you hungry? We haven’t eaten since tomorrow. (Ocellated Antbirds, credit PhilSlosberg)

From the perspective of a bivouac-checking bird seeking a reliable food source, these varying phases are significant. When the ant colony is stationary, it may be relatively easy to find, but its raids will be sporadic; when the colony is nomadic, it may be more difficult to find, but its raids will be quite regular. Clearly, a bird will do better if it can keep track of multiple stationary colonies that conduct raids only sporadically, if it can quickly find nomadic colonies based on their prior locations and previous movements, and if it can remember whether particular colonies are in phases in which they’re likely to conduct raids.

The researchers identified these conditions as providing a potential testing ground for MTT. While the birds obviously can’t be interviewed, their environment may elicit behavior that shows that they have an “episodic-like memory” (that is, they can recall the what-where-when aspects of past events) and that they can take action in anticipation of future motivational states independent of their current needs (that is, they can plan flexibly for the future).

After noting that the birds appear to form specific memories about locations (since they return in the morning after evening bivouac checks), the researchers hypothesize that the birds may remember which colonies are in which locations and what phase the colony is in, “and that they may be using episodic-like memory if they prefer to check those bivouacs from army ant colonies in the nomadic phase.” Moreover, they continue:

Time travel jokes never get old! (Spotted Antbird, credit Mike Danzenbaker)

We suspect that future planning could be involved in bivouac-checking bird behavior because birds check bivouacs when sated (conferring no immediate benefit), a behavior that does not make sense until the next morning on return to the bivouac when the bird finds the ants raiding again and encounters its next meal (a delayed benefit). Because bivouac checking occurs after foraging at a raid, there is no immediate benefit to conducting this behavior in terms of acquiring a meal in the next few minutes. Instead, the benefit occurs the next morning when the ants begin raiding again; bivouac-checking birds return and are the first to begin foraging at the raid. This could indicate a dissociation between their current state (sated) and a future need (will need to eat tomorrow), which suggests anticipation of future events. (Citations omitted.)

Logan and her colleagues call for additional field research and, if their hypotheses are supported, laboratory experiments that will enable experimenters to vary bivouac locations and colony phases under controlled circumstances, and to determine whether the birds use specific memories and flexible future planning or whether they engage in automatic behavior using vision, smell, circadian rhythm or other cues in checking on bivouacs.

At this point, the researchers’ hypotheses need additional experimental support, but it’s already clear that they’ve made some keen observations about specialized behavior in the wild and have opened the door to substantially expanded testing for mental time travel in animals. As more researchers come up with similarly elegant ways of investigating abilities previously thought to be unique to humans, I think we will see additional barriers fall.

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¹As regular readers know, this is a recurrent AnimalWise theme. Time and again we humans have claimed that we are the only ones to have a particular skill, only to discover later on that, in fact, many animals may share the same or comparable abilities with us. Prior posts have discussed this phenomenon in areas including tool use (many different fish, crested rats, ants, dolphins, chimpanzees, crows), language (bees and prairie dogs), analogic reasoning (capuchins and baboons), grief and mourning in various animals, and self-recognition (dogs, magpies).

²Logan, C., O’Donnell, S., & Clayton, N. (2011). A case of mental time travel in ant-following birds? Behavioral Ecology DOI: 10.1093/beheco/arr104.

Once there was an arrogant young village lord who, deciding that old people were useless, banished them to the mountains to die. Although the villagers were distressed, they obeyed rather than face severe punishment. One young farmer couldn’t bear to follow this cruel decree, though, and hid his aged mother away in a safe and secret room.

Several years later, an invader arrived, announcing that he’d spare the village only if three tasks could be performed. First, he must be presented with a box containing one thousand ropes of ash. Next, a silk thread must be drawn through a small hole that bent seven times along the length of a log. Finally, he must be given a drum that sounded without being beaten.

In each case, the village lord offered rewards, cajoled and threatened the townspeople, but nobody knew what to do; all were in despair. The tasks all seemed impossible. Each time, though, the farmer asked his mother and she knew the answer: soak ordinary rope in salt water before burning it; tie the silk thread to an ant at one end of the hole and place sugar at the other; put a bumblebee in a drum and it will buzz as it tries to escape. The village was spared.

