Fish can be smarter than primates

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Fish can be smarter than primates

October 07, 2016 - 08:21

Read this fascinating article, first posted in Nautilus magazine, by clicking on the title or picture.

Intelligence is shaped by the survival requirements that an animal must face during its everyday life, according to cognitive ecology. Some birds can remember where they buried tens of thousands of nuts and seeds, which allows them to find them during the long winter months; a burrowing rodent can learn a complex underground maze with hundreds of tunnels in just two days; and a crocodile can have the presence of mind to carry sticks on her head and float them just below an area where herons are nesting, then pounce when an unwary bird swoops down to collect nesting material.

What about the mental abilities of fishes? Notwithstanding the liberties taken by filmmakers in popular movies like The Little Mermaid, Finding Nemo, and its sequel, Finding Dory, can fishes really think?

Here’s an example of fish intelligence, courtesy of the frillfin goby, a small fish of intertidal zones of both eastern and western Atlantic shores. When the tide goes out, frillfins like to stay near shore, nestled in warm, isolated tide pools where they may find lots of tasty tidbits. But tide pools are not always safe havens from danger. Predators such as octopuses or herons may come foraging, and it pays to make a hasty exit. But where is a little fish to go? Frillfin gobies deploy an improbable maneuver: They leap to a neighboring pool.

How do they do it without ending up on the rocks, doomed to die in the sun? With prominent eyes, slightly puffy cheeks looking down on a pouting mouth, a rounded tail, and tan-gray-brown blotchy markings along a 3-inch, torpedo-shaped body, the frillfin goby hardly looks like a candidate for the Animal Einstein Olympics. But its brain is an overachiever by any standard. For the little frillfin memorizes the topography of the intertidal zone—fixing in its mind the layout of depressions that will form future pools in the rocks at low tide—while swimming over them at high tide.

The goby’s skill was demonstrated by the late biologist Lester Aronson at the American Museum of Natural History, in New York City. Around the time that rats were wowing scientists with their cognitive mapping skills, Aronson constructed an artificial reef in his laboratory. He compelled his gobies to jump by poking a predator-mimicking stick into one of his constructed tide pools. Fishes who had had the opportunity to swim over the room at “high tide” were able to leap to safety 97 percent of the time. Naive fishes who’d had no high-tide experience were only successful at about chance level: 15 percent. With just one high-tide learning session the little gobies still remembered their escape route 40 days later.

A recent study has found that the brains of rock pool–dwelling goby species are different from those of goby species that hide in the sand and don’t need to jump to safety: The brains of the jumpers have more gray matter devoted to spatial memory, whereas the sand dwellers have a greater neural investment in visual processing.

Forming cognitive maps and recalling them weeks later illustrates more than a frillfin goby’s prodigious talent for avoiding a leap of faith. It also exposes the human prejudice to underestimate creatures that we don’t understand.

Being able to remember something is as useful to a fish as to a finch or a ferret, and the study of fish memories is not a new thing. In 1908, Jacob Reighard, a professor of zoology at the University of Michigan, published a study in which he fed dead sardines to predatory snapper fishes. Some of the sardines were dyed red, some not. The snappers didn’t mind, and gobbled both types. But when Reighard made the red sardines unpalatable by the gruesome method of sewing stinging medusa tentacles into their mouths, the snappers soon stopped eating the red ones. Notably, the snappers still wouldn’t touch red sardines 20 days later. This experiment not only demonstrates a snapper’s memory, but also his capacities to feel pain and to learn from it.

Another study of fish memory comes from Culum Brown, who collected adult crimson-spotted rainbowfish from a creek in Queensland, Australia, and transported them to his lab. They are named for a kaleidoscope of bright colors arranged in bands of scales along their flanks. Adult rainbowfish are about 2 inches long, and Brown guessed these ones were between one and three years old. He placed the fishes in three large tanks, about 40 to a tank, and allowed them a month to get used to their surroundings.

