Inside Animal Minds: Bird Genius

PBS Airdate: June 24, 2015

NARRATOR: What are they thinking? What really makes them tick?

BRIAN HARE (Duke University): Oh, look at that face!

NARRATOR: Is there any way to get inside the animal mind?

BRIAN HARE: What I really want to know is: What is it like to be an animal? What's it like to be inside their head? And what are the problems they have to solve? And how do they think? And are they like us, or are they like something totally different?

NARRATOR:They have some amazing abilities. Is it instinct, training or something else? Cutting-edge animal science reveals new answers, getting inside their heads in ways never before possible.

MARK SPIVAK (Comprehensive Pet Therapy): Without proper training, the dogs would just run scared from the M.R.I.

NARRATOR: We put different species to the test in search of the roots of animal intelligence. Who are the best problem-solvers? Who wins the battle of the super senses? Dive deep into the animal experience, to explore their language, relationships, even emotions.

FRANS DE WAAL (Emory University): If you start giving one of them grapes, which are far better than cucumber, then the one who gets cucumber becomes very upset.

NARRATOR: Are they more like us than we ever thought possible?

DIANA REISS (Hunter College): Having a sense of self might go with complex understanding of others.

NARRATOR: In this episode, “How smart is this ‘birdbrain?'”

ALEX TAYLOR (University of Auckland): Imagine that you're a crow. Here's your food, in a deep hole. How would you go about, with the tools available to you on this table, solving this problem?

NARRATOR: They use tools, and pick locks. But what happens in a brainy smackdown between this bird and man's best friend?

DOG OWNER: Come on, concentrate.

NARRATOR: How did a creature with such a tiny brain get so smart?

NICOLA “NICKY” CLAYTON (University of Cambridge): A crow's brain, in relative terms, is as big as a chimpanzee.

BRIAN HARE: Why is it that that animal can solve those problems? Why would we observe that level of flexibility in that species of bird that we don't observe in another species?

NARRATOR: Inside Animal Minds: Bird Genius, right now, on NOVA.

We've always admired birds for their grace and beauty, but we don't usually think of them as incredibly bright. After all, isn't “birdbrained” the very essence of stupidity? But now, scientists are discovering bird brains that put most other animals to shame.

That's no surprise to Lloyd Buck. Lloyd handles birds for TV and film, and one of his stars is a raven, named Bran.

LLOYD BUCK (Bird Handler): Well, this is Bran, and he's a three-year-old raven. We've had him since he was about 10 days old, so he's what you call “complete social imprint” on humans, but he's particularly bonded with me. We share a very, very close bond.

NARRATOR: Captive ravens can live 60 years or more, so Lloyd and Bran are in for a long-term relationship. But, right now, Bran wants to explore his relationship with the camera.

LLOYD BUCK: Oh, sorry. Going to hold finger? No. Sorry. He likes your camera. It's the highest point.

NARRATOR: To keep his demanding bird occupied, Lloyd gives Bran puzzles to solve on his own.

Here's a problem Lloyd first presented to Bran a few months ago, in his aviary, where he has a birdbath: he places a piece of food inside a plastic bottle and crushes it, so the food is trapped.

But this doesn't stop Bran. First, he adds water. Next, he swishes it around, and the liquid carries the food past the restriction and out.

That is a clever piece of problem solving.

LLOYD BUCK: Good boy!

NARRATOR: Bran wasn't taught to solve this problem. Lloyd just gave him the challenge one afternoon and left Bran alone to try to find a solution himself.

LLOYD BUCK: So, we've presented him with that problem, and through his own intelligence and problem-solving abilities, he worked out to use his own water, what he had around him, to his advantage, which I think shows a lot of intelligence.

NARRATOR: People who've observed crows and ravens closely have said that they are pretty clever creatures. But in recent years, new experiments are probing deeper, trying to solve the secrets of their problem-solving brains.

And beyond birds, researchers are discovering more and more animals doing things we once thought were strictly human.

So, how smart are these creatures? Inside their minds, are they analyzing and solving problems the way we do? Or are all these animals' skills more like parlor tricks, the result of training and fuelled by instinct?

BRIAN HARE: What I really want to know is: What is it like to be an animal? What's it like to be inside their head? And what are the problems they have to solve? And how do they think? And are they like us, or are they like something totally different?

NARRATOR: From the beginning, one way that humans have solved problems has been by using tools. It was once considered proof of our superior intellect, but it turns out, all kinds of animals use tools. Even an octopus, a close relative to clams and oysters can do it.

Off the coast of Indonesia, this veined octopus finds a discarded coconut shell on the seafloor, and uses it to protect itself from predators. First it crawls inside the hard shell, then it uses its eight arms to carry it off.

JUSTIN GREGG (Animal Cognition Researcher): People used to think that tool use was unique to humans, but of course that has never been the case. Ever since Darwin, we've known that animals have been using tools, but what's really unique is tool manufacturing.

Humans, of course, manufacture a huge array of tools for different purposes.

NARRATOR: And, for centuries, we thought that only humans were smart enough to make a tool. All that changed in the 1960s, when Jane Goodall discovered chimpanzees breaking all the rules.

JANE GOODALL (File Footage): I saw this dark shape hunched over a termite mound. He's making arm movements as though he's sliding it across the ground, and, obviously, eating.

NARRATOR: Not only did Goodall see chimps using blades of grass as tools to fish for termites, but she also witnessed them making tools by stripping leaves off twigs.

Her research supervisor was amazed.

JANE GOODALL (File Footage): He sent his famous reply, “Now, we have to redefine ‘man,' redefine ‘tool' or accept chimpanzees as humans.”

NARRATOR: Goodall's discovery shattered our ideas about what sets us apart from the rest of the animal kingdom. We had to accept that animals were smarter than we'd given them credit for.

BRIAN HARE: She created basically an environment that we have to think about their minds, and we have to recognize the fact that, in many cases, animals may have abilities that we thought were the province of humans.

NARRATOR: Today, animals with impressive skills and brainpower can be found on land and sea and in the air. And some of the most surprising, can be found here: New Caledonia.

Lying nearly a thousand miles east of Australia, this remote Pacific island is home to an animal hailed by some as one of the smartest on Earth. In part because, along with humans and chimps, it is an expert toolmaker. Meet the New Caledonian crow.

In the wild, the crows shape hooked sticks and use them to spear grubs. But today, biologist Alex Taylor is designing an experiment to see if crows can use tools in new ways to solve problems.

Alex works with wild birds, which he releases after a three-month period. This one is nicknamed 007. 007's mission is to get a tasty piece of meat out of this narrow plastic box.

ALEX TAYLOR: What we have here is our deep hole. This has got some meat in.

NARRATOR: The meat is positioned so deep in the narrow box, it's out of reach of 007's beak. But Alex has placed a number of other objects nearby. The question is, can 007 use them to get the piece of meat?

ALEX TAYLOR: Imagine that you're a crow. Here's your food, in a deep hole. How would you go about, with the tools available to you on this table, solving this problem?

NARRATOR: 007's toolkit includes a short stick hanging on a piece of string, three stones inside wooden cages and a longer stick trapped in a plastic box.

First, the crow must use the short stick to get the stones and then use all three stones to get the long stick.

ALEX TAYLOR: And now the crows can take this and probe it into the hole and roll, much better than I can, the food out of the hole and get themselves a nice tasty reward.

NARRATOR: It's a complicated task. 007 is familiar with the individual pieces of the puzzle. He's done each of them separately for a treat. For example, he's used stones to get a piece of meat out of the trapdoor box. But this is the first time he's seen the tools arranged like this: eight, separate stages that must be completed in a particular order, if the puzzle is to be solved.

At first, he takes time to check things out, then goes for the little stick. He tries to use it to reach the meat, but it's too short, so he sets off to get the first stone.

Got it!

But he doesn't seem to know what to do with it. He gets another stone, but he appears to be stuck.

Now, something seems to click. He puts the first stone into the box, where the long stick is trapped, then the second stone and returns to collect the last one. He's got the long stick and goes right for the meat, the final stage. Success!

007 successfully executed all eight tasks to collect the out of reach treat. How did he do it? One of the striking things is how skillfully 007 employs a number of different tools to get what he wants. That's because New Caledonian crows are born tool-users.

Auguste von Bayern is an expert in corvids, the family of birds that includes crows, ravens, jays and rooks, like this one.

New Caledonian crows have evolved with several physical features that allow them to more easily manipulate objects, particularly sticks.

AUGUSTE VON BAYERN (University of Oxford): New Caledonian crows are famous for their very straight beak, and it turns out this is an adaptation to tool use. This is really striking because other corvids have curvy beaks. You can see this very well in the rook.

NARRATOR: The straight beak allows the New Caledonian crow to hold tools in front of it, in its line of vision. But that's not all. New Caledonian crows have eyes set closer together than other birds, which means there is a significant overlap of what their two eyes can see. This helps the crow to focus on the end of a tool.

AUGUSTE VON BAYERN: They can see the working end of the tool extremely well and look into the narrow holes and see what they're doing.

NARRATOR: Tools aren't a recent discovery for the New Caledonian crow. They've been using them for so long, they have physically adapted to tool use.

AUGUSTE VON BAYERN: No other adaptation like this has been described in any other tool-using animal, and so it's fairly special.

NARRATOR: So the eight-stage puzzle didn't pose too much of a physical challenge for the crow, but how did it figure out which order to perform the tasks? What was going on in its mind? Did it imagine the entire solution to the puzzle? Was it just using trial and error, step by step? Was it conditioned by its training on the individual parts? Or is the answer somewhere in between?

BRIAN HARE: Can animals, essentially, imagine or infer or reason about how to solve a problem they've never seen before and come up with a solution that then they can act on?

NARRATOR: On the face of it, the crow's abilities seem impressive. But, look closely enough, and the natural world is filled with examples of animals behaving in what look like clever ways.

The spider spins a web that is precision-engineered to catch flies. Turtles navigate through thousands of miles of featureless ocean, returning to the same beaches every year to lay eggs. It's as if they hold a nautical map in their heads.

So, are the crows really so unusual?

To begin to find out, we need to delve into the animal mind and see how other animals solve problems. Like the honeybee, a small animal that is able to do something that seems incredibly smart.

Insect expert Adam Hart is interested in how bees solve a very difficult problem. Inside a typical hive there are about 40,000 honeybees. Every day, they face the challenge of having to feed themselves. The pollen and nectar that bees eat is only available when the flowers are in bloom, so in spring and summer the bees have to collect enough of it to eat and enough to turn into honey to keep the hive going through the winter.

ADAM HART (University of Gloucestershire): Sometimes they can fly more than six kilometers to get enough nectar and pollen back, because they need a plentiful and vast supply.

NARRATOR: Finding enough food is a huge logistical challenge, but the bees have an almost incredible solution.

Adam has set up an observation hive. It's completely dark inside, and, so, infrared cameras reveal what's going on.

ADAM HART: Initially, it looks very chaotic. It looks like bees are everywhere. But you can see some vibrations going on and some movements, which are actually part of a very sophisticated communication system.

NARRATOR: The bees perform a striking behavior that's key to solving the problem of gathering enough food. It's called the “waggle dance.”

ADAM HART: The waggle dance is a very sophisticated way of directing foragers towards nectar in the environment; it's telling them where to go.

NARRATOR: This bee has found a good source of food, and she's performing a set of very precise movements to tell the others exactly where to find it.

ADAM HART: It tells them the direction and the distance of the nectar.

The best way to understand how the waggle dance actually works is to get up high, because then you can get an understanding of the landscape in which the bees are operating.

NARRATOR: The meaning of the waggle dance was first proposed in the 1940s, but it wasn't proven until 2005, when scientists were able to track bees using radar technology.

This church tower gives Adam a bee's-eye view of the countryside. From up here, it's easy to see where the sun lies over the landscape and where it would be if it were on the horizon. One of the dancing bees in the hive was waggling at an angle of five degrees from a vertical line. So, if this tower were a massive bee hive, the waggle dance would be telling us that the nectar is five degrees from the relative position of the sun.

ADAM HART: But they can also advertise distance, because the duration of that waggle run, that central component, tells the bees how far away the resource is, the closer it is, the shorter the waggle run.

NARRATOR: So honeybees survive the winter by using what we call geometry: they compute angles and distances and then transmit that information to their hive-mates. How can a small insect, with such a tiny brain, do something so incredibly sophisticated?

