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Monkeys With Better Social Networks Stay Warmer in the Winter

It’s three in the morning in South Africa, in the middle of winter. Temperatures have dropped to just below freezing and a vervet monkey—silver-furred and black-faced—is very, very cold. Soon, the rising sun will heat the land to a much nicer 25 Celsius, but for now, the vervet faces five hours of bitter chill. So, it seeks out some friends for warmth. And as they huddle together in a shivering heap, tiny thermometers in their bodies record their temperatures.

Richard McFarland from the University of the Witwatersrand implanted the devices in a dozen vervets in January 2011. His goal: to see if their social ties could help these wild animals to cope with wildly varying temperatures.

McFarland is no stranger to such research. In 2008, he studied two groups of Barbary macaques—stocky, stump-tailed monkeys, living wild in Morocco’s Atlas Mountains. He found that those with more social ties were more likely to survive the winter of 2008—an exceptionally cold and snowy season that killed 30 of them. It was the first study to show that an animal’s social connections can affect its odds of surviving a bout with the elements. The question was: why?

One possibility was that the well-connected macaques were better at keeping warm, because they could more easily find partners to huddle with or could huddle in bigger groups.

To test that idea, McFarland’s team travelled to the opposite end of Africa. They tranquilised a dozen female vervets and surgically implanted wax-sealed temperature recorders into their abdomens. When the monkeys came to, the team released them and counted how many social partners they had—that is, how many other vervets they groomed and were groomed by. Nineteen months later, the team recovered the recorders and the precious data they contained.

The data revealed that during winter, the monkeys’ core temperatures were often three degrees lower at night than in the day. As the months wore on, these fluctuations became increasingly severe. But the more partners the monkeys had, the steadier their body temperatures were. Sociability meant stability.

These results put a new twist on the value of group-living among primates. In some now-classic studies, Joan Silk from the University of California, Los Angeles, showed that young baboons are more likely to survive if their mothers have strong social bonds. There could be many reasons for this, but one popular idea is that such bonds help animals to deal with stress. Certainly, well-connected monkeys have lower stress hormones than isolated ones, and that alone might give their immune systems a break, and improve their survival. The same applies to humans—people with bigger social networks tend to have better physical and mental health.

But the vervets show that social ties have another important benefit. “Better-networked monkeys stay warmer in winter,” says Katie Hinde from Harvard University, who was not involved in the study. “That has the potential to protect animals from illness and leave them with more calories for building babies.”

And unlike Silk’s baboons, “it’s not just strong bonds that matter,” says Louise Barrett from the University of Lethbridge, who led the research. “Weak bonds matter too. Having a lot of partners that you can call on means you can have a bigger huddle, or find a partner if yours is already busy. There’s a utilitarian function to maintaining a lot of bonds.” In other words, quantity matters as much as quality. This effect might even be important in keeping a vervet group together, and stopping its members from splintering into smaller factions of tightly knit—but very cold—individuals.

Huddling isn’t the only way in which groups stay warm, either. Vervets cement their friendships by grooming each other, and that improves the insulating properties of their fur. “It’s like fluffing a duvet,” says Barrett.

“I think this study has important implications for the behavioural ecology of personality,” adds Hinde. She wants to know the vervets’ personality traits affect their social networks and how that, in turn, affects their survival and reproductive success. Do gregarious monkeys stay warmer than live longer than loners? And how does that vary between parts of Africa with different climates? In regions where temperatures swing more manically throughout the day, do monkeys have better social integration?

Reference: McFarland, Fuller, Hetem, Mitchell, Maloney, Henzi & Barrett. 2015. Social integration confers thermal benefits in a gregarious primate. Journal of Animal Ecology http://dx.doi.org/10.1111/1365-2656.12329

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Social Spiders Pick The Best Careers For Their Personalities

I was a terrible scientist; I’m much better at being a writer. I lack the creative spark for designing clever experiments, but I can fashion a decent metaphor. My intellectual skittishness stops me from narrowing in on a single field, but it’s a boon when it comes to dealing with a broad spectrum of topics. It took me two unsuccessful years as a PhD student to work this out, and to find a job that’s better suited to my skills and temperament. Because of that, I envy the spider Anelosimus studiosus. It naturally falls into the right career.

While most spiders hunt alone, there are a few hundred species of social spiders that live in colonies. A.studiosus is one of them. Up to 50 individuals gather together to spin large collective webs, which ensnare larger prey than each spider could trap on its own.

