A Blog by Ed Yong

Weird Worms Swim in Huge Green Circles

FLPA, Alamy
FLPA, Alamy

If you find yourself walking along the beaches of the English Channel, you might come across a mat of green goo, as if someone had tipped a jar of mint sauce onto the beach. But if you get down on your hands and knees, and stare at the goo with a magnifying glass, you’ll see its true nature.

Worms.

Little green worms, each just a few millimetres long, writhing together in their millions.

Their formal name is Symsagittifera roscoffensis, but Channel Islanders call them mint sauce worms for obvious reasons. Their green colour comes from the algae in their bodies, which provide them with nutrients by harnessing the sun’s energy. The algae also gave the creatures their other name, favoured by early 20th century biologists: “plant-animals.”

One of those biologists, Frederick Keeble, wrote a whole book about these creatures in 1901. Eight decades later, Nigel Franks from the University of Bristol picked up a copy at a second-hand bookstore for the princely sum of 50 pence. Intrigued, he set out to find them, and it took him several trips to the island of Guernsey to do so. “It’s hard to find a patch of them but once you find them, they’re there in huge numbers,” he says. “They’re hugely impressive. When you see them, you’ll think they’re algae.”

Franks scooped up a group of them and started studying their behaviour. He quickly realised that if he added enough of them to the same pool of shallow water, they’d start swimming in mesmerising circular mills, with hundreds of individuals in rotating green rings. “They did them at the drop of a hat,” says Franks. “It was such a telltale symptom of really strong social interactions.”

Having spent most of his career studying the collective behaviour of ants, Franks was the perfect audience for the worms’ display. He knew that many other social animals will produce circular mills, for varying reasons. Army ants do it if you isolate a group of them, slavishly following each other’s chemical trails until they die from exhaustion. Fish do it when confronted by predators. Even virtual animals will form mills if you program them with simple rules. So what about the worms?

By studying videos of the animals, Franks and his colleagues showed that they interact strongly with one another, often swimming in parallel with just a millimetre between them. As their densities increase, they grew disproportionately closer. The mills, it seems, arise from these close-quarter interactions, and from the worms’ tendency to curve in a particular direction. (It’s notable that almost all the mills spin clockwise.)

Using this information, Franks’ colleague Alan Worley built a computer simulation in which virtual worms behaved according to simple rules, and yet spontaneously produced circular mills just like their real counterparts.

Green mint sauce worms.
Green mint sauce worms.
Photograph by Stevie Smith

“But many different models of individual interactions can reproduce the same kind of collective patterns,” says Guy Therauluz, another collective motion researcher at Paul Sabatier University. “Deciphering the real social interactions at work between worms is a task that remains to be done.”

Franks plans to do that. It’s possible, he says, that the worms are dribbling some kind of chemical behind themselves, which the others follow. Or perhaps they are reacting to turbulence in the water. “The rules have yet to be worked out,” he says.

He also wants to know why the worms behave in this way and he has a fascinating suggestion. Perhaps the worms are social sunbathers. By gathering in large mats of biofilms, bound together by mucus that they themselves secrete, they can stabilise their position on sandy beaches or tidepools. In Franks’ words, they “behave collectively as a social seaweed”.

Individual worms are also known to head towards light sources that are almost too bright for them, and would max out the abilities of their algal partners. They could deal with that problem in a mat by ducking down into the darker centre once they’ve had their fill of light. Franks compares them to emperor penguins huddling against bitter Antarctic winds: these flocks continuously rotate as individuals at the edge wheedle their way into the centre.

Dora Biro from the University of Oxford praises Franks’ attempt to explain not just the how of the collective motion, but also the why—something that has been overlooked by scientists in this field.  “The hypothesis is very interesting,” she says. “It would be great to find support for it through future work, including observations in the wild on the formation of the biofilm, and the role of milling in the process.”

Franks is just getting started with the mint sauce worms, but he sees them as great subjects for understanding collective behaviour in animals. Other scientists have analysed their bodies, the way they grow, and their powers of regeneration—but only ever one at a time. “I suspect that if people looked at populations more, as we have been fortunate enough to do with these things, they’d see more and more examples of strange microscopic organisms showing social behaviour like this,” Franks says.

A Blog by Robert Krulwich

You’ll Find the Biggest Male Appendage in the World—at the Beach

So tell me: Of all the males on our planet—and I’m talking all, scale be damned, from the littlest insects to the biggest of whales—who’s got the most impressive appendage? Who (you should pardon the expression) is our Biggest Daddy?

And I don’t mean just sex organs, impressive as they sometimes are. I’m talking about any outstanding male appendage—whatever guys have that thrills the ladies, the obvious non-penile example being the peacock tail, which as we all know when fully displayed makes peahens dream of George Clooney.

Picture of a peacock with its feathers fanned out
Photograph by Richard I’Anson, Getty
Indian Peafowl, or Peacock, displaying tail feathers.. Photograph by Richard I'Anson

Impressive? Yes. The problem being that between trysts, a superheavy tail must be a drag to lug around. It costs energy to maintain and more energy to get up and unfurled. But the drive to reproduce is a powerful thing, and sexual selection, as Darwin taught us, just keeps pushing the limits of bigness.

Obviously, there is such a thing as too big. I imagine it gets awkward to be a walrus with tusks curling dangerously close to your chest.

Picture of a pacitic walrus with very long tusks lying on rocks
Photograph by Yva Momatiuk & John Eastcott, Minden Pictures / National Geographic
Pacific Walrus (Odobenus rosmarus) bull portrait on coastal rocks in haul-out cove, summer, Round Island, Bering Sea, Bristol Bay, Alaska. Photograph by Yva Momatiuk & John Eastcott / Minden Pictures / National Geographic

And the weight of these things? Not the absolute weight, but the proportional weight—that’s another limitation. How much can a guy carry? According to Douglas Emlen in his wonderful book Animal Weapons: The Evolution of Battle, while the rack of bone that sits atop a male caribou is hugely impressive (those antlers can weigh 20 pounds and stretch five feet across) …

Picture of a caribou with large antlers amid a lush green landscape on a misty day next to an equal sign that says ''8%''
Photograph by Bob Smith, National Geographic Creative
Close up portrait of a male caribou, Rangifer tarandus. Photograph by Bob Smith, National Geographic Creative

… as big as they are, they account for only 8 percent of the male’s total body weight. Moose and elk have even larger antlers, but even the biggest elk antlers equal only 12 percent of its body weight. So that’s doable. Once upon a time, 11,000 years ago, there was a deer (called Megaloceros giganteus, or the Irish elk) that wandered Europe and Asia, and those guys had boney tops so insanely branched, so crazily big, that our prehistoric humans painted them worshipfully onto the cave walls at Lascaux.

Picture of an Irish elk painted onto the wall at Lascaux cave next to a ''less than'' sign that says 20% next to it
Photograph by Sisse Brimberg, National Geographic Creative
Prehistoric artists painted a red deer on a cave wall. Photograph by Sisse Brimberg, National Geographic Creative

But even these antlers, 12 feet across and wildly branched, weighed less than 20 percent of the total animal.

Go Small to Get Big

You have to drop down to the insect family, to a group of horned beetles, to find a big appendage that approaches a third of the animal’s body weight. There are several beetles that have fighting, clamping horns almost the size of their bodies, and a thing like that growing out of your skull, writes Emlen, “is a little like having your leg sticking up out of your forehead.” You feel it.

Picture of a rhinocerous beetle on wood
Photograph by altrendo nature, Getty
Rhinoceros Beetle, male, Columbia, South America, Photograph by altrendo nature

But if you’re looking for the male who wears the crown, whose appendage is so big, so startling, so colorful, so attractive, so monstrous, and therefore unequaled in the animal kingdom—if you’re looking for the champ? Well …

He’s not in the African savannah. He doesn’t have a tusk. He’s not especially large. You have to look down to see him, down near your feet when you’re at the beach. This is him:

Picture of a fiddler-type crab standing on sand and waving a claw in the air
Photograph by Michael Nichols, National Geographic Creative
Loango National Park, Gabon. A fiddler-type crab with claw raised standing outside its burrow, Photograph by Michael Nichols, Getty

He’s a fiddler crab. And that appendage is his claw. And while sizes vary from crab to crab, the biggest fiddler crab claws weigh roughly half the body weight of the animal. Half! That’s nature’s biggest appendage, says Emlen. And what is it for? Not for feeding. The claw is useless at mealtime. Males eat with their other, smaller claw only. But, says Cornell biologist John Christy, the claw’s bright colors definitely attract female attention. It can also snap down and inflict real harm, so they’re potential weapons. But mostly, he discovered, males use them—I kid you not—to wave.

