Social Learning in Tortoises

In a previous post, AnimalWise saluted the red-footed tortoise (Geochelone carbonaria) for its Ig Nobel Prize achievements but, in doing so, may have unfairly maligned the tortoise’s cognitive capabilities. To atone for any past disparagement, this post is dedicated to an impressive, and perhaps surprising, red-footed tortoise intellectual accomplishment.

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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ResearchBlogging.orgWilkinson, 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.

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A Yawning Divide? Contagious Yawning and Empathy in Animals

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

Tortoise yawning? I don’t think so!

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

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

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

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

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

Apes and Monkeys and Dogs, Oh My!

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

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

Chimpanzees

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

Monkeys

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

Dogs

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

Future Directions

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

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

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

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

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

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

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

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

Lizards Shed Reputation as Slow Learners

A new study has shown that anoles (Anolis evermanni), a tropical tree-dwelling lizard found in Puerto Rico, are surprisingly good problem-solvers who have cognitive abilities that rival those of birds known for their highly flexible behaviors.

Manual Leal, a professor at Duke University, led a study in which six anoles were given a series of challenges designed to test their behavior flexibility, cognitive abilities and memory.  In these experiments, the lizards were presented with a platform containing two wells, one containing a food reward and the other empty. The wells were covered with tight-fitting opaque discs of differing colors and patterns, and the lizards were given 15 minutes to obtain the reward.

Anole Lizard: will you quit messing with my dinner if I drop that whole GEICO thing? (photo credit: Manuel Leal, Duke University)

According to Leal’s research paper, which was published online on July 13, 2011, in the Journal of the Royal Society: Biology Letters1, two-thirds of the lizards were able to solve the puzzle and find the food reward, a “completely unexpected” result since:

The correct response required major changes to what has previously been considered highly stereotyped foraging behavior, which consists of scanning the environment for moving prey items and striking them from above. In our experiment, motion cues were absent and striking from above was ineffective at dislodging the disc. Lizards used multiple strategies to remove the disc. The first was a modified strike, laterally biting the disc and lifting it away from the reward. The second strategy required the lizard to advance on the disc with its head held against the substrate, using its snout as a lever to push the disc out of the way…. This strategy is not a natural foraging behaviour that has at least been witnessed, and may demonstrate an entirely novel solution, which is one of the main criteria used to recognize behavioural flexibility.

Here’s a video from the New Scientist2 that shows one of the lizards in action:

When the tests were repeated with the disc colors associated with the reward reversed, two of the lizards continued to flip the original disc in an unsuccessful search for the reward, but the remaining two, nicknamed Plato and Socrates by Leal’s team, figured out that the discs had been changed and solved the problem again, reversing their previously learned color associations. (This sort of test is known as a “reversal learning” test.) Although there haven’t been many studies of cognition in reptiles, Plato and Socrates’ success appears to be particularly notable since prior evidence had suggested that reptiles do better at solving puzzles involving location change than ones involving altered visual cues.

Finally, Leal and his team were surprised to discover that the anoles were able to solve the challenges presented in these experiments in only one-third the attempts needed by birds given similar tasks in comparable experiments. While the researchers did not draw any definitive conclusions about this, they did note that, due to the slower metabolisms of the cold-blooded anoles, they could be tested only one time a day, and that the tempo at which the tests were performed might have some bearing on the number of attempts required.

Perhaps because people don’t expect displays of cognitive flexibility in reptiles, Leal’s research has generated a fair bit of media attention, including articles in The Economist3, ScienceNOW4MSNBC5, BBC Nature News6 and LiveScience7. Enjoy!

Now, after a long week, I think I’m going to go out and lie on a warm rock and then get some dinner.

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1Leal M, & Powell BJ (2011). Behavioural flexibility and problem-solving in a tropical lizard. Biology letters PMID: 21752816.

2New Scientist, “Smart lizard solves a problem it’s never seen before,” July 13, 2011.

3The Economist, “Cold Blooded Cunning,” July 14, 2011.

4ScienceNOW, “Tropical Lizards Get Brainy,” July 12, 2011.

5MSNBC, “Don’t underestimate the brainpower of a lizard,” July 13, 2011.

6BBC Nature News, “Lizard has problem solving skills,” July 13, 2011.

7LiveScience, “Lizards Are Wizards At Solving Food Puzzle,” July 12, 2011.

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