All the colony members look the same, but they don’t all behave in the same way. The females can be aggressive or docile. It’s surprisingly easy to suss out their personalities: just put two of them in a small box overnight and check on them the next morning. If they’re both docile, they will have built a joint web in one corner of the box. If one of them is aggressive, the pair will be at opposite corners (you can then pair each individual with a known docile spider to confirm its personality).

Colin Wright from the University of Pittsburgh has now found that these personality types do different jobs within the web, creating a natural division of labour. They’re a little like ants and termites, where small workers clean and forage, and big soldiers guard and defend. But unlike these social insects, the social spiders don’t have distinctive castes with different physiques. Instead, their roles are defined by their personalities.

Social spider web. Joe Lapp
Social spider web. Joe Lapp

When Wright’s team, led by Jonathan Pruitt, first started studying A.studiosus, they couldn’t work out what the docile spiders did. They didn’t seem to repair webs, repel invaders, or catch prey. “The prevailing theory was that they were probably social parasites, a sort of selfish variant that freeloaded on the success of aggressive spiders,” says Wright.

But when the researchers checked the fates of colonies in the wild, they found that those with a mix of docile and aggressive members were more likely to survive than those with just a single type. The docile members were clearly doing something important.

It turns out that they act as the colony’s babysitters. They spend most of their time standing watch over the eggs, sitting amid clusters of spiderlings, or directly feeding the youngsters by regurgitating food—just like a mother bird might. Meanwhile, the aggressive spiders generally avoid these tasks; instead, they spend most of their time building the communal web, catching prey, and defending their colonies. (Although aggressive spiders repel docile ones in a simple container, the two types happily share webs—their different tasks mean that they rarely interact.)

The team also found that across the spiders show a perfect match between aptitude and career. That is, they tend to do the jobs that they’re best at.

Compared to the docile spiders, the aggressive ones are better at repelling a rival species of spider from their webs, at building webs that restrained crickets for longer, and at successfully subduing crickets that landed in their webs. This is probably because the docile females rarely respond to intruders—even prey—and when they do respond, they do so slowly.

By contrast, the docile spiders were better at looking after the colony’s young. When challenged with large broods, they raised twice as many to the point when the youngsters no longer needed care. That’s probably because  they’re less likely to fight with their youngsters over food. They’re also less likely to eat the spiderlings—one of the more important signs of a good parent.

“Rarely are results of a study so clear and interpretable,” says Wright. “We thank our spiders for being such a pleasure to work with.”

The results clearly show that something as subtle and hidden as a spider’s personality can help to organise its society. “Most people are more concerned with the physical characteristics of a species, and the idea that spiders have personality sounds somewhat like the topic of a children’s book,” he says. “But spider personalities are very real, and if you overlook them, at least in this species, you miss so much of the story!

For now, it’s not clear why the spiders naturally fall into their respective careers, or even what drives their different personalities in the first place. They seem to be largely heritable, but no one knows whether the spiders also learn to behave in a certain way, or if they can switch their personalities in certain situations.

And there’s another crucial piece of missing information, says Trine Bilde From Aarhus University, who has also studied social spiders: it’s not clear if the two types of spider are actually helping each other. “We don’t know whether docile females are fostering offspring of aggressive females, or if the aggressive females are sharing their catch with docile females,” she says.

The team are now trying to answer these questions. In the meantime, Wright suggests that biologists should pay more attention to personality types, when trying to understanding how animal societies work. For example, division of labour, of the kind that Wright studied, has been linked to the evolutionary origins of physically distinct castes in ants, bees and termites. But while physical castes only exist in a narrow range of animal groups, “individual differences in personality have been detected in almost every animal system imaginable,” says Wright.

“We feel that, in just about every instance, one could simply replace the word caste with personality,” says Wright. As with the spiders, this approach could help scientists to discover hidden variations in the behaviour of animals that otherwise look exactly the same—variations that could shape the structure of their societies in important ways.

Reference:  Wright, Holbrook & Pruitt. 2014. Animal personality aligns task specialization and task proficiency in a spider society. PNAS http://dx.doi.org/10.1073/pnas.1400850111

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A Thousand Worms Merge Into a Living Tower

What’s creepier than a worm rearing up on its tail to snag a passing insect? A thousand worms uniting into a single living, writhing, waving tower to snag a passing insect.

Pristionchus pacificus is a nematode or roundworm—one of 25,000 species that are among the most numerous animals on the planet. This particular nematode infests the bodies of scarab beetle larvