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.
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.
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.
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 muchworse 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.
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, itdid it twice.
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.
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.
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.”
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
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.
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.”
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.
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.
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.
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.
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.
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