ADAM HART: It's instinct. It's hardwired into the bee's brain. And we know that, because, if you take older bees out of the hive, the younger bees, who have never been exposed to the waggle dance, will spontaneously begin waggle-dancing and doing this behavior. It's absolutely built in, it's instinctive.

This is an evolved behavior, an evolved instinct, which leads to the higher survival of honeybees.

NARRATOR: Instinctive behavior is often crucial to the survival of a species. But the animals don't need to have any real understanding of what they're doing.

MARIO PESENDORFER (University of Nebraska): Animal behavior often appears very complex, but there might be very simple rules underlying the pattern that we see.

NARRATOR: So what about the New Caledonian crow?

Researchers have found that, like bees and their waggle dance, young crows will instinctively pick up sticks with their beaks, even if they've never seen another crow do it.

But was 007 acting just on instinct, when he solved the eight-stage problem? Nicky Clayton, one of the world's leading experts on corvids, is convinced that it's something more.

NICKY CLAYTON: The behavior of the New Caledonian crow, when it's solving one of these problems, is far more complex than anything that would be solved by an instinctive mechanism.

NARRATOR: So, if it isn't pure instinct, what is it?

Scientists disagree about what exactly is going on in the mind of a crow, like 007, or a raven, like Bran, when they're solving problems. Some researchers think the animals are instinctive tool-users and can be conditioned by training to use them in ways that just appear clever. But others believe that animals show real smarts when they tackle novel problems that they've never seen before.

To demonstrate this, we set up a little competition to solve another puzzle, between Lloyd Buck's raven, Bran, and an animal a lot of people think of as pretty smart: a dog.

Actually two dogs: French poodles named Itchy and Scratchy.

It's a specially designed puzzle box. Inside the blue ball there's a tasty snack that each contestant likes to eat: rat meat for Bran, a doggy treat for Itchy and Scratchy.

The challenge is to remove the blue ball from the two plastic boxes. First, the contenders have the chance to familiarize themselves with parts of the puzzle box. As usual, Lloyd leaves Bran to investigate on his own.

LLOYD BUCK: That's a good boy.

NARRATOR: The dogs are introduced to the components by their owner.

DOG OWNER: Itchy, come on, Itchy! Come on, concentrate. Look!

NARRATOR: The outer box has a hinged door that can be opened by pulling on a pink ball, tied to the door with a string. Another ball and string can then be used to pull out the inner box. Then a third ball and string must be pulled to remove the lid, freeing the blue ball, which holds the treat.

And now, the moment has come. The animals are about to face the test for the first time. This is dog versus raven.

DOG OWNER: Itchy, solve this. Solve that. Okay, I'll be back. Solve it.

NARRATOR: Bran gets the tasty treat. The dogs didn't seem to even realize there was problem there to solve, despite some guidance. But Bran was so quick, we have to use a high-speed camera just to see how he did it; an emphatic win for Bran and his corvid kind.

It's clear that corvids, like these, have a knack for solving problems that involve getting food out of hard-to-get places, even in situations they've never seen before.

While dogs are very good at paying attention to humans and can be trained to carry out complicated tasks, they're not so good at tackling novel problems like this one, despite the fact that there's food involved.

BRIAN HARE: Why is it that that animal can solve those problems? Why would we observe that level of flexibility in that species of bird, that we don't observe in another species?

NARRATOR: Here, at Cambridge University, in England, Nicky Clayton is trying to find out how the corvid mind works. She sets up experiments to break down the different abilities these birds use to solve problems. And she gives one of them, a Eurasian jay, named Hoy, a particular challenge.

First, he's presented with a plastic tube. When he puts a rock in at the top, a tasty food reward, a worm, comes out at the bottom.

When he's got the hang of that, Nicky gives him a new test. She drops some worms, his favorite food, into a tube of water, out of reach and leaves a pile of stones next to it.

NICKY CLAYTON: There's a delicious, tasty worm floating on the top. At the moment it's out of reach.

NARRATOR: Then, Hoy picks up a stone and drops it in the tube. Does Hoy actually understand that a sinking stone will cause the water level to rise, and this in turn will allow him to reach the worm?

When Nicky gives him the same tube, but this time with the worm sitting on sand instead of water, Hoy does not use the stones. Nicky believes he understands the difference.

NICKY CLAYTON: He seems to understand that it's only any good if there's a liquid in the tube.

NARRATOR: It's a very useful skill when it comes to solving problems: the ability to make a connection between cause—the stone—and effect—the rising water level.

ALEX TAYLOR: Cause and effect is the ability to understand what causes what. Why did a particular event occur? If you can identify that, so, you know what causes it, and that means, as humans, we're able to recreate that same cause to get that same effect, that's a really powerful skill.

NARRATOR: To figure out step one, putting stones in the tube, Hoy took the knowledge from the training task and transferred it to the new one. This is another skill many corvids display when tackling problems: the ability to think flexibly, to use information learned in one situation and apply it to another.

NICKY CLAYTON: Flexible thinking is the ability to transfer information, knowledge, from one problem to a brand new problem. So, it's applying knowledge to new contexts.

NARRATOR: And this is how the New Caledonian crow solved the multi-stage problem.

BRIAN HARE: New Caledonian crows need flexibility in their environment they evolved in to process food, and to be able to get access to food in new ways, using tools in, in settings they may not have encountered before.

NARRATOR: This also explains how Bran quickly solved the puzzle box. The birds were thinking flexibly, an ability that seems to be missing in dogs.

So why are some animals better at solving problems than others? It's something we don't yet fully understand, but one thing we do know is that the answer lies somewhere in here: the animal brain itself.

NICKY CLAYTON: So what you can see here are a couple of pickled brains. That's a crow brain, and that's a dog brain.

NARRATOR: The dog's brain is clearly bigger than the crow's brain, and so you might expect dogs to be smarter than crows. But we've seen that's not the case; crows can solve complex problems that dogs can't. So, there must be more to cleverness than just brain size.

To explore what that might be, Nicky's gathered a range of preserved animal brains collected by Victorian naturalists. The first thing we see is that the brains are all different sizes, but when they're arranged in order of the size of the animal they come from, we see a pattern.

NICKY CLAYTON: So, the bigger the body, the bigger the brain, and it seems that in fact, the bigger the body the more brain you need to control it.

NARRATOR: Most of the time, there's a straight-line relationship between the mass of the body and the mass of the brain. Larger animals need more extensive nervous systems to coordinate their bigger bodies. Their sense organs are also bigger, so they require greater amounts of neural tissue to process all of the extra information being gathered. You can calculate how big you'd expect any animal's brain to be, by its body size.

NICKY CLAYTON: This is where the dog occurs. It's bang on the line, just what you'd expect, given its body size.

NARRATOR: Most animals are more or less on the line, but not all. Some animals sit above the line, as we humans do. Our brains are very large for our body mass. The difference between expected brain size and actual brain size is known as the encephalization quotient, or EQ. The further above the line, the greater the EQ.

So where is the crow?

NICKY CLAYTON: The crow's brain is above the line, so that means that it's got a much bigger brain than you'd expect for its body size, in fact it's twice as big.

NARRATOR: As bizarre as it may seem, while the dog's brain is about 10 times as big as the crow's brain, in absolute size, in relative terms, the crow's brain is twice as big as the dog's.

BRIAN HARE: So maybe evolution has really forced them to invest more in their brains, and that's partly what makes them so flexible.

NARRATOR: And the crow isn't alone in having a brain twice as big as we'd expect.

NICKY CLAYTON: The crow is the same distance above the line as that of the chimpanzee, in other words a crow's brain, in relative terms, is as big as that of a chimpanzee.

NARRATOR: These big-brained animals share some impressive skills, including the manufacture of tools. This highlights another key concept in problem solving, the ability to innovate.

Alice Auersperg works with an endearing and inquisitive type of bird, the Goffin's cockatoo, an Asian parrot. Like the crows, these are big-brained birds but with a playful personality. Alice studies these animals to find out how adept they are at innovating.

ALICE AUERSPERG (University of Vienna): My Goffin cockatoos are extremely, very, very curious. So, when they see an object, for example, let's say a human, they go for shoelaces, watches, glasses.

NARRATOR: To investigate what's going on in the minds of these parrots, Alice created this: the lockbox. Trapped inside is a tasty nut, securely held behind this elaborate locking mechanism.

To see how it opens, we need to employ the services of a master safecracker, or Muppet, as he's known.

Before Muppet begins, any humans in the room have to put sunglasses on. This is so that the bird can't take any cues from eye movement. Muppet has done this before. He wasn't taught by Alice, but watched other birds do it. And now he delivers a master class in operating the lockbox.

He quickly removes the pin and then the screw. He easily discards the central bolt, which, in turn, allows him to shift the locking wheel. This then releases the final bolt, and voila! He's reached the nut inside.

Now, for the second part of the experiment: the transfer test.

ALICE AUERSPERG: After the cockatoos had cracked the problem, we tested whether they were only running through sequence of learned behaviors or whether they could react flexibly to changes.

NARRATOR: To make sure Muppet hasn't just learned the sequence by heart, Alice can change the lock sections around, or even remove them entirely. This creates a completely new challenge for Muppet.

Alice removes the middle part, the bolt. With the bolt gone, the upper section is now redundant, leaving only the lower parts in operation. The question is whether Muppet can see the new problem, and work out a new solution.

If he doesn't understand how the locks work, he'll repeat what he did before and go for the pin at the top. But if he recognizes that the problem has changed, and that removing the pin at the top is unnecessary, he'll go right for the wheel.

So now: the moment of truth. Muppet ignores the pin and screw at the top and goes straight for the wheel and then the bolt. And he's in, in less than 10 seconds.

This is the first time Muppet's seen this configuration and he gets it right. Alice believes this provides crucial insight into his mind.

ALICE AUERSPERG: The birds in the transfer test spontaneously reacted to novel changes that they had never encountered before. That indicates that this is, cannot be trial and error learning.

NARRATOR: Since Muppet went straight for the middle bolt, it seems he has some understanding of how the lock system works and can apply it to different problems.

He's one of a small group of animals that can do this. But the problems are right in front of them. We humans can take problem-solving a step further: we use our minds to project into the future and anticipate problems, before they even happen, and plan to avoid them.

It's something we long thought only humans could do, but can these clever animals do it, too? There is a common behavior in the animal world which seems to be all about planning for the future. It's called caching. It's what squirrels do in autumn, hiding nuts in the ground so they can be dug up and eaten in the winter.

Here, on the island of Santa Cruz, off the coast of California, lives a bird that has caching down to a fine art: the island scrub jay, another clever corvid.

Mario Pesendorfer is in the middle of a three-year project to find out more about them.

MARIO PESENDORFER: We're looking at the habitat called “Oak Chaparral,” which is home to the island scrub jay. And it's dominated by these scrub oaks, and this is where the scrub jays, the island scrub jays, get their acorns.

NARRATOR: Scrub jays love acorns. But they aren't available all year around. On Santa Cruz, boom time comes in autumn when the oak trees drop their acorns. This is when the jays get busy.

MARIO PESENDORFER: They pick up the acorns and they fly with them somewhere, and they hide them in the ground, and that's what we call “scatter hoarding,” because they scatter their hoards all over the place. So they store their food for the winter all over their territory and then they come and get it back when it's raining and cold and there's nothing else that they can eat.

NARRATOR: Mario uses G.P.S. to keep an inventory of the acorns the jays put away in hidden caches. There's quite a few to keep track of. In fact, each jay caches thousands of acorns.

MARIO PESENDORFER: They take out 5,- to 6,000 acorns a year, out into this landscape and hide them all over in little cracks and crevices and below other plants.

NARRATOR: But, of all these, how many can they find again?

MARIO PESENDORFER: Of 6,000 acorns that they cache, we think that they recover about a third.

NARRATOR: These scrub jays aren't the only corvids that cache food. Another American corvid, the Clark's nutcracker, caches seeds in even greater numbers.

MARIO PESENDORFER: It remembers up to 10,000 caching locations a year, quite accurately. And they are often spaced up to 20 kilometers or 30 kilometers apart.

NARRATOR: The ability to remember thousands of locations is impressive enough, but these corvids go further. They have a sense of when they buried each piece of food and know when they need to retrieve it.

JUSTIN GREGG: They know that if they hide certain kinds of food, they have a timeframe that they need to get worms, for example, faster than nuts, because worms will rot. So, they have to be faster about getting the worms.

It suggests they have a more sophisticated idea about the way that they are hiding their food.

