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This Squid Has Glowing Eyeshadow That Acts Like An Invisibility Cloak

Galiteuthis
Galiteuthis. Credit: MBARI

The oceans of the world are home to animals that render themselves invisible with glowing eyeshadow.

They’re called glass squid and, as their name suggests, they are largely transparent. They’d be impossible to see in the darkness of the open ocean were it not for their eyes—the only obviously opaque parts of their bodies.

These animals live between 200 and 1000 metres below the ocean surface, where water is mostly dark. Still, some sunlight penetrates to these depths, and this light is hundreds of times brighter than anything reflected horizontally or upwards. As such, any predator looking upwards at a glass squid would see the squid’s eyes in dark silhouette against a relatively light background.

To hide itself, a glass squid uses a trick that’s common among many oceanic animals: counter-illumination. Two organs under its eyes, known as photophores, give off a dim light, which perfectly matches the weak light coming from the surface. Their glow cancels out the squid’s silhouette so that, from below, instead of just being mostly invisible, it is completely invisible.

It helps that the glass squid’s eyes stick out from the side of its head, and are controlled by powerful muscles. No matter where the squid’s body is pointing, its gyroscopic eyes always stay in the same position, with the light-producing photophore beneath them.

But that still leaves a significant problem. Without any guidance, light would leave the photophore in every direction, making the squid hard to see from directly below, but very conspicuous from other angles. Its glowing invisibility cloak would also be a beacon, were it not for yet another cunning anatomical feature.

Amanda Holt and Alison Sweeney from the University of Pennsylvania have now reported in the Journal of the Royal Society Interface that a glass squid’s photophore consists of long, skinny cells that are shaped like hockey sticks—they run parallel to the eye, and then take a sharp downward turn. The walls of these cells are lined with reflective proteins that turn them into living optic fibres. They channel the photophore’s light along their length and then downwards, into the ocean’s depths.

“They’re a way of building a literal pipe for light,” says Holt.

But wait, there’s more!

When the duo first saw the fibres, they “thought it was going to be straightforward and boring,” says Sweeney. “Oh, there are little fibres. That’s cute. We’ll describe how they work and move on.” But when they looked more closely, they noticed that the fibres are really leaky. That is, they’re not perfectly reflective. A little light always pours out along their length.

They don’t have to be like that. A few easy structural changes would turn them into perfect light guides. Instead, “they’re really inefficient,” says Sweeney. “We struggled with that for a while, before realising: Oh, that’s part of the point.”

In the deep ocean, most light comes from directly above, but a small fraction still travels at oblique angles. So the squid’s counter-illuminating light also needs to work in many directions. That’s why the photophore fibres are leaky. They’re like the diffusers that you can stick on a camera to spread the light from a flash over a large area.

Holt confirmed this by creating simulating of the fibres and calculating how much light they send sideways and downwards. She also calculated the light levels in the squid’s mid-water habitat and, again, calculated the amount of light travelling sideways and downwards. The two ratios matched.

“I remember sitting in my office comparing the two, and my jaw dropped,” says Sweeney. “I thought there must have been a mistake and we couldn’t possibly have been that lucky the first time round. But we were.”

So the glass squid’s photophores are omnidirectional invisibility cloaks. They obscure the animal’s eyes by perfectly matching the light coming in from every direction (at least, in the lower half).

The squid shows how imperfections can actually be a good thing—a lesson that, according to Sweeney, engineers should pay attention to. “Over and over in biology, we see that evolution harnesses disorder in very clever ways to make better devices than what you’d get with highly ordered structures,” she says. “Thinking [about this] will help engineers to leverage the disorder in their systems rather than trying to get rid of it.”

What Hyena Giggles Really Say

A spotted hyena in Kenya. Photo by Liaka ac, CC BY-SA 2.0.
A spotted hyena in Kenya. Photo by Liaka ac, CC BY-SA 2.0.

Spotted hyenas may be the chattiest carnivores on the planet. They whoop, rumble, low, and laugh, announcing their presence wherever they go. But what do all these calls mean?

Zoologist Kay Holekamp laid out the spotted hyena repertoire in a 2011 New York Times field journal. So far as we humans are able to understand, each category of call carries a general meaning that can be modulated by the sender to varying effect. Spotted hyenas low when they want to team up, “alarm rumble” to raise a red flag to approaching danger, and groan to greet cubs at a den, who then “squitter” to demand milk from mom. And their trademark giggle? That’s nervous laughter. Spotted hyenas usually titter when they’re being attacked, harassed by another member of their clan, or frustrated.

But there are more details embedded in hyena calls than we usually pick up on. In a 2007 study, Holekamp, Kevin Theis, and colleagues reported that spotted hyena whoops – their haunting, long-distance calls – reflect details about the age, and sometimes sex, of the hyena sending the signal. By looking at the acoustic details of 117 whoop bouts from 60 different hyenas, the researchers were able to discern that whoops become deeper with age and that the calls of non-juvenile males and females could be distinguished from each other (perhaps because the larger females have bigger chests that give them a deeper pitch). If you were a hyena, your whoop would carry essential information about who you are.

Mother hyenas grunt to draw their cubs out, and those cubs "squitter" to beg for milk. Photo by Budgiekiller, CC BY-SA 2.5.
Mother hyenas grunt to draw their cubs out, and those cubs “squitter” to beg for milk. Photo by Budgiekiller, CC BY-SA 2.5.

A hyena’s giggle is even more distinctive. A 2010 study by Nicolas Mathevon and colleagues on 695 giggles made by the University of California, Berkeley’s captive hyena clan (shuttered last year, sadly) found that the carnivore’s characteristic laugh carried cues about the sender’s age, status in the clan, and perhaps individual identity. This is all critical information for a social predator. If you’re going to work as a group, you need to know who’s talking as well as what’s being said.

And while some of these details might be lost on other species, hyena chatter can carry critical information for their carnivorous neighbors. Cheetahs, zoologist Sarah Durant discovered through playback experiments, will leave an area if they hear the sounds of lions or hyenas. In fact, Durant observed, the sleek cats were even less likely to go on the hunt after hearing the calls from their competitors. What was the point of bringing down dinner if a hyena might swoop in and steal it?

Lions are another matter. Despite their regal reputation, these burly felids often play the part of kleptoparasites. Lions have no qualms about bullying weaker carnivores off their kills, and, as argued by Hugh Webster and colleagues after playback experiments, lions will eavesdrop on the calls of other species to zero-in on an easy meal. Wild dog calls always generated interest, the researchers found, but male lions or mixed groups of male and female lions would also approach spotted hyena vocalizations in the hope of some grub on the go. At least hyenas can mitigate the risk of losing their lunch. One population in Zimbabwe started traveling in mid-size groups, rather than forming large foraging parties, in response to an influx of lions.

Short of a Babel fish, we’ll never be able to translate hyena giggles down to the level of “Hey! That’s my wildebeest leg!” or “Get lost, you mangy lion!” But hyenas don’t need the broadened vocabulary we have to keep their clans together. Their set of a dozen or so calls seems to suit them fine, with each hyena adding their own unique voice to the chorus.

References:

Durant, S. 2000. Living with the enemy: avoidance of hyenas and lions by cheetahs in the Serengeti. Behavioral Ecology. doi: 10.1093/beheco/11.6.624

Mathevon, N., Koralek, A., Weldele, M., Glickman, S., Theunissen, F. 2010. What the hyena’s laugh tells: sex, age, dominance and individual signature in the giggling call of Crocuta crocuta. BMC Ecology. doi: 10.1186/1472-6785-10-9

Theis, K., Greene, K., Benson-Amram, S., Holekamp, K. 2007. Sources of variation in the long-distance vocalizations of spotted hyenas. Behaviour. doi: 10.1163/156853907780713046

Webster, H., McNutt, J., McComb, K. 2010. Eavesdropping and risk assessment between lions, spotted hyenas, and African wild dogs. Ethology. doi: 10.1111/j.1439-0310.2009.01729.x

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How a 5-Ounce Bird Stores 10,000 Maps in Its Head

It weighs only four or five ounces, its brain practically nothing, and yet, oh my God, what this little bird can do. It’s astonishing.

Photograph by Diana Tomback
Photograph by Diana Tomback

Around now, as we begin December, the Clark’s nutcracker has, conservatively, 5,000 (and up to 20,000) treasure maps in its head. They’re accurate, detailed, and instantly retrievable.

A Clark's nutcracker with a thought bubble full of maps
Photograph by Glenn Bartley, Alamy; Maps courtesy of jaffne, Flickr; GIF by Becky Harlan

It’s been burying seeds since August. It’s hidden so many (one study says almost 100,000 seeds) in the forest, meadows, and tree nooks that it can now fly up, look down, and see little x’s marking those spots—here, here, not there, but here—and do this for maybe a couple of miles around. It will remember these x’s for the next nine months.

How does it do it?

32 Seeds a Minute

It starts in high summer, when whitebark pine trees produce seeds in their cones—ripe for plucking. Nutcrackers dash from tree to tree, inspect, and, with their sharp beaks, tear into the cones, pulling seeds out one by one. They work fast. One study clocked a nutcracker harvesting “32 seeds per minute.”