“Up and down, up and down, again and again,” writes Emlen, “they raise their claws high and drop them. Dozens of times each minute, thousands of times per hour, hour after hour … ” They look a little silly doing this, like a lonely fan trying to start a stadium wave. Check out this fellow:

Why are they waving? It’s a warning. “Look what I’ve got!” the male is saying to any male who would trespass into his burrow. “This thing is going to pound you if you come near, so stay away!” In effect, Emlen writes, “fiddlers are employing their claws as warnings rather than instruments of battle.” And it works. “An overwhelming majority of contests end before they ever begin, without anything even resembling a fight. A mere glance at a big claw is sufficient to deter smaller males.”

The male has built a tunnel, which leads to a nesting burrow. His claw has attracted a lady, and she’s down below raising his family. His job is to stay on top, waving till she’s done or he drops. It’s a tough life, lifting that gigantic appendage over and over, using up energy, constantly getting bothered by would-be challengers. The male can’t eat. Not while he’s guarding. His food is at the water’s edge, which is down lower on the beach. So he stands there, day after day, getting hungrier, until eventually, Emlen says, “Even the best males run out of steam and are forced to abandon their burrows to go feed and refuel. The instant they leave, others will claim their burrows.” And then they become challengers and have to start all over again.

So while it may be glamorous to top the list of Biggest Appendage Ever, what with the lifting, the waving, the straining, the not eating, the worrying about how long you’ll last, it might be better to have a medium-size claw and not have to be always worrying about the biggest bullies at the beach. Yes, the big claw does dramatically increase your chances of producing babies, which, as Darwin will tell you, is the whole point. But if I were a fiddler crab lucky enough to have the biggest appendage in the world, I think I’d get myself a nail file (claw file?), erase my genetic advantage, and spend lazy afternoons sipping pond scum by the ocean’s edge. I like a gentler life.


Douglas J. Emlen’s book, Animal Weapons: The Evolution of Battle, is a fascinating account of how animal weaponry, both offensive (claws, horns, teeth) and defensive (armor, shelter, thorns, claws again) parallel human weaponry, both offensive (arrows, lances, swords, missiles, A-bombs) and defensive (armor, castles, spying). It’s a compelling, fun, often scary analysis. And David Tuss’ drawings, especially his animals, made me jealous.

A Blog by Ed Yong

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

A Blog by Robert Krulwich

What Do Snails Think About When Having Sex?

It starts with a light, soft touch, one tentacle gently reaching out, hesitant, hopeful, hanging lightly in the air. There’s a pause. Skin touches skin. One softly strokes the other and slides closer, and then, carefully, they wrap themselves together, stroking, probing, entwining. They glisten as they move, and because they are snails, everything happens very slowly. The rubbing, the rapture, the intensity of it all—snail sex is extraordinarily lovely to look at. (If you aren’t at your office desk or on a train where people can see your screen, I’ve got one about a garden snail named Chip who’s trying to lose his virginity, or take a quick peek—30 seconds will do—of this coupling in a garden.)

Lovely but So Dangerous

Garden snails make love in the open—on garden patios, in clearings on the forest floor—and they do it luxuriantly for one, two, three hours at a time, under the sky, where they can be seen by jays, orioles, frogs, snakes, shrews, mice, beetles, and other animals that might want to eat them. Snails can’t make quick getaways, so exposing themselves like this is dangerous, crazily dangerous. What’s going on? What’s making them so impervious, so deeply preoccupied with each other? Here’s one answer: Snail sex is very complicated. Snails have a lot to think about when they make love—because they’re hermaphrodites.

Unlike you, garden snails can produce sperm like males and carry eggs like females at the same time.

Drawing of a proud snail, with its hands on its shell hips
Drawing by Robert Krulwich
Drawing by Robert Krulwich

Which is both an advantage and a problem. Professor David George Haskell, a Tennessee biologist, once squatted down on a patch of forest floor and watched what you just saw in that video—a snail couple going at it—except with a magnifying glass and only a few feet from the action. What he noticed was their mood. Hot as it was, he writes in his book The Forest Unseen, “Their extended courtship and copulation is choreographed like cautious diplomacy.” Snails don’t pounce, they circle. They “slowly edge into position, always ready to pull back or realign.” Their sex is tense, charged, on, off, then on again, “a prenuptial conference over the terms of the union.” What are they negotiating about?

In most animals, snails included, sperm is plentiful, cheap to produce, and fun to unload. So one presumes that both copulating snails are eager to get that part done.

A drawing of two snails, both looking at each other with thought bubble exclamation points above their heads
Drawing by Robert Krulwich
Drawing by Robert Krulwich

Eggs, on the other hand, are limited and hard to produce—and therefore precious. You don’t let just anybody fertilize your egg sack. So, in Haskell’s imagination, if one of these snails picks up “a whiff of disease” on the other, it may be happy to poke but is not at all interested in being poked. No one wants its precious eggs fertilized by a sick dad, so the receiving snail might lock its partner out of its opening while also trying to penetrate it. This could produce feelings of frustration, confusion, and even unfairness in the other.

A drawing of two snails looking at each other, one with an exclamation mark thought bubble and one with an X through an exclamation mark thought bubble
Drawing by Robert Krulwich
Drawing by Robert Krulwich

“In hermaphrodites,” writes Haskell, “mating becomes fraught, with each individual being cautious about receiving sperm while simultaneously trying to inseminate its partner.” Sexually speaking, two snails with four minds—a foursome in a twosome—makes for complex fornication. That’s why snails are always on tiptoe, Haskell thought as he watched them on the forest floor: They have so much to figure out.

Picture of a brown snail peering its head around to the side
Photograph by © Tetra Images / Alamy
Photograph by © Tetra Images / Alamy

Hermaphrodite Abundance

So why be a hermaphrodite? Are there a lot of them? Well, here’s a surprise: They’re everywhere.

Eighty percent of the plant kingdom produces both seeds (pollen) and eggs (ovules) and can give or receive, making them hermaphroditic. They’ve learned that when the weather gets wet or cold, bees can’t be depended upon to buzz by and pollinate, so they have a we-can-do-this-ourselves backup plan.

Animals, generally speaking, are sexual, divided into male and female. But, writes Stanford biology professor Joan Roughgarden in her book The Genial Gene, if you subtract insects, which make up more than 75 percent of the animal kingdom and are not hermaphrodites, we are left, she calculates, “ … with a figure of 1/3 hermaphrodite species among all animal species.” That’s a hunk of hermaphrodites.

So Who’s a Hermaphrodite?

They’re not animals we pay much attention to (flukes, flatworms, killifish, parrot fish, moray eels, barnacles, slugs, earthworms, and tapeworms, among many others), but they are switch-hitters: They can either give or receive or switch sides during their lifetime. “All in all,” writes Roughgarden, “across all the plants and animals combined, the number of species that are hermaphroditic is more-or-less tied with the number who has separate males and females, and neither arrangement of sexual packaging can be viewed as the ‘norm.’”

Anyone who thinks that male/female is nature’s preference isn’t looking at nature, says Roughgarden. And she goes further.

Adam and Eve or AdamEve?

She wonders, Which came first, the hermaphrodite or the male/female? We have lived so long with the Adam and Eve story—Adam first, Adam alone, Adam seeking a mate, God providing Eve—that the question seems almost silly: Of course complex animals started with males and females.

Painting of Adam and Eve in the Garden of Eden, Eve is offering Adam an apple
Adam and Eve, 1537 (panel), Cranach, Lucas, the Elder (1472-1553) / Kunsthistorisches Museum, Vienna, Austria / Bridgeman Images
Adam and Eve, 1537 (panel), Cranach, Lucas, the Elder (1472-1553) / Kunsthistorisches Museum, Vienna, Austria / Bridgeman Images

But Roughgarden wonders if animals started as hermaphrodites …

Composite of Adam and Eve painting, creating one person
Composite image of Adam and Eve created by Becky Harlan from original paintings by Lucas Cranach © [Royal Museums of Fine Arts of Belgium, Brussels / photo : Guy Cussac, Brussels]
Composite image of Adam and Eve created by Becky Harlan from original paintings by Lucas Cranach © [Royal Museums of Fine Arts of Belgium, Brussels / photo : Guy Cussac, Brussels]

… and then “hermaphrodite bodies disarticulate[d] into separate male and female bodies?” How would that have happened? Roughgarden cites a paper she did with her colleague Priya Iyer.