Ultimately, the lord finds out that they have all been saved by the wise old mother, and from that time on elders in the village are revered.

Shifting scenes now from the mountains of long-ago Japan to the plains of today’s Africa, it turns out that older matriarch elephants are much like the heroic old Japanese mother – they are the ones with the answers, the ones that can save their fellow elephants from outside threats with the wisdom they have accumulated through experience.

Listen to your Grandmother! (image copyright ElephantVoices)

As we know from the decades of observation and research performed by Cynthia Moss and her colleagues in Kenya and Tanzania, matriarch elephants act as group leaders, holding together their families and providing behavioral guidance during times of crisis. Many observers believe that the oldest matriarchs – those with the most experience and greatest ecological knowledge – make the best decisions, but until recently it has proved to be difficult to quantify the relevant skills in a manner conducive to experimental testing.

In a March 2011 paper published online in the Proceedings of the Royal Society B, however, a team of scientists led by Karen McComb of the University of Sussex reported on a clever set of experiments that tested whether older Amboseli National Park matriarchs were better than their younger counterparts at assessing the perceived threat posed by various lion roar recordings.

While African elephants are able to fend off most natural predators, they have to watch out for lions, who occasionally prey upon younger calves. Also, even though lionesses perform the, ahem, lion’s share of the hunting for the pride, male lions actually pose a greater threat to elephants. Male lions, despite their generally well-deserved reputation for laziness, are, on average, half again as large as females and much stronger, giving them a better chance of overpowering a vulnerable young elephant.

Accordingly, the researchers assembled lion “playbacks” in four separate categories – single female roars, single male roars, three female group roars and three male group roars – which they then played to 39 elephant family groups over a period of slightly more than two years. Because of the extensive demographic information compiled by the Amboseli Elephant Research Project, they knew the age of the matriarch in each of the 39 families.

After playing the different roars, the researchers analyzed video of the elephants’ responses, focusing particularly on the behavior of the matriarchs. They documented specific defensive reactions, including prolonged listening to the roars, whether the family bunched around the matriarch after hearing the roars, the speed and intensity of any bunching behavior, and whether the matriarch changed her direction and moved toward the source of the playback.

Here are two brief videos, one showing an elephant family reacting to lion roars and the other narratively describing the reactions as reflected in still images:

…

…

After recording all of the responses, the research team performed statistical analyses and sorted their results by matriarch age. They found that, while matriarch age did not have an impact on how the elephants reacted to varying number of lions (all elephant families consistently ratcheted up the intensity of their response when the number of lions roaring went from one to three), it did have a strong impact on the elephants’ response to the more serious threat presented by male lion roars, with male roars leading to more prolonged listening and intensive defensive bunching in families led by older matriarchs.

As the researchers put it:

Our work provides the first direct experimental evidence that older matriarchs are in fact able to make better decisions when faced with ecological challenges — in this case, the presence of dangerous predators. It thus bridges an important gap between theoretical predictions about how knowledge might be expected to affect leadership and empirical studies, which to date have been largely confined to observational accounts.

Based on these findings, I’m quite confident that the older matriarchs will do quite well on their next set of tasks involving burning ropes, crooked logs and drums. Now, if only that was enough to keep humans from invading their villages….

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The Japanese folktale can be found, among other places, in The Wise Old Woman/retold by Yoshiko Uchida; illustrated by Martin Springett. ISBN: 0689505825.

McComb, K., Shannon, G., Durant, S., Sayialel, K., Slotow, R., Poole, J., & Moss, C. (2011). Leadership in elephants: the adaptive value of age Proceedings of the Royal Society B: Biological Sciences, 278 (1722), 3270-3276 DOI: 10.1098/rspb.2011.0168.