NARRATOR: But how sophisticated? Could these birds really have a sense of time? It's a question that's greatly intrigued Nicky Clayton. She studies western scrub jays, close relatives of the Santa Cruz birds, also renowned for their caching behavior.

Nicky wants to discover whether they can do more than just remember where and when they've buried food in the past.

NICKY CLAYTON: If they can travel back in their mind's eye, to think about the past, can they also travel forward in the mind's eye, to think about the future?

Can they plan ahead?

NARRATOR: To find out, Nicky creates an experiment based on a very human annoyance, waking up to find breakfast is off the menu.

For six days, the birds are housed in this aviary, split into three zones. In the middle is the dining room, where the birds are fed during the day. And at either end are the bedrooms, where they are kept at night.

But there's a twist.

Kept overnight in this bedroom on the right, the birds are served an early breakfast. But kept overnight in this room on the left, they get no breakfast and go hungry 'til mid-morning.

The birds experience this daily routine for almost a week.

NICKY CLAYTON: So we give them three lots of experiences of waking up in the hungry room, and three lots of experiences of waking up in the room that serves breakfast. But the important point is that the birds themselves didn't know which room they'd end up in, on any given day.

NARRATOR: But then Nicky starts allowing the birds to cache food. She places trays full of sand in both the hungry and breakfast rooms. The birds can use these to bury dead grubs in. The question is, where will they choose to store the food?

Nicky wants to know if the birds can use their experience of the hungry and breakfast rooms and plan for the future.

For Nicky, the results are clear.

NICKY CLAYTON: The birds cache about five times as much in the hungry room as they cache in the breakfast room.

NARRATOR: The scrub jays store five times more grubs in the room where no breakfast is served, than in the room where they are well-fed.

NICKY CLAYTON: They can imagine what they're going to need the following morning, when they wake up hungry, so they can solve a problem before it's even happened. So what this experiment shows is that the birds can plan for the future.

NARRATOR: Nicky believes the jays' caching behavior is far more than mere instinct. She thinks they have a grasp of the past, but can also anticipate future need.

NICKY CLAYTON: It's called mental time travel. It's the ability to go backwards and forwards in the mind's eye, so it's about projecting yourself in time, to remember the past and to imagine the future.

NARRATOR: It's a skill that is very important to us humans.

ALEX TAYLOR: We're able to remember what we were doing yesterday, we're able to plan what we want to do tomorrow. And this ability to mentally travel in time has really allowed humans to take over the world in a way that no other animal species has.

NARRATOR: In humans, mental time travel is not a skill we're born with. It takes a while to develop. To demonstrate this, these children are about to undergo the candy challenge. The task is simple. Each child is given a piece of candy. They're told if they leave it uneaten, then they'll get a second one 15 minutes later. The question is whether they'll imagine their future selves happy with two candies or will the lure of instant gratification be too much?

It's a skill that some are clearly better at than others.

NICKY CLAYTON: I think this cognitive capacity is highly sophisticated. We know that young children don't start developing these kind of skills until they're at least four years of age.

NARRATOR: So, whether you're a bird or a human, mastering mental time travel has its advantages. To solve new problems, it really helps if you can understand cause and effect, think flexibly, apply what you've learned to new situations and plan into the future.

It's a rare skill set, and the animals that have it are a diverse group, from the chimps to the parrots to the corvids. So, what's special about these animals? What could they possibly have in common?

NICKY CLAYTON: On the face of it, of course, crows and chimpanzees are very different.

NARRATOR: The key is not the physical nature of these animals, but the conditions that have made them what they are.

BRIAN HARE: There's some common pressure. There's something common about the environments or the experience of those animals through their life that's pushing them to become more intelligent.

NARRATOR: These animals live in challenging environments. Sometimes their favorite foods aren't readily available. They have to be flexible in order to survive.

JUSTIN GREGG: So, there is definitely a relationship between having to find food in complicated ways, having to deal with new, ever-changing environments, and those things that we would put under the definition of intelligence.

NARRATOR: Having a varied diet and being flexible in their search for food seems to have increased their chance for success. But there's something else that crows and parrots seem to share. They live in groups.

BRIAN HARE: When we see animals that can solve more complex problems than others, one of the threads that people are excited about, is maybe it's something about the complexity of their social organization that animals that have to deal with social complexity are the same animals, the same species that are solving many of these difficult problems.

NARRATOR: Whether they walk or fly, some of the best problem-solvers in the animal kingdom may not be quite so different from one another as they first appear.

Researchers are trying to figure out exactly why complex social lives might create better problem-solvers. Could one explanation be that the animals share knowledge? If they come up with a good idea, can they pass it on?

New Caledonian crows have lots of good ideas. They are precision tool-makers. This one is in the process of crafting something we'd normally expect only of humans. It's making a hook that it will use to catch prey.

Alex Taylor is investigating whether these birds are able to share their tool-making skills with each other.

ALEX TAYLOR: What the crows have done is they've rounded off the end, and they've actually carved out a tip onto the end of the tool, so this tool works as a functional hook. Now, this is really impressive, because no other species actually makes hook tools, apart from ourselves, not even chimpanzees.

NARRATOR: And of even more interest to Alex are these intricately cut tools from the leaves of the pandanus tree. Unlike the hooks, there are distinctly different types of pandanus tool.

ALEX TAYLOR: This is a single-step pandanus tool. Essentially, it's a rectangular piece of leaf that's been cut out from a larger piece of leaf. But the crows have gone further than making a simple rectangle. They also make two-stepped tools. What we've got is a step so now the end is nice and fine, so now the crow can get the tool into small areas.

NARRATOR: The third, and most elaborate type of tool is called a multi-step pandanus tool.

ALEX TAYLOR: This tool has a series of steps cut into it, and it has that very fine tip and, again, that broad end.

NARRATOR: And across the island, different groups of crows use different types of these tools. In the south, more simple fragments are found, but as we move north, the crows start to favor more complex, multi-stepped tools.

That means that different groups of crows have their own ways of doing things. And in human society we call this “culture.”

BRIAN HARE: Animals are creating innovations, and they're actually passing them on to future generations, by learning from one another. And, basically, what we can conclude is that there are many species of animals that have simple forms of culture. Humans are not alone for having culture, not at all.

ALEX TAYLOR: So we're seeing different populations that have a single tradition. We've been collecting tools for the last 15 to 20 years, and these traditions have persisted.

NARRATOR: So are parents passing down these tool designs to their offspring?

A rare glimpse of how this might happen has been captured on camera. Of all the birds, these crows have one of the longest juvenile periods or childhoods; youngsters stay with their parents for two years.

Here, an adult bird is using a stick to probe for grubs hidden inside a log. A juvenile stands by and watches. The adult departs and leaves the stick in the hole. The younger bird can now try the tool out, although this one has some way to go before becoming an expert like its parents.

It looks like one way ideas spread through the crow population is through family groups, the social circle. And Alex's research suggests something even more extraordinary: that with each generation of crows, the tools are honed and improved.

ALEX TAYLOR: The crow's tools have got progressively better over time. As they've passed on these tool designs between them, they've added small tweaks, and this has made the designs more and more efficient.

NARRATOR: The New Caledonian crow has only been closely studied since the early 1990s. In that short period, scientists have revealed problem-solving skills that seem similar to those of our closest cousin, the chimpanzee. But perhaps the most exciting thing is that we're just beginning to get a glimpse into the minds of these animals.

BRIAN HARE: We keep finding, over and over again, that we share the planet with other animals that do remarkable things that we thought only we do.

NARRATOR: And who knows what else they might be capable of?

Inside Animal Minds: Dogs & Supersenses

PBS Airdate: April 16, 2014

NARRATOR: What are they thinking?

BRIAN HARE (Duke University): Oh, look at that face!

NARRATOR: Is there any way to get inside the animal mind?

BRIAN HARE: What I really want to know is what is it like to be an animal, what are the problems they have to solve? And how do they think? And are they like us, or are they like something totally different?

NARRATOR: They have some amazing abilities. Is it instinct, training or something else? Cutting-edge animal science opens a new window on the roots of animal intelligence, exploring their language, relationships, even emotions.

FRANS DE WAAL (Emory University): If you start giving one of them grapes, then the one who gets cucumber becomes very upset.

NARRATOR: Are they more like us than we ever thought possible?

DIANA REISS (Hunter College): Having a sense of self might go with complex understanding of others.

NARRATOR: In this episode: “Who wins the battle of the super senses?”

ALEXANDRA HOROWITZ (Barnard College, Columbia University): They have hundreds of millions more receptors in their nose than a person does.

NARRATOR: But could a dog smell time?

CHRISTINE THRELKELD: Five o'clock, he's there, at the door, waiting for him.

NARRATOR: How do different species experience the world?

BRIAN HARE: There are animals that have completely different senses than we have. It would be close to impossible to conceive what that might be like.

NARRATOR: A new look Inside Animal Minds: Dogs and Super Senses, right now, on NOVA.

What's going on inside animal minds? How can we even begin to understand them, what they know and how they think?

ALEXANDRA HOROWITZ: If we're interested in knowing anything about what an animal experiences, I think we have to know the kind of information that they perceive, and that's all about their senses.

BRIAN HARE: I think our senses are on the front line of everything we're doing mentally.

NARRATOR: But when it comes to the sensing the world, all animals are not created equal.

We humans rely on five primary senses, but some animals have the power to perceive things in ways we can't even imagine. Can we ever understand how their super senses shape their minds and their behavior?

Scientists are trying to step into the skin and fur and feathers of all kinds of creatures to try to discover how they sense their world. And they're finding that some of the most impressive powers of perception can be found very close to home.

As any dog owner knows this animal can be a bit obsessed with smell.

ALEXANDRA HOROWITZ: So, for a dog, I think you have to understand that they are going to experience the world through their nose. The dog's entire experience will be about sniffing everything they encounter in the world.

NARRATOR: But just how good is this nose?

ALEXANDRA HOROWITZ: The dog's sense of smell is much, much, much more acute than the human's sense of smell.

NARRATOR: To find out just how powerful a dog's sense of smell can be, we're putting a particular pooch to the ultimate test. Neil Powell trains sniffer dogs, and one of his top performers is Fern. Today, she's going to try to sniff out something that's been hidden, a canister containing meat. But here's the twist: the canister is not hidden in the woods or even on dry land; it's at the bottom of this lake, 20 feet under water.

NEIL POWELL (National Search and Rescue Dog Association, United Kingdom): So, this is an ultimate for the dog's scenting ability. It's, it's probably as difficult as it gets.

NARRATOR: Fern has been trained to detect bodies that have come to rest beneath the surface of the water. Several hours ago, a team dropped the meat in the lake and recorded its position with G.P.S.

Neil only knows roughly which section of the lake it's in, an area equal to about 30 acres. The question is can Fern find the exact spot?

The team's search technique is to systematically crisscross the lake starting at the downwind end. Then, around 10 minutes after they start to crisscross the surface,…

FERN: Bark!

NARRATOR: …Fern gives her signal.

She's clearly picked up the scent, but it takes over an hour of going back and forth to pinpoint the exact spot where Fern indicates it's the strongest.

NEIL POWELL: Bear her up to the wind, John. Right round, John. I'd put her there, John.

NARRATOR: Neil marks her choice with a buoy. Now, the team that hid the canister moves in to check it against the G.P.S. reading they took earlier. And, amazingly, Fern is within just a few feet.

Fern was able to do this because, like all sniffer dogs, she has a powerful and well-trained nose.

NEIL POWELL: There you go, clever girl. Good girl, clever girl.

NARRATOR: Dogs' olfactory powers are so potent, they can be harnessed to find all kinds of things by sensing just a whiff of drugs, or guns or people. They hunt for victims in disasters like earthquakes and avalanches, all thanks to a nose engineered to detect the most minute traces of a scent.

A big secret of the dog's nose is that it splits the flow of incoming air into separate streams, with one fully dedicated to smelling. The smelling tract is lined with special tissues, densely packed with sensors.

ALEXANDRA HOROWITZ: They have hundreds of millions more receptors in their nose than a person does. And they have more elaborate brain organs to receive and comprehend that olfactory information.

NARRATOR: Dogs can smell traces of a substance in parts per trillion. That's the equivalent of being able to taste a spoonful of sugar dissolved in two Olympic size swimming pools.

Some experts believe that dogs are so in tune with the changing scent of their environment that they can smell things we would never even realize could have a smell. For example, is it possible that a dog could smell time?

For humans, time is a concept. To keep track of it, we depend on clocks. But could it be that all a dog needs to keep track of time is its nose?