These seeds are not for eating. They’re for hiding. Like a squirrel or chipmunk, the nutcracker clumps them into pouches located, in the bird’s case, under the tongue. It’s very expandable …

Drawing of one clark's nutcracker bird without seeds in its cheeks, and another clark's nutcracker with its cheeks full of seeds
Drawing by Robert Krulwich

The pouch “can hold an average of 92.7 plus or minus 8.9 seeds,” wrote Stephen Vander Wall and Russell Balda. Biologist Diana Tomback thinks it’s less, but one time she saw a (bigger than usual) nutcracker haul 150 seeds in its mouth. “He was a champ,” she told me.

Next, they land. Sometimes they peck little holes in the topsoil or under the leaf litter. Sometimes they leave seeds in nooks high up on trees. Most deposits have two or three seeds, so that by the time November comes around, a single bird has created 5,000 to 20,000 hiding places. They don’t stop until it gets too cold. “They are cache-aholics,” says Tomback.

When December comes—like right around now—the trees go bare and it’s time to switch from hide to seek mode. Nobody knows exactly how the birds manage this, but the best guess is that when a nutcracker digs its hole, it will notice two or three permanent objects at the site: an irregular rock, a bush, a tree stump. The objects, or markers, will be at different angles from the hiding place.

a drawing of clark's nutcracker looking at a tree stump and a mountain in the spring, with arrows pointing between the bird, the mountain, and the stump
Drawing by Robert Krulwich

Next, they measure. This seed cache, they note, “is a certain distance from object one, a certain distance from object two, a certain distance from object three,” says Tomback. “What they’re doing is triangulating. They’re kind of taking a photograph with their minds to find these objects” using reference points.

Psychologist Alan Kamil has a different view. He thinks the birds note the landmarks and remember not so much the distances, but the angles—where one object is in relation to the others. (“The tree stump’s 80 degrees south of the rock.”) These nutcrackers are doing geometry more than measuring.

a drawing of clark's nutcracker looking at a tree stump and a mountain in the rain, with arrows pointing between the bird, the mountain, and the stump
Drawing by Robert Krulwich

However they do it, when the snow falls and it’s time to eat, they’ll land at a site. “They will perch on a tree,” says Tomback, “on a low branch, [then light onto the ground, where] they pause, look around a bit, and they start digging, and in a few cases I’ll see them move slightly to the right or to the left and then come up again.”

She’s convinced that they’re remembering markers from summer or fall and using them to point to the X spot—and, “Lo and behold, these birds come up with their cracked seeds,” she says. “And it’s really pretty astounding.”

In the 1970s, Stephen Vander Wall ran a tricky little experiment. He shifted the markers at certain sites, so that instead of pointing to where the seeds actually were, they now pointed to where the seeds were not. Like this …

Picture of a clark's nutcracker standing between two X's and looking confused
Drawing by Robert Krulwich

And the birds, as you’d expect if they were triangulating, went to the wrong place.

But at sites where he left the markers untouched, the birds got it right. That’s a clue that each of these birds has thousands of marker-specific snapshots in their heads that they use for months and months. When the spring comes and the birds have their babies, they continue to visit old sites to gather seeds until their chicks fledge.

The mystery here, the deep mystery, is how do they manage to store so much data in their heads? I couldn’t possibly do what they do (I can’t even remember all ten digits in a phone number, so I’d be one very dead nutcracker in no time). Is their brain organized in some unique way?

Is their brain plastic? Can it grow more neurons or more connections when it needs to? Chickadees are also food hiders, and they do grow bushier brains when they need to, expanding in the “remember this” season and contracting afterward. Do Clark’s nutcrackers do that? We don’t know.

Whatever it is they do, I want what they’ve got.

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Caffeine Makes For Busy Bees, Not Productive Ones

A caffeinated bee is a busier bee. It’ll work harder to find food, and to communicate the location of said food to other bees. It will, however, misjudge the quality of the food it finds, and so make its colony less productive. The irony of writing about this as I sip an unwisely strong espresso at 10 pm is not lost on me.

The caffeine in coffee might give me a mental kick, but many plants rely on its bitter taste to deter plant-eating animals. Others, however, seem to bait themselves with caffeine, doping their nectar with low concentrations of the stuff. Why add a bitter deterrent to a liquid that’s meant to entice and attract pollinators?

Geraldine Wright from Newcastle University found one possible answer in 2013, when she showed that caffeine can improve a honeybee’s memory. Wright fed the insects with caffeine at concentrations that would affect their bodies, but that wouldn’t register as a bitter taste. She found that these bees were three times more likely to remember a floral scent. So, by providing caffeine, plants ensure that their pollinators are more likely to learn the link between their distinctive scents and the tasty nectar they provide.

What about the bees? Do they benefit from being drugged like this? One might think so, because they can more efficiently find the food they need. But Margaret Couvillon from the University of Sussex thinks otherwise.

She trained honeybees to forage from two feeders full of sugar water, one of which had been laced with a small amount of caffeine. She found that the caffeinated bees made more visits to the feeders. Once back in the hive, they were more likely to perform the distinctive waggle dance that tells other bees where to find food, and they performed the dance more frequently. And this means that a hive which exploits a caffeinated flower will send out about four times as many workers to that flower.

That wouldn’t be bad if this newly energised armada of workers was behaving more efficiently. But they’re not. Couvillon’s team showed that they’re more likely to persist with a caffeinated food source, even when that source no longer becomes useful. They also become faithful to their chosen feeder and become less likely to stray to a different host plant.

So, there’s the rub. Even though caffeine improves bee memory, it also causes them to overvalue caffeinated plants over decaffeinated ones that offer the same amount of energy. As the team writes, “The effects of caffeine in nectar are akin to drugging, where the pollinator’s perception of the forage quality is altered, which in turn changes its individual behaviours.”

By simulating these effects, Couvillon showed that if 40 percent of plants in the environment produce small amounts of caffeine—a realistic proportion—bee colonies would produce around 15 percent less honey every day.

They still need to test this prediction in real-world experiments. But if the results check out, it suggests that plants use caffeine as more than a deterrent against undesirable animals, but also as a way of manipulating desirable ones.

See amazing honeybees in “Hello, Honey! 10 Sweet Pictures of Bees.”

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With Sonar-Reflecting Leaves, Plant Lures Bats to Poo in it

Imagine a bat flying through the jungle of Borneo. It calls out to find a place to spend the night. And a plant calls back.

The plant in question is Nepenthes hemsleyana—a flesh-eating plant that’s terrible at eating flesh. It’s a pitcher plant and like all its kin, its leaves are shaped like upright vases. They’re meant to be traps. Insects should investigate them, tumble off the slippery rim, and drown in the pool of liquid within the pitcher. The pitcher then releases digestive enzymes to break down the corpses and absorb their nitrogen—a resource that’s in short supply in the swampy soils where these plants grow.

But N.hemsleyana has very big pitchers that are oddly short of fluid and that don’t release any obvious insect attractants. And when Ulmar Grafe from the University of Brunei Darussalam looked inside them, he saw seven times fewer insects than in other pitchers.

Instead, he found small bats.

Grafe enlisted the help of Caroline and Michael Schöner from the University of Greifswald, a wife-and-husband team who had worked on bats. Together, they repeatedly found the same species—Hardwicke’s woolly bat—roosting inside the plants, and nowhere else. In some cases, youngsters snuggled next to their parents.

The plant had adapted to accommodate these tenants: that’s why their pitchers are roomier than average, and have little fluid. And the bats repay them with faeces. Bat poo—guano—is rich in nitrogen, and the team found that this provides the pitcher with a third of its supply. The carnivorous plant has largely abandoned its insect-killing ways and now makes a living as a bat landlord.

This was all published in 2011. Since then, the Schöners and Grafe have discovered another extraordinary side to the relationship between the bat and the pitcher. “It started when we were searching for the plants in the forest,” says Michael Schöner. “We had a lot of difficulty. The vegetation is dense and the pitchers are green.”

This problem should be even worse for the woolly bats. They navigate by echolocation: they make high-pitched squeaks and visualise the world in the reflecting echoes. “Inside these forests, you get a reflection from everything, every single plant and leaf that’s there,” says Schöner. To make matters worse, the bats must distinguish N.hemsleyana from a closely related, similarly shaped, and far more common species, that’s unsuitable for roosting. How do they do it?

In South America, there are flowers with a similar problem: they are pollinated by bats, and must somehow attract these animals amid the clutter of the rainforest. They do it by turning their flowers into sonar dishes, which specifically reflect the calls of echolocating bats. The Schöners wondered if their pitcher plant had also evolved acoustic cat’s eyes.

They contacted Ralph Simon from the University of Erlangen-Nürnberg, who showed up with a robotic bat head.

It has a central loudspeaker and two microphones that look like a bat’s ears. He used it to “ensonify” the pitchers with ultrasonic calls from various directions, and measure the strength of the echoes.