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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Truppa, 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

Recently, the blackspot tuskfish (Choerodon schoenleinii) became a media sensation when it was captured in photos using a rock as tool to open a clam. Apparently not happy with the print media attention afforded to its relative, the orange-dotted tuskfish (Choerodon anchoago) has taken the behavior to the movies, digging up a clam with its pectoral fin, swimming about five meters with it, and then crushing it open using a rock as an anvil:

…

As reported in the latest issue of Coral Reefs, a diver off the coast of Palau observed the orange-dotted tuskfish using a rock as a tool on three separate occasions, capturing the above footage on the final instance. The paper notes that three separate genera of wrasses (the Choerodon that have been in the news lately, as well as the Halichoeres and Thalassoma) have now been seen using similar sideways head movements to slam bivalves against rock anvils, suggesting that this may be a “deep-seated behavioral trait” in wrasses and, potentially, other groups of fishes.

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Bernardi, G. (2011). The use of tools by wrasses (Labridae) Coral Reefs DOI: 10.1007/s00338-011-0823-6

You may wonder whether the forces of convergence are a recent phenomenon, a product of human technology, or whether they may have deeper roots in the natural world. In fact, convergence can and does occur in the realm of biological evolution, albeit at a more comfortable pace. For example, “convergent evolution” occurs when different species independently evolve similar solutions to comparable evolutionary pressures. A classic example of this is the development of wings and the ability to fly by birds, bats and pterosaurs:

Diagram of wing morphology and/or and comparative network hub structure of Twitter, Facebook and Google+ (image credit: National Center for Science Education)

Consider also the independent evolution of sleek, torpedo-shaped bodies by fish, cetaceans and ichthyosaurs:

Sleek ocean swimmers (image credit: All About Reptiles)

Closer to home, scientists at the Max Planck Institute for Evolutionary Anthropology have concluded that we may be undergoing a process of cognitive convergent evolution with dogs based on our social relationships over thousands of years with these “best friends” of ours. In a paper published in Trends in Cognitive Sciences, Brian Hare and Michael Tomasello reviewed a large number of studies focused on canine, human, and non-human primate social and communicative skills and reached some interesting conclusions.

Proof of convergent canine-human evolution (source unknown)

They began their analysis by focusing on research showing how well domestic dogs do at interpreting human social and communicative behavior. For example, dogs excel at tests in which experimenters hide food in one of several opaque containers and then signal where it has been hidden by pointing, gazing, bowing or nodding, or placing markers in front of the target location. The dogs easily interpret this type of cue, passing tests such as these on the first attempt and performing correctly even when humans try to trick them by walking towards the wrong container while pointing in the opposite direction to the correct container.

Also, studies have shown that dogs are aware of what humans can see. For instance, if a human turns around during a game of fetch, the dog will almost invariably bring the ball back around the human and drop the ball in front of his face. Similarly, dogs have shown that they prefer to beg for food from humans whose eyes are visible than from ones whose eyes are covered with a blindfold or bucket, but are more likely to approach forbidden food when a human’s eyes are closed.

Indeed, dogs actually consistently outperform chimpanzees and other primates at these types of skills, even though, in areas of non-social cognitive performance, dogs do not do so well. For example, non-human great apes are much better at making inferences about the location of hidden food based on non-social cues (such as a tilted board that might be tipped up by hidden treats) and at tests that require them to achieve food rewards by, for example, reeling in food attached to strings.

With this in mind, Hare and Tomasello turned to whether domestic dogs’ specialized social skills are likely to be due to convergent cognitive evolution with humans or whether another explanation is more plausible.

First, they considered the possibility that dogs learn to recognize human social cues based on their experiences growing up in human households. They found, however, that studies show that even puppies as young as nine weeks old are adept at solving problems using human pointing and gaze cues, and that puppies raised without much exposure to humans are equally skilled at interpreting these cues.

Then, they considered whether domestic dogs may have simply inherited their social skills based on their common ancestry with wolves, since wolves are, after all, pack hunters who need to be able to follow complex social interactions with other wolves and with prey. However, although wolves are generally equal to or better than domestic dogs at memory tests and tasks involving general problem-solving abilities, wolves (even those raised by humans) are simply unable to match the performance of dogs at spontaneously using human social cues to solve problems.