Meet the Threlkeld family: Christine, Johnny, Faye, Mark and Jazz, their Hungarian Viszla.

JOHNNY THRELKELD (Jazz's Owner): I think he's great. When we go for walks, I have him off the lead all the time. Really good, really good.

NARRATOR: They're convinced Jazz can tell time, because he knows exactly when his master, Johnny, is about to return home at the end of the day.

JOHNNY THRELKELD: As soon as I drive in the drive, I can see him at the window. As soon as I come in the door, he's always at the door, waiting for me to come home.

NARRATOR: And to witness this, we left cameras running all over their house for a week.

The family have a regular routine. Christine and Johnny always leave the house at the same time in the morning, leaving Jazz to his own devices. And every afternoon, Christine comes home at 4 p.m. But it's what Jazz does next that's intriguing. Every afternoon at around 4:40, about 20 minutes before Johnny comes home, Jazz always leaps up onto the sofa, as if he's waiting for him.

He's like a canine alarm clock.

CHRISTINE THRELKELD (Jazz's Owner): Between half four and five, Jazz is always looking out for Johnny. When Johnny comes in, well, it's off that chair, right to the back door, and by the time Johnny's there, at the door, he's there waiting for him.

NARRATOR: It seems as if Jazz somehow knows that Johnny's coming home. It's a claim made by many dog owners.

JOHNNY THRELKELD: I think he's quite intelligent.

NARRATOR: So how does Jazz do it?

Now, it could just be that Christine's coming home sets Jazz's clock. We know it's not because he needs dinner or a walk, because Christine's dealt with that.

There's a theory that a dog's sense of smell could play a role. While Johnny is out of the house, the smell he leaves behind gradually fades over the hours, so, could it be that when Johnny's scent drops to a particular level, Jazz senses he's about to return?

ALEXANDRA HOROWITZ: A story like that makes perfect sense to me. I think it's possible that dogs are, in some way, telling time through the day by odor concentrations.

NARRATOR: To test this theory, at the end of the week, Christine changes her routine. On her way home, she swings by Johnny's soccer club to get some of his freshly worn t-shirts. And then, when she gets back, at her usual time, she wafts them around the living room to spread Johnny's smell. If Jazz is using the fading smell of Johnny to sense the passage of time, then this should be the equivalent of re-setting the clock.

So, will Jazz know what time it is?

It's now less than half an hour before Johnny normally comes home, but, remarkably, Jazz, for the first time, keeps dozing.

CHRISTINE THRELKELD: It's now 4:48. Jazz only lifted his head for about 30 seconds. He's lying flat out again, enjoying the heat of the radiator.

NARRATOR: Now Johnny's back, and to Jazz, it seems to come as a complete surprise.

CHRISTINE THRELKELD: He definitely wasn't looking for him. It was as if he was quite content. He didn't know what the time was. I think the smell of the clothes that I had brought in had obviously confused him.

NARRATOR: Now, this little experiment with one dog doesn't prove anything. There could be any number of things Jazz is reacting to. But it's intriguing that dogs' sense of smell might allow them to grasp something as abstract as time.

ALEXANDRA HOROWITZ: So, that, to me, is wonderful, because it really shows that for dogs, smell might give them a sense of time, which, personally, I can't imagine in my head, with the types of smells that I perceive.

NARRATOR: It turns out, lots of animals use their senses and interact with the world in ways profoundly different from us, especially if that world is under water.

Dolphin senses are extremely difficult to study in the wild, but here, at the Dolphin Research Center, in Florida, scientists are investigating the extraordinary sensory talents of a few dolphins, born in captivity, like Tanner.

ARMANDO RODRIGUEZ (Dolphin Research Center): Looking up, please. That a boy!

NARRATOR: Researcher Armando Rodriguez has devised an experiment to demonstrate Tanner's abilities. Tanner has been trained to mimic a swimmer's behavior. And he's given the command to “imitate” with this hand signal.

Today, the swimmer is Wade, a dolphin trainer.

Wade will perform an action in the water that Tanner has to copy.

ARMANDO RODRIGUEZ: We ask the trainer in the water to actually do that action, and ask Tanner, then, to imitate.

NARRATOR: But it's not as simple as it sounds, because during the experiment, Tanner will be blindfolded. The team is careful to make sure Tanner has no idea which action the trainer will perform.

ARMANDO RODRIGUEZ: We actually show the trainer in the water the action. We don't want to say it, in case Tanner can get a cue from that.

Are you ready? Imitate.

NARRATOR: Armando gives Tanner the signal to imitate, and then puts an eyecup over his other eye. So can Tanner imitate Wade's actions, despite being blindfolded?

Wade is upside down, and Tanner is upside down, too. Wade spins. And Tanner spins.

ARMANDO RODRIGUEZ: Good boy! Excellent, Tanner, give me five.

NARRATOR: And finally, the bob; Wade bobs up and down and Tanner does exactly the same thing.

ARMANDO RODRIGUEZ: Good. Good, Tanner. You're running out, huh? Very good.

You know, I see this every day, and I still cannot get over how extraordinary it is that he does this.

NARRATOR: So how does Tanner do it?

Scientists believe that although Tanner, like all dolphins, has pretty good vision, he doesn't need his eyes to “see” under water, because he's able to sense his surroundings in minute detail, thanks to the very special way he uses his sense of hearing.

Dolphins have no external ears, but their inner ears provide excellent hearing under water. And they put them to amazing use in a process called echolocation.

Here's how it works: the dolphin uses a special organ behind the forehead to emit focused pulses of sound or clicks. The sound waves from the clicks bounce off other objects in the water, echoing back to the dolphin. Instead of external ears, a cavity in the jaw picks up and amplifies those returning sound waves, before sending them on to the inner ears on either side of the dolphin's head.

Echolocation is very similar to the sonar submarines use. In fact, it was scientists in the Navy, wanting to improve their sonar, who first figured out how dolphins do it. They attached small devices to different parts of the dolphin's head. These produced sounds, which the dolphin responded to. The strongest response was measured when the device was on the dolphin's jaw.

This is how scientists believe Tanner can copy Wade. He is using echolocation to essentially “see” Wade's body and what it's doing in the water.

To us, a dolphin's echoes may sound like a cacophony of random clicks, but listen to what happens when we slow them down. This is a return echo from an Atlantic cod, while this is what's bouncing back to the dolphin from a different fish, a mullet.

The sound waves don't simply tell the dolphin about the outer form of the fish. They can reveal shapes inside the fish as well.

Some researchers believe that dolphins can tell different kinds of fish apart by reading the echoes bouncing off their internal organs.

JUSTIN GREGG (Animal Cognition Researcher): It's probably one of the most important, if not the most important sense for most dolphins.

NARRATOR: Echolocation has given dolphins a clear evolutionary edge.

ARMANDO RODRIGUEZ: If they're travelling at night, they're going to need the navigation; if they're travelling in murky water, they're going to need to be fed, so that they'd be able to detect a fish. It's a wonderful thing to have.

NARRATOR: Lots of animals use one of our five familiar senses in completely unfamiliar ways. Starfish see, but not like we do. A basic light-sensitive eye at the end of each arm can form simple images, helping them to find their way around the seafloor. Butterflies and moths have no nose, but their sense of smell may be even more sensitive than a dog's, because of their antennae, fine-tuned to detect just a few molecules of scent.

For many creatures throughout the animal kingdom, the secret to their survival has been the evolution of super senses. And these aren't always simply more powerful versions of our five senses. Sometimes, animals perceive things that our bodies are incapable of sensing.

BRIAN HARE: There are animals that have completely different senses than we have, that it would be close to impossible to conceive what that might be like.

NARRATOR: One of these animals thrives here, off the island of Bimini, in the Bahamas: the shark.

Sharks are extremely successful predators. They can smell tiny quantities of blood, over huge distances, and feel the miniscule vibrations of prey in the water. But sharks have another sense that we humans do not share.

Researcher Eric Stroud has devised an experiment to demonstrate, with young lemon sharks.

ERIC STROUD (SharkDefense Technologies LLC): We've just captured a juvenile lemon shark, and to do an experiment, right now, we need to turn it upside down, and—this is called tonic immobility—and after a few moments, the shark will go into a sleep-like state, a comatose state.

NARRATOR: With the shark at rest, Eric will test its sensitivity to something a human would be completely oblivious to, a magnet.

ERIC STROUD: And this is perfect to conduct an experiment, because right now, nothing is bothering it. And we're going to introduce a magnet and see if the shark is going to give some kind of response.

I don't want the shark to cheat it. I don't want the shark to see it, and so I'm going to put a small blinder in there, so he can't see me coming, and now, I'm going to put the magnet in the water and approach the shark.

That was a great response. What we had there was a repellent response. The shark did not like this magnetic field.

NARRATOR: Almost as if he'd had a powerful light flashed in his eyes, the shark was acutely sensitive to Eric's magnet. As a control, Eric does the same experiment with a piece of lead.

ERIC STROUD: And we don't get a response. This proves that it's not just any piece of metal that can interfere with the shark, it really has to be magnetic.

NARRATOR: Sharks are clearly affected by a magnetic field, but they don't typically encounter magnets in their environment. So why have they developed this sense?

ERIC STROUD: What we did in that experiment is we induced a very strong electromagnetic field, the movement of a magnet can induce an electrical current.

NARRATOR: Magnets generate a weak electrical field, a flow of charge, and so do the muscular movements of prey, including their beating hearts.

ERIC STROUD: When an animal is beating or it's moving, the muscles generate a very weak electromagnetic field, and that's what they are gearing in on. They can locate the heartbeat of, say, a crab or stingray, underneath the sand.

NARRATOR: It's another tool in their predatory arsenal, making it even harder to hide from a shark, all thanks to an ingenious piece of sensory anatomy. Sharks have organs called the “ampulla of Lorenzini,” which appear as dark openings along the front of their noses.

These are the ends of tiny tubes filled with a jelly. The jelly can register voltage differences between the tube's opening and its base, beneath the shark's skin. These are exquisitely sensitive, able to pick up billionths of a volt.

So we've seen the effect of a magnet on a young shark, but could it have any effect on a full grown one?

Eric is heading out from Bimini to Triangle Rocks, a well-known gathering place for large Caribbean reef sharks. He's joined by his colleague, marine biologist Pat Rice.

Together, they've come up with a plan to test a shark's magnetic sense against one of their most powerful instincts, their urge to eat.

ERIC STROUD: We've just arrived at the Triangle Rocks, that's south of South Bimini Island. And when we set up here, six Caribbean reef sharks arrived. And these are adult sharks, and they vary between maybe two to three meters. There's really, there's one big one down there.

NARRATOR: With the sharks gathered around the boat, Pat gets ready to dive in.

PATRICK RICE (Marine Biologist): This is probably my hundredth dive with these particular sharks. And if you aren't afraid of them, they will stay away from you, usually, unless, you know, sometimes, when they get into a feeding frenzy, they can…all bets are off then.

Here we have a Pelican™ case full of magnets.

See if I can get one off, here. You can see how powerful they are, takes a Herculean task to get them apart.

These are barium ferrite, ceramic magnets, very powerful. And so, it's probably a good idea to keep the cameras away from them, at least a meter, because anything that's magnetic memory can be wiped clean. So, we don't want to lose the shot.

NARRATOR: At the surface, Eric distracts the sharks by feeding them, while Pat sets up the experiment on the ocean floor.

ERIC STROUD: Right now, the key is to try and keep the sharks near the surface, so that the divers can set up the experiment down there, and the sharks are above them.

NARRATOR: Twenty-five feet below, Pat makes two circles on the sand, one with magnets and one with bricks. He places the same amount of bait in the center of both of them.

All the sharks up by the boat will now be able to smell the food. The question is, will the magnets stop them from eating the bait?

PAT RICE: Here comes a shark, and he ate right off the control.

NARRATOR: One shark bypasses the magnets on the left and goes straight into the brick circle on the right, to take the bait.

So, will they take an interest in the bait inside the magnet circle, now that the brick circle is empty? Another animal moves in, but before it can grab the bait, it turns away. It seems to know there's food there, but it won't go inside the ring of magnets.

PAT RICE: Jess, get more bait.

NARRATOR: Pat puts fresh bait in the bricks.

PAT RICE: They're getting a little feisty down here.

NARRATOR: But he's barely had time to retreat when a shark goes straight for the brick circle again.

PAT RICE: We can't get it down fast enough. More bait, Andy.