The team found that the back wall of N.hemsleyana—the bit that connects its lid to its main chamber—is unusually wide, elongated, and curved. It’s like a parabolic dish. It strongly reflects incoming ultrasound in the direction it came from, and over a large area. Other pitcher plants that live in the same habitat don’t have this structure. Instead, their back walls reflect incoming calls off to the sides. So, as the woolly bats pepper the forest with high-pitched squeaks, the echoes from N.hemsleyana should stand out like a beacon.

Is this what actually happens? To find out, the team modified the pitchers’ reflectors. They enlarged them by building up the sides with tape, reduced them by trimming the sides with scissors, and cut them off entirely (while propping the lids up with toothpicks). Then, they hid the modified plants among some shrubbery, and placed them in a tent with some bats.

The bats took much less time to approach the pitchers with enlarged or unmodified reflectors than those with trimmed or amputated ones. And when given a choice, they mostly entered pitchers with natural, unaltered reflectors. They seem to be attracted to strong echoes but when they get close, they make a more considered decision about whether they have found the right species.

The team also found that the woolly bats produce the highest-pitched calls ever recorded from a bat. They don’t need such high frequencies to hunt their prey and, indeed, other insect-eating bats are nowhere near that high-pitched. Instead, the team believes that the calls are particularly well suited to detecting targets in cluttered environments. Between these squeaks and the plant’s reflectors, both partners can find each other in the unlikeliest of circumstances. The bat gets a home, and the plant gets its faecal reward.

Reference: Schöner, Schöner, Simon, Grafe, Puechmaille, Ji & Kerth. 2015. Bats Are Acoustically Attracted to Mutualistic Carnivorous Plants. Current Biology http://dx.doi.org/10.1016/j.cub.2015.05.054

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Nature’s Most Amazing Eyes Just Got A Bit Weirder

Eyes are testaments to evolution’s creativity. They all do the same basic things—detect light, and convert it into electrical signals—but in such a wondrous variety of ways. There are single and compound eyes, bifocal lenses and rocky ones, mirrors and optic fibres. And there are eyes that are so alien, so constantly surprising, that after decades of research, scientists have only just about figured out how they work, let alone why they evolved that way. To find them, you need to go for a swim.

Eyes of the peacock mantis shrimp. The black bands show where it's looking. Credit: Mike Bok
Eyes of the peacock mantis shrimp. The black bands show where it’s looking. Credit: Mike Bok

This is the eye of a mantis shrimp—an marine animal that’s neither a mantis nor a shrimp, but a close relative of crabs and lobsters. It’s a compound eye, made of thousands of small units that each detects light independently. Those in the midband—the central stripe you can see in the photo—are special. They’re the ones that let the animal see colour.

Most people have three types of light-detecting cells, or photoreceptors, which are sensitive to red, green and blue light. But the mantis shrimp has anywhere from 12 to 16 different photoreceptors in its midband. Most people assume that they must therefore be really good at seeing a wide range of colours—a “thermonuclear bomb of light and beauty”, as the Oatmeal put it. But last year, Hanna Thoen from the University of Queensland found that they’re much worse at discriminating between colours than most other animals! They seem to use their dozen-plus receptors to recognise colours in a unique way that’s very different to other animals but oddly similar to some satellites.

Thoen focused on the receptors that detect colours from red to violet—the same rainbow we can see. But these ultra-violent animals can also see ultraviolet (UV). The rock mantis shrimp, for example, has six photoreceptors dedicated to this part of the spectrum, each one tuned to a different wavelength. That’s the most complex UV-detecting system found in nature. Michael Bok from the University of Maryland wanted to know how it works.

Like us, mantis shrimps see colour with the help of light-sensitive proteins called opsins. These form the basis of visual pigments that react to different wavelengths of light, allowing us to see different colours. If a mantis shrimp has six UV receptors, it should have at least six opsins that are sensitive to different flavours of UV.

Except it doesn’t. Bok could only find two.

To which: huh?

How could there possibly be six types of photoreceptors with only two opsins? There was one possibility. Something could be filtering the light hitting the different receptors.

The rock mantis shrimp. Credit: Mike Bok.
The rock mantis shrimp. Credit: Mike Bok.

Here’s an analogy: say you’ve got a big crowd lining up in front of six security guards, each of whom must shout out when they spot someone with a specific name. One recognises Adams, another targets Bobs, and so on. But the guards aren’t too bright; they wouldn’t know Adam if he introduced himself. So you make their job easier. You rig the queuing system so that only Adams line up in front of Adam-blocking guard, only Bobs reaching the Bob-blocker, and so on. The guards shout pretty much indiscriminately, but they still do their jobs correctly. They’re not specific; you impose specificity onto them.

That’s exactly what happens in the mantis shrimp’s eye. When light enters the units in its eye, it must first pass through a crystalline cone, which lies over the receptors. Bok found that these cones contain UV-blocking substances called MAAs (or mycosporine-like amino acids, in full). There are four, possibly five, of these, which block slightly different wavelengths of UV. Combine these filters with the two underlying opsins, and you get six different classes of UV receptor.

Many marine animals have one or two MAAs. They use these as sunscreens to block UV from reaching their skin and eyes, and causing damage that could eventually lead to cancer. The mantis shrimps also use MAAs to block UV but for a unique purpose: to turn their eyes into incredibly sophisticated UV detectors.

Where do the MAAs come from? It’s not clear. No animal can make these chemicals themselves, so they must get them from their environment, possibly from their diet or from microbes. But two of the MAAs that Bok discovered have never been seen before, so it’s possible that the mantis shrimps can somehow change any incoming MAAs into five different types.

“We presented these results last summer at a big vision conference and one of my colleagues said: Now, you’ve solved all the problems. What are you going to do next?” says Tom Cronin, who led the study. “We sort of feel that way. The big problem now is: What does this all have to do with vision?” Why do mantis shrimps have such ridiculously complicated eyes? That’s the big question, and no one really knows.

The team are now trying to study how mantis shrimps react to different UV signals. For example, they find some short wavelengths of UV so repulsive that they’ll avoid food that’s paired with those wavelengths. Maybe this has something to do with aggressive signals? Mantis shrimps have rich social lives and they might communicate with ultraviolet patterns reflecting off their bodies.

“That’s the leading hypothesis but it has its own problems,” says Cronin. “Signals don’t evolve unless you have the visual system to see them. So you generally don’t have a system in place to see signals unless it’s there to see something else.”  So the team are also looking at the patterns of UV light in the places where mantis shrimps live. But even if that line of research pans out, many animals share the same waters, and none of them have such a complex eye. So why does the mantis shrimp?

When I spoke to Marshall last year, he said that the mantis shrimp’s style of vision might help it to process images very quickly without much contribution from its brain. That might be useful to a predator that uses some of the fastest strikes in the animal kingdom. But of course, that’s still a hypothesis.

And there’s another baffling layer of complexity: the receptors that detect red to violet colours are connected to different nerves than the ones that detect UV, and both streams lead to different parts of the brain. The mantis shrimp didn’t just evolve an absurdly over-engineered way of seeing, it did it twice.

Reference: Bok, Porter, Place & Cronin. 2014. Biological Sunscreens Tune Polychromatic Ultraviolet Vision in Mantis Shrimp. Current Biology http://dx.doi.org/10.1016/j.cub.2014.05.071

More on mantis shrimps:

Mantis shrimps have a unique way of seeing

The Mantis Shrimp Sees Like A Satellite

Mantis shrimp eyes outclass DVD players, inspire new technology

The mantis shrimp has the world’s fastest punch

Why are stabby mantis shrimps much slower than punchy ones?

How mantis shrimps deliver armour-shattering punches without breaking their fists

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The Only Way To Hide From A Sea Catfish Is To Stop Breathing

A bristle worm, buried in the sand at the bottom of the ocean, might seem safe. Nothing can see it. The overlying sediment masks its scent. It doesn’t disturb the surrounding water.  It does, however, still need to breathe. As it does, it releases spurts of carbon dioxide, which makes the water above its burrow ever so slightly more acidic. The change is tiny, fleeting and restricted to a 5 millimetres zone around the burrow’s entrance.

It’s enough for the Japanese sea catfish.

Like all catfishes, this species has long whiskers or barbels sticking out of its face. They house tastebuds that allow the animal to detect chemicals in the water around it. But John Caprio from Louisiana State University has discovered that the barbels are also pH meters. They are so sensitive that they can pick up the tiny changes in acidity produced by a breathing worm. When this predator swims ahead, a simple exhalation gives its prey away.

Caprio’s discovery, published today, is the culmination of around 25 years of on-and-off work. He has long been fascinated how the nervous system encodes information about taste and smell. “Why are there these two chemical senses, when you have just one visual one and one auditory one?” he says. “These systems evolved in vertebrates in the water, so you have to go and ask the fish.”

By 1984, Caprio travelled to Japan to work with marine catfish. He had already worked with similar animals in the Gulf of Mexico, and he wanted to know if their Japanese counterparts taste the world in a similar way. But as he exposed the fish to various chemicals, he noticed something odd. One particular group of amino acids—the building blocks of proteins—triggered a powerful reaction in a nerve within the fish’s barbels.

