The “Yellow Snow” Test for Self-Recognition

The Mirror Self-Recognition Test

The mirror self-recognition (MSR) test has long been used to assess whether an animal is self-aware, whether it has a sense of self. In the classic version of the test, a colored mark is placed on an animal’s body in such a way that it can only be seen in a mirror. To pass the test, the animal must spontaneously use the mirror to detect the mark and then scratch or otherwise direct activity toward it, thereby indicating recognition of the image in the mirror as itself and not some other animal.

Not only is self-recognition considered to be an indication of higher cognitive functioning, but it has also been seen as a potential springboard to even more sophisticated abilities, such as being able to attribute mental states to other individuals (sometimes referred to as “theory of mind”).

To date, only a relatively few animals have passed the MSR test, including certain primates, dolphins, elephants, and, as we saw in a prior post, magpies.

But is the test itself biased? We humans rely heavily on our eyesight and may naturally – anthropocentrically – have settled on a test that is based on visual interpretation.

What about animals who rely more on their sense of smell – dogs, for instance? Well, Marc Bekoff, Professor Emeritus of Ecology and Evolutionary Biology at the University of Colorado, Boulder, wondered about this too.

The Yellow Snow Test

Over a five year period, Bekoff performed a study1 in which he diligently tracked the behavior of his own dog, Jethro, when Jethro encountered clumps of snow saturated with his own and other dogs’ urine (“yellow snow”) while walking freely along a bicycle path in Colorado on winter mornings.

Snow pile, snow pile, on the ground, who’s the finest smelling hound? (photo: Walter Jeffries)

Bekoff would wait until Jethro (a neutered male German Shepherd and Rottweiler mix) or other known female and male dogs urinated on snow, and then scoop up the clump of yellow snow as soon as Jethro was elsewhere and did not see him pick it up or move it (Bekoff used clean gloves each time and took other precautions to minimize odor and visual cues). Bekoff then moved the yellow snow varying distances down the path so that Jethro would run across the displaced urine: (i) within about 10 seconds, (ii) between 10-120 seconds later, or (iii) between 120-300 seconds later. After Jethro arrived, Bekoff recorded how long he sniffed at the yellow snow, whether he urinated over it using the typical male raised-leg posture, and whether urination immediately followed the sniffing (“scent marking”).

After compiling and statistically analyzing the data, Bekoff found that Jethro paid significantly less attention to his own displaced urine than he did to the displaced urine of other dogs. For example, when Jethro encountered the yellow snow within 10 seconds, he sniffed for longer than 3 seconds only about 10% of the time when it was his own urine, compared to over 80% of the time when it was other dogs’ urine. (Jethro did tend to have longer sniffs at his own urine when he arrived after more than 10 seconds, but in all scenarios he still sniffed significantly longer at the other dogs’ urine.) Likewise, he very rarely urinated over or scent-marked his own yellow snow, but frequently did so with the yellow snow of other dogs, particularly other males.

The following table summarizes the data collected (note that the reference to “120-150s” in the Arrives column appears to be erroneous, and should instead read “120-300s”):

In sum, Jethro’s behavior clearly demonstrates that he was able to discriminate the scent of his own urine from that of other dogs. Of course this is just one set of tests on one dog, but would it surprise anyone if other dogs showed similar abilities?

Is there a fundamental difference between an animal recognizing its own image in a mirror and one recognizing its own scent in yellow snow? There certainly are different cognitive process involved (Bekoff himself has suggested that the yellow snow test may be more indicative of a sense of “mine-ness” in dogs than of a sense of “I-ness”2).

At a minimum, though, the yellow snow test stands as a useful warning that we humans need to be careful not to make quick judgments about animal intelligence or cognitive capacity (or lack thereof) based on tests that are well-suited to humans, but that fail to match the skills and abilities of the particular animal.


1Bekoff, M. (2001). Observations of scent-marking and discriminating self from others by a domestic dog (Canis familiaris): tales of displaced yellow snow Behavioural Processes, 55 (2), 75-79 DOI: 10.1016/S0376-6357(01)00142-5.

2Bekoff, M. Considering Animals—Not “Higher” Primates. Zygon 38, 229-245 (2003).

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

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

Genetic comparisons offer one such clear illustration.

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

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


The Human-Chimpanzee Genome Comparison

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

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

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

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

The research team summed up these findings:

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

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

What Explains the Greater Positive Selection in Chimps?