NARRATOR: The sharks grab the food as soon as it's laid down inside the bricks. Pat has replenished it four times.

PAT RICE: They're pretty hungry today.

NARRATOR: But they don't touch the food—a delicious fishtail—inside the magnets.

Unlike this experiment, in which the electric field is overwhelmingly strong and repels the sharks, in the wild, much weaker electric fields produced by the moving muscles of fish and other creatures can actually attract them.

PAT RICE: We may never really understand fully how a shark is perceiving the world around it, and, in this particular case, we don't have an electric sense, we have to kind of guess.

NARRATOR: Sea creatures have evolved their own special ways to perceive their watery worlds, to find prey and help them navigate. But what if your world is not under water or on land but in the air.

Consider these birds zipping around in the sky. They've got a lot to take in, plus they need to migrate hundreds of miles every year. Yet, if they're going to defy gravity, they can't be weighed down by a big brain.

BRIAN HARE: If you're a bird and you need to fly, you're going to have to have a way to do it so that your brain doesn't weigh so much you can't get there.

NARRATOR: Birds on the wing can move in any direction they choose. In some environments, there's the constant risk of collision. What's more, predators in the air, like hawks, can attack from anywhere. So bird brains need to take in information from every direction.

Many can see down, up, left, right, in front and behind, all at the same time. And yet, with nearly 300-degree vision, a swallow can pull complex maneuvers at 40 miles an hour, within inches of buildings.

It's an incredible amount of visual data to process, all achieved with a tiny brain. A swallow's brain weighs about one gram, a thousand times lighter than ours. So how on earth do birds do it?

Clues might come from this reconstruction of an experiment, based on research originally conducted at the University of Queensland and Australian National University. It involves some boards with stripes painted on them, and a starling, named Arnie.

BIRD HANDLER: Are you ready?

MARTIN STEVENS: We're going to get him to fly down this corridor.

And to begin with, we'll have these stripes horizontal, and we'll time—using these precision timing gates—how long it takes him, and then we're going to switch the boards, so that the stripes are vertical and we'll see how that changes things.

NARRATOR: To get a precise measurement of Arnie's speed as he flies down the corridor, the starling must fly through a light beam at the start and at the finish. To make sure the results are reliable,…

MARTIN STEVENS: Yes, that worked.

NARRATOR: …Arnie must complete at least 10 successful flights.

MARTIN STEVENS: Yes, that worked.

NARRATOR: He's performing admirably. His flight times, from one end of the corridor to the other, are coming in at less than 2 seconds.

MARTIN STEVENS: We've got 10. Now, what we're going to do is change the boards and make them vertical. And we're going to try again and see how that affects the speed that the birds go at.

NARRATOR: With the stripe pattern changed, the team repeats the experiment.

MARTIN STEVENS: That was the slowest time, so far.

NARRATOR: Could the vertical stripes really have slowed Arnie down?

Once we have a complete set of flight times, we can compare how fast Arnie flew through the vertical stripes versus the horizontal. The average speed for the horizontal stripes was 16.5 feet per second, but for the vertical stripes it was only 15.3 feet per second. These results confirm that the vertical stripes slowed the bird down by more than a foot per second.

MARTIN STEVENS: The reason why we see this comes down to a neat trick called “optic flow.”

NARRATOR: Optic flow is the way animals' eyes sense motion, and birds use it to help them determine how fast to fly. When Arnie flies through horizontal stripes, the pattern changes very little.

MARTIN STEVENS: That pattern of information is very smooth and very continuous, just as it would be if the bird is flying through an open environment with objects way off in the distance.

NARRATOR: But the vertical stripes create an entirely different illusion.

MARTIN STEVENS: That's interpreted as the bird being in a very cluttered environment with lots of objects, like trees, that it has to fly between and navigate past. And so what it does, it flies more slowly.

NARRATOR: When Arnie flies through the vertical stripes, the pattern changes constantly. His brain may be perceiving the lines as nearby obstacles, and that makes him fly cautiously, over a foot per second slower.

The bird is able to make these adjustments based on minimal visual information. Whether sharks or dolphins, birds or butterflies, all these animals make decisions based on what their senses tell them. And most of them, like us, perceive the world with multiple senses.

So how do they put it all together?

BRIAN HARE: Evolution can design an organism in a lot of different ways, in terms of how they listen to their senses. And so, you can see an organism that is able to integrate all their sensory input at the same time, you can have another organism that may prioritize one sense over another.

NARRATOR: The way animals prioritize their senses can have a profound impact on their behavior, especially if those senses seem to be delivering conflicting information. So, how do animals decide which sense to trust the most?

Some intriguing research is delving into this question with our trusted companion, the dog, and comparing it to its closest relative, the wolf.

Wolves are genetically almost identical to dogs. The animals can even interbreed. But in the 10,000 years or more since some were domesticated, wolves haven't changed much in appearance, while dogs have been bred to take on an astonishing variety of shapes and sizes. But how different are dogs and wolves inside their minds? Do they use their senses in the same way?

Here, at Wolf Park, in Indiana, animal behaviorist Kathryn Lord is trying to find out. She's studying a group of 10 wolves born in captivity, who now roam over a territory of about 75 acres.

Like most mammal predators, wild wolves rely on their nose to track down prey. Without it, they would starve. At Wolf Park, all the wolves have been raised by humans and have no need to hunt for their supper, but they haven't lost their acute appreciation of smelling. And, as Kathryn has found, they seem to have some expensive taste.

KATHRYN LORD (University of Massachusetts): So, I'm going to spray this bottle of Chanel No5 over there to see if we can't get some scent rolling.

So they come over here and actually start pushing their head and shoulder into the ground and rolling around in it.

NARRATOR: Dog owners might recognize this kind of behavior, but to scientists, it's a bit of a mystery. Some think that wolves developed this as a strategy to carry interesting odors back to their pack.

KATHRYN LORD: We're not completely sure why wolves actually do this behavior. This particular perfume, as well as a number of perfumes, have a musk in them, which may be similar to some pheromones, which are very important to wolves. It may make them more attractive to have the scent on them, or they may just be trying to show other wolves that they've found an interesting scent. We really don't know.

NARRATOR: Pheromones are natural chemicals that can send signals from one animal to another, signals about fear or food or finding a mate. Smell clearly plays a central role in a wolf's life, as it does for a dog.

KATHRYN LORD: So, dogs and wolves both have an excellent sense of smell. They both seem to inhabit the same sensory world.

BRIAN HARE: Let's go!

NARRATOR: But as important as smell is, are wolves and dogs slaves to their noses?

As most dog owners know, in addition to being great sniffers, these animals watch us very closely with their eyes and seem very interested in what we do. So what role does vision play in how dogs understand the world?

Brian Hare has recruited dogs from across the country to test how they use visual information, particularly when that information is provided by a human.

One of the simplest examples is the pointing test.

BRIAN HARE: And now, watch where her gaze goes…right at me.

Stay.

Right. So, what we've got here is a very simple experiment. We've got two people, we've got two cups. We've hidden food in both cups. And we have a dog, of course. And all I'm going to do is I'm going to gesture at one of the two cups. And the question is, does the dog go where I gesture or to the other cup?

Now, it can't be that she's just using her smell, when she makes her decision, because there's food in both cups. So, let's see what she does.

NARRATOR: Both cups are hiding food and smell equally appetizing, so there's only one reason for Sisu to choose between them:…

BRIAN HARE: Okay, Sisu, you ready? Okay.

NARRATOR: …the visual signal Brian is giving her.

BRIAN HARE: Okay, Sisu.

Good job. And there's one here, too.

All right, so she did use my gesture there. Sometimes I'll point to the right and sometimes I'll point to the left. But let's do it again, because it could be chance.

Hey. Okay, Sisu. All right.

So what we've seen is that Sisu really relies on my visual gestures. She's not relying on her nose. If I'm there and tell her something, she's much more happy to use that information than to rely on her nose.

NARRATOR: It's not too surprising.

BRIAN HARE: Okay, Kai.

NARRATOR: Many dogs will eagerly follow visual cues and gestures given by humans, like pointing.

BRIAN HARE: Kai, is it there?

NARRATOR: But we also know they have great noses. So what happens when the two senses, vision and smell, go head to head?

To find out, Brian is going to put Dexter's nose in direct conflict with Dexter's eyes.

BRIAN HARE: So, we're going to actually show Dexter where we're going to hide the food, so he can remember where he saw it. But then what we're going to do is we're going to close his eyes and shift where it's hidden. We're going to actually move it to the other location. So, that means he could potentially smell where it is, the question is, does he use what he saw to find the food or does he rely on his nose. So let's see what he does.

All right, Dexter. Oh, look at that face! Oh, you're killing me. All right, Dexter, are you ready, buddy?

Okay, that's where it's going to be.

NARRATOR: This time, there's food under only one cup.

BRIAN HARE: Okay, now, close your eyes.

NARRATOR: And with Dexter's eyes covered, Brian now moves that food to the other cup. Poor Dexter's senses are in direct conflict. Does he trust his eyes or follow his nose?

BRIAN HARE: Okay, Dexter, find it.

Aww, what happened? It's a trick!

It's over here. It was a trick.

Are you ready, Dexter? Are you ready? Okay, we're going to put it over here. Here it is. It's right there. Close your eyes.

Okay, Dexter, go get it.

NARRATOR: Again and again, Dexter, like most dogs, goes, not to where he can smell the food, but where he saw Brian put the food.

BRIAN HARE: Okay, Dexter, get it.

Aww.

NARRATOR: But what about wolves? Will they pay attention to visual cues from humans in the same way?

Back at Wolf Park, researchers are investigating.

Kathryn Lord reared this group of wolves from birth, so, unlike wolves born in the wilderness, who avoid humans, these can be quite friendly. Still, they are wild animals and potentially dangerous, and Kathryn knows to be careful in their presence.

KATHRYN LORD: If I was very hurt, if I had a broken leg, or if I was very sick, I probably wouldn't come in, just because I'd be sending them signals that might lead to that sort of behavior. But otherwise, they're very well socialized to humans, so that's not usually too much of a concern.

NARRATOR: Growing up with exposure to humans and receiving treats from them, this grey wolf, Fi, responds to certain types of information that a wild wolf wouldn't. She comes when her name is called.

KATHRYN LORD: Fi!

NARRATOR: And Fi can also follow Kathryn's pointing. She seems to be just as capable as a dog of understanding what it means.

But other tests with dogs and wolves reveal a dramatic difference in their priorities, when it comes to paying attention to people. When researchers from Oregon State gave wolves a closed container with a tasty treat inside, the animals focused intently on getting the food out, but pet dogs, given the same container, tend to focus on their owners.

Only when the humans actively encourage them, do the dogs really work at getting the container open. So, it's not that wolves can't pay attention to humans, but they seem to know when they don't need to.

KATHRYN LORD: If they were students in a classroom, the wolf would be focusing down on the test and solving the problem, the dogs would be cheating, by looking at somebody else's test. So, the dogs need us to solve the problem, whereas the wolves are perfectly capable of doing it on their own.

NARRATOR: This is one of the key changes that occurred in the wolf mind when they were domesticated and evolved into dogs: they became extremely willing to watch and pay attention to us. This may explain why, in some cases, a dog will choose to follow human gestures instead of its own extremely powerful nose.

ALEXANDRA HOROWITZ: We're kind of suppressing dogs' olfactory experience. We are in control, for the most part, of owned domestic dogs' lives.

NARRATOR: So how did this transformation take place? Kathryn believes this difference between wolf and dog minds may be closely linked to how the animals process sensory information in the earliest weeks of life.

Kathryn raises wolf pups from a very young age.

KATHYRN LORD: The wolf pups are great. So, we get them at about 10 days of age. So, at that point, they can't see, they can't hear and they can't smell. And they can't really walk either. They're just, kind of, little puddles of fur. And so you, basically, are a warm water bottle that feeds them milk. So, we bottle feed them every four hours. It's very intensive; you're with them twenty-four-seven. It's the only way you can socialize them.

NARRATOR: There's a brief period of time when baby animals are open to new experiences and become socialized. It's known as the “exploration window,” and it's a chance for them to learn who and what is safe, while they're protected from predators.

Kathryn found that, in wolves, this window opens very early, at two weeks, when only the pups' sense of smell is working, and they are still blind and deaf. Over the next few weeks, the pups start to see and hear, but also, gradually, become more fearful of new sensations.

Dog puppies also have an exploration window, but it opens slightly later.