At first, it didn’t make sense. There didn’t seem to be any common thread to the amino acids that sent the nerve into overdrive. Then, Caprio worked it out. “I suddenly realised that all of them, even though they were very different, would change the pH of a solution,” he says.

The pH scale typically runs from 0 (extremely acidic; red on litmus paper) to 14 (extremely alkaline or basic; blue on litmus paper). Hydrochloric acid has a pH of 0; drain cleaner is 14. Distilled water is perfectly neutral at 7. Seawater is slightly basic at around 8.2.

Detecting pH changes isn’t a weird ability; you’re doing it right now. Sensors in your brainstem detect the pH of your blood, which reflects how much carbon dioxide is dissolved in it. If the pH falls too much, you automatically start breathing more quickly. If it goes up, your breaths slow down. But these sensors are internal ones; by contrast, the catfish’s barbels are the first known animal sensors that detect pH changes in the surrounding world.

And that’s very odd, because pH values in the ocean are incredibly stable. Between the 18th and 20th centuries, the pH of the surface ocean has fallen by just 0.1 of a unit, and it took all the carbon dioxide released by all human activity around the entire world to pull that off. In this world of constancy, why would a fish need such an exquisite pH sensor? It’d be like having an altitude meter in a world that’s completely flat.

Japanese sea catfish, Plotosus japonicus. Credit: Kagoshim Aquarium.
Japanese sea catfish, Plotosus japonicus. Credit: Kagoshim Aquarium.

Caprio batted some ideas around with his Japanese colleagues, and they reasoned that the pH sensors could help the fish to find its prey. Japanese sea catfish eat bristle worms—we know that because fishermen have found loads of the worms inside their stomachs. The worms hide in U- or Y-shaped burrows, and the catfish search for them by cruising along the ocean floor at night.

When Caprio’s team placed the worms in beakers, they found that the pH of the water just above the burrows falls by 0.1 to 0.2 units. That’s well within the range that the barbels can spot. Indeed, when the team placed artificial worm-filled tubes in tanks containing catfish, the fish would always swim over and suck the worms out—even in pitch darkness.

The team repeated the same experiment without any worms; they just hooked up a pipe to the artificial tubes, and released a small squirt of sea water with a pH of 7.9—slightly more acidic than the tank water at 8.1. “Immediately, the fish’s behaviour changed. It went straight into food searching behaviour,” says Caprio. They would even bite the end of the tube. “That was very consistent; we never saw that when we pumped in water with the same pH [as the tank].”

But why has the catfish evolved this astonishing sense, when it has so many others at its disposal? It has taste, smell, sight, and the ability to sense pressure changes in the water.

Caprio thinks that a pH sense offers several advantages. Taste and smell can react to chemicals in the water that come from rotting flesh, but pH changes always mean the presence of live prey. And close prey too. An extra burst of acidity doesn’t last long in the sea, so if the catfish sense a drop in pH, it means that food is right there. “It doesn’t have to search; it goes into feeding mode,” he says.

But wait: the sea catfish can also detect the minute electrical signals given off by its prey. Sharks, rays, and platypuses have the same ability, and they use it to uncover hidden meals just like the sea catfish does. “Why does it need an extra sense in addition to electroreception?” asks Caprio. “I can’t answer that.”

Also, what are the pH sensors? Are they the same as the ones that help our brainstem to control our breathing? Where are they? They’re definitely in the barbel and the lip, so perhaps they’re all over the fish’s head. What carries information from these sensors to the brain? And what will happen to the catfish’s ability as the world’s oceans become more acidic? Will its other senses keep it well-fed, or will it suffer?

Unfortunately, Caprio probably won’t be the one to answer these questions. “All the authors of this paper are at the end of our scientific careers,” he says. “Three have already retired. One will. I’ve been at LSU for 38 years. We’re hoping this report alerts the young folks in the field to follow the question, because we probably won’t.”

Reference: Caprio, Shimohara, Marui, Harada & Kiyohara. 2014. Marine teleost locates live prey through pH sensing. Science http://dx.doi.org/10.1126/science.1252697

Related: “Swimming Tongue” Catfish Sense Chemicals in Prey’s Breath

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Man-Made Electromagnetic Noise Disrupts a Bird’s Compass

For three years, the experiment wouldn’t work, and Henrik Mouritsen couldn’t figure out why.

He had captured European robins and placed them in funnel-shaped cage in a windowless room. The funnel was lined with blotting paper, which preserved the marks of the robins’ feet as they tried to escape. Typically, the birds would try to flee in a consistent direction. Robins, after all, can sense the Earth’s magnetic field with an internal compass in their heads. Even when they can’t see the sun, moon, stars or any other landmark, this compass helps them find their way.

Scientists first noticed this in the 1950s, and they’ve used the funnel experiment ever since to study the magnetic sense of robins and many other birds. It’s a classic. Mouritsen had done it many times before.

But when he moved to the University of Oldenburg around a decade ago, the experiment stopped working. “We tried all kinds of things. We changed the light intensity, the size and shape of the funnels, the food the birds were getting, whether they were kept indoors or outdoors,” says Mouritsen. “We tried it all but it didn’t work. I had a very frustrating time.”

Then, in 2006, his postdoc Nils-Lasse Schneider said, “Should we try putting a Faraday cage around them?” That’s a conductive enclosure that shields its contents from electric fields by channelling electricity through its own walls (here’s a demo). If electric fields were somehow disrupting the birds’ compass, a Faraday cage would fix the problem. “I thought that probably wouldn’t help but I was desperate,” says Mouritsen. The team laboriously erected a grounded aluminium cage around the robins’ hut and connected it to an electrical supply.

When the birds were exposed to background electromagnetic noise in their unscreened huts, they flew in random directions. When the Faraday cage was on, their compass started working again. “It was like flipping a switch,” says Mouritsen.

It was an astonishing result, and one that Mouritsen knew he needed to check carefully. As he writes, “seemingly implausible effects require stronger proof’’. Many small studies have claimed that man-made electric and magnetic fields could affect animal biology and human health, and many people have anecdotally claimed that they’re highly sensitive to such fields. But whenever scientists investigate those claims through proper experiments—double-blind trials with a large sample size—the effects vanish. (Here’s a good PDF summary of the evidence.)

“I had no intention of publishing study number 225 of that kind,” says Mouritsen. So, his team, led by Schneider and student Svenja Engels, repeated the experiment, again and again. It took a long time—they were already three years behind and had other work to pursue. But after 7 years, they had run many double-blind trials involving many birds. Several generations of students independently worked on the study. The results were always the same.

At one point, someone forgot to connect the grounding to the cage, and the birds stopped orienting again. When Mouritsen discovered the problem, he decided to make it part of the experiment. Without telling the students who were checking the birds, he and Schneider would randomly disconnect or connect the grounding. The birds still behaved as predicted: switching off the cage disrupted their bearings. “My first reaction was, ‘It can’t be’, and the first reaction of most people to this paper will be, ‘It can’t be’,” says Mouritsen. “But I’m sure it is.”

This has nothing to do with wi-fi, mobile phones, or power lines. By deliberately adding electromagnetic fields inside the grounded huts, the team showed that they were sensitive to frequencies between 2 kilohertz and 5 megahertz. With that range, the culprits are likely to be either AM radio signals or fields produced by electronic equipment in the university, although it’s hard to narrow the source down any further.

It’s not clear if wild birds are being affected. It’s not clear. Populations of night-time migrating songbirds are falling, but there could be many causes for that including hunting and light at night. Disrupting a bird’s magnetic compass isn’t even a dealbreaker; it could still use the sun and stars to navigate. But if skies are overcast and these other cues are lost, a faulty compass might become a bigger impediment.

If man-made electromagnetic fields are affecting wild birds, they would only do so in very specific places. When the team moved their huts to a rural location 1 kilometre outside of Oldenburg, with natural background levels of electromagnetic noise, the robins could orient themselves even when the Faraday cage was off. This suggests that the disruptions only happen near cities, where electronic devices are common.

But Roswitha Wiltschko has done 40 years of successful experiments with robins in a downtown district of Frankfurt. “We never used any shielding, and our controls were excellently oriented,” she says. “The situation at the University of Oldenburg must be particularly bad, and it makes one wonder about the source of this disrupting field. It doesn’t seem to be the usual case within cities.”

Mouritsen’s results are also puzzling because the electromagnetic fields around his university are very weak. They’re weaker than the Earth’s own magnetic field. They’re 100-1000 times below the exposure limits that the World Health Organisation recommends. They’re so weak that they really shouldn’t be able to affect biological tissues. And yet they’re altering the sensory system of a bird.

That’s weird, but it also supports a longstanding idea about how a bird’s magnetic compass works—one that involves quantum physics.

Birds have a molecule called cryptochrome in their eyes. When light strikes cryptochrome, it shunts an electron over to a partner molecule, creating a pair of ‘radicals’—molecules with solo electrons. These unpaired electrons have a property called “spin” and they can either spin together, or in opposite directions. The two states can flip from one to another, and they lead to different chemical outcomes. This is where the Earth’s magnetic field comes in. Weak though it is, it has enough energy to influence the flips of the radical pair. In doing so, it can affect the outcome of the pair’s chemical reactions.

The cryptochrome idea was proposed in 2000 and it’s still controversial, even among biologists who study magnetic sense. If it’s right, it could explain how electromagnetic field as weak as those Mouritsen measured could affect his caged robins. “This is speculative, but I think our findings are very strong evidence that the magnetic compass sense of these birds must be fundamentally quantum mechanical,” he says.

These results don’t mean that electromagnetic fields are negatively affecting human health. “We are certainly not saying that,” says Mouritsen. “We don’t know, but I’m pretty sure that there’s not going to be a dramatic effect.”

Indeed, the magnetic compass of birds is a special sense—one that can exploit (and be disrupted by) the tiny energies of low-level electromagnetic noise. The same isn’t true for vision, smell or touch, which is why the robins couldn’t orient but were otherwise unaffected. Mouritsen’s discovery might apply to animals that also have magnetic senses, and it’s still unclear if humans have such a sense.

“The results are very intriguing, but it is unknown whether they are relevant to humans,” says Maria Feychting from the Karolinska Institute, who studies the health effects of magnetic fields. “They suggest that migratory birds may be sensitive, and these birds may have a specialised system that is not present in mammals/humans.”

Reference: Engels, Schneider, Lefeldt, Hein, Zapka, Michalik, Elbers, Kittel, Hore & Mouritsen. 2014. Anthropogenic electromagnetic noise disrupts magnetic compass orientation in a migratory bird. Nature http://dx.doi.org/10.1038/nature13290

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The Mantis Shrimp Sees Like A Satellite

The most extraordinary eyes in the animal kingdom belong to the mantis shrimps, or stomatopods—pugilistic relatives of crabs and prawns, which are known for delivering extremely fast and powerful punches. Their eyes sit on stalks and move independently of one another. Each eye has “trinocular vision”—it can gauge depth and distance on its own by focusing on objects with three separate regions. They can see a special spiralling type of light called circularly polarised light that no other animal can. And they have a structure in their eyes that’s similar to technology found in CD and DVD players, only much more effective.

And now, Hanne Thoen from the University of Queensland has found that mantis shrimps see colour in a very different way to all other animals.

Most people have three types of light-detecting cells, or photoreceptors, in their retinas. These are sensitive to red, green and blue light, respectively. Birds, reptiles and many fish have a fourth photoreceptor that detects ultraviolet light. Four is plenty. Mathematical models tell us that you only need four receptors, maybe five, to effectively encode the colours within that range.

The mantis shrimp has twelve different photoreceptors.

Eight of these cover the parts of the spectrum that we can see, while four cover the ultraviolet region. That seems like a ludicrous excess. If four or five receptors are all an animal needs, “why on earth do stomatopods need 12 channels?” says Justin Marshall, who led the new study.

The obvious answer is that they’re very good at discriminating between different colours. That would be a handy skill: mantis shrimps live in coral reefs, which are bursting with colours. Many of them are brightly coloured themselves, and use their lurid body parts to communicate with one another. “With 12 receptors, you’d think that they can detect colours much better than any other animal,” says Marshall.

“Actually, they’re much worse!”

Thoen discovered their surprising ineptitude by studying a small species called Haptosquilla trispinosa. She presented the animals with two optic fibres, each displaying a different colour. If they attacked the right one, they earned a tasty snack. Thoen then changed the colour of the off-target fibre to the point when the mantis shrimp could no longer tell the difference between the two.

If a human did this test, we’d be able to tell the difference between colours whose wavelengths are 5 nanometres apart—compare the left and middle columns in the image below. A mantis shrimp would struggle with that. The can only discriminate between colours with a 15-25 nanometre difference—compare the middle and right columns.

Mantis-shrimp-colours
A human could tell the difference between the colours in the left and middle columns with a 50% accuracy. A mantis shrimp could only do the same for the colours in the middle and right columns.

Despite their 12 photoreceptors, mantis shrimps are worse at telling apart different colours than humans, honeybees and butterflies.

“Thoen is a very careful scientist, so the data are completely convincing, if quite surprising,” says Tom Cronin from the University of Maryland, Baltimore County, who studies mantis shrimp vision. “We certainly would have predicted a much more competent sense of color discrimination than this!  However, behaviour is the ultimate test of what an animal can do, so this is what the animals say that they are capable of.“

They must be using the information from those receptors in a very strange way.

We see colours by making comparisons between our three receptors. By comparing the outputs of the red and green receptors, we can tell the difference between reds and greens. And by comparing their combined output against that of the blue receptors, we can discriminate between blues and yellows. This is called the “colour opponent process” and it’s what every colour-sighted animal does.

Every animal… except the mantis shrimps. Given their poor performance in Thoen’s tests, they cannot possibly be making these comparisons. What are they doing instead?

“The simple answer is: Dunno,” says Marshall. “I’ll admit right up front we don’t fully understand.”

Their working hypothesis is that the mantis shrimps analyse the outputs from all of their 12 receptors at once. Rather than making comparisons between those receptors, they pass the entire pattern of outputs onto the brain, without any processing. “One could imagine that they have a look-up table in their brain,” says Marshall. So rather than discriminating between colours like we do, their eyes are adapted for recognising colours.

“Oddly enough, the closest device to stomatopods would be a satellite,” says Marshall. “Remote sensing algorithms have look-up tables of colour to fill in the image that the satellite forms.”

Marshall suggests that this way of dealing with colour should be much faster than ours, since there is no need to send the photoreceptors’ signals through any intermediary neurons. And speed matters for mantis shrimps. These ambush hunters attack their prey with rapidly unfurling arms, which end in either stabbing spears or pounding clubs. The clubbed species, known as smashers, can hit their targets with the force of a rifle bullet and deliver the fastest punches in the animal kingdom. They need fast eyes to complement their fast arms.

And they only have a small brain. “A mantis shrimp only has a fraction of our cortical processing power, yet it handles 4 times more input,” says Nicholas Roberts from the University of Bristol. “The non-comparative processing system they have evolved represents a novel solution for increasing data acquisition while minimising any downstream processing overhead.”

Of course, this is still conjecture. Thoen and Marshall have shown that mantis shrimps definitely don’t see colours in the same way as us, but what they actually do is a mystery. Now, they’re trying to work out what happens to signals when they leave the photoreceptors, and how these cells are connected to the brain.

Cronin also wants to know “whether these animals combine their colour receptor signals in different ways for different tasks. Perhaps analysis of mate displays or colour signals demands a more thorough discrimination than food recognition.”

Marshall adds that the mystery is relevant to one of the most important questions in neuroscience: How does a nervous system make sense of information from the outside world. “This is clearly a very different way of computing that information,” he says. “It’s not just about weird shrimp biology. It touches on a number of neuroscience questions.”

Reference: Thoen, How, Choiu & Marshall. 2013. A Different Form of Color Vision in Mantis Shrimp. Science http://dx.doi.org/10.1126/science.1245824

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Why Are Reindeer Eyes Golden In Summer But Blue In Winter?

When Glen Jeffery first took possession of a huge bag full of reindeer eyes, he didn’t really want them.

Jeffery is a neuroscientist from University College London who studies animal vision, and his Norwegian colleagues had been urging him to study the eyes of reindeer. They wanted to know how these animals cope with three months of constant summer sunlight and three months of perpetual winter darkness. “I thought it was a dumb idea,” says Jeffery. The animals would probably adapt to the changing light through some neurological trick. The eyes weren’t the right place to look.

But the Norwegians persisted, and they eventually sent him a bag full of eyes, taken from animals killed by local Sami herders. The eyes were divided into two sets—one from animals killed in the summer, and another from those killed in the winter. Jeffery started dissecting them. “I opened them up and went: Jesus Christ!” says Jeffery. “Hang on. They’re a different colour”

In the summer, reindeer eyes are golden. In the winter, they become a deep, rich blue. “That was completely unexpected,” says Jeffery.

That was 13 years ago. Since then, he has been working to understand the secrets behind the chameleon-like eyes, along with Karl-Arne Stokkan from the University of Tromsø and others.

The bit that actually changes colour is the tapetum lucidum or “cat’s eye”—a mirrored layer that sits behind the retina. It helps animals to see in dim conditions by reflecting any light that passes through the retina back onto it, allowing its light-detecting cells a second chance to intercept the stray photons. The tapetum is the reason why mammal eyes often glow yellow if you photograph them at night—you’re seeing the camera’s flash reflecting back at you.

Most mammals have a golden tapetum, and so do the reindeer in summer. So why does this layer become blue in winter? Through years of dissections and measurements, Jeffrey’s team think that they have the answer. And it begins in darkness.

Credit: Alexandre Buisse

In dark conditions, muscles in your irises contract to dilate your pupils and allow more light into your eyes. When it’s bright again, the irises widen and the pupils shrink. The same thing happens in reindeer, but the interminable Arctic winter forces their pupils dilate for months rather than hours. Over time, this constant effort blocks the small vessels that drain fluid out of the eyes. Pressure builds up inside the eyeballs, and they start to swell. “The animal’s moving towards glaucoma,” says Jeffery.

These events also change the tapetum. This layer is mostly made up a collagen, a protein whose long fibres are arranged in orderly rows. As the pressure inside the eye builds up, the fluid between the collagen fibres gets squeezed out, and they become more tightly packed. The spacing of these fibres affects the type of light they reflect. With the usual gaps between them, they reflect yellow wavelengths. When squeezed together, they reflect… blue wavelengths.

So: as reindeer spend months of darkness, their permanently dilated pupils lead to swollen eyes, compressing the fibres in their tapetum and changing the colour of light they reflect.

The team also think that this makes the eyes more sensitive. They tested the retinas of reindeer eyes, both isolated ones and those still in the heads of live, anaesthetised animals, and found that the blue winter ones are at least a thousand times more sensitive to light than the golden summer ones.

Jeffery explains that when yellow light reflects off the tapetum, most of it bounces straight out again. The retina gets just one more chance to intercept it. But blue light gets scattered. “Instead of the photons bouncing back out of the eye, they bounce around and gets captured, which increases the sensitivity” says Jeffery.

But other scientists aren’t convinced by this explanation. Dan-Eric Nilsson, a vision expert from Lund University, is excited that the sensitivity of the reindeer eyes and the colour of their tapetum change with the seasons. Both are interesting, but the latter does not explain the former.

Here’s his argument: Let’s say that the retina captures around 50 percent of the light that enters the eye, and that the tapetum reflects all of the rest. The retina captures half of these reflections, ending up with 75 percent of the original total. Even if you assume that the retina was infinitely inefficient, the most the tapetum could do is to double its sensitivity. And Jeffery’s team found that the retina becomes around a thousand times more sensitive in winter. “They’ve found an interesting phenomenon, but failed in explaining it,” says Nilsson. He suspects that, instead, the reindeer is changing the levels of light-sensitive pigments in its retina.

Trevor Lamb, another eye expert at the Australian National University, agrees. “I wouldn’t be at all surprised if the retina managed to increase its sensitivity during winter through some kind of intra-retinal changes, quite separate from the tapetal ones,” he says, “but that is pure speculation on my part.”

But Jeffery’s team has another piece of evidence for their hypothesis—one which they mention briefly in their new paper but will outline more fully in a future one. “We got halfway through this project and everything’s cruising brilliantly, and we suddenly hit a brick wall,” he says. “We suddenly found animals with a green tapetum.”

It turned out that these reindeer had been bought from Sami herders and kept in large pens, where they could just about see the sodium street-lights of nearby towns. Their pupils partly dilated during the winter, the pressure in their eyes increased a little, their collagen fibres became slightly squeezed together, and their tapetums stopped halfway along their yellow-to-blue transformation. Et voila. Green tapetum.

“And we measured the sensitivity in their eyes,” says Jeffery. “Way down.”

It could still be that the changes in the eyes are independently changing the colour of the tapetum and the sensitivity of the retina. It’ll require more evidence to link the two, but both observations alone are still pretty cool. As Nilsson say, “I am not aware of any other seasonal changes in the visual optics. In that respect, this is a novel and exciting discovery.”

Reference: Stokkan, Folkow, Dukes, Nevue, Hogg, Siefken, Dakin & Jeffery. 2013. Shifting mirrors: adaptive changes in retinal reflections to winter darkness in Arctic reindeer. Proc Roy Soc B http://dx.doi.org/10.1098/rspb.2013.2451

PS: If, like me, you do a Google image search for tapetum lucidum pictures, you’ll find several images where the eyes look topaz, rather than yellow. This is very different from the deep, rich blue of the reindeer’s winter eyes. Partly, it happens because digital cameras automatically adjust the pictures they take. But it’s also because golden tapetums do have a topaz fringe, which takes over the reflections if you photograph the animal from an angle.

Update: This article has been corrected from an earlier version, which suggested that the colour difference was obvious when Jeffery opened up the bag, not the actual eyes. Thanks to Hester van Santen for pointing out the error.

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“Deaf” Frog Hears By Using Its Mouth As An Echo Chamber

Gardiner’s frog shouldn’t be able to hear. This dime-sized amphibian doesn’t have the right equipment for it.

In your head, sound waves pass through the flappy bits of your ear and vibrate a taut membrane—the eardrum. On the other side, three tiny bones transfer these faint air-borne vibrations into the fluid-filled inner ear, amplifying them along the way. In the inner ear, little hairs detect the vibrations and convert them into electrical signals that travel to your brain. This is how you hear, and it all depends upon the eardrum and the three bones within the so-called middle ear. Without these structures, 99.9 percent of the energy of incoming sound waves would be lost.

Gardiner’s frog doesn’t have a middle ear or an eardrum. It ought to be deaf.

And yet, it sings. When Renaud Boistel used loudspeakers to play recordings of the frog’s calls, other males would start calling in response. So, how does this “deaf” frog manage to hear? Boistel has a possible answer—they use their mouths.

A delightful chart showing some of the world's tiniest frogs, all doing jazz hands. Credit: Xiaphias
A delightful chart showing some of the world’s tiniest frogs, all doing jazz hands. Credit: Xiaphias

Gardiner’s frog is one of the smallest amphibians in the world. At its maximum size of 11 millimetres, it’s barely bigger than a fingernail. It’s part of a whole family of tiny frogs called sooglossids, found in the Seychelles Islands off the east coast of Africa. All of them lack middle ears, but all of them can apparently hear their own calls.

To find out how, Boistel’s team at the University of Paris-Sud analysed the frog’s skull with a very high-resolution X-ray scanner. This showed that the inner ear is completely surrounded by a capsule of bone, which might help to conduct incoming sound. But when they ran simulations of sound waves travelling through the frog’s skull, they found that these were still severely weakened by the time they reached the inner ear, despite the adjacent bone.

The simulations also ruled out another possible idea—that earless frogs might use their lungs to carry vibrations into their inner ears. That might be true for some species, but Gardiner’s frog has small lungs that don’t make good contact with its sides. They’d be terrible sound transmitters.

Gardiner's frog, viewed through X-ray holotomography. Credit: Renaud Boistel
Gardiner’s frog, viewed through X-ray holotomography. Credit: Renaud Boistel

But the team’s simulations also revealed something odd—a burst of pressure within the frog’s mouth. When the team added the animal’s mouth to their simulations, they found that it resonates at a frequency of 5,738 Hertz. Sounds of this frequency cause the mouth to reverberate strongly, turning it into an amplifier.

And guess what the average frequency of the frog’s call is? It’s 5,710 Hertz—roughly an F note, four octaves above middle C.

Gardiner’s frog seems to have a mouth that’s perfectly adapted for amplifying the calls of other Gardiner’s frogs, compensating for the lack of a middle ear. And it probably helps that the tissues between the mouth and inner ear are unusually thin.

This might explain why, in Boistel’s playback experiments, Gardiner’s frog reacts to the calls of its own kind, but not those of other frogs. Maybe its own calls are the only things it can hear.

“The idea is fascinating,” says Albert Feng from the University of Illinois. He proposed a similar idea back in 2011, to explain how another tiny frog, the Kihansi spray toad, could hear. However, Feng says the evidence that Boistel has provided is still tenuous and inconclusive, and he thinks they need to test their idea through experiments. For example, they might keep the frog’s mouth open, or briefly fill it with moistened cotton balls to see if they can still hear.

Reference: Boistel, Aubina, Cloeten, Peyrind, Scotti, Herzog, Gerlach, Pollet & Aubry. 2013. How minute sooglossid frogs hear without a middle ear. PNAS http://dx.doi.org/10.1073/pnas.1302218110

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Honeybees can move each other with electric fields

A honeybee returns to its hive after a productive visit to a nearby field of flowers, rich in pollen and nectar. It starts to dance. By waggling its body and strutting in a figure-of-eight, it conveys the duration and direction of the food source to its hive-mates. It was Karl von Frisch, an Austrian scientist, who first deciphered the waggle dance back in 1923. Now, 90 years after his pioneering work, we’re still learning amazing things about the messages that are exchanged within the hive.

When bees fly through the air outside the hive, they collide with charged particles, from dust to small molecules. These impacts tear electrons away from their cuticle—their outer shell—and the bee ends up with a positive charge. When they return to the hive and walk or dance about, they give off electric fields. And Uwe Greggers from the Free University of Berlin has shown that they can detect these fields with the tips of their antennae. Despite our long history with the honeybee, there could still be a secret world of electric communication within the hive that we know nothing about.

We’ve known that insect cuticle builds up electric charge since 1929, almost as long as we’ve known about the waggle dance code. “Many colleagues thought that the bees have a charge but it doesn’t matter. It’s too small,” says Greggers. But when he actually took measurements of living bees, he found that they can produce voltages of up to 450 volts! The insects’ waxy cuticles are responsible—they’re so electrically resistant that a substantial charge can build up and stay there.

Since the 1960s, scientists have speculated that these charges could be useful during pollination. Flowers, after all, tend to have a negative charge on clear days. When bees approach, pollen can actually fly through the air to their bodies. And just last month, Daniel Robert from the University of Bristol showed that bumblebees can detect the electric fields of flowers, and use them to tell the difference between recently visited blooms and fresh ones.

But what about social communication? Can the bees themselves detect each other’s electric fields? Can they extract useful information from them?

To find out, Greggers created Pavlov’s bees. He exposed them to artificial electric fields that mimic those found in the hive, before giving them a rewarding sip of nectar. Soon, he found that the field alone was enough to make them extend their tongues in anticipation of a tasty treat, just like Pavlov’s dogs salivating at the sound of a bell.

Greggers found that the bees detect these fields with their flagella—the very tips of their antennae. Picture a bee, dancing away in a tightly packed hive with many neighbours in close proximity. As it waggles, it also vibrates its wings. As the dancer’s positively-charged wing get closer to a neighbour’s positively-charged antenna, it produces a force that physically repels the antenna. As the dancer’s wing swings back to its original position, the neighbour’s antenna bounces back too. With their electric fields, the bees can move each other’s body parts without ever making contact. (Sure, the beating wing also pushes air past a neighbour’s antenna, but Greggers found that the force produced by the incoming electric field is ten times stronger.)

The bee detects these forces with small touch-sensitive fibres in the joints of their antennae, which send electrical signals towards the insect’s brain. If Greggers immobilised the joints by covering the antennal joints with wax, the bees couldn’t learn to associate electric fields with nectar rewards.

These signals from the fibres are intercepted and processed by a structure called Johnston’s organ within the antennae. By recording the activity of neurons in this organ, Greggers showed that it does indeed fire when an electrically charged object—like a Styrofoam ball—is brought close to the flagellum.

“This is a remarkable discovery,” says Robert. “After all these years of studies on bees, one comes to realise yet another secret aspect to their language. The exact function of such electric sense is not entirely clear but the evidence is strong that electric communication can take place between bees in the hive.

Indeed, now that Greggers has shown that honeybees can detect each others’ electric fields, the big question is: Do they? Is their electric sense an actual part of their everyday lives? To find out, Greggers now wants to study the electric fields of waggle-dancing bees. If he can interfere with the audience’s ability to detect those fields, will that disrupt their ability to interpret the dance?

PS: When I wrote about Roberts’s discovery about bees sensing the electric fields of flowers, the most common comment was something like: “Aren’t our own man-made electromagnetic fields screwing the bees over? The short answer is: No. The fields produced by our technology are actually much lower in energy than those produced by the bees themselves. “They should be naturally protected,” says Greggers. “Unless a bee-keeper puts their hive directly under a high-voltage electric wire outside, the effects should be limited.”

Reference: Greggers, Koch, Schmidt, Durr, Floriou-Servou, Piepenbrock, Gopfert & Menzel. 2013. Reception and learning of electric fields in bees. Proc Roy Soc B http://dx.doi.org/10.1098/rspb.2013.0528

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Bees Can Sense the Electric Fields of Flowers

A bumblebee visits a flower, drawn in by the bright colours, the patterns on the petals, and the aromatic promise of sweet nectar. But there’s more to pollination than sight and smell. There is also electricity in the air.

Dominic Clarke and Heather Whitney from the University of Bristol have shown that bumblebees can sense the electric field that surrounds a flower. They can even learn to distinguish between fields produced by different floral shapes, or use them to work out whether a flower has been recently visited by other bees. Flowers aren’t just visual spectacles and smelly beacons. They’re also electric billboards.

“This is a big finding,” says Daniel Robert, who led the study. “Nobody had postulated the idea that bees could be sensitive to the electric field of a flower.”

Scientists have, however, known about the electric side of pollination since the 1960s, although it is rarely discussed. As bees fly through the air, they bump into charged particles from dust to small molecules. The friction of these microscopic collisions strips electrons from the bee’s surface, and they typically end up with a positive charge.

Flowers, on the other hand, tend to have a negative charge, at least on clear days. The flowers themselves are electrically earthed, but the air around them carries a voltage of around 100 volts for every metre above the ground. The positive charge that accumulates around the flower induces a negative charge in its petals.

When the positively charged bee arrives at the negatively charged flower, sparks don’t fly but pollen does. “We found some videos showing that pollen literally jumps from the flower to the bee, as the bee approaches… even before it has landed,” says Robert. The bee may fly over to the flower but at close quarters, the flower also flies over to the bee.

This is old news. As far back as the 1970s, botanists suggested that electric forces enhance the attraction between pollen and pollinators. Some even showed that if you sprinkle pollen over an immobilised bee, some of the falling grains will veer off course and stick to the insect.

But Robert is no botanist. He’s a sensory biologist. He studies how animals perceive the world around them. When he came across the electric world of bees and flowers, the first question that sprang to mind was: “Does the bee know anything about this process?” Amazingly, no one had asked the question, much less answered it. “We read all of the papers,” says Robert. “We even had one translated from Russian, but no one had made that intellectual leap.”

To answer the question, Robert teamed up with Clarke (a physicist) and Whitney (a botanist), and created e-flowers—artificial purple-topped blooms with designer electric fields. When bumblebees could choose between charged flowers that carried a sugary liquid, or charge-less flowers that yielded a bitter one, they soon learned to visit the charged ones with 81 percent accuracy. If none of the flowers were charged, the bees lost the ability to pinpoint the sugary rewards.

But the bees can do more than just tell if an electric field is there or not. They can also discriminate between fields of different shapes, which in turn depend on the shape of a flower’s petals and how easily they conduct electricity. Clarke and Whitney visualised these patterns by spraying flowers with positively charged and brightly coloured particles. You can see the results below. Each flower has been sprayed on its right half, and the rectangular boxes show the colours of the particles.

 

Coloured particles reveal the electric fields of flowers. From Clarke et al, 2013
Coloured particles reveal the electric fields of flowers. From Clarke et al, 2013

The bees can sense these patterns. They can learn to tell the difference between an e-flower with an evenly spread voltage and one with a field like a bullseye with 70 percent accuracy.

Bees can also use this electric information to bolster what their other senses are telling them. The team trained bees to discriminate between two e-flowers that came in very slightly different shades of green. They managed it, but it took them 35 visits to reach an accuracy of 80 percent. If the team added differing electric fields to the flowers, the bees hit the same benchmark within just 24 visits.

How does the bee actually register electric fields? No one knows, but Robert suspects that the fields produce small forces that move some of the bee’s body parts, perhaps the hairs on its body. In the same way that a rubbed balloon makes you hair stand on end, perhaps a charged flower provides a bee with detectable tugs and shoves.

The bees, in turn, change the charge of whatever flower they land upon. Robert’s team showed that the electrical potential in the stem of a petunia goes up by around 25 millivolts when a bee lands upon it. This change starts just before the bee lands, which shows that it’s nothing to do with the insect physically disturbing the flower. And it lasts for just under two minutes, which is longer than the bee typically spends on its visit.

This changing field can tell a bee whether a flower has been recently visited, and might be short of nectar. It’s like a sign that says “Closed for business. Be right back.” It’s also a much more dynamic signal than more familiar ones like colour, patterns or smells. All of these are fairly static. Flowers can change them, but it takes minutes or hours to do so. Electric fields, however, change instantaneously whenever a bees lands. They not only provide useful information, but they do it immediately.

Robert thinks that these signals could either be honest or dishonest, depending on the flower. Those that carpet a field and require multiple visits from pollinators will evolve to be truthful, because they cannot afford to deceive their pollinators.  Bees are good learners and if they repeatedly visit an empty flower, they will quickly avoid an entire patch. Worse still, they’ll communicate with their hive-mates, and the entire colony will seek fresh pastures. “If the flower can signal that it is momentarily empty, then the bee will benefit and the flower will communicate honestly its mitigated attraction,” says Robert.

But some flowers, like tulips or poppies, only need one or two visits to pollinate themselves.  “These could afford to lie,” says Robert. He expects that they will do everything possible to keep their electric charge constant, even if a bee lands upon them. They should always have their signs flipped to “Open”. Robert’s students will be testing this idea in the summer.

Many animals can sense electric fields, including sharks and rays, electric fish, at least one species of dolphin, and the platypus. But this is the first time that anyone has discovered this sense in an insect. And in the humble bumblebee, no less! Bees and flowers have been studied intensely for decades, maybe centuries, and it turns out that they’ve been exchanging secret messages all this time.

Now, Robert’s team is going to take their experiments from the lab into the field, to see just how electrically sensitive wild bees can be, and how their senses change according to the weather. “We are probably only seeing the tip of the electrical iceberg here,” he says.

Reference: Clarke, Whitney, Sutton & Robert. Detection and Learning of Floral Electric Fields by Bumblebees. Science http:/dx.doi.org/10.1126/science.1230883

Thanks to Liz Neeley for a chat about dishonest signalling, which inspired part of this piece.