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

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

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

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

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


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

Birds Display Their Animal Magnetism

In today’s post, I’d like to talk about something that many animals can do, and that humans simply cannot. I’m not referring to flying, breathing through gills, spinning webs, or running at 70 miles an hour across the African Savanna. I don’t even mean echolocation or pheromone detection or electroreception or polarized light detection, although some of these may be topics for future posts.

No, today I’d like to focus on magnetoreception, or the ability to sense the Earth’s magnetic fields as a means of perceiving one’s direction or location.

Many animals are able to sense magnetic fields, including honeybees, fruit flies, sea turtles, newts, lobsters, salmon, sharks and even bacteria, but some of the more in-depth and interesting research has been centered around migratory birds’ ability to use the Earth’s magnetic fields as a navigational aid as they make their long journeys.

For some reason, I've always felt strangely drawn to the North... (photo from Wikipedia, credit: Thermos)

While there are many aspects of this phenomenon that are still a mystery to us, scientists currently believe that there are two primary biophysical pathways that may explain how birds are able to navigate using the Earth’s geomagnetic fields. These two pathways are currently believed to coexist and complement each other, even though they involve very different processes.1

No, it's simple: just take a left at Norway and then bear right at Finland ... you can't miss it. (photo from Wikipedia, credit: Ernst Vikne)

The first pathway involves the use of iron-based receptors (crystals of a mineral known as magnetite) in the upper beak that can receive and transmit signals of a magnetic field directly to the bird’s brain via a specific nerve (the trigeminal nerve); the second pathway involves the activation of proteins called cryptochromes in the bird’s retina that, after being exposed to blue light, are sensitive to magnetic fields, enabling retinal cells to convert magnetic signals into visual ones and to transmit these signals to a specific sensory processing region (known as Cluster N) within the area of the bird’s forebrain responsible for vision.2

This second pathway may actually enable the bird to create images based on the magnetism fields – in other words, to actually see the Earth’s magnetism and use it as a navigational aid during migration, even during the dark of night.

Aside from being this being pretty cool, what is one to make of this from the standpoint of comparative cognition? Do we chalk one up for the birds (and the honeybees, fruit flies, sea turtles, etc.) and concede that humans are rather lacking in an important cognitive area?

I can already hear the objections. How can you compare this to those characteristics that truly set humans apart from the rest of animals? This is simply a heightened sensory ability, kind of like good eyesight or a fine sense of smell, and not that significant from the standpoint of higher cognition.

This is a fair point and an understandable (if anthropocentric) way to look at it, but there are still a couple of things you may want to consider:

First, we shouldn’t be overly dismissive of the amount cognitive sophistication involved in the long distance navigational feats. Think about it: migratory birds are able to travel, day and night, in all kinds of weather conditions, over great distances – sometimes thousands of miles – with a level of precision beyond our reach until the advent of GPS systems (thank you, Garmin). This sort of navigation is no simple process, either, as sensory input from multiple sources must be assessed, weighted, properly prioritized, reconciled and synthesized, all on a dynamic basis and in an environment when cues are constantly changing.

Also, consider whether this is another area where we humans may be tempted to slant the playing field to our advantage. While it’s easy to imagine our downplaying the significance of magnetoreception from a cognitive standpoint (after all, I just did), remember that we have no trouble in justifying to ourselves why “non-cognitive” human features, such as opposable thumbs and bipedalism, ought to be considered as important factors in distinguishing our capabilities from those of other animals. The point is not to argue that opposable thumbs weren’t critical to our becoming highly sophisticated tool-makers and users (I assume they were), but rather to suggest that we should be as flexible in thinking about factors pertinent to animal cognitive abilities as we are to those pertinent to our own.

Anyhow, time to fly away for the evening – see you soon!


1University of Oldenburg, Department of Biology and Environmental Sciences, Animal Navigation website, visited July 21, 2011.

2See, e.g., Heyers, D., Zapka, M., Hoffmeister, M., Wild, J., & Mouritsen, H. (2010). Magnetic field changes activate the trigeminal brainstem complex in a migratory bird Proceedings of the National Academy of Sciences, 107 (20), 9394-9399 DOI: 10.1073/pnas.0907068107, and Heyers, D., Manns, M., Luksch, H., Güntürkün, O., & Mouritsen, H. (2007). A Visual Pathway Links Brain Structures Active during Magnetic Compass Orientation in Migratory Birds PLoS ONE, 2 (9) DOI: 10.1371/journal.pone.0000937.