KATHYRN LORD: The big difference is when they start to explore their world. So, dogs don't begin to explore their world until four weeks of age, so that's two weeks later than the wolves. And so, when the dogs start to explore their world, they can already see, hear and smell.

NARRATOR: But while the dogs have all their senses powered up, when they're getting to know their world, wolves, with fewer senses working, will be exposed to far fewer sensory experiences before their fear of the unfamiliar is firmly in place.

Kathryn believes this is one of the main reasons wild wolves avoid humans.

KATHYRN LORD: Even a well-socialized wolf is very different from a well-socialized dog. The, the wolves are more fearful of novelty, in general, than a dog is.

NARRATOR: Dog puppies can be exposed to all sorts of sights, smells and sounds during their exploration window, so, when they're older, more things will feel familiar, and they'll be more open to new situations. This may help explain why dogs can so easily form close friendships with other animals, whether human or not.

KATHYRN LORD: The ability of dogs to be flexible is what allowed them to come into our environment, in the first place, and probably allowed them to be domesticated.

NARRATOR: The early wolves that evolved into dogs were perhaps quite different from the wolves of today. As pups, they may have had a later window of exploration, leaving them more open to forming close relationships with humans. For Kathryn, what might seem a small difference in timing, during development, has had a profound impact on how these two animals use their senses and may be a key factor in creating the dog mind: comfortable around humans and primed to become a close companion.

We're so close to our dogs that some of us imagine we can guess what's on their minds. But for scientists, it's a lot more complicated.

BRIAN HARE: One of the big questions, of course, that people have always been interested in is, do animals think, at all? And in asking that question about animals, it makes you think about what is thought and what drives what we are thinking about?

NARRATOR: For decades, animal researchers have relied on behavior to try to determine how animal minds work, but now things could be changing, because for the first time we may have a direct window inside the animal mind.

Neuroscientist Greg Berns is adapting a medical technique to study the activity of brain cells in dogs.

GREGORY BERNS (Emory University): Okay, stand by, we're going to start the noise.

M.R.I. is a technique that's been used in humans for over 20 years. Normally, we use it to study what the brain looks like, but with a few tricks we can do what's called functional M.R.I., which looks at brain activity, and by analyzing the data, we can figure out which parts of the brain are doing what.

But doing M.R.I. on animals is an entirely different game, mainly because of the requirement that the subject has to hold absolutely still.

NARRATOR: The need to keep still makes it impossible to scan most animals, unless they're sedated, which is not a good way to study brains in action.

MARK SPIVAK (Comprehensive Pet Therapy, Inc.): One, two, three steps.

NARRATOR: But Greg has teamed up with Mark Spivak to train dogs for the unfamiliar conditions they'll face inside an M.R.I. machine.

One key requirement is a steady supply of snacks.

MARK SPIVAK: Well, a lot of humans have difficulty taking an M.R.I. First of all, there's the enclosure, which provokes anxiety in many humans. Second, there's the absolute motionlessness required, and then, there's the noise.

NARRATOR: To block out the M.R.I. noise, the dogs are trained to wear special ear covers.

MARK SPIVAK: Without proper conditioning and training the dogs would just run scared from the M.R.I.

Come here, girl.

NARRATOR: Those that pass the test graduate to the real thing, like Kady.

M.R.I. is a non-invasive procedure, at the very cutting edge of animal science, and it's beginning to reveal fascinating insights.

GREG BERNS: Patricia we're going to begin the first scan with the localizer. Are you ready?

NARRATOR: One of Greg's earliest experiments is revealing an important clue as to what happens in a dog's brain, when it receives information from its senses.

First, Kady is looking at a visual signal.

GREG BERNS: So Kady's in the scanner, right now, and Patricia's actually giving Kady hand signals. So, we've already taught the dogs, through lots of practice, that this means food, okay? So, every time Patricia puts this signal up, we're going to be looking in her brain, what that response is. And we're actually going to be looking at a very specific area, called the “caudate nucleus.”

We also have another hand signal that looks like this, and that means no reward.

NARRATOR: After scanning many dogs, Greg's results reveal the area of the dog's brain that responds.

GREG BERNS: If we look very closely we find that the area that's common to all the dogs corresponds exactly to the same part of the human brain that responds to reward. Rewards like money, music, food, all the things that humans like, it's also activating in the dog's brain.

NARRATOR: Even though Kady isn't actually seeing food, she can take a piece of visual information and interpret it, to anticipate that she will receive food, and she's responding emotionally, just like we do.

GREG BERNS: This was pretty amazing, because it didn't have to be that way. Dogs could be so different from us they might have responded completely differently, but that doesn't seem to be the case.

NARRATOR: And this reveals a complex chain of brain activity.

GREG BERNS: Ever since Pavlov, people have viewed animals as what we call Pavlovian machines, stimulus-response robots, basically. And what we're finding is that there's a tremendous amount of processing going on in their brains that actually looks a lot like what happens to humans, in exactly the same circumstances.

Dogs, and probably most animals, have brains and minds that are far more sophisticated than we ever gave them credit for.

NARRATOR: It's one of the great mysteries: What are animals thinking? Now, we are gaining ever-greater insights into their senses, painting a clearer picture of how the creatures around us perceive their world, whether it be dramatically foreign to our own or remarkably familiar.

Inside Animal Minds: Who's the Smartest

PBS Airdate: April 23, 2014

NARRATOR: What are they thinking?

BRIAN HARE (Duke University): Oh, look at that face!

NARRATOR: Is there any way to get inside the animal mind?

BRIAN HARE: What I really want to know is what is it like to be an animal, what are the problems they have to solve? And how do they think? And are they like us, or are they like something totally different?

NARRATOR: They have some amazing abilities. Is it instinct, training or something else? Cutting-edge animal science reveals new answers. We put different species to the test, in search of the roots of animal intelligence. Who are the best problem solvers? Who wins the battle of the super senses?

In this episode, “What makes an animal smart?”

LORI MARINO (Emory University): Up until a million years ago, the brainiest species were dolphins and whales.

NARRATOR: What can we learn from their language, relationships, even emotions?

FRANS DE WAAL (Emory University): If you start giving one of them grapes, then the one who gets cucumber becomes very upset.

NARRATOR: Are they more like us than we ever thought possible?

BRIAN HARE: We're not the only species that has soap operas going on every day of their lives.

NARRATOR: Inside Animal Minds: Who's the Smartest? Right now, on NOVA.

Which animals are the smartest and how did they get this way?

Dolphins have long been hailed as the cleverest creatures in the sea. There's no doubt they're quick learners, and, in captivity, they can be trained to perform stunning tricks. Not only can they follow hand signals, but they can even learn the meaning of written symbols.

Why would a mammal that spends most of its time under water and has flippers instead of hands have these kinds of skills? Throughout the animal kingdom, you can find creatures with extraordinary talents: elephants with impressive memories, birds that solve complicated puzzles, and tool-making chimpanzees. They inhabit utterly different worlds and come in a wide variety of shapes and sizes, but is it possible that these animals could all get their smarts in similar ways?

Because, whether they walk, swim or fly, the cleverest animals on Earth, including us humans, seem to have one thing in common: we live in groups. So, could social living be the key to creating the most powerful minds?

Around the world, animal researchers are trying to find out. And this is one of their favorite subjects. Everyone knows that dolphins can put on incredible shows, but their greatest performances take place far from the crowds, because here, in the wild, these animals execute the most amazing tricks when they work as a team.

In these shallow waters off the coast of Florida, dolphins band together to get the better of fast-moving fish. Here's how their trickery works: one dolphin swims in a circle; it whips up a wall of muddy water, corralling any fish inside. Three other dolphins wait, just outside the ring of mud. As the fish try to leap out of the muddy ring and escape, they jump right into the open mouths of the waiting dolphins. Soon, a dolphin swings around again to create another corral.

They seem in perfect synch, as if they've planned every move together. But what's really going on?

Are they strategizing and communicating with each other, the way we would? Or are they simply drawn together on the hunt by pure instinct? One big reason to suspect that something more complex is going on is this: the dolphin brain.

When you look at the size of most animal brains, there's usually a pretty direct link to the size of their bodies. The bigger the body, the bigger the brain. But some animals defy expectations.

Humans have much more grey matter than other animals our size. So do chimps and whales, and so do dolphins. So, how did their brains get big?

LORI MARINO: The six-million-dollar question has always been, “Why do dolphins and whales have large brains?”

NARRATOR: Neuroscientist Lori Marino is trying to answer that question by hunting down some very ancient clues. She travels all over the country, studying fossils, to trace the evolution of the dolphin brain.

LORI MARINO: One of the things we wanted to find out with this research was exactly when they got their large brains.

NARRATOR: Here, at the Smithsonian Institution, she and her colleague Mark Uhen are examining fossil skulls of the dolphin's ancient ancestors, early whales called “archaeocetes.” Some archaeocetes were huge, ferocious predators, with gigantic teeth. Compared to modern dolphins, their bodies were massive. Growing up to 55 feet long, in their day, nearly 40 million years ago, they were the biggest animals on Earth.

Today, examining fossil skulls of early whales, Lori is trying to estimate the size of the brains that once sat inside. In ancient fossils, the space where the brain was housed is often filled with sediment. But a C.T. scan can see through the sediment and reveal the exact dimensions.

LORI MARINO: We were absolutely thrilled to see the results of the study, because it gave us information no one had before.

NARRATOR: When Lori examines the C.T. scans of this giant killer's skull, she discovers not everything was big.

LORI MARINO: This animal had a very big body and a very small brain.

NARRATOR: But a few million years later, things started to change.

LORI MARINO: But then, something happened, and what we see is a shift.

NARRATOR: When Lori looks at more recent dolphin ancestors, dating to about 30-million years ago, she discovers, in evolutionary terms, a fairly sudden shift. Bodies and teeth shrank, but at the same time, brains got bigger.

LORI MARINO: The brain of the early dolphins and whales increased in size, sometimes many-fold.

NARRATOR: The dolphin brain got big and stayed that way. In fact, for millions of years, until early humans came along, the dolphin had the most powerful brain on the planet.

LORI MARINO: Up until about a million years ago, the brainiest species on the planet were not primates, they were dolphins and whales. We are just a very recent kid on the block.

NARRATOR: The question is why did the brain change?

LORI MARINO: Everyone would like to know why there was this shift in relative brain size, with dolphins, and it really is a mystery. It suggests that they embarked on a very different evolutionary path than their ancestors.

NARRATOR: Lori thinks that path was a social one. No longer giant, toothy beasts, individuals could increase their chances for survival by joining forces.

LORI MARINO: Perhaps they needed to hunt together. Perhaps they needed to band together against predators. So these new animals were smaller and not as formidable, and so they kind of needed each other.

NARRATOR: Today, more than 30 different kinds of dolphins swim the seas, including the bottlenose dolphin, the spotted dolphin and the orca, or killer whale, the largest of all dolphins. Most live in groups, or pods, usually of a few dozen individuals. Sometimes, pods will come together, forming a mega-pod, numbering in the hundreds or thousands. It seems clear that today's dolphins need each other, but why would they need big brains, too?

To find out, we need to dive deep into the dolphin world. Here, in the Caribbean waters, near the island of Bimini,…

KELLY MELILLO SWEETING (Dolphin Communication Project): Okay, Al, we're ready when you are.

NARRATOR: …researchers Kathleen Dudzinski and Kelly Melillo Sweeting have spent years tracking wild spotted dolphins, carefully observing and recording their interactions, trying to decipher the secrets of dolphin society.

Today, the scientists encounter a gathering of dolphins swimming together. There are about 16, of mixed sexes and ages.

KATHLEEN DUDZINSKI (Dolphin Communication Project): What we definitely saw was a socializing group of dolphins. They were interacting, playing, they were affectionate with one another.

NARRATOR: By observing these dolphins year after year, researchers are beginning to get a clearer picture of what dolphin society is really like. Compared to many land mammals, dolphin society is extremely complex and dynamic, and many of the relationships they form might surprise you.

The only connection that follows a predictable pattern is the one between a mother and her calf. Among spotted dolphins, the two will stay together for about three years, until the youngster is weaned.

After that, almost anything goes. Males and females who mate don't form long-term relationships, but sometimes, adult females do and help each other out with babysitting duties.

KEL SWEETING: White Blotch was one adult female that we saw very consistently for 10 years, and she was notorious as a babysitter. She would come to the boat, and she'd have her own calf, and she'd have two or three extras in tow. And we know they only have one calf at a time, and so it was a very clear example of that babysitting and taking turns.