Next, the researchers sought evidence for the evolution of social skills in dogs through their long-term relationship with humans. They looked at a population of domesticated foxes, where the selection for breeding had been based solely on the tendency of individual foxes to be non-aggressive and fearless around humans. Interestingly, these foxes were just as adept as dogs in using and interpreting human social cues, and far better than a population of control foxes that had been bread randomly with respect to their attitude towards humans.

Based on all of these comparative findings, Hare and Tomasello concluded that the best explanation for dogs’ specialized social skills is that they evolved as a consequence of dogs having been domesticating by humans, representing a case of convergent cognitive evolution. Interestingly, Hare and Tomasello went further and, based on their review of the research on domesticated foxes, concluded that the evolution of specialized social skills in domesticated dogs may actually have been an incidental byproduct of an initial decision to select based solely on nonaggression (as opposed to social intelligence).

Finally, turning to primate evolution, Hare and Tomasello speculated that a similar process may have contributed to differences between human and chimpanzee social skills. Under what they refer to as the “emotional reactivity” hypothesis, they predicted that differences in temperament between humans and other primates may help explain some of humans’ extraordinary social cognitive abilities. They point to studies showing that chimpanzees’ willingness to cooperate with each other can often be limited by lack of social tolerance for one another resulting from fear and/or aggression, and contrast this to a more socially tolerant temperament that may ultimately have enabled our hominid ancestors to develop flexible forms of cooperation and communication. In other words, humans underwent a form of self-domestication leading to greater social abilities, thereby convergently evolving with our canine companions who were undergoing the same process.

I’m not sure I entirely buy the notion that we humans are so exceptionally tolerant, but I have noticed that you’ve started to look a bit like your dog. In a future post, we may look at whether we may also be evolving to be more like members of the cat family:

Which one is the lion? (source unknown)

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Hare, B., & Tomasello, M. (2005). Human-like social skills in dogs? Trends in Cognitive Sciences, 9 (9), 439-444 DOI: 10.1016/j.tics.2005.07.003

Nevertheless, we do sometimes succeed in delaying immediate gratification for the sake of something better in the future, in remembering those clichés about “good things come to those who wait” that our parents and grandparents inflicted on us. Undoubtedly, this is something we’re able to achieve because we’re humans, because we can be goal-directed and can prevail over our impulses, because we are more than unthinking animals who are captives to their immediate needs. Right?

Not so fast.

It is true that many animals seem unable to defer gratification, with prior experiments showing that animals such as rats, pigeons and chickens will rarely choose a delayed food reward over an immediate one, even if the delayed reward is much more attractive and the delay is only a few seconds. (From an evolutionary standpoint, this sort of impatience may make a lot of sense when an animal faces competition and future opportunities for food are unknown. “Life is uncertain, have dessert first!”)

To date, the major exception has appeared to be in primates: chimpanzees, bonobos, rhesus macaques and capuchin monkeys have demonstrated that they can wait for up to five minutes or so if that enables them to obtain a desirable food reward – a level of performance comparable to that of humans. (Interestingly, tests have shown that we humans seem to be much better at deferring money rewards than food rewards. Perhaps this, too, has a basis in natural selection, as food has been obviously always been an imperative, whereas money has existed for only an evolutionary blink of the eye.)

Also, while all of this might lead one to conclude that the ability to delay gratification lies solely within the province of humans and our closest relatives, it now turns out that corvids, the famously smart bird family (see prior AnimalWise posts here and here and here and here) that includes ravens and crows, may be every bit as patient.

When's dinner going to be ready? (from Wikipedia, photo credit: Cj005257)

As described in a paper published last week in Biology Letters, a team led by Valérie Dufour of the University of Strasbourg recently found that crows (Corvus corone) and ravens (Corvus corax) are able to tolerate delays of over five minutes in order to obtain a better reward, and that they may use the same sort of tactics to distract themselves while they wait as humans do.

In this study, six crows and six ravens were first trained to exchange tokens for food rewards, and then were given a series of “delayed exchange” tests. In each test, a bird would be handed an initial piece of food, which it could either eat immediately or, upon receipt of a signal after a designated waiting period, exchange for a more a desirable reward that it could see throughout the testing period. If the bird ate the initial reward or tried to exchange it too early, the test would end, but if it waited until the proper signal after the waiting period had elapsed – success, a better reward!