They propose that maybe the earliest animals started out as both sperm and egg carriers, and a subgroup got especially good at inserting their penises into enclosures, aiming, and directing the sperm to its target (the authors call it “home delivery”). They did this so effectively that they needed fewer and fewer eggs and essentially became sperm sharpshooters or, as we call them now, “males.”

That development gave others a chance to give up sperm altogether to concentrate on chambering their eggs in nurturing nooks, thereby becoming “females,” and so more and more animals found it advantageous to be gendered.

Ayer and Roughgarden aren’t sure this happened. They say that, on available evidence, the story can go “in either direction.”

The alternate view is almost the story you know. It’s Adam and Eve, with a twist: In the beginning, early animals were gendered—except when it was inconvenient.

If, for example, you imagine a group of, well, let’s make them snails …

Drawing of a group of snails standing in front of a volcano erupting
Drawing by Robert Krulwich
Drawing by Robert Krulwich

… and something awful happens—there’s a terrible disease, an ice age, a new ferocious predator, or maybe a volcanic eruption…..

Drawing of a snail all alone after the fallout of a volcanic eruption, standing in front of a volcano puffing smoke
Drawing by Robert Krulwich
Drawing by Robert Krulwich

… so that we’re left looking at a lone individual, all by itself, looking around for a reproductive opportunity, crawling across the landscape, hoping to bump into somebody, anybody, to reproduce with, and after a long, long, anxious period, it finally sees what it’s been looking for. It crawls closer, closer, the excitement building.

Drawing of a snail in a vast and sunny landscape seeing another tiny snail in the distance
Drawing by Robert Krulwich
Drawing by Robert Krulwich

But as it gets within wooing range, it suddenly sees that—oh, no—it’s the same gender!

A drawing of two snails with moustaches
Drawing by Robert Krulwich
Drawing by Robert Krulwich

No possibility of babymaking here. And this happens half of the time. (Statistically, that’s the likelihood.) Now instead of being your friend, male/femaleness is your enemy. What wouldn’t you give for a hermaphrodite, a he/she snail that could, in a pinch, be whatever sex you need it to be. With a hermaphrodite, you can (again statistically) always make a baby. What a relief. So maybe that’s what happened. Gender difference disappears when gender no longer helps produce more babies (and when you don’t have to stick around and be a parent).

Which is the true story? We don’t know. Maybe the only story is that nature is flexible. When gender is useful, you get genders. When not, you don’t. What we forget, being humans, is that there are so many ways to flirt, to combine, to make babies—and the world is full of wildly different ways to woo. Tony Hoagland knows this. He’s not a scientist but a poet who lives in New Mexico, and in his poem entitled “Romantic Moment,” he imagines a boy on a date who sits next to his girl imagining … How shall I put this? … how the Other Guys do it.
 

Romantic Moment by Tony Hoagland

After the nature documentary we walk down,
into the plaza of art galleries and high end clothing stores

where the mock orange is fragrant in the summer night
and the smooth adobe walls glow fleshlike in the dark.

It is just our second date, and we sit down on a rock,
holding hands, not looking at each other,

and if I were a bull penguin right now I would lean over
and vomit softly into the mouth of my beloved

and if I were a peacock I’d flex my gluteal muscles to
erect and spread the quills of my cinemax tail.

If she were a female walkingstick bug she might
insert her hypodermic proboscis delicately into my neck

and inject me with a rich hormonal sedative
before attaching her egg sac to my thoracic undercarriage,

and if I were a young chimpanzee I would break off a nearby tree limb
and smash all the windows in the plaza jewelry stores.

And if she was a Brazilian leopard frog she would wrap her impressive
tongue three times around my right thigh and

pummel me lightly against the surface of our pond
and I would know her feelings were sincere.

Instead we sit awhile in silence, until
she remarks that in the relative context of tortoises and iguanas,

human males seem to be actually rather expressive.
And I say that female crocodiles really don’t receive

enough credit for their gentleness.
Then she suggests that it is time for us to go

to get some ice cream cones and eat them.


Thanks to the poet Thomas Dooley for suggesting Tony Hoagland’s poem, and to Mr. Hoagland for giving us permission to print it here in full. Reading “Romantic Moment” I giggled a little to think of eating ice cream on a sugar cone as a homo sapien mating ritual—but thinking back, I think he’s onto something. The poem can be found in Tony Hoagland’s collection Hard Rain.

Acoustic Fats, Ear Trumpets, and How Whales Hear

Up until a few days ago, I had never heard a blue whale. I wasn’t even aware they made sounds that my primate ears could pick up. But, thanks to Australian Antarctic Division researchers, I was able to listen to the massive mammal for the first time:

It’s an incredibly soothing sound. Certainly moreso than Jeff Bridges and his singing bowls. But I’m probably not hearing the blue whale’s “song” as it’s meant to be heard. My ears are all wrong.

I take in sounds through my ear canal. But modern whales are weird. As their four-legged ancestors slipped into the sea and took up permanent residence there, evolution granted whales an entirely different way of hearing that relies on “acoustic fats” that help transmit sounds to a specialized “ear trumpet” on the skull.

But when did whales evolve this alternative auditory apparatus? To answer that question, National Museum of Natural History researchers Maya Yamato and Nicholas Pyenson looked to fetal whales and fossils to determine when whales started listening through acoustic funnels.

Yamato and Pyenson scrutinized 56 fetal whales collected during the heyday of 20th century commercial whaling, as well as specimens saved by the Smithsonian from bycatch and strandings. This sample encompassed ten different living whale lineages, which was critical because of differences in the way the two main groups of modern whales listen to the sea.

Toothed whales – odontocetes – have acoustic funnels that are oriented forward and connect to acoustic fat in the jaw. This is probably because a forward-facing ear is essential to accurately reading returning pings from echolocation. But some baleen whales – mysticetes – have acoustic funnels oriented more toward the side. By studying the early development of the ear trumpets in each of these lineages, Yamato and Pyenson were able to outline how this common structure diverged amongst the whales.

In both toothed and baleen whales, Yamato and Pyenson found, the acoustic funnel starts out as a forward-facing, V-shaped structure made by the malleus and goniale bones of the ear. As toothed whales grow, the acoustic funnel extends forward from the bones to the acoustic soft tissues, but, among some baleen whales, the acoustic funnel shifts to the side. Why this happened isn’t entirely clear, but it may have something to do with baleen whales communicating with low-frequency sounds over long distances and no longer needing the forward-directed hearing of their echolocating cousins.

Since the acoustic funnel starts off the same way in both toothed and baleen whales, Yamato and Pyenson hypothesize, the feature must have been present in the last common ancestor of both, around 34 million years ago. And the fossil record bears this out. Adult specimens of fossil baleen whales such as Aetiocetus and Albertocetus have forward-oriented ear funnels. This means that head-on hearing was probably the default state for both baleen and toothed whales, only later modified by humpbacks, minkes, and their relatives. Sadly for me, though, this means that even if I could learn to speak whale, I wouldn’t be able to properly understand a whale without some pretty drastic modifications to my head.

Reference:

Yamato, M., Pyenson, N. 2015. Early development and orientation of the acoustic funnel provides insight into the evolution of sound reception pathways in cetaceans. PLOS ONE. doi: 10.1371/journal.pone.0118582

Sciencespeak: Cricoarytenoideus

American alligators are chatty reptiles. They start out their lives chirping for their mother’s help as they push themselves out of their eggs, and, as they grow up, the knobbly archosaurs communicate with a suite of hisses, rumbles, and bellows.

But how do alligators make such sounds? Anatomists have known that alligators and other crocodylians vocalize through their larynx for over a century and a half, but the acoustic abilities of the reptiles have not been as extensively-studied as those of birds and mammals. A new study by Tobias Riede and colleagues is helping to remedy that, including the discovery that a hitherto-unappreciated muscle helps create the crocodylian chorus.

The alligator vocal apparatus isn’t all that different from ours. The reptiles have a larynx and multilayered membranes called vocal folds – better known as vocal chords – that alter airflow as they dilate and vibrate. But to get those parts into the right positions to make sound, alligators rely on muscles.