On testing day, he removed three males and two females at random from their home tanks and put them in an experimental tank, equipped with a pulley system that allowed a vertical net (the trawl) to be pulled along the length of the tank. The mesh size of the trawl was less than half an inch, allowing the fishes a clear view to the other side without being able to squeeze through its holes. A single, slightly bigger hole measuring three-quarters of an inch across was placed at the trawl’s center, providing an escape route when it was dragged from one end of the tank to the other.

The fishes were given 15 minutes to adjust to their new environment, then the trawl was dragged from one end to the other over a period of 30 seconds, stopping just over an inch from the end. The trawl was then removed and placed back at its starting position. This constituted one “run” of the experiment. Four more runs followed, at 2-minute intervals. Five groups of five fishes were tested in 1997, then tested again in 1998.

In the 1997 trials the rainbowfish panicked during the first run, darting about erratically and tending to cling near the tank edges, apparently not knowing what to do to escape the approaching trawl. Most of them ended up trapped between the glass and the net. Thereafter, their performance improved steadily, and by the fifth trial each shoal of five was escaping through the hole.

When the same fishes were retested 11 months later—having not seen the experimental tank or the trawl in the intervening period—they showed much less panic than they had the previous year. And they found and used the escape hole, on the first run, at about the same rate as they had by the end of the 1997 runs. “It was almost as if they had had no break and had 10 runs in a row!” Brown told me. Eleven months is nearly one-third of a rainbowfish’s life span. That’s a very long time to remember something that has happened to you on only one occasion.

On July 12, 2009, while diving off the Pacific islands of Palau, evolutionary biologist Giacomo Bernardi witnessed something unusual, and was lucky enough to capture it on film. An orange-dotted tuskfish uncovered a clam buried in the sand, picked up the mollusk in his mouth, and carried it to a large rock 30 yards away. Then, using several rapid head-flicks and well-timed releases, the fish eventually smashed open the clam against the rock. In the ensuing 20 minutes, the tuskfish ate three clams, using the same sequence of behaviors to open them.

Bernardi is thought to be the first scientist to film a fish demonstrating tool use, and his video unveils how the enterprising tuskfish doesn’t uncover the clam in a manner we might expect—by blowing jets of water from his mouth. He actually turns away from the target and snaps his gill cover shut, generating a pulse of water the same way that a book creates a puff of air when you close it fast. And it’s more than tool use. By using a logical series of flexible behaviors separated in time and space, the tuskfish is a planner. This behavior brings to mind chimpanzees’ use of twigs or grass stems to draw termites from their nests. Or Brazilian capuchin monkeys who use heavy stones to smash hard nuts against flat boulders that serve as anvils. Or crows who drop nuts onto busy intersections and then swoop down during a red light to retrieve the fragments that the car wheels have cracked open for them.

But what Bernardi saw that day was not exceptional. Scientists have noticed similar behavior in green wrasses, also called blackspot tuskfishes, on Australia’s Great Barrier Reef; in yellowhead wrasses off the coast of Florida; and in a sixbar wrasse in an aquarium setting. In the case of the sixbar wrasse, the captive fish was given pellets that were too large to swallow and too hard to break into pieces using only his jaws. The fish carried one of the pellets to a rock in the aquarium tank and smashed it, much as the tuskfish did the clam. The zoologist who observed this, Łukasz Paśko from the University of Wroclaw in Poland, saw the wrasse perform the pellet-smashing behavior on 15 occasions, and it was only following many weeks of captivity that he had first noticed it. He described the behavior as “remarkably consistent” and “nearly always successful.”

Hard-nosed skeptics might point out that this sort of thing isn’t real tool use because the fishes aren’t wielding one object to manipulate another, as we do with an axe splitting a log for firewood, or a chimpanzee does by using a stick to get to the tastiest termites. Paśko himself refers to the wrasses’ actions as “tool-like.” But this is not to demean the behavior, for as he points out, smashing a clam or a pellet with a separate tool is simply not an option for a fish. For one thing, a fish isn’t equipped with grasping limbs. In addition, the viscosity and density of water makes it difficult to generate sufficient momentum with an isolated tool (try smashing a walnut shell underwater by throwing it against a rock). And clasping a tool in his mouth, the fish’s only other practical option, is inefficient because fragments of food would float away, only to be snatched up by other hungry swimmers.

Just as the tuskfish uses water as a force for moving sand, the archerfish also uses water as a force—only this time as a hunting projectile. These tropical marksmen, averaging about 7 inches in length and sporting a row of handsome black patches down their silvery sides—mostly inhabit brackish waters of estuaries, mangroves, and streams from India to the Philippines, Australia, and Polynesia. Their eyes are sufficiently wide, large, and mobile to allow binocular vision. They also have an impressive underbite, which they use to create a gun barrel of sorts. By pressing their tongue against a groove in the upper jaw and suddenly compressing the throat and mouth, archerfishes can squirt a sharp jet of water up to 10 feet through the air. With an accuracy in some individuals of nearly 100 percent at a distance of 3 feet, woe betide a beetle or a grasshopper perched on a leaf above the backwaters where these fishes lurk.

The behavior is notably flexible. An archerfish can squirt water in a single shot, or in a machine gun–like fusillade. Targets have included insects, spiders, an infant lizard, bits of raw meat, scientific models of typical prey, and even observers’ eyes—along with their lit cigarettes. Archerfishes also load their weapons according to the size of their prey, using more water for larger, heavier targets. Experienced archers may aim just below their prey on a vertical surface to knock it straight down into the water instead of farther away on land.

Tool use by fishes, so far as we know, seems confined to a limited number of fish groups. Brown suggests that wrasses in particular may be the fishes’ answer to the primates among mammals and the corvids (crows, ravens, magpies, and jays) among birds in having a greater-than-expected number of examples of tool use. It could just be that living underwater offers fewer opportunities for tool use than living on land. But we do know that the tuskfishes (a member of the wrasse family) and archerfishes are prime examples of evolution’s boundless capacity for creative problem solving, and they might turn out to have plenty of company among other fishes.

Tool use by fishes, so far as we know, seems confined to a limited number of fish groups. Brown suggests that wrasses in particular may be the fishes’ answer to the primates among mammals and the corvids (crows, ravens, magpies, and jays) among birds in having a greater-than-expected number of examples of tool use. It could just be that living underwater offers fewer opportunities for tool use than living on land. But we do know that the tuskfishes (a member of the wrasse family) and archerfishes are prime examples of evolution’s boundless capacity for creative problem solving, and they might turn out to have plenty of company among other fishes.

For millennia, birds have been diving into the water to catch fishes. Sometimes the tables are turned. In February 2011 at Schroda Dam, a man-made lake in Limpopo Province, South Africa, scientists documented on film something that locals had reported seeing before. As a quartet of barn swallows skimmed just above the water, a tigerfish leaped up and snatched one of the birds out of midair.

The swallow capture wasn’t an isolated incident. The research team that published it reported about 20 separate swallow-snatching incidents per day, which represents as many as 300 barn swallows meeting their maker during the 15-day survey.

The four ecologists describe two distinct methods of attack being used by the tigerfishes. One involves skimming along the surface immediately behind the swallow, then launching to catch it. The other is a direct upward attack initiated from at least 1.5 feet below the surface. The advantage of the first approach is that the fish need make no adjustment for the surface-image shift due to light refraction at the water surface, which from underwater makes the swallow appear to be behind where it actually is. One disadvantage of this method is that it may compromise the element of surprise. Obviously, at least some of these fishes have learned to compensate for the distortion angle of the water surface, or else they would have no success with the second method.

This behavior raises a host of questions. How long have tigerfishes been doing this? How did it originate? How was it transmitted through the tigerfish population? And why aren’t swallows taking evasive action to avoid being caught, such as flying farther above the water?

I decided to ask the lead author of the tigerfish bird predation studies, Gordon O’Brien, a freshwater ecologist from the University of KwaZulu-Natal’s School of Life Sciences, in Pietermaritzburg, South Africa: “The tigerfish population in Schroda Dam was only established very recently from the lower reaches of the Limpopo River, in around the late 1990s. So the population there is very ‘young,’ ” replied O’Brien. “Although tigerfish are faring well within most of their range, in South Africa they are declining due to numerous human impacts. As a result, tigerfish have been placed on the South African protected species list, and introductions to man-made habitats are ongoing.”

I asked O’Brien how the bird-hunting behavior originated. He explained that from a tigerfish’s perspective the dam is very small, and that he believes the population has been forced to adapt or perish. He and his colleagues saw many larger individuals in very poor condition around the period when this behavior was first recorded in 2009.

O’Brien also had quite a bit to say about the ways in which bird hunting is transmitted through tigerfish populations: “This seems to be a learned behavior. Smaller individuals are not as successful and prefer a ‘surface chase’ approach to ambushing and striking from deeper below the surface, where the individual has to compensate for the light refraction. ... We know that tigerfish are very opportunistic and are attracted to heightened activity of other individuals—they get into some sort of a feeding frenzy. When the swallows return on their migrations the sight is quite spectacular and I think that it is during this period that the younger [tigerfishes] learn the behavior.”

Avivory is not unique to tigerfishes. Largemouth basses, pikes, and other predatory fishes have been witnessed on rare occasions leaping up to grab small birds perched on reeds near the surface. Large catfishes were recently filmed catching pigeons who come to drink from the shallows of the River Tarn in southern France; they use the same ambush technique used by orcas to catch sea lions, lunging and beaching themselves temporarily as they try to grab the prey with their mouths.

The authors of the discovery at Schroda Dam cite published notes from 1945 and again in 1960, from other locations in South Africa, by biologists who suspected that tigerfishes were catching birds in flight. Maybe one enterprising tigerfish made a lucky strike at an unsuspecting swallow, then honed his or her skill through practice. The behavior could have spread through the population by observational learning, which fishes can be very good at, as archerfishes demonstrate.

However it started, it has the hallmarks of flexible, cognitive behavior: It is opportunistic, since it is unusual behavior for the species; it requires practice to develop, and skill (and no doubt many failed attempts) to execute; it is almost certainly transmitted through observational learning; and different methods are used.

f fishes can innovate and learn to perform exacting, risky maneuvers to catch food, can they also reason their way through a space-time puzzle designed by humans? Imagine you are hungry and I offer you two identical pieces of pizza. I also tell you that the one on the left will be removed in 2 minutes, while the other one will not be taken away. Which piece will you eat first? Assuming you’re hungry enough to eat both pieces, you will almost certainly start with the piece on the left.

Now imagine you are a fish—a cleaner wrasse, in this instance—and you are offered a similar situation: two plates of identical food that differ only in their color. If you start eating from the blue plate, then the red plate is removed; if you choose red first, the blue plate is left where it is and you can have both. Since we can’t simply tell a fish that the red plate will be removed first, the fish has to learn it by experience. Elsewhere, similar experiments have been done with three species of brainy primates: eight capuchin monkeys, four orangutans, and four chimpanzees.

Who do you think did better? If you guessed it was one of the apes, no pizza for you. The fishes solved the problem better than any of the primates. Of the six adult cleaner wrasses tested, all six learned to eat from the red plate first. It took them around 45 trials to figure it out. In contrast, only two of the chimpanzees solved the problem in less than 100 trials (60 and 70, respectively). The remaining two chimps, and all of the orangutans and monkeys, failed the test. The test was then revised to help the primates learn, and all of the capuchins and three of the orangs got it within 100 trials. The other two chimps never did.

The researchers—10 scientists in Germany, Switzerland, and the United States—then presented the successful subjects with reversal tests, in which the plates suddenly took on the opposite roles. No one took well to this bit of deviousness. And only the adult cleaner wrasses, capuchin monkeys, and Orangutans switched preferences within the first 100 trials.

Several juvenile cleaner wrasses were also tested, and they performed markedly worse than the adult fishes, indicating that this is a mental skill that must be learned. One of the study authors, Redouan Bshary, even tried the test on his 4-year-old daughter. He set up an equivalent “foraging” trial, placing chocolate M&M’s on distinctive permanent and temporary plates. After 100 trials she had not learned to eat from the temporary plate first.

The authors draw a key conclusion: “The sophisticated foraging decisions which cleaner wrasses demonstrate ... are not easily achieved by other species with larger and more complexly organized brains.” But these skills did not come out of the blue (so to speak). The wrasses’ shrewd choice of which plate to eat from first resembles decisions these cleanerfishes have to make in the wild during interactions with client reef fish. And the logic of the experiment was deliberately designed to mimic that situation. Brain size be damned, if it’s critical to a species’ survival then that species will most likely be good at it.

Because cleanerfishes make their living by gleaning tidbits from the bodies of other fishes who have their own agendas, they need to be more attentive to the possibility that that food source might swim away at any moment. Bananas don’t do this; transient client fishes do. And cleaners get a lot of practice. Even on a slow day at the office, cleaner wrasses service hundreds of clients. When business is booming, they can have more than 2,000 interactions per day with a great variety of clients—some of them “regulars” who are residents of the reef, others (perhaps other species) “visitors” who are just passing through. Cleaners are able to discriminate between the two, and they start by servicing visiting clients who will swim off and visit another cleaner at another station if not inspected immediately. Regulars will still be around later on. Red plate, blue plate.

If you’re like me, you’re rather disappointed in the performance of the primates in what to us seems like a fairly straightforward mental challenge. “The apes’ unexpected lack of success appeared to be due to frustration with the task,” write the authors. It certainly isn’t because they are stupid. Great apes are renowned for solving puzzles, some of which they do better than humans can. For instance, chimpanzees far outperform humans in a spatial memory task with numbers randomly scattered on a computer screen. They also have the wits to use Archimedes’ principle—which exploits an object’s buoyancy—when confronted with a peanut sitting at the bottom of a clear narrow tube. Unable to dislodge the peanut or to reach into the tube, they will retrieve water from a nearby source, carry it in their mouths, and squirt it into the tube until the peanut floats within reach. Some inventive chimps will even urinate into the tube. Orangutans are renowned for their escape artistry, being able to pick locks. But those are different types of skills.

When fishes outperform primates on a mental task, it is another reminder of how brain size, body size, presence of fur or scales, and evolutionary proximity to humans are wobbly criteria for gauging intelligence. They also illustrate the plurality and contextuality of intelligence, the fact that it is not one general property but rather a suite of abilities that may be expressed along different axes. One of the reasons that the concept of multiple intelligences is so appealing is that it helps explain how one person can be an excellent artist or an accomplished athlete yet do rather poorly at, say, mathematical or logical tasks. It diminishes the importance we have historically placed on “intelligence” as defined by a selection of human abilities that’s too narrow even for our own species.


Jonathan Balcombe is the director of animal sentience at the Humane Society Institute for Science and Policy and the author of four books, including Second Nature and Pleasurable Kingdom. You can follow him on Twitter @jonathanbp1959

Excerpted from What a Fish Knows: The Inner Lives Of Our Underwater Cousins by Jonathan Balcombe. Published by Scientific American / Farrar, Straus and Giroux. Copyright © 2016 by Jonathan Balcombe. All rights reserved.

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