Tooling Around Underwater

Tool Time For Tuskfish

As reported last week in ScienceNOW1, a professional diver exploring the Great Barrier Reef off the coast of Australia recently snapped the first photos of a fish using tools. The diver, Scott Gardner, came across a blackspot tuskfish (Choerodon schoenleinii) that was hovering over a sandy area near a rock with a clam in its mouth. The tuskfish rolled on its side and, with a repeated cracking noise, slammed the clam against the rock until the shell fractured. Here’s one of the photos that Gardner took of the industrious (and hungry) tuskfish:

Tuskfish cracking open clam (photo credit: Scott Gardner)

While there have been anecdotal accounts of other fish using tools, this is the first time that this type of behavior has been caught on film.

What Is Tool Use, Anyhow?

In an interesting aside, this incident has brought to the forefront some of the ways in which it is difficult to define, and reach agreement upon, exactly what constitutes “tool use” in animals.  As noted in the ScienceNOW article, there has been previous debate over whether stingrays and archerfish targeting jets of water to capture prey constitutes tool use (is a solid external object necessary for there to be a tool?), as well as whether tool use “requires the animal to hold or carry the tool itself, in this case the rock.”

The research paper regarding this tuskfish behavior, which was published in the most recent issue of Coral Reefs2, the official Journal of the International Society for Reef Studies, argues that the tuskfish using the rock as an anvil to open the clam conforms to a definition of tool use first formulated by Jane Goodall back in 1970, that tool use is “the use of an external object as a functional extension of mouth or hand in the attainment of an immediate goal.” The paper adds: “The use of a rock as an anvil rather than a hammer could be considered a sign of intelligence considering the ineffectiveness of manipulating a freely suspended tool in water. The images certainly provide an interesting starting point for further comparative studies on tool use in fishes.”

The ScienceNOW article describes how Culum Brown, a behavioral ecologist at Macquarie University in Sydney, Australia, and a co-author of the Coral Reefs paper:

argues that it’s not logical to apply the same rules to fish as to primates or birds. For one thing, fish don’t have anything but their mouths to manipulate tools with, and for another, water poses different physical limitations than air. ‘One of the problems with the definition of tool use as it currently stands is it’s totally written for primates,’ he says. ‘You cannot swing a hammer effectively underwater.’

Those of you who pay close attention may already have noted that the definition of tool use can stir controversy. For example, beginning at the 10:34 mark in her video presentation relating to the awesome octopus, Maggie Koerth-Baker describes two very divergent definitions that might lead to different conclusions about whether the octopus engages in tool use: (a) a stricter definition that requires that an animal use a solid object to solve an “immediate problem,” rather than just to provide defense, and (b) a broader definition holding that tool use occurs whenever an animal modifies an object so as to alter some aspect of its environment.

Food For Thought

In considering tool use by animals, here are some things you might want to ponder:

  • Which of the above definitions makes the most sense to you?
  • Does it matter whether the behavior is performed by a captive animal (like the New Caledonian crow) or in the wild?
  • Are definitions of tool use inherently anthropocentric and subjective? That is, are we trying to come up with a definition that basically requires the behavior to look like something a human would do (if it really is a tool, then I should be able to see the Craftsman logo) before we accept it?
  • Is it significant whether the behavior is widespread? That is, if the behavior is only observed once or twice, is it a fluke? If the behavior is widespread, is it mere instinct?
  • Is nest building by birds an example of tool use?


There will undoubtedly be more AnimalWise posts about tool use. In the meantime, if you run across any tuskfish, you should look very closely to see if you can see their very small, teeny-tiny tool belts. They really are quite cute.

Here are some more photos (note, the following pictures may not be suitable for small children and clams):

More Scenes from "Crouching Tuskfish, Hidden Clam" (photo credit: Scott Gardner)


1ScienceNOW, “Diver Snaps First Photo of Fish Using Tools,” July 8, 2011.

2Jones, A.M., Brown, C., Gardner, S. Tool use in the tuskfish Choerodon schoenleiniiCoral Reefs. DOI:10.1007/s00338-011-0790-y.

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