A muscle called the glottal adductor does some of the work. Depending on which part of the muscle contracts, either the top or the bottom of the vocal folds close. Anatomists have known about this for quite a while. But Riede and coauthors also found that alligators have another important muscle involved in the way other reptiles vocalize, but was thought to be unimportant to crocodylians.

The muscle’s name is a bit of a tongue-twister – cricoarytenoideus. It originates on the first ring of cartilage in the larynx and extends to two other cartilaginous anchors – called the basihyoid and arytenoid, respectively – and the vocal folds. What the muscle does depends on how it contracts. When the rear of the muscle contracts, the whole larynx is pulled back and the vocal folds are held tenser. When front of the muscle contracts, the vocal folds open wide.

How retracting the larynx contributes to an alligator’s vocal repetoire isn’t entirely clear yet. Studying soft tissues while in-use by a toothy owner is quite difficult. All the same, the cricoarytenoideus and other aspects of the alligator’s larynx shows that they have a great deal of vocal control that’s comparable to what’s seen in mammals and birds. And through such comparisons, biologists may be able to give paleontologists a better idea of what the vocal anatomy of long-extinct creatures was like. We may never be able to reconstruct a tyrannosaur’s roar, but, thanks to its living avian and crocodylian relatives, we may be able to narrow down the range of sounds such charismatic, prehistoric creatures were capable of creating.

Reference:

Riede, T., Li, Z., Tokuda, I., Farmer, C. 2015. Functional morphology of the Alligator mississippiensis larynx and implications for vocal production. The Journal of Experimental Biology. doi:

A Blog by Ed Yong

On the Origin of Colourful Monkey Faces

“Can you hear that?” says James Higham.

I can. It’s a loud screeching noise in the background of our phone call.

“That’s a female rhesus freaking out,” he says.

Rhesus macaques have featured heavily in lab experiments, but this particular loud female is part of a wild group, living in Puerto Rico. Higham, an anthropologist from New York University, is studying them. He is interested in their faces, which vary from a dull pink to a vivid red. Specifically, he wants to know if the females judge the males on the intensity of that colour.

“I’m stood about 5 metres away from a sub-adult male and he’s with a 3-year-old female, and they’ve been mating a lot,” he says. “There are lots of other monkeys here, and the big, blue Caribbean sea around me.” As field work goes, it’s not hard.

The same couldn’t be said for the other group of funky-faced monkeys that Higham has been studying—the guenons. These African monkeys are known for their beautiful and diverse faces. De Brazza’s monkey has a white moustache and beard, and an orange sun rising on its forehead. The crowned guenon: dark eyeshadow, a black quiff, a pair of white forehead highlights, and a luxurious golden beard. The red-eared guenon: a drunk’s pink nose, a black brow ridge, white tufts around its eyes, and—yes—red ears. Every species of guenon, and there are between 24 and 36 of them, has its own distinctive facial marks.

Why?

In the 1980, zoologist James Kingdon suggested that they recognise members of their own species by their faces. Many of these monkeys live in the same place, and some travel in large mixed groups. They live, feed, and watch out for predators together, but when it comes time to mate, their faces help them to find partners of their own kind.

The idea made sense; testing it has been difficult. For a start, guenons live in forest canopies and move quickly. It’s hard to look at their faces, let alone look at them looking at each other’s faces.

Their patterns are also complicated, so how do you objectively compare them? If two guenons have yellow sideburns and pink noses, but differently shaped brows and differently coloured eyes, are they similar? A bit different? Very different? Humans are terrible at this kind of task; we have to limit ourselves to comparing specific features, which Kingdon found frustrating.

Higham opted for a different approach. He and postdoc William Allen took hundreds of photos of 22 guenon species in various zoos and wildlife sanctuaries, and analysed them with the eigenface technique—a facial recognition programme developed in the 1980s. It can quantify how distinctive two faces are by comparing them across many features simultaneously.

The technique revealed that guenon species have more distinctive faces when they live together. This supports Kingdon’s hypothesis that the colourful facial palettes help neighbouring monkeys to recognise their own kind, despite sharing the same forests. By contrast, if the faces were adaptations to something in the monkeys’ environment—say, light levels—then species that live together should look more similar. In fact, it’s the opposite.

Next, Higham and Allen wanted to know if the monkeys could glean any more information from each other’s faces. Could guenons tell each other’s age or gender? Could they recognise individuals, as we humans can?

The duo used a computer programme to analyse 541 images from the same photo set, on the basis of either overall patterns or specific features—like the brightness, colour, shape, or size of their eyebrows and nose spots. They wanted to see if the programme could, based on these traits, classify the monkeys by species, age or gender, or recognise individuals. For example, after seeing photos of different monkeys, could the programme accurately identify one in a new photo? Likewise, after seeing photos of monkeys of both genders, could it tell if a new monkey was male or female?

The programme flunked the age and gender tests—there’s apparently nothing in a guenon’s face that reveals either characteristic. But it excelled at both species and individual recognition. The former isn’t surprising but the latter is.

As Kingdon suggested and Higham confirmed, guenons have evolved to look as different as possible when they live together. The need for differences between species ought to constrain the differences within them. “If you start looking very different from others of your species, you run the risk of being mistaken for something else,” says Higham. This kind of “stabilising selection” should lead to distinctive species but lookalike individuals—and yet that’s not what he found. One guenon can potentially tell its neighbours apart with a glance.

Of course, there’s no guarantee that what the programme is seeing is what the guenons actually see. Higham is now carrying out some experiments to see if the differences that the computer can glean are actually obvious to the monkeys themselves. He has even played around with drones to see if he can get a closer view of the guenons as they clamber through the canopy.

In the meantime, he thinks that his methods will be broadly useful to scientists who study animal signals. “There’s a lot of work on colour signals in animals and a lot of it is quite simple, like: This lizard patch varies from pale pink to bright pink,” he says. “But a lot of these signals are very complex. So, how do you measure them?” Computer learning offers an option. “That’s true whether it’s a guenon or a paper wasp or a paradise flycatcher or anything really.”

References: Allen, Stevens & Higham. 2014. Character displacement of Cercopithecini primate visual signals. Nature Communications. http://dx.doi.org/10.1038/ncomms5266

Allen & Higham. 2015. Assessing the potential information content of multicomponent visual signals: A machine learning approach. Proc Roy Soc B. http://dx.doi.org/10.1098/rspb.2014.2284

 

A Blog by Ed Yong

The Silence of the Crickets, The Silence of the Crickets

In 2003, Marlene Zuk travelled to the Hawaiian island of Kauai and heard something very strange—nothing. A disquieting quiet. An absence of chirping. A silence of the crickets.

Zuk had been studying crickets in Kauai since 1991, back when the insects were both noisy and plentiful. But every time she went back, she heard fewer and fewer of them. In 2001, she heard a single calling male. By 2003, the silence was complete.

The crickets hadn’t disappeared. Zuk would go for nighttime walks and see multitudes of the insects in the light of her headlamp. If anything, there were more of them than before. They just weren’t calling out. When she dissected them, Zuk found out why.

Male crickets call with two structures on the backs of their wings—a vein with several evenly spaced teeth (the file) and a raised ridge (the scraper). When the cricket rubs these together, the effect is like running your nail along the teeth of a comb—you get a thrrrrrrrrrrrp sound. But on all the silent Kauai crickets, the file was growing at a weird angle and had all but disappeared. Their wings were flat.

This change hobbled their courtship songs, but likely saved their lives. In the 1990s, Zuk’s team discovered that the crickets were targeted by a parasitic fly, whose larvae burrow inside them and devour them alive. The flies finds the crickets by listening out for their songs and they’re so effective that, in the early 90s, they had parasitised a third of the males. In 2002, the cricket population had fallen dramatically, and Zuk thought that they were done for.

But the silent males escaped the attention of the fly. As they bred and spread, they carried the flatwing mutation with them. By 2003, the cricket population had rebounded. And in fewer than 20 generations, they had gone from almost all-singing to almost all-silent. The crickets have become a classic textbook example of rapid evolution.

Then, a few years later, the team found that exactly the same thing had happened on the neighbouring island of Oahu! In 2005, for the first time, they found four flatwing males on the island. By 2007, half the males were flatwings.

At first, they thought that the flatwing mutation arose once on Kauai before spreading to Oahu. That made sense: with just 70 miles between the islands, it seemed possible—likely, even—that boats or strong winds carried the flatwing males across to Oahu. When they arrived, they bred with the locals, and their beneficial mutation spread.

