Monkeys in the mirror and the nature of science

Charles Darwin wondered if animals were aware of themselves. Allowed to visit a rare orangutan in the London Zoo, he brought a mirror and observed the ape apparently make faces at its own reflection. It’s hard to say for sure that the orangutan really was aware that its reflection was its own. Over a century later, a scientist named George Gallup turned Darwin’s idea into a more rigorous test. He would secretly put a mark on an animal’s forehead and see if it noticed the difference the next time it passed a mirror.

Human adults pass this test, but young children don’t, suggesting that our self-recognition takes time to develop. Some chimpanzees (our closest relatives) seem to pass this mirror test, but others fail it. Orangutans also show mixed results. Beyond the primates, studies have indicated that magpies, dolphins, and elephants pass the mirror test. In a new paper in PLOS One, Luis Populin of the University of Wisconsin publish what may be the first compelling evidence that monkeys pass the mirror test too.

It’s a surprising result because people have tried to find evidence of self-recognition in monkeys before. Most scientists failed. The Harvard primatologist Marc Hauser claimed in 1995 that the cotton-top tamarin could pass the mirror test, but that paper was one of several that Harvard now claims were tainted by Hauser’s misconduct. Populin and his colleagues came across their first clues of self-recognition by accident. They had implanted electrodes in the skulls of rhesus monkeys for a different study. They keep mirrors in the monkey cages just to stimulate the animals, and they noticed that the monkeys started spending a lot of time looking at themselves in the mirrors after surgery.

To see if the monkeys were really aware that their appearance had changed, the scientists put different mirrors into the cages. Some were big and some were small. Some were made of ordinary glass, while others were painted glass. The monkeys looked much more often into the real mirrors than the blackened ones. The scientists then introduced an even bigger mirror into the cages, which allowed the monkeys to see their whole bodies. The mirror hung from the top of the cage so they could turn it around. The video above shows a monkey without an implant inspecting one of these big mirrors. It doesn’t use any of the gestures it might if it met another monkey. Instead, it seems to be inspecting its body. Every nook and cranny, in fact.

I asked two experts on self-recognition, Lori Marino and Frans de Waal, both of Emory University, what they thought of the paper.

Marino was enthusiastic:

I’ve been reading this article over and over again all morning and have looked at the videos. Here is my reaction: I think that this is potentially a very important study. The videos are absolutely convincing. At first I thought it was the saliency of the implanted head device that made a difference but the videos show that monkeys without the device also use the mirror and, even more importantly, the monkeys are using the mirror to explore OTHER parts of their bodies, i.e. genitals. That can’t be explained away in some sort of ‘stimulus saliency’ explanation, as far as I can tell. There are two areas that I wish I had more information about. First, exactly what was their prior mirror exposure? Is there anything they can report about how long that was and if there were any interactions with the monkeys during that prior time that could have made a difference in terms of the outcome of this study? Second, they report that the monkeys “failed the mark test” but there is no information given about the methods used in the mark test. It would be important to know how that was conducted.

With all that said, this is – by far – the most compelling evidence for MSR in monkeys to date. I have been trying to find an alternative explanation for the results – and haven’t come up with one yet. I’ll continue to return to it to see if any come to mind. I think that these findings show that self-awareness is not an all-or-nothing phenomenon as Gallup has asserted. I don’t find this conclusion particularly surprising because it has been extremely difficult for anyone to come up with an explanation for the supposed “discontinuity” between great apes and monkeys. I think the reason for this is that there is none.

De Waal was more circumspect:

It is hard to say what is going on as the cap may be seen as a “supermark,” as the authors call it, but it is of course a mark that is not only seen but also felt. As a result, the monkeys have two sources of feedback at the same time, the image in the mirror and the sensation of something new on their head. This is different from the classical mark test, which has only one source of information (visual). It seems clear that the convergence of these two sources of perception is helpful to achieve self-inspection, and this is an interesting finding, but the authors still need to explain why rhesus monkeys apparently cannot do the same with just the visual information.