The researchers ran the tests with different types of reward (which they labeled as low-, medium- and high-quality) and with varying waiting periods (from 2 to 640 seconds).

Not surprisingly, the birds were generally more willing to exchange for the most highly preferred rewards and, as the following graphic illustrates, had a harder time as the delay period increased (with both crows and ravens maxing out at 320 seconds, or slightly over five minutes):

Interestingly, when the birds had to wait 20 seconds or longer before being able to exchange, they usually placed the “reward in the hand” on the ground and/or cached it in nearby crevices. The researchers believed this to be a distractive strategy, as “[t]hese behaviours probably alleviate the cost of waiting: not having to hold the food distracts the bird’s attention from it.”

As someone who routinely has to put snack food out of reach or even out of sight in order to prevent Homer Simpson-like devouring, this explanation makes a lot of sense to me. (For those of you who would prefer a more uplifting example of a strategy for avoiding temptation, I invite you to think about Ulysses having himself lashed to his ship’s mast so that he can safely listen to the songs of the Sirens.)

In any event, delaying gratification is significant because it involves, on some level, making a judgment about the future and the likelihood of achieving a prospective reward. While it’s not clear whether this entails a full “sense of self,” it is worth (re)noting that corvids are one of the few animals that have demonstrated the ability to recognize themselves in mirrors, a cognitive test that’s often used to measure whether an animal has at least rudimentary self-awareness.

Once again, corvids are no bird brains!

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Dufour V, Wascher CA, Braun A, Miller R, & Bugnyar T (2011). Corvids can decide if a future exchange is worth waiting for. Biology letters PMID: 21920957.

Rosati, A., Stevens, J., Hare, B., & Hauser, M. (2007). The Evolutionary Origins of Human Patience: Temporal Preferences in Chimpanzees, Bonobos, and Human Adults Current Biology, 17 (19), 1663-1668 DOI: 10.1016/j.cub.2007.08.033.

Heilbronner, S., & Platt, M. (2007). Animal Cognition: Time Flies When Chimps Are Having Fun Current Biology, 17 (23) DOI: 10.1016/j.cub.2007.10.012.

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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¹Biro, 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.

Maybe all we need to do is to look at the world the way it is, a world that could well be called … The Planet of the Ants!

So, why is it that we should feel just a wee bit threatened by these small six-legged colonizers? Here are just a few reasons.

Quadrillions of Ants

Burning Man seems more crowded every year, doesn't it? (photo credit: Mehmet Karatay)

Like us, ants thrive just about anywhere, with the exception of Antarctica and a few isolated islands. Moreover, while there are approximately seven billion of us on the planet, conservative estimates put the number of ants at between one and ten quadrillion.¹ That’s between 150,000 and 1,500,000 ants for each and every one of us. At the higher figure, this means that, if you were to put all the world’s ants onto a giant scale, they would weigh about as much as all of the humans on the planet put together.² In fact, on average, it has been estimated that ants make up 15–20% of the terrestrial animal biomass on Earth (and more than 25% of the animal biomass in tropical regions).³

Our tendency as humans is to unquestioningly assume that we are far and away the most successful species that has ever been. If we take a step back, though, and simply consider the above numbers and the possibility that an animal’s success is most properly measured by the degree to which it has been able to thrive in various environments, perhaps we should already be feeling a pang of doubt about how incontestable our supremacy really is.

Ants Teach

While many animals are able to learn through imitation, ants are the only non-mammal known to engage in interactive teaching.⁴ In at least one species of ant, knowledgeable workers actively teach inexperienced nest mates where to find food through a process known as “tandem running,” in which the lead worker ant recruits an inexpert follower, and then makes sure that the follower stays on track, slowing down when it lags and speeding up when it gets too close.

Ants Learn

Ants are also able to engage in so-called latent learning, whereby they memorize information that they cannot use at once, but that may be useful later on – a behavior that’s been labeled as “planning.”⁵ Specifically, ants have been shown to be able to reconnoiter potential new living spaces, retaining information about relative desirability and tailoring their choices based on how urgently the need to move is.