NARRATOR: And it's not just the females who form close relationships and collaborate to make life easier. Male dolphins compete with one another to find mates, but sometimes two or three males will form an alliance, to work together to hunt and to attract females.

Often, these relationships last for many years, even entire lifetimes.

KATHLEEN DUDZINSKI: I do believe that dolphins have friendships and favorites. And that their social interactions are developing friendships they might have that might last a lifetime.

NARRATOR: Those in close relationships keep in touch, literally, by tapping each other's pectoral fins. But even if they're in some kind of alliance or friendship, dolphins like these will regularly mingle with others.

This flexible social structure is known as a “fission-fusion” society. Human society is also fission-fusion. During an average day we will move from small family groups to larger groups of colleagues to mid-size gatherings of friends.

Dolphins form all sorts of relationships, just like we do. And they change over time. It's a complicated and bustling social world. And it's this social complexity that some scientists think could hold the key to the evolution of bigger brains.

LORI MARINO: When you're a social animal, there's a lot that you need to keep track of. There's all kinds of relationships, all kinds of interactions, hierarchies, collaborations that may occur.

BRIAN HARE: There's a very nice relationship between social complexity that you observe in a species organization and the size of their brain.

NARRATOR: So how do dolphins use their big brains to navigate their social lives? Is it possible that some of that brain is powering a complex system of communication? After all, whenever dolphins get together, the water can get very noisy.

Dolphins make all kinds of sounds: fast-paced clicks that sound like a creaky door; loud outbursts that resemble squawking birds; and high-pitched whistles.

For decades, researchers have been trying to figure out what it all means. But in the 1960s, one controversial scientist took an alternative approach. Neuroscientist John Lilly was convinced that dolphins were much more intelligent than people had previously thought.

DIANA REISS (Hunter College): John Lilly was a neurophysiologist who was the first to really suggest that dolphins might be highly intelligent. He was the first to really, sort of, light the fire and get a lot of us interested. He talked about them as “humans of the sea.”

JOHN LILLY (Neuroscientist): And I just want to talk to such ancient characters and find out, you know, if they have any wisdom for us.

NARRATOR: Rather than deciphering their language, Lilly decided the quickest route to communicating with dolphins would be to teach one of them how to speak English. And he set out to do just that, with one of the strangest animal experiments ever devised.

DIANA REISS: John Lilly did an experiment that involved building a dolphin house. And what he did was he bought property, and he flooded the first floor, so the dolphin could actually live in this first floor area.

NARRATOR: With the dolphin, named Peter, living in less than four feet of water, it wasn't a very humane approach. But the idea was to keep Peter in close contact with his teacher.

DIANA REISS: He actually had a woman living there, with the dolphin, in a very intense time, where she tried to teach this dolphin English.

NARRATOR: The young woman was Margaret Howe, and she lived, ate and slept here for two and a half months, trying to teach Peter every day.

This is a sound recording of Margaret counting, while Peter attempts to imitate her.

MARGARET HOWE: One, two, three, four, five.

PETER: Ahh, ahh, ahh, ahh, ahh.

MARGARET HOWE: One, two, three, four, five, six.

PETER: Ahh, ahh, ahh, ahh, ah, ah, ah, ah, ah, ah.

It's safe to say the dolphin house experiment was both unethical and a complete failure.

DIANA REISS: What the dolphins did was not English. They could imitate the number of syllables they were hearing, but they couldn't formulate in English. They don't have the kind of articulatory system we have.

NARRATOR: In spite of its shortcomings, Lilly's work got a lot of attention and inspired the Hollywood film The Day of the Dolphin.

THE DAY OF THE DOLPHIN CLIP: What do you know about linguistics?

The fictional scientist, played by George C. Scott, seemed to have better luck teaching his dolphin to count “one, two, three,” in English, than John Lilly ever did.

For real life scientists, Lilly's work showed that any idea of teaching dolphins human language was probably a fantasy. Today, researchers are focused intently on trying to decipher the dolphin's own system of communication, and they've been using underwater microphones to record all those clicks, squawks, and whistles, hoping to find patterns and discover what they actually mean.

But there's a problem. Dolphins make sounds under water by vibrating tissues in their nasal cavities, a bit like the way we humans vibrate our vocal cords. They usually don't open their mouths or make any visible signs.

JUSTIN GREGG (Dolphin Communication Project): Dolphins are essentially ventriloquists. They produce sound, and you can't see anything. Nothing changes on their facial expression or even their blowholes. So, they can be making sounds without moving, and you have no idea who made the sound.

NARRATOR: But now, researchers have come up with a pioneering new technique to “listen in” on dolphin conversations.

VINCENT JANIK (University of St. Andrews): We're going out today to try to find wild dolphins and attach tags to them.

NARRATOR: Biologist Vincent Janik is on a quest to eavesdrop on wild dolphins and try to decipher the dolphin communication code.

VINCENT JANIK: They are little recording tags that can give us information about their sounds that they're making and also give us information about their behavior, as they're in the bay, their own wild environment.

NARRATOR: Today, a bottle-nosed dolphin's been captured in shallow water. The researchers work rapidly to minimize distress to the animal.

To solve the problem of capturing the exact sounds made by a particular dolphin, Vincent's team uses suction cups to attach a recording device directly to the animal's head. It's small enough for a dolphin to ignore.

VINCENT JANIK: Nicholas, Nicholas, get signal?

SCIENTIST: Roger that.

VINCENT JANIK: Okay.

NARRATOR: If it were uncomfortable, the dolphin could easily use the seabed to knock it off.

It will now record all the sounds that the dolphin makes and, using G.P.S., will keep track of its movements.

SCIENTIST: Five, four, three, two, one.

NARRATOR: The dolphin's released and soon joins some other tagged dolphins. The scientists constantly observe them, so later, they'll be able to match their behavior to the sounds they're making.

SCIENTIST #1: What's going on over there? There's lots of splashing. I think that's a dorsal fin.

SCIENTIST #2: Yeah, they're two dolphins.

VINCENT JANIK: What we can look at is what the animal's doing: whether it's travelling, whether it's foraging, whether it's socializing with others, those, those kinds of things, we can observe from the surface.

NARRATOR: After a few hours, the devices fall off on their own and float to the surface so the team can retrieve them and begin analyzing the dolphins' sounds.

At first hearing, it's a cacophony, a whole range of dolphin clicks, whistles and pulses. Today, we know that the creaky-door clicks are the sounds dolphins use for echolocation.

They work like sonar pings, dolphins listen for the echoes of the clicks, as they bounce off objects in their environment. This plays a crucial role in helping them locate their prey and navigate in murky water. But Vincent is interested in other kinds of dolphin sounds, the ones they use for communication.

Sometimes, there are patterns, certain sounds consistently made when a dolphin is doing a particular action, like this one…

[Bray sound]

VINCENT JANIK: One sound that we've found, is the so-called “bray” sound, which dolphins produce when they find fish. And it's a sound that brings in other dolphins, as well.

NARRATOR: And when dolphins are aggressive, playful or not, they often produce lower frequency sounds, known as burst pulses.

[Burst pulses]

These kinds of calls are common in the animal kingdom, but there is one kind of sound dolphins make that is much more unusual. It's called the “signature whistle.”

VINCENT JANIK: Every dolphin has its own signature whistle that's different from all others. Within a population, you have very, very different whistles for every, every animal. The function of the whistle, really, is to broadcast its identity and also to stay in touch with other group members. The closest in our language, perhaps, is really if I would say, “I'm Vincent, and I'm over here.”

NARRATOR: Dolphins have good vision, but if the water is murky or individuals get separated, Vincent believes they use signature whistles to help keep a group together.

VINCENT JANIK: If an animal gets lost, it will also produce that whistle to try to make contact again. And that's something that we often see between mothers and calves. When the calf wanders off and is far away and eventually wants to get back to its mother, what it does is start to produce its signature whistle.

NARRATOR: It is rare for animals to have unique calls that correspond to particular individuals, but dolphins aren't the only animals to use vocal calls as a way of identifying each other.

One other animal known to do this inhabits a world completely different from the dolphins' underwater domain.

The Amboseli National Park, in Kenya, is home to some of the most social animals on the planet: elephants.

KAREN MCCOMB (University of Sussex): The thing about this park that is outstanding is the visibility of the elephants, a population, more than a thousand elephants, which we know individually.

NARRATOR: Karen McComb has been observing elephants here for decades, trying to unlock the secrets of elephant society and communication.

KAREN MCCOMB: It's being able to get inside animal minds and get into a social world that's actually rather different from ours that will tell us what elephants are really thinking.

NARRATOR: Elephant society is a family affair, especially for females. They stay with their mothers, sisters, aunts and cousins for their entire lives. The oldest female, known as the matriarch, is the leader. Young males stick with their mothers until they're about 10 years old, and then they leave the social group to live independently.

And elephants are always on the move.

KAREN MCCOMB: Elephants have this really unusual and complex social system. So, instead of just staying put and communicating with their immediate neighbors, they sort of move, in relation to each other, in a very fluid, fission-fusion way.

NARRATOR: Females and young males spend time with lots of elephants in groups of different sizes. And they communicate with dozens of different kinds of calls. Some rumbles are such low frequency, they're out of range of human hearing, but elephants can detect them from miles away.

Karen believes that their calls are crucial for the elephants to keep track of friend and foe.

KAREN MCCOMB: They'll come into contact with many, many other families as they move and feed. And they will be making decisions about which families it's safe to feed next to and which they should avoid.

NARRATOR: To find out how elephants make those decisions, Karen designed an experiment. It involves years of painstaking research and some very powerful speakers.

Karen has made a library of elephant contact calls and is going to play some to a group of elephants who are on the move and see how they react. First, she plays a call from an elephant from a different group, but a friendly one. The elephants just keep on walking, and their behavior doesn't change.

But when Karen plays a call from an elephant they don't know well, their behavior is very different. The elephants abruptly stop their march. They turn toward the unfamiliar voice, gather closer together, and move directly toward the sound, in what Karen says is a defensive show of force.

Karen tested twenty-one families and found that the elephants consistently distinguished between friend and stranger, recognizing up to a hundred different voices.

She believes that a lot of their brain power and memory is going into keeping track of other elephants, the ones they do and do not know, who is safe to be around and who might pose a threat.

And it could be the same with us.

JUSTIN GREGG: We have these relationships that we need to maintain, throughout our lives, with friends and enemies. And you have to remember who owes you a favor, and that sort of complexity seems to go hand in hand with the evolution of larger brains.

NARRATOR: It's not enough to be simply social. The animal world is full of social creatures, and plenty of them have some of the tiniest brains around.

JUSTIN GREGG: There are a lot of different kinds of social behavior of social animals. Insects, for example, termites and ants, are extremely social. They can't live by themselves, they need each other for everything that they do.

NARRATOR: Ants live in colonies, sometimes with millions of members, and divide labor between workers and soldiers. The collective might of termites can result in the construction of huge, elaborate mounds. And social living, along with an intricate communication system, is crucial to bees, with tens of thousands of individuals working together to find food and raise their young.

All these animals are highly social, and together, they can accomplish wonders, but each individual has a miniscule brain.

JUSTIN GREGG: Ants are always essentially working together toward one goal, to help each other out, to make the colony a success. Now, dolphins are on the other end of the spectrum, sometimes they cooperate, sometimes they are competing with each other.

So when you enter this element of both cooperating and competing, at the same time, in order to survive, this new kind of social complexity and intelligence blossoms.

NARRATOR: Cooperation and competition side by side: this is the recipe for a really complicated social life. And animals who live this way, often have big brains. But whether one leads to the other is still unclear.

Part of the challenge for scientists is figuring out how much animals like dolphins might understand about their social lives.

Dolphin cognition expert Diana Reiss has spent years trying to find out. She works with dolphins at the National Aquarium, in Baltimore. Keeping dolphins in captivity is controversial, and aquariums in the U.S. haven't captured wild dolphins for two decades.

Diana believes it's only in the controlled environment of aquariums that you can unlock some of the secrets of the dolphin mind.

DIANA REISS: Hello, how are you doing?

NARRATOR: Here, she can carry out experiments not possible in the wild.

The aquarium has an observation chamber, nicknamed “the pit.” It's cramped, but from here Diana has an excellent view of the dolphins' underwater behavior.

DIANA REISS: It's a beautiful bubble ring.

NARRATOR: This dolphin is making bubble rings, a behavior observed both in captivity and in the wild.