But that’s not what happened.

In a new study, Sonia Pascoal from the University of St Andrews has found that this case of evolutionary déjà entendu is actually an example of convergence. The two populations of crickets, threatened by the same eavesdropping parasite, independently evolved similar flattened wings, at pretty much the same time, in just a handful of years.

Normal wings versus flatwings. Credit: Nathan Bailey.
Normal wings versus flatwings. Credit: Nathan Bailey.

Pascoal’s first clue was that the wings of the silent Kauai crickets look different on those of the silent Oahu ones. You can even tell the two groups apart by eye.

Genetic tests revealed even bigger differences. On both islands, the flatwings are caused by a mutation on a single gene, somewhere on the X chromosome. But both mutations arose independently!

Pascoal’s team looked for genetic markers that flank the flatwing mutation and are inherited together with it. They found more than 7,000 of these, but only 22 were common to both populations. This strongly suggests that the two flatwing mutations arose independently of one another. They seem to have arisen on different versions of the X chromosome. They may even have arisen on different genes or on different parts of the same gene.

“It was quite a surprise!” says Nathan Bailey who led the new study (which Zuk is also part of).  “There is solid evidence that evolution can act in the proverbial blink of an eye, but the bulk of this comes from laboratory studies where it is much easier to control conditions. What’s unique about these crickets is the nearly simultaneous appearance of the mutations on two islands.”

The team still have to identify the mutations (or gene) responsible for the flat wings. They also want to know why they arose and what they do. Did the two populations have different starting conditions, that influenced the mutations they eventually gained? Is there a hotspot in the cricket genome where mutations that shape the wings can easily emerge? And do the mutations lead to flat wings in the same way?

The answers will come in time. Just as Zuk’s discovery of the silent crickets gave us a great example of rapid evolution to study, this new discovery provides an excellent opportunity to look at convergent evolution in its earliest stages.

“Many studies that examine convergent evolution are faced with the difficulty that the appearance of mutations that cause similar adaptations in different populations may have occurred very long ago,” says Bailey. “That makes it difficult to tell whether traits with similar functions were derived independently, or whether they share a common ancestry.” I wrote about one such example last week: scientists only recently realised that large, flightless birds like ostriches, emus and rheas evolved their grounded, giant bodies independently of one another.

But on Kauai and Oahu, Zuk and her colleagues have found an example of convergent evolution, happening in real-time. “It’s an extraordinary opportunity,” says Bailey.

Reference: Pascoal, Cezard, Eik-Nes, Gharbi, Majewska, Payne, Ritchie, Zuk & Bailey. 2014. Rapid Convergent Evolution in Wild Crickets. Current Biology. http://dx.doi.org/10.1016/j.cub.2014.04.053

A Blog by Ed Yong

Elephants Hear Age, Gender, Ethnicity in Human Voices

To most people, elephants sound the same. Unless, you’re very experienced, it would be hard to tell the difference between two elephants based solely on their voices. They, however, have no such problems with us.

Karen McComb and Graeme Shannon from the University of Sussex have now shown that wild African elephants can tell the difference between the voices of humans from two ethnic groups, and react accordingly. They can even discriminate between the sounds of men and women, and adults and boys.

This ability matters because, to an elephant, not all humans are equal. They have no quarrel with the agriculturalist Kamba. But they often come into conflict with the cattle-herding Maasai over access to water or land, and they sometimes leave these clashes with a flank full of spears.

Back in 2009, Lucy Bates and Richard Byrne from the University of St Andrews showed that elephants at Kenya’s Amboseli National Park can distinguish between the smell of Maasai and Kamba clothes. If they sniffed eau de Maasai, they were more likely to flee into long grass. They behaved in the same way if they saw the distinctive red colour of Maasai clothes. McComb and Shannon’s study is a sequel of sorts. They showed that elephants can rely on sounds as well as smells to assess the threats they face.

The team recorded 20 Maasai and 15 Kamba saying “Look, look over there, a group of elephants is coming” in their respective languages. They then played these recordings to 48 family groups of Amboseli elephants. The herds obviously couldn’t understand the meaning of the words, but they could tell the difference between the two languages. When they heard the Massai voices, they were much more likely to bunch up into defensive clusters and sniff the air with their trunks. They knew which group was more dangerous.

They also seemed to know which people within the groups pose the greatest threat: they behaved defensively when they heard Maasai men rather than women, and adults rather than boys. “I don’t find this at all surprising, since voice pitch alone enables that distinction,” says Byrne. “But the details that differ between Maasai and Kamba languages are presumably more subtle.”

But when McComb and Shannon altered the Maasai recordings so that the male and female voices had the same pitch, the elephants could still tell them apart. They must have been picking up on some features that are subtler than mere frequency.

Still, that’s not surprising. Elephants are big-brained and extremely intelligent. They communicate with a wide range of sounds. They are long-lived, so they can build up a substantial lifetime of experience, and they live in tightly knit social groups, so youngsters can benefit from the knowledge of their elders. “The surprising thing was just how clued up they were,” says McComb. “They were really able to make these distinctions very well and they rarely got it wrong.”

They can also tailor their responses to different predators. Their main threats are humans and lions. In an earlier study, McComb and Shannon found that elephants can tell the difference between the roars of male and female lions. They react to these roars by forming defensive circles and then noisily mobbing the source of the sound. (Watch them react below.)

But when they heard the Maasai voices, they were much less aggressive. “Coming towards humans with spears would be very detrimental,” McComb deadpans. “They behaved as if they were expecting to see Maasai.” They also went into stealth mode; they only made audible noises 10 percent of the time after hearing Maasai speech, compared to 67 percent after hearing lion roars.

In a related study, Joseph Soltis, who works at Disney’s Animal Kingdom, found that elephants react differently to two distinct threats: talking humans and buzzing bees. Bees can sting elephants in vulnerable places like their eyes or inside their trunks, and elephants are so scared of this that they’ll flee if they hear buzzing.

Soltis’ team showed that Kenyan herds make distinct alarm calls when they hear either humans or bees, and they can modify the tempo and pitch of the calls to show how urgent the threats are. They also react accordingly. When the researchers played the calls back to the elephants, they found that both alarms would prompt the herds to keep watch and run away. But the bee alarm specifically makes them shake their heads, presumably to knock away any nearby stings.

These studies are testament to the keen intelligence, rich social lives, and sophisticated communications of these largest of land animals. As Ferris Jabr beautifully writes, “To look an elephant in the face is to gaze upon genius.”

But the results also speak to the sad history of conflicts between humans and elephants. These conflicts must have played out many times over for the animals to build up enough experience about which humans are the most dangerous.

“The level of spearing has gone down quite considerably in recent years,” says McComb. The Maasai are now partners in Amboseli National Park. They also get compensated if elephants accidentally kill their livestock, which stops them from spearing the animals in retaliation. Still, the sound of Maasai still sets them on edge. This suggests that once at least some members of the family have a bad run-in with humans, the others learn from her and the fear stays in the group.

Still, McComb adds that “elephants are very good at living alongside humans by avoiding dangerous situations. But when we start doing something dramatically different, like a huge increase in poaching or using automatic weapons, they can’t adapt fast enough. That’s when we need to step in and protect them.”

Fritz Vollrath from Oxford University, who was involved in the bee study, adds, “Knowing how elephants perceive their social and physical environments and how the communicate their perceptions between one another will allow us to not only better understand them but also to better protect them in the wild.”

References: McComb, Shannon, Sayialel & Moss. 2014. Elephants can determine ethnicity, gender, and age from acoustic cues in human voices. PNAS http://dx.doi.org/10.1073/pnas.1321543111

Soltis, King, Douglas-Hamilton, Vollrath & Savage. 2014. African Elephant Alarm Calls Distinguish between Threats from Humans and Bees. PLoS ONE http://dx.doi.org/10.1371/journal.pone.0089403

More on elephant behaviour:

And more from McComb:

A Blog by Ed Yong

The Secret Ingredient in Eau De Goat

Sometimes, for science, you have to make fashion accessories for animals. I’ve written about swift backpacks, cheetah collars, and beetle mittens. Now, from Ken Murata from the University of Tokyo, comes the goat cap. It’s a custom-made helmet with a few gas-absorbing balls inside. Its purpose is to collect a dose of ‘eau de goat’, so the team could identify the secret ingredients that allow male goats to turn females on.

If you have a herd of female goats or sheep, you can quickly shunt them into the fertile part of their sexual cycles by introducing a male. Something in his scent triggers hormonal changes in the females, who start to ovulate, or produce egg cells.

This “male effect” was discovered decades ago, but no one knew which molecules were responsible. They seemed to be classic examples of ‘primer pheromones’, which work by triggering long-lasting physical changes in their targets, rather than suddenly changing their behaviour.

To identify these mystery pheromones, Murata’s team analysed the odour samples collected by their gas-absorbing caps. Specifically, they were looking for chemicals that were released by normal males but not by castrated ones that don’t induce the male effect. They ended up with a long list of candidates. Now they had to test them.

They knew that the male pheromones act on a particular group of neurons in the female’s brain, which release a hormone called GnRH. This “GnRH pulse generator” works like clockwork, releasing a fresh burst of GnRH every 27 minutes or so. The size and frequency of these pulses dictates a female’s reproductive cycle. For example, she produces an especially large surge of the hormone just before her most fertile phase.

The neurons produce a volley of coordinated electrical activity whenever they released a hormone pulse, and Murata could detect these bursts by sticking electrodes in the right place. He could then waft different scents past their noses to see how the pulse generator responded.

When he held a cup full of male hair up to the female’s noses, their GnRH neurons produced a volley of activity, no matter where they were in their 27-minute cycle. A cocktail of 18 newly identified compounds from the male goats also worked. And eventually, the team found that a single chemical called 4-ethyloctanal did the trick. It seems to be the key ingredient behind the male effect.

4-ethyoctanal has a citrus tang, but it’s one easy chemical reaction away from a substance responsible for a goat’s distinctive “goaty odour”. This is the first time anyone has found the substance in a natural source, and it just so happens that it’s a primer pheromone.

Peter Brennan from the University of Bristol says the discovery is important. “There are relatively few instances in mammals where an individual compound has been positively identified as having a pheromonal effect,” he says. “There are fewer still in non-rodent species that have commercial importance.”

After more work, farmers may be able to use 4-ethyloctanal to more precisely control the reproduction of their herds. And Murata’s group have assembled an even bigger team to find a similar pheromone in an even more commercially important animal—the cow.

“I would expect that what they find in the goat will be true for other mammals and can be more easily studied in more traditional scientific models such as the mouse,” says Lisa Stowers from the Scripps Research Institute notes. But she says that “this finding is unlikely to translate to human reproduction”, since we don’t seem to have any pheromone-detecting neurons similar to the ones that Murata studied in his goats.

There are still some missing pieces to the puzzle, though. Tristram Wyatt form the University of Oxford adds that “4-ethyloctanal is likely to be one of a number of molecules working synergistically.” After all, Murata’s team showed that their 18-molecule cocktail still partly affected the females even when 4-ethyloctanal was removed.

And other stimuli could potentially block the pheromone’s effects—something we still know little about. “In more natural situations, the male effect in sheep (and likely goats) comes especially from exposure to unfamiliar males,” says Wyatt. “So, there is also memory of individual chemical profiles of previously encountered males which blocks the effect of pheromone.”

Stowers adds that the team haven’t shown how the pheromone actually affects the GnRH neurons or how a brief sniff can lead to long-lasting changes over the course of several days. Yukari Takeuchi, one of the study’s leaders, agrees. He says the acid test for their hypothesis would be to expose females to synthetic 4-ethyloctanal and to watch their reproductive behaviour change in the absence of any actual males. To do that, they need to create a device that will continually release the pheromone, and they are building one right now. Their days of goat accessories aren’t over yet.

Reference: Murata, Tamogami, Itou, Ohkubo, Wakabayashi, Watanabe, Okamura, Takeuchi & Mori. 2014. Identification of an Olfactory Signal Molecule that Activates the Central Regulator of Reproduction in Goats.

Current Biology http://dx.doi.org/10.1016/j.cub.2014.01.073

A Blog by Ed Yong

Why Jump-Yipping Prairie Dogs Are Like Yawning Humans

If you watch a group of black-tailed prairie dogs for long enough, you’ll eventually see a delightful move called the “jump-yip”. One of these little ground squirrels lifts its front half off the ground, stretches its arms out, throws its head back, and makes a “wee-oo” sound.

The behaviour is contagious. Nearby prairie dogs do the same thing, and jump-yips cascade through the colony like a Mexican wave through a stadium.

People have seen this endearing behaviour since at least the 1920s, but no one has really understood its purpose. Prairie dogs will jump-yip in all sorts of situations: when they’ve been taken unawares; when keeping watch from their burrows; when defending their territories; when meeting other prairie dogs; or when a predator has left. In all cases, they’re less likely to run away after jump-yipping than immediately before, and the behaviour is most often interpreted as an “all-clear” sign. It means, supposedly, that danger has passed.

That can’t be right, according to James Hare from the University of Manitoba. “They are every bit as inclined to perform the display when predators were present as when they were absent,” he says. For example, he noticed that wild black-tailed prairie dogs would jump-yip while a coyote was visibly passing through their town. All was not clear, but they jump-yipped nonetheless.

Hare came to a different conclusion after two years of watching 14 prairie dog towns. (These rodents live in large colonies that can span hundreds of acres and include hundreds, thousands, or maybe even millions of individuals.)

He found that the critical thing isn’t what a jump-yipping prairie dog is doing at the time of its display, but how its neighbours react. Specifically, if more of its neighbours jump-yip too, and if the Mexican wave lasts longer, the instigator then spends more time foraging.

These results suggest that the jump-yips are a prairie dog’s way of quickly checking up on its neighbours, including how many there are and how alert they are. It’s the equivalent of a human soldier shouting, “Sound off!” A strong response means that the colony is being collectively vigilant, and the instigator can be a little more relaxed. This explains why the prairie dogs jump-yip in so many different contexts.

“There have been a variety of hypotheses for why prairie dogs perform jump-yips, with no firm answers,” says Con Slobodchikoff, who has been studying prairie dog communication for decades. “This study provides solid data that helps to explain why these animals use this form of communication.”

There are other examples of contagious displays that spread through a group. Yawning is an obvious one. If I yawn in public, chances are that nearby people (or even dogs) might start doing it too. You might be yawning just reading this.

Some scientists view contagious yawns as a sign of empathy—an indication that we’re tapping into the psychological states of our peers. After all, they’re more common in people who score more highly on tests of self-awareness and empathy, and we’re more likely to yawn contagiously when close friends and family yawn than when strangers do so. Perhaps it’s a way of doing a quick mental check on people around us, and boosting our collective attentiveness.

Hare thinks that the jump-yips of prairie dogs play a similar role. He wonders if these simple contagious behaviours are precursors to more advanced mental skills like “theory of mind”—the ability to know what others are feeling and thinking. After all, by responding to their neighbours’ reactions, a jump-yipping black-tailed prairie dog seems to have at least a rudimentary awareness of the mental states of its peers.

Reference: Hare, Campbell & Senkiw. 2013. Catch the wave: prairie dogs assess neighbours’ awareness using contagious displays. Proceedings of the Royal Society B http://dx.doi.org/10.1098/rspb.2013.2153

A Blog by Ed Yong

Chameleons Convey Different Info With Different Body Parts

If you describe someone as a chameleon, you probably mean that they’re great at blending in, at changing their behaviour to suit different social situations. You probably don’t mean that they make their heads really bright when they’re about to get in a fight. The latter, however, would be more fitting.

Chameleons are famed for their ability to change colour, and people usually assume that this helps them to camouflage themselves from predators or prey. But in 2008, Devi Stuart-Fox and Adnan Moussalli showed that chameleons probably evolved their dynamic palettes to be social rather than secretive, to stand out rather than blend in.

The duo studied 21 species and sub-species of South African dwarf chameleons and found that those that undergo the most dramatic colour changes show stronger contrasts between different body parts, and stand out more strongly against their normal environments. It was communication not disguise that drove their capacity for colour change.

But what are they communicating? It’s possible that their messages are very sophisticated because they can change colour very quickly, and control the hues of different body parts independently. Their bodies don’t just flip between two settings. They’re dynamic living displays. And Russell Ligon and Kevin McGraw from Arizona State University have now shown that chameleons can convey different information by changing the colours of different body parts.