Ants Can Learn to Navigate Mazes

Ants can be trained to remember multiple visual patterns presented in a fixed sequence, enabling them to navigate mazes.⁶ Ok, I’m not sure how exactly this leads to world domination, but it is definitely pretty cool.

Ants Practice Agriculture

Approximately 50 million years ago (and, accordingly, approximately 49+ million years before Homo Sapiens first arose as a species), ants began engaging in agriculture.⁷ Today, different species of leafcutter ants have adopted a purely agrarian lifestyle, feeding exclusively on gardens of fungus that they actively weed and cultivate, feed with fresh-cut leaves, and keep free from parasites and other pests.⁸ Here’s a video of some fungus farming ants:

Ants Engage in Animal Husbandry

Some ants raise aphids and feed on the sugary honeydew the aphids secrete when “milked” by the ants’ antennae. The ants are careful with their herds, keeping predators and parasites away, moving the aphids from one feeding location to another, and often bringing the aphids with them when they migrate.⁹ Here’s a video of ants tending to their aphids:

Ants Sometimes Enslave Other Ants

Certain types of ants are incorrigible slave-makers, raiding other colonies of ants and making captured slaves perform all routine tasks for their masters, including brood care, foraging, and even feeding slave-maker workers who are unable to feed themselves.¹⁰ Obviously, this isn’t a particularly attractive ant characteristic, but unfortunately it is one that may seem all too familiar to us humans.

Ants Use Tools

That’s right, tools. For example, some ants transport liquid and other non-solid food by dropping bits of leaves, sand or mud pellets or pieces of wood into a pool of food and, after the food has soaked in, using these objects to carry the meal back to their nests.¹¹ Other ants use pebbles and soil pellets as weapons, dropping them on other ants or ground-dwelling bees, and then attacking and killing their competitors.¹²

Ants Build Cooperative Solutions

Hey, watch your foot! You're stepping on my head! (photo: Mlot, Tovey & Hu)

Ants, including army ants, are known to self-assemble into living bridges or ladders that allow them to cross gaps while on the move. When a single ant cannot make it across alone, other ants will successively grab on, steadily lengthening the bridge until it’s long enough to reach the destination. These structures, which can span significant distances and can even cross water, are then used by the rest of the colony and may stay in place for hours, until traffic dies down.¹³ Comparably, fire ants self-assemble into waterproof rafts to survive floods. These rafts can be made up from anywhere from a few hundred to many thousand ants and are incredibly durable, allowing ants to sail for months at a time as they migrate.

Ants Have “Collective Intelligence”

The concept of collective intelligence has been hot lately, with a number of books and articles describing how groups can make collectively make sophisticated decisions and solve complex problems, even where each individual in the group knows very little, collectively a g (think of the analogy of each individual acting as a neuron, and the group as a whole acting as a collective brain). Collective intelligence is a topic unto itself, one we may address in future posts, but for now suffice it to say that if ants truly can make wise decisions as a group, we humans may really have something to envy!

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¹Holldobler, B & E. O. Wilson (2009). The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies. New York: W. W. Norton. p. 5. ISBN 0-393-06704-1.

²Ibid.

³Schultz, T. (2000). In search of ant ancestors Proceedings of the National Academy of Sciences, 97 (26), 14028-14029 DOI: 10.1073/pnas.011513798.

⁴Franks, N., & Richardson, T. (2006). Teaching in tandem-running ants Nature, 439 (7073), 153-153 DOI: 10.1038/439153a; Richardson, T., Sleeman, P., McNamara, J., Houston, A., & Franks, N. (2007). Teaching with Evaluation in Ants Current Biology, 17 (17), 1520-1526 DOI: 10.1016/j.cub.2007.08.032.

⁵Franks, N., Hooper, J., Dornhaus, A., Aukett, P., Hayward, A., & Berghoff, S. (2007). Reconnaissance and latent learning in ants Proceedings of the Royal Society B: Biological Sciences, 274 (1617), 1505-1509 DOI: 10.1098/rspb.2007.0138.

⁶Chameron, S., Schatz, B., Pastergue-Ruiz, I., Beugnon, G., & Collett, T. (1998). The learning of a sequence of visual patterns by the ant Cataglyphis cursor Proceedings of the Royal Society B: Biological Sciences, 265 (1412), 2309-2313 DOI: 10.1098/rspb.1998.0576; Reznikova, Z. 2008: Experimental paradigms for studying cognition and communication in ants (Hymenoptera: Formicidae). Myrmecological News 11: 201-214.

⁷Schultz, T., & Brady, S. (2008). From the Cover: Major evolutionary transitions in ant agriculture Proceedings of the National Academy of Sciences, 105 (14), 5435-5440 DOI: 10.1073/pnas.0711024105.

⁸Ibid.; Schultz, T. (1999). Ants, plants and antibiotics. Nature, 398 (6730), 747-748 DOI: 10.1038/19619.

⁹Nielsen, C., Agrawal, A., & Hajek, A. (2009). Ants defend aphids against lethal disease Biology Letters, 6 (2), 205-208 DOI: 10.1098/rsbl.2009.0743; Styrsky, J., & Eubanks, M. (2007). Ecological consequences of interactions between ants and honeydew-producing insects Proceedings of the Royal Society B: Biological Sciences, 274 (1607), 151-164 DOI: 10.1098/rspb.2006.3701.

¹⁰Pohl, S., & Foitzik, S. (2011). Slave-making ants prefer larger, better defended host colonies Animal Behaviour, 81 (1), 61-68 DOI: 10.1016/j.anbehav.2010.09.006; Brandt M, Foitzik S, Fischer-Blass B, & Heinze J (2005). The coevolutionary dynamics of obligate ant social parasite systems–between prudence and antagonism. Biological reviews of the Cambridge Philosophical Society, 80 (2), 251-267 PMID: 15921051; Hölldobler, B. & Wilson, E.O., 1990. The Ants, Harvard University Press.

¹¹FELLERS, J., & FELLERS, G. (1976). Tool Use in a Social Insect and Its Implications for Competitive Interactions Science, 192 (4234), 70-72 DOI: 10.1126/science.192.4234.70.

¹²See, e.g., Pierce, J. (1986). A Review of Tool Use in Insects The Florida Entomologist, 69 (1) DOI: 10.2307/3494748.

¹³Mlot NJ, Tovey CA, & Hu DL (2011). Fire ants self-assemble into waterproof rafts to survive floods. Proceedings of the National Academy of Sciences of the United States of America, 108 (19), 7669-73 PMID: 21518911.

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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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.

What’s also quite fascinating is that the long post-reproductive life of human females – up to a third of a woman’s lifespan or more – is extremely rare: menopause appears to be unique to humans and (somewhat controversially) certain other great apes, as well as to certain toothed whales, including short-finned pilot whales and killer whales. (It’s possible that other species of cetacean may undergo menopause, but this hasn’t been established yet; also, more to come about elderly elephant matriarchs in a later post…)

To grandmother's house I go! (Photo: © Alice MacKay, Cascadia Research)

So, why is post-reproductive life is so rare? If the grandmother hypothesis applies to great apes and toothed whales, why isn’t it at work with other long-lived animals who live in socially-cooperative societies? Also, if evolution favors post-reproductive life because it provides distinct social advantages, why did menopause evolve in humans and toothed whales, given the very different social structures of humans and whales?

A fascinating study published last year in Proceedings of the Royal Society B³ by Rufus Johnstone of the University of Cambridge and Michael Cant of the University of Exeter may offer plausible answers to these questions.

In a nutshell, they found that, although humans, pilot whales and killer whales have quite different social systems, in each case older females become, on average, more genetically related to those with whom they associate. By contrast, in most other long-lived complex mammal societies, older females become increasingly less related to those in their local groups as they age.

Did grandma pinch you on the cheek too? (photo credit: NOAA)

The researchers began by developing a mathematical model that would allow them to draw general conclusions about age-related changes in the genetic relatedness of long-lived social animals as individual group members disperse, die and are replaced over time. (For those interested in such things, they based their approach on the “infinite island” model that is commonly used in considering the process of gene flow among a set of subpopulations.)

With their model in hand, the researchers analyzed three relevant social scenarios:

1. Males Move On. In the large majority of social animal societies, males tend to move on as they mature, ultimately mating with unrelated females they find within new social groups. In this type of society, the researchers’ model determined that, over time, an older female will become less related to her group mates as she ages. She starts out in a highly related group that includes her father, but over time her older male relatives die, and her sons, and the sons of her relatives, leave the group and are replaced by unrelated males from other groups. Her average genetic relationship to the females in the group doesn’t change much, but since her relatedness to local males declines, overall her genetic connection to the group lessens as she gets older.
2. Females Move On. Conversely, evidence suggests that during the course of human evolution, women were the ones that were more likely to move on to start families in new environments. (In support of this proposition, Johnstone and Cant cite the behavior of other great apes, human DNA variation patterns, and social patterns among human forager societies, evidence they concede is “far from conclusive.”) In this type of society, where males stay at home and females disperse, an older female tends to become more related to her fellow group members over time. She begins her reproductive life in new surroundings where she has few genetic ties to those around her, but as she produces sons who are likely to remain in the group, her relatedness to local males builds up over time. Again, because the degree of her relatedness to other females stays fairly constant – she starts out with little relation to the females in her new group and this doesn’t change much as her daughters leave and are replaced by new unrelated females – her overall genetic connection to the group increases as she ages.
3. Males and Females Stay Put, But Mating Occurs Between Different Groups. In the resident killer whale and pilot whale societies studied, males and females stay with their natal groups for life, but mating occurs non-locally, that is, between females and males from other groups. In this final scenario, even though the social structure is quite different from “female moves on” societies, the results are the same: an older female tends to become more related to her fellow group members over time. A female begins her reproductive life separate from her father and her paternal relatives (who belong to a different group), but as she has male offspring her relatedness to males within her group grows over time. Once again, her relatedness to other females stays more or less constant, meaning that her overall genetic affinity with her group increases as she grows old.

Thus for human and certain whale societies, in contrast to most other social animal groupings, a female’s relatedness to her group increases as she becomes older.

Johnstone and Natal next considered the fitness costs of reproduction. They noted that having children imposes costs on other breeders within one’s group due to increased competition for food, resources and mating opportunities, whereas cessation of reproduction confers a benefit, due to a corresponding reduction in competition. Then, using a using a statistical model involving an “inclusive fitness” approach to generate quantitative results for the three scenarios described above, they reached a not-surprising conclusion: in scenario 1 (males move on), it is less advantageous for older females to “help” younger generations by stopping their own breeding, whereas in scenarios 2 and 3 (the human and toothed whale scenarios), non-breeding “help” is favored by evolution, as it confers advantages on a younger generation that is progressively more related to the older helper.

So there you have it. Does Johnstone and Natal’s analysis sound plausible? It certainly offers a neat way of finding an underlying similarity in great ape and whale societies that may explain menopause and support the grandmother hypothesis in these very distinct groups.

No wonder cetaceans often look like they’re grinning – they’ve been spoiled by their grandmothers!

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¹See, e.g., Lahdenperä, M., Lummaa, V., Helle, S., Tremblay, M., & Russell, A. (2004). Fitness benefits of prolonged post-reproductive lifespan in women Nature, 428 (6979), 178-181 DOI: 10.1038/nature02367; Shanley, D., Sear, R., Mace, R., & Kirkwood, T. (2007). Testing evolutionary theories of menopause Proceedings of the Royal Society B: Biological Sciences, 274 (1628), 2943-2949 DOI: 10.1098/rspb.2007.1028.

²See, e.g., Kachel, A., Premo, L., & Hublin, J. (2010). Grandmothering and natural selection Proceedings of the Royal Society B: Biological Sciences, 278 (1704), 384-391 DOI: 10.1098/rspb.2010.1247.

³Johnstone, R., & Cant, M. (2010). The evolution of menopause in cetaceans and humans: the role of demography Proceedings of the Royal Society B: Biological Sciences, 277 (1701), 3765-3771 DOI: 10.1098/rspb.2010.0988.