A dolphin blows out an air bubble from its blowhole and then flicks it with its tail to create a ring shape. Bubble rings appear to have no practical purpose, except for entertainment. It's another dolphin behavior we can relate to: the ability to play.

Diana wants to find out what else we share on an even more fundamental level. She's investigating whether dolphins recognize themselves as individuals. Do they each have a sense of “self?”

Diana places a one-way mirror inside the observation window.

DIANA REISS: So now, we're looking through a window, and they'll be seeing the mirror.

NARRATOR: The dolphins can't see people inside the pit. All they see are their own reflections.

Dolphins don't behave like this, staying in one place and staring, if they simply meet another dolphin. Another extremely unusual action is this curious fin wiggling.

DIANA REISS: This looks nothing like what they do when they're socially interacting with another.

NARRATOR: They also look inside their mouths or closely at their eyes.

DIANA REISS: They do perform all sorts of odd behaviors, much like we might do in front of the mirror to see what we look like, when we do that new dance step or when we just want to see how we look in a new, in a new outfit.

NARRATOR: They seem to be using the mirror like a tool, to see parts of their bodies that are usually out of view. This all supports the idea that dolphins must be aware they're looking at themselves.

Dolphins share this ability to recognize themselves in a mirror with just a few other animals. Elephants do it and so do chimpanzees. But the vast majority, including dogs, don't.

And, interestingly, neither do young humans. Before they're 18 months old, most children fail to point out a red dot painted on their cheek.

This boy assumes he's looking at another child.

Only when they're about two, does a child first realize that the mark is on her own cheek. She now knows the reflection is of herself.

Eventually, a human child's self-awareness will go far beyond recognizing her own body in a mirror. She'll be aware of her own thoughts and be able to contemplate the thoughts of others.

But is the same true for other animals, like dolphins? Diana thinks it might be.

DIANA REISS: Having a sense of self would go, I shouldn't say hand in hand, I could say flipper to flipper, with complex understanding of others.

NARRATOR: So, if animals like dolphins recognize themselves as individuals, how much do they understand about the other creatures around them? It's a question debated by animal researchers.

BRIAN HARE: The big question is not, “Do animals think?” The big question is, “Do they think about others' thinking?”

NARRATOR: Thinking about others' thinking is something we humans do all the time.

BRIAN HARE: As humans, we are remarkable, because we can imagine what it's like, in some context, to be someone else. That's an amazing ability we see in humans.

NARRATOR: This ability we have to imagine what it's like to be another person is known as “theory of mind.”

ALEXANDRA HOROWITZ (Barnard College, Columbia University): Theory of mind is the idea that humans, all humans, normally develop an understanding that other people have different minds than our own; that what I know is different than what you know; and that what I want is different than what you want.

And that's a big question for animal researchers: whether any non-humans animal also, eventually, or at all, develops a theory of mind.

NARRATOR: It's extremely difficult to prove that an animal thinks about other animals' thoughts, but some of the most interesting research has been done with our closest relatives, the chimpanzees.

Primatologist Frans de Waal works with chimpanzees at the Yerkes Primate Center, in Atlanta.

When an animal, like a chimp, is aware that another chimp has a different perspective on the world, it could give it an advantage. Chimpanzee groups have a strict ranking system. At the very top, is the most powerful chimp, the alpha male. He's in charge of the group, and every other chimp has a position of rank below him, from the most dominant to the most subordinate.

Frans has set up an interesting experiment to find out how a low-ranking animal behaves when it gets valuable information that a more dominant member does not know.

Could one chimp actively deceive another?

FRANS DE WAAL (Emory University): Most studies that are on deception are observational, anecdotal studies, but, nowadays, we do experiments also, on it, and, so you can, for example, hide food. One chimp knows where it is, the other one doesn't know where it is, and then you can see if deception goes on between them.

NARRATOR: The experiment involves two chimps, Rita and Missy. Rita is the more dominant.

At the start of the experiment, the chimps are in their sleeping quarters. One of the keepers goes into the outdoor enclosure and hides a banana under the red tube. Missy is allowed to watch through a window, and, so, she sees the keeper hide the banana.

Rita can see Missy watching through the window, but she can't see what's going on outside.

Then they let the chimps out.

Rita, the dominant chimp, comes out first. If she knew where the banana was hidden, she'd simply help herself. But only Missy, the subordinate, saw the banana being placed under the red tube. Rita just saw Missy watching, so the two have very different perspectives on the same situation.

Missy notices Rita close to the food and sits on top of the tube. She seems to be playing it cool.

Rita now wanders off. When she's far enough away, Missy goes for the banana. Frans believes that Missy has successfully deceived Rita.

He's observed this kind of behavior in chimps, but it's rare in other animals.

So if animals can deceive others, what would that say about their minds?

DIANA REISS: When we think about deception, you have to, sort of, understand the rules of the game. Deception is manipulating the rules of the game. So a highly social animal, who understands the rules of the game and then changes it, somehow, for its own benefit, or to make a joke, perhaps, or to achieve something, shows a level of sophistication.

NARRATOR: We humans are very good at it.

So, are the most successful animals natural born liars?

BRIAN HARE: If you live in a complex social group, you're competing against others who eat the same thing you do, who mate with the same individuals that you might want to mate with. So, if you can somehow manipulate the behavior of others, then you're going to have, potentially, a competitive advantage.

NARRATOR: But social living is not just about lies and deceit. Deception can only get you so far.

FRANS DE WAAL: There's a big disadvantage to deception—and that's why it is not so often used—is that, if I do that too often, to you, you may catch on, and, at some point, you don't trust me anymore.

NARRATOR: Frans believes that primates, as they negotiate their social lives, are very aware of the competition. And so he's come up with another experiment, this one to test their sense of justice.

Do they realize if they're being treated fairly or not, compared to others?

FRANS DE WAAL: Normally, you would think the only thing an animal should care about is, “What do I get for my task? I work, I get rewards,” but, no, they're comparing with what the other one is getting.

NARRATOR: Frans begins the fairness test with the capuchin monkey. These small, clever animals are kept in large enclosures, but for the short duration of the test, they're in a lab area. Each monkey carries out a simple task: they have to give a small stone to the experimenter, in exchange for a reward.

When both get a reward of cucumber, everyone's happy. But watch what happens when the one on the right receives a grape reward, instead.

FRANS DE WAAL: If you start giving one of them grapes, which are far better than cucumber, then the one who gets cucumber becomes very upset and becomes agitated, emotionally agitated.

NARRATOR: It turns out, quite a few creatures, including ravens and dogs, will protest if they get the short end of the stick, as if they know that they're being treated unfairly. But what about a concern for injustice for the other guy?

Research with one of our closest relatives, a highly social chimp, called a bonobo, is revealing some surprises.

At the Lola ya Bonobo orphanage in the Congo, animals spend most of their days in the forest, but come inside for short periods of time for experiments like this.

One bonobo is inside an enclosure. The door is locked and can only be opened from the other side. Here, another bonobo, a stranger, is given a delicious pile of fruit.

So, what will she do?

BRIAN HARE: We recently discovered that bonobos can share with strangers, that they actually will sacrifice their own food for the opportunity to interact with another bonobo they've never met before. That's not something that we thought another species would do. When we think about nature as “red in tooth and claw,” that you would share with somebody you don't share any genes with, it's not in your family, they're not even in your group, I thought that was something that humans did. So the fact that a bonobo does that is remarkable.

It's the closest you can think of to doing charity in animals.

NARRATOR: Among the most social animals, there's growing evidence for active concern for the wellbeing of others. Recently, it was reported that elephants will console an animal in distress by gently touching it with their trunks. And elephants do something else, which might demonstrate powerful feelings of connection to others of their species.

KAREN MCCOMB: Elephants, through observational evidence, seem to have a really unusual interest in the dead of their own species, either fresh carcasses or skulls. The very interesting thing is that the interest seems to persist after death.

NARRATOR: Karen McComb has devised an experiment to find out more. She takes the skulls of elephants killed by poachers, to make a miniature graveyard in the path of an approaching herd.

Now, she just observes.

KAREN MCCOMB: Yep, I think we've definitely got the beginnings of a reaction here. Some of the younger females are starting to respond. They've picked up a whiff of the skulls. The male is swinging his trunk towards the skulls and jawbones, as well.

NARRATOR: A few animals, including chimps, will be curious about the corpse of a companion, touching and investigating the body. But only elephants take an interest in the skulls and bones of their own kind long after death.

KAREN MCCOMB: We've got the females clustering around the skull and they are touching the jawbones. You see the way that the ends of the trunks are moist there? That's enhancing the scent that they're getting. You wouldn't see that in any other species, except for humans.

NARRATOR: To test whether this intense response was specific to elephant skulls and not just a reaction to a new object, Karen has done exactly the same thing with skulls from other animals.

KAREN MCCOMB: If you present elephants with the skulls of other large herbivores, and the biggest herbivores you can get—rhino, buffalo skulls—you do not get that level of interest. Given the choice between the three, they make a beeline for the elephant skull. And they're particularly interested, actually, in elephant ivory, that they will spend a massive amount of time investigating, picking it up, carrying it off, touching it. They are definitely able to recognize, distinguish the skulls and other remains of elephants from other species.

NARRATOR: This kind of behavior seems very familiar to us humans.

KAREN MCCOMB: Obviously, we are intensely involved and interested in death, in the sense that our relationships continue beyond that. And it's very interesting that this highly social animal seems to also have a social interest that extends beyond death.

NARRATOR: As we watch these elephants gently touch the remains of their dead, it's impossible to know exactly what is driving their curiosity or whether these animals might be experiencing emotions similar to what we would feel, like grief.

What scientists like Karen do know is that for highly social creatures, relationships are essential for survival.

So, with so much time and brain power spent reading social situations, could these animals be better prepared to gauge an interaction with another species?

One such interaction was reported not long ago in the waters near Hawaii, where a group of divers was swimming at night, photographing manta rays.

Unexpectedly, a lone dolphin swims close to the divers. They notice that the dolphin is tangled in a thin fishing line and has a hook stuck in its fin. Without help, he will probably perish.

JUSTIN GREGG: And it approaches this diver, as if it knows that the diver can possibly help out. And that's, in fact, what the diver does. It very gently cuts away the fishing line. It takes quite a while. The dolphin actually has to go up for air, and then come back down again.

NARRATOR: The entire process takes about seven minutes.

JUSTIN GREGG: So, the question is, what was the dolphin thinking?

My guess is the dolphin was just approaching the diver and then probably figured out that the diver was intending to help at that stage. So, did it come swimming out of the deep to solicit a diver's help? Probably not, but it certainly was smart enough to figure out that the diver could help once the diver started helping.

NARRATOR: When the fishing line has been removed, he swims away. It is a remarkable encounter between two species.

Witnessing the behavior of all these social animals, it's hard not to connect, to see some parallels with our own complicated lives.

BRIAN HARE: I mean, part of the experience of being human, as a species, is a bit lonely. And I think one of the really fun things about studying other animals is, over time, we learn that, actually, we're not the only really social species. We're not the only species that has, literally, soap operas going on every day in their lives.

And we're not the only species that has many of the same problems we experience. Whether it's that, “Oh, my gosh, I have to deal with my family member, who is driving me crazy, but they're my family so I have to support them;” or, you know, “Gosh, I have this friend that I like to hang out with, but they keep taking advantage of me;” or the fact that, “Oh, this guy, who he thinks he's so much bigger than me and he can do whatever he wants…I have to get my friends together and be nice to them, so they'll help me.”

These are all things that we experience together, with lots of other social animals on the planet. So, I think it's not just trying to understand what the life of animals are like. I think part of it is that it makes us feel part of nature and that we're not here alone. There are other animals that experience things that we also experience.

NARRATOR: And it could be that these kinds of experiences, these challenges that we face every day as social animals, have played a key role in the evolution of bigger and smarter brains, because in certain situations, the creature who can cleverly negotiate, who can lend or extend a helping hand, is often the one with the best chance of survival.

BRIAN HARE: I think we often think about evolution as always the biggest, strongest, most competitive individual is the one that's going to survive and reproduce. But I think we see, again and again and again and again, in evolution, that that's not the case at all. Other times, what's going to be favored is things that lead to better cooperation, so that you can work together to solve problems you otherwise couldn't solve on your own.

And that requires tolerance. That requires, actually, not dominance, but sometimes a lack of dominance. And so, when we study a wide variety of species, you see things beyond just it's always the big guy that wins.