The hallmark of the mark test is its spontaneity, purely on the basis of visual input, so in this sense this is different. Rhesus monkeys have been tested many times and never pass the test. I think you need to talk to Dr. Gordon Gallup and see what he thinks. It is unclear to me what to conclude, but this study is quite different from e.g. the magpie study, which applied a purely visual test.

The idea that mirror self recognition is a black & white distinction (you either have it or you don’t) was first challenged in another monkey study that we conducted, in which we showed that capuchin monkeys do not seem to see a stranger in the mirror: they seem to distinguish the monkey in the mirror from another monkey, strange or familiar. As a result, we proposed a gradual scale of self awareness. The piece of intriguing information presented here may support this view, but I am sure many scientists would want more tests and more controls.

[Update: New Scientist reports that Gallup shares De Waal’s reservations.]

[Update: Peter Roma, who published a 2007 paper in which he failed to find evidence for self recognition in monkeys, rejects the new one:

Although the video samples are provocative, I cannot agree with the conclusion (and title) of the paper.

The lack of social behaviors towards the mirror is irrelevant because the monkeys all had an extensive history with mirrors prior to the study, so there was no reason to expect social responses after years of habituation to reflective surfaces. To anthropomorphize, they may still think the monkey in the mirror is another animal, but over the years they’ve learned that he’s harmless.

The examples of putative genital viewing were not convincing either. The authors repeatedly asserted that the monkeys used the mirrors to view areas they could not see directly, but monkeys can see their genitals unaided, and they play with them all the time with or without mirrors! Even the video samples show the monkeys looking at their genitals directly then viewing the same area(s) in the mirror. This is why scientists do the mark test!

In my view, the most compelling evidence was the first video of the monkey touching the head implant while holding the mirror. There is no doubt that the monkeys could not see the implant without a reflective surface, but the key here is whether or not this self-examination behavior occurred more frequently in the presence of the mirror vs. without. The authors report increased incidence of touching “unseen” areas in the presence of the mirror (figure 2C), but these data include touching the cranial implant and the genitals. I suspect these data are artificially inflated by what the authors perceive as mirror-guided genital examination, which even in the video examples did not appear to be anything more than typical stereotyped “acrobatic” behaviors often seen in individually-housed rhesus monkeys. The authors provide no data on the frequency of just cranial implant touching with vs. without mirrors, and no visual evidence except for the single incident from the video. Why wouldn’t they report the number of implant explorations independently of the genital viewing?

My primary concern is that all monkeys failed the mark test, and the strongest apparent evidence of mirror self-recognition (MSR) was only seen in two monkeys following cranial surgery–a manipulation with strong tactile cues that could elicit exploration regardless of the mirror’s presence. Their argument rests largely on the assertion that the cranial implant is a “super mark” that somehow awakened a latent ability in the monkeys to self-recognize, but it’s unclear why the implant would be more visually salient than a brightly contrasting color marking on the face. The more parsimonious conclusion is that the tactile sensation of the implant was enough to elicit exploration, but even then, the authors provide no evidence that implant exploration occurred more frequently in the presence of the mirror vs. without.

If the authors’ hypothesis is true that a cranial implant serves as a “super mark,” then their procedures warrant replication, which frankly they should have done before making such a bold assertion. Currently within the Order Primates, the overwhelming preponderance of evidence still limits MSR and the fundamental cognitive precursor to a “sense of self” to the apes.

This back-and-forth is not just interesting in itself, both for what it says about monkeys and what it says about ourselves. It also says something about science. If you read some of the more extreme comments about the Hauser affair, you’ll find some people trying to indict the entire line of research into how human and animal minds evolved. This new paper, and its reception, shows just how absurd that radical rejection is. Science is bigger than individual scientists, and the mirror test will survive.

[Update: PLOS One paper linked fixed]