The duo set up duels between male veiled chameleons—a large species that grows up to two feet long, and has a reputation for being aggressive. When males meet each other, they react aggressively. They hiss, rock and curl their tails. They turn sideways and change the shape of their bodies from a narrow tube into a flat panel, filled with bright stripes and fleckles of green, turquoise, orange, yellow, lilac and charcoal.

“The changes essentially, turn the chameleon’s entire body into a billboard advertisement,” says Ligon. “The situation can escalate rather quickly. If neither chameleon backs down, they fight with full-body lunges and bites.” This usually lasts for just a few seconds, before one combatant realises he’s outmatched and backs down. Ligon and McGraw only had to intervene in one of their staged bouts, when a smaller rival pushed his luck so far that his opponent drew blood.

As the lizards squared off, the duo photographed them every four seconds, and measured the brightness and colours of 28 body parts. They also converted their photos according to the technical specifications of chameleon eyes, to see the individuals as other chameleons would see them.

Veiled-chameleon2They found that the brightness of the chameleons’ stripes predicted how likely they were to approach their rivals. This factor alone accounted for 71 percent of the variation in their motivation. Meanwhile, the brightness of their heads predicted their odds of actually winning their fights, and accounted for 83 percent of the variation in their fighting ability. (To a lesser extent, the speed of their colour change also says something about their combat skills.)

So, if you were a veiled chameleon facing off against a rival, pay attention to their stripe. If it becomes much brighter, they’re fixing for a fight. If their head becomes really bright, and does so quickly, they’re one tough lizard, and they’ve got a good chance of winning. And ignore the actual colours—making big jumps from one hue to another doesn’t tell you very much.

Stuart-Fox, who was not involved in the study, praised it for being the first to look at colour change as it would be perceived by actual chameleons—something that no one has done before when assessing contests.“It shows for the first time that the speed of colour change can affect contest dynamics – a discovery only possible because of the sophisticated way they quantified colour change,” he says.

Why do different body parts convey different information? “If I had to guess, I would say that these links exist because selection favoured the display of signals which could be accentuated at different, appropriate stages of an aggressive interaction,” says Ligon.

Chameleons are slow-moving, and their fights progress through a series of gradual stages. When they’re threatening each other, they face side-on, so it makes sense for their stripes to communicate their motivation for a fight. When they actually come to blows, they face head-on; again, it makes sense that their heads should signal their prowess in combat.

So far, Ligon and McGraw have found some intriguing correlations. Next, they want to start doing experiments, by controlling the changing colours of a chameleon model or robot to see how a rival reacts. Ligon also wants to know how the males use their colour-changing abilities during courtship, rather than just combat. “There’s a lot left to be done,” he says.

Reference: Ligon & McGraw. 2013. Chameleons communicate with complex colour changes during contests: different body regions convey different information. Biology Letters http://dx.doi.org/10.1098/rsbl.2013.0892

A Blog by Ed Yong

Newly Discovered Organ Helps Koalas Bellow At Elephant Pitch

Koalas may look cute and placid but come the mating season, the males produce a bellow that… well… is not the sound you expect them to make. As they inhale, they sound like a loud, creaky door. As they exhale, they sound like someone belching vigorously. Put these together, and you get a continuous racket that sounds like an angry Wookiee.

The bellows are surprising to passers-by, but they perplex scientists too. Koalas just shouldn’t be able to make a sound that low.

Mammals make calls using an organ in our throats called the larynx, or voicebox. When air passes through the larynx, it vibrates a pair of membranes called the vocal folds (or vocal cords). These create sound waves in our nose and mouth. We can control the pitch of those waves by using muscles in the larynx to change the tension in the vocal cords. The size of the cords also matters—it sets the lowest possible noise that we can make. This is why small mammals can only manage high-pitched squeaks, while big species can produce rumbling bass.

The koala is an exception. The lowest pitch of its bellows has a frequency of 27 Hertz—at least three octaves below middle C, and 20 times lower than you’d expect for an animal of their size. It’s the pitch you’d expect from an elephant.

Now, Benjamin Charlton from the University of Sussex has discovered their secret. He found a completely new organ in the koala’s throat that allows them to make their rumbling bellows. No one had seen it before and, as far as we know, no other mammal has evolved something similar.

The new organ is a pair of vocal folds that look and work very much like the ones in the larynx. But these are found at the velum—the junction where the koala’s windpipe branches into it nose and its mouth. Charlton calls them the velar vocal folds, or VVFs.

Cross-section through the head of a koala. Credit: Charlton et al, 2013. Current Biology.
Cross-section through the head of a koala. Oral tract in blue, nasal tract in yellow, soft palate in light red, velar vocal folds in dark red, larynx in dark blue, laryngeal vocal folds in green. Credit: Charlton et al, 2013. Current Biology.

The VVFs are 3 times longer than the vocal folds in the larynx, as well as 15 times wider, 14 times deeper, and almost 700 times heavier. Charlton calculated that their huge size allows them to produce extremely deep pitches, as low as 10 Hertz, and to belt out these frequencies with tremendous power.

To test this idea, he placed suction pumps inside the cadavers of three male koalas and sucked air in through their noses. Sure enough, the velar vocal folds vibrated, and produced deep sounds that are remarkably like those of living, bellowing males.

Why has the koala evolved this special organ? It’s not clear, but Charlton suspects that it helps to enhance information about a male’s quality. The bellows may be an exaggerated signal but they’re still honest ones. Bigger males probably have bigger vocal velar folds and produce deeper, louder bellows, in a way that a smaller male just can’t duplicate. Females could use these cues to judge the quality of potential mates.

The team wants to check if other related mammals have the same folds but for now, it looks like they’re a koala innovation.  “It appears that this remarkable adaptation has evolved independently in the koala specifically to produce their exceptionally low-pitched mating calls,” says Charlton.

This isn’t the only new body part that’s been discovered recently. In 2012, Nicholas Pyenson found a volleyball-shaped organ in the mouths of the biggest whales, which helps them to coordinate their titanic mouthfuls. And in 2011, John Hutchinson discovered a sixth toe in the feet of elephants—a stiletto heel in the world’s biggest platform shoes.

I love discoveries like these. They’re testament to the continuing importance of old-fashioned disciplines like anatomy and dissections. Koalas, whales and elephants are familiar and charismatic creatures and it’s wonderful to think that their bodies could hold secrets that only a careful scalpel will reveal.

Reference: Charlton, Frey, McKinnon, Fritsch, Fitch & Reby. 2013. Koalas use a novel vocal organ to produce unusually low-pitched mating calls. Current Biology http://dx.doi.org/10.1016/j.cub.2013.10.069.

A Blog by Ed Yong

Are Marmoset Monkeys Taking Turns To Talk?

When we talk to one another, we take turns. This simple rule seems to apply to all human conversation, whether the speakers are English city-dwellers or Namibian hunter-gatherers. One person speaks at a time and, barring the occasional interruption, we wait for our partner to finish before grabbing the conch. Timing is everything: cutting someone off is rude; leaving pregnant pauses is awkward. You need to leave a Goldilocks gap—something just right.

There are variations, certainly. New Yorkers are reputedly fond of “simultaneous speech” while Nordic cultures apparently love long, lingering pauses. But when Tanya Stivers analysed turn-taking across varied cultures, she found more similarities than differences. As I wrote in 2009:

“Stivers [collected] video recordings of conversations in ten different languages from five continents – from English to Korean, and from Tzeltal (a Mayan language spoken in Mexico) to Yeli-Dyne (a language of just 4,000 speakers used in Papua New Guinea). She found that… in all ten cultures, speakers shoot for as little silence as possible without speaking over each other, and the majority of answers follow questions after virtually no delay or overlap. The average delays certainly varied from language to language, but [the] extremes were only a quarter of a second off from the international average.”

The universal nature of turn-taking fascinated Asif Ghazanfar, a psychologist at Princeton University who studies monkey behaviour. “Taking turns acts as the foundation for more sophisticated forms of communication. You can’t share information if you’re constantly chattering over each other,” he says. “So how does that evolve?”

Our close relatives—the other great apes—provide few clues. They don’t actually vocalise very much and when they do, there’s no evidence that they take turns. So, Ghazanfar turned to another primate—the common marmoset, a tiny monkey that looks not unlike Back to the Future’s Doc Brown.

Although marmosets aren’t especially sophisticated communicators, they do regularly call to one another. Together with Daniel Takahashi and Darshana Narayanan, Ghazanfar placed 27 pairs of common marmosets  in opposite corners of a room, separated by an opaque curtain. Both monkeys called out, and although the pace of their exchanges was much slower than a human conversation, the team saw similarities in their rhythms.

For a start, they rarely interrupted one another. Each one waited for about 5 to 6 seconds after its partner finished before sounding off itself. The partners also ‘conversed’ with a steady rhythm, technically known as coupled oscillation. Both monkeys left a predictable interval between their calls, and their vocals slotted neatly into the silences created by their partner. And to confirm that they really are coordinated, the team showed that if one partner sped up or slowed down, the other followed suit.

“That’s what we do in conversation all the time,” says Ghazanfar. “If you speak to someone who’s speaking fast, you’ll start doing it too. We’re reporting the same for marmosets.”

Of course, there’s more to human turn-taking than that. We use sophisticated tricks to work out when it’s our turn to speak. We pay attention to grammar, meaning, inflection, body language and eye contact, and there’s no evidence that the marmosets are doing any of that. But nonetheless, the results are very similar—a coordinated vocal see-saw.

The marmosets also behaved in the same way whether they were paired with familiar cagemates  or complete strangers. That’s another feature they share with humans, and it sets them apart from, say, duetting birds, which only coordinate their vocals under very specific circumstances. “That’s not the case here,” says Ghazanfar. “One marmoset could have a conversation with any other marmoset.”

Common_Marmosets
Common marmosets. Credit: Dario Sanchez.
Common marmosets. Credit: Dario Sanchez

But Margaret Wilson, a psychologist from the University of California, Santa Cruz who studies turn-taking in both humans and animals, is not convinced. “The paper doesn’t demonstrate turn-taking in any interesting sense,” she says.  “I think the authors have failed to appreciate just how weird human turn-taking is.” Wilson explains the weirdness beautifully, so I’m going to yield the floor without interruptions:

When humans take turns, there is a cyclic structure to the extremely short gaps between speakers’ utterances.  A between-turn gap of, say, 200 milliseconds is more likely to be broken by the second speaker at certain regular intervals (say, odd multiples of 50 ms) than during the “troughs” between those intervals.  That is, short silences are not of arbitrary length, but reflect a cyclic passing back and forth of who has the “right” to speak next.  The troughs represent moments when the right to speak has shifted back to the original speaker, hence the second speaker inhibits speech during those fractions of a second.  And this is happening at the order of tens of milliseconds.  This “structured silence” can only be explained by extremely tight coupling of some oscillatory mechanism in the brains of the two speakers.“

And there’s no hint of that complexity in the marmosets’ exchanges. The cycles in their conversations span their actual calls rather than just the gaps between them. That just means their timing’s not completely random. And with long silences between turns, they could just have been calling and then responding to their partner’s call, as many other animals do.

But if there’s one thing Wilson agrees with, it’s that the question’s worth asking. “Turn-taking is fundamental to human conversation, so the question of whether it occurs in other social animals is extremely interesting,” she says.

Consider that humans talk so much more than other apes. Many scientists have suggested that this vocal sophistication is rooted in manual gestures—the arm and hand movements that chimps and gorillas use a lot. These became increasingly complex and eventually, the brain circuits for gestures got glommed onto vocals. But Ghazanfar isn’t a fan of this idea. “They have to come up with some magical thing that switches from manual to speech,” he says.

If marmosets take turns, that points to a different hypothesis. Like humans, they are cooperative breeders. Males and females work together to raise their young, typically as a monogamous pair and often with help from older siblings. “The idea is that this strategy of cooperative breeding specifically makes them more friendly,” says Ghazanfar. Turn-taking may be a symptom of this temperament—a by-product of breeding habits that make for a generally more cooperative primate.

Maybe the same thing happened during human evolution? “There could have been a tweak in the way we raise our offspring, which led to more prosocial behaviour,” says Ghazanfar. “And once you have that general prosociality, you may be more inclined to make more contact with other members of the species.”

It’s an interesting scenario, and one that has parallels in domestic dogs. There’s a popular idea that dogs evolved from wolves that were drawn to human settlements, perhaps to scavenge off our garbage. Individauly with more docile temperaments were best-suited to these forays, and gradually became better at reading human cues and gestures. You select for a certain temperament, and many other traits get yanked along for the evolutionary ride.

Of course, this is still conjecture, and the common marmosets are just one (contested) data point. The next step would be to check for turn-taking in other cooperatively breeding primates, such as tamarins, or related species that don’t share the same reproductive habits.

Reference: Takahashi, Narayanan & Ghazanfar. 2013. Coupled Oscillator Dynamics of Vocal Turn-Taking in Monkeys. Current Biology http://dx.doi.org/10.1016/j.cub.2013.09.005

A Blog by Ed Yong

Tree-Killing Worm, Please Make Your Way To The Boarding Gate

Meet the microscopic worm that can kill forests. It’s called the pinewood nematode (Bursaphelenchus xylophilus) and though each one is barely a millimetre long, they can collectively bring down a towering pine tree.

Once it gets into a tree, the nematode spreads through the trunk, branches, and roots. It feeds on the cells lining the pine’s resin canals, causing resin to leak into other vessels that carry water around the tree. Cut off from their water supply, the pine’s needles turn yellow and brown. The change is dramatic. Within just a few months, the tree wilts and dies. This pine wilt disease has claimed millions of pines, especially in Europe and East Asia, causing huge problems for ecosystems and the forestry industry alike.

But the nematode can’t spread to new trees on its own. Instead, it hitches a ride on pine sawyer beetles—substantial, finger-sized insects with long antennae and sharp mandibles.

The nematodes hide inside the breathing tubes that carry oxygen around the beetles’ bodies. They emerge only to enter the open wounds caused when the insects nibble on pine twigs. They spread through the tree and kill it—that’s perfect for the beetles, which lay their eggs in dead or dying wood. Their larvae eat the wood until they transform into adults and fly off in search of fresh pines. And before they do, they’re boarded by nematodes.

These two partners enjoy a tight, mutually beneficial relationship. The beetle brings the nematode to fresh victims, while the nematode creates the conditions that the beetle needs to reproduce.

But timing is everything. The nematode goes through four larval stages and it can only colonise beetles in the last of these—L4. The beetles, meanwhile, can only host the nematodes as adults. Fortunately, the duo have a way of synchronising their complex life cycles.

The pine wilt nematode. Credit: USDA Forest Service Region 2, Rocky Mountain Region Archive, Bugwood.org
The pine wilt nematode. Credit: USDA Forest Service Region 2, Rocky Mountain Region Archive, Bugwood.org

Lilin Zhao from the Chinese Academy of Sciences has found that the beetles produce a chemical signal when they transform into adults. This tells the nematode that its ride will soon be ready, and that it should enter the L4 stage. It’s a molecular announcement that says the insect will soon be ready for boarding.

Zhao’s team first noticed that although the beetle grub is surrounded by nematodes inside a pine tree, very few of these worms are in the L4 stage. They only transform en masse when the insect reaches the last stages of pupation and is about to emerge as an adult.

To work out why, the team analysed the chemicals on the beetle’s surface at different life stages. They found four that are mass-produced at the end of its pupal stage. When the adults emerge, they give off waves of this chemical stew. And when Zhao dabbed the cocktail onto stage-three nematodes, they quickly transformed into stage-four.

The substances in question are all fatty acid esters—long chains of carbon and hydrogen atoms with a couple of oxygen atoms at the end. Insects commonly use these chemicals as pheromones, but the pine sawyers make four very specific ones—ethyl palmitate, ethyl stearate, ethyl oleate and ethyl linoleate—and they do so in bulk.

These signals are very specific. Similar esters don’t trigger the nematodes’ transformation, nor do those from beetles other than the pine sawyers. That’s important—many beetles bore into wood and it would be counter-productive for the nematodes to get a boarding announcement from an insect that can’t serve as its host.

It’s possible that this discovery could be used to save pine trees from the nematodes, by somehow disrupting the worms’ ability to synchronise their lives with that of their beetles. But for now, it serves as yet another example of the intimate partnerships that exist between different animals, and the signals that seal those alliances.

Reference: Zhao, Zhang, Wei, Hao, Zhang, Butcher & Sun. 2013. Chemical Signals Synchronize the Life Cycles of a Plant-Parasitic Nematode and Its Vector Beetle. Current Biology http://dx.doi.org/10.1016/j.cub.2013.08.041