More on electric senses:

More on bees and pollination from National Geographic:

 

Stereo Mole Noses

Never underestimate a mole.

It’s easy to have low expectations for these creatures. My own experience with moles is limited to the sight of their carcasses at my doorstep, laid there by our triumphant and generous cat. Stretched out on the cold bluestone, they look like little more than eyeless pouches of fur.

Ken Catania of Vanderbilt University has gone a long way to redeeming the mole. In the 1990s, he did some of the first studies of star-nosed moles, a species with 22 oddly finger-shaped tentacles flaring from its nostrils. He discovered that those tentacles are an exquisitely sensitive touch organ with 25,000 sense receptors. It uses this bizarre star to rapidly scan its tunnels for food, sweeping back and forth a dozen times a second. It takes a fifth of a second from encountering a piece of food for the star-nosed mole to eat it, making it the fastest eater on record in the animal kingdom. (Here’s a story I wrote about Catania in the New York Times, plus a wonderful illustration of its fast-acting anatomy.) Catania’s research landed the star-nosed mole in Guiness Book of World Records.

Recently, Catania thought it would be interesting to compare an awesomely sensitive creature like the star-nosed mole with a pathetically equipped relative. He chose the Eastern mole, the common species that I so often find dead on my doorstep.

Scalopus aquaticus seems, on paper, like a supremely mediocre mole. It has no star on the end of its nose. Other mole species that lack a star still have lots of touch sensors on their faces. But these sensors are delicate bits of tissue, and Eastern moles, adapted to life in drier, harder ground, have lost them. They are blind, and their ears are only sensitive to low-frequency sound.

So Catania started observing eastern moles search for food. Instead of stumbling around, they turned out to be, in their own way, just as impressive as their star-nosed relatives. Despite being starless and blind, they consistently headed straight for the food.

Catania decided to study the moles formally, by building a special box. One half of the box was a holding chamber, in which he could put a mole. It was divided from the other side by a wall with a closed doorway in the center. On the other side of the box, Catania drilled 15 pits, arranged in a semi-circle at equal distances from the door. Into one of those pits Catania would drop a chunk of earthworm, and then he would opened the door. The mole would squirm through and explore the new part of the box. Every time, the mole headed straight for the hidden food.

The only way that Catania could imagine the mole could manage this was by smell. But the mole’s sense of smell would have to do more than just tell it that there was a worm somewhere in the box. It would have to direct the mole to the precise spot where the worm had been placed.

How animals smell their way to food is still fairly mysterious. One method that’s been well supported by experiments is to play the hot-cold game with your nose. If you get closer to food, its smell will get stronger. If you move away, it gets weaker.

Another possibility is that the moles can smell in stereo. They can compare signals from their two nostrils to judge how far to the left or right a smell is. We use stereo for our hearing, using the differences between what our left and right ears detect to pinpoint the source of a sound. Perhaps moles can do the same with their noses.

Other scientists had found some suggestive evidence that rats could smell in stereo, but Catania was not entirely convinced. After all, ears are separated on either side of the head, but nostrils are right next to each other. How they could get a different signal across such a small distance was hard to fathom.

So Catania did a series of experiments. He used an air pressure sensor to record when the moles took a sniff. As you can see from this video (sniffs marked by white spots), sniffing was a vital element of their search.

Catania then manipulate the noses of the moles in various ways to see if he could alter their performance. In one experiment, he plugged up one nostril. Now, instead of finding their food with 100% accuracy, the moles consistently failed. And they failed in a consistent way. If their left nostril was blocked, they veered off to the right. And if their right nostril was blocked, they veered to the left.

This reliable error suggested that they did, indeed, rely on both nostrils, each providing information about the smells on each side. Catania then ran another experiment in which he inserted tubes into the mole noses. The air flowing into each nostril crossed over to the other one, where it was detected by the nerve endings there.

Now the moles got hopelessly lost. Instead of simply getting biased information that steered them off course in a consistent way, the moles were overwhelmed by confusion.

Catania concludes that moles probably use both stereo and hot-cold strategies to find food. From a distance, hot-cold works well. Closer up, where smells can get much stronger over even a short distance, the moles switch to stereo.

It will be interesting to see if other animals show such clear evidence of smelling in stereo too. Catania has some evidence that star-nosed moles aren’t so good with stereo smell, which he’s now following up on. It’s possible that eastern moles took a capacity found in many mammals and evolved it into a much more powerful form to adapt to their particular kind of life in the hard ground. I’m not too eager to have pipes shoved up my nose, but I’m awfully curious to find out if we humans share the gift of the mole.

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The Real Wisdom of the Crowds

In 1907, Sir Francis Galton asked 787 villagers to guess the weight of an ox. None of them got the right answer, but when Galton averaged their guesses, he arrived at a near perfect estimate. This is a classic demonstration of the “wisdom of the crowds”, where groups of people pool their abilities to show collective intelligence. Galton’s story has been told and re-told, with endless variations on the theme. If you don’t have an ox handy, you can try it yourself with beans in a jar.

To Iain Couzin from Princeton University, these stories are a little boring. Everyone is trying to solve a problem, and they do it more accurately together than alone. Whoop-de-doo. By contrast, Couzin has found an example of a more exciting type of collective intelligence—where a group solves a problem that none of its members are even aware of. Simply by moving together, the group gains new abilities that its members lack as individuals.

Couzin–one of National Geographic’s Emerging Explorers–has spent his whole career studying animals that move in shoals, flocks and swarms. His early work involved ants and locusts but when he started his own lab at Princeton, he thought he’d upgrade to a smarter group-living species. Unfortunately, he ended up with the golden shiner—a small, bland, minnow-like fish that’s dumb beyond the telling of it.

Consider this: shiners have a natural preference for darkness. Plop a shoal of them into a pool of water, and they’ll head for the shadiest bits. This is something that animals do all the time: They track gradients in their environment. A migrating robin might follow the Earth’s magnetic field, a moth might follow the scent of a flower, or an ant might track the pheromones laid by its nest-mates. But single shiners are laughably bad at this.

Andrew Berdahl and Colin Torney from Couzin’s team discovered their ineptitude by projecting shifting patterns of light over a shallow pool and adding the shiners in increasing numbers. Overhead cameras tracked their movements, and the team calculated how good they were at chasing the shadows.

The solo fish did so badly that they were almost swimming randomly. Only larger shoals were good at avoiding the shifting light. Even then, Berdahl and Torney found that the shiners’ movements were far more influenced by what their neighbours were doing, than by how bright the environment was.

That’s the key. The individual fish aren’t tracking anything. That would involve realising, for example, that it’s getting darker over there compared to over here, and swimming over there. Instead, they obey one very simple rule—swim slower when it’s dark. Each fish just reacts to how bright it is in its current position. How bright or dark is it right here? That’s a scalar measurement. It’s the shoal that converts these local readings into a vector.

To understand how this works, imagine that a shoal of swimming shiners grazes a patch of shadow. The fish that first enter the shade slow down. But the rest of the shoal doesn’t shoot off into the distance. Shiners have a strong instinct to stick within a certain distance of their neighbours. They almost behave like a rigid block, so if one end slows down, the rest of them swivel… right into the shade.

Once inside, they all slow down. They start bunching up together like cars in a traffic jam.  And if the shadows move, so they find themselves in light, they start swimming faster again and leave.

Berdahl and Torney’s discovery flies against the “many wrongs” principle, which biologists have invoked to explain the migrations of natural groups since 1964. The idea is that groups can track gradients in their environment because each individual makes an imperfect decision about where to go. When the crowd pools their estimates, they cancel out each other’s errors, and mutually arrive at the best possible vector. It’s just Galton’s ox again, but applied to migrations.

But the shiners are patently not pooling estimates—the individuals are so bad at tracking gradients of light that it’s hard to believe that they’re making estimates at all. But by adhering to the simple instinct that keep them together as a shoal, the shiners can transform acts of individual detection into an act of group navigation.

That’s collective intelligence! The shiners’ ability to stay in shade emerges from neighbourly interactions of dumb units. The fish aren’t pooling decisions that each individual makes on its own—they’re collectively processing information. By moving as one, they can compute as one.

Couzin suspects that this phenomenon is goes well beyond shiners, and might apply across a variety of migrating animals. After all, the rules that shiners obey are so simple that they should be a doddle for natural selection to produce. You don’t even need a brain to pull off the same trick—just the ability to respond to the environment, and to stay as a group. Cells can do that. All sorts of animals can do that.

This may be important for conservation. Couzin’s team showed that the shiners’ ability to follow the light suddenly collapsed when they shoals fell below a certain size. And we have repeatedly slashed the group sizes of many animals by hunting them or destroying their habitats. If those groups become sufficiently fractured, and their numbers fall below a certain threshold, they may lose abilities that they only have en masse.

Reference: Berdahl, Torney, Ioannou, Faria & Couzin. 2013. Emergent Sensing of Complex Environments by Mobile Animal Groups. Science http://dx.doi.org/10.1126/science.1225883

More on Iain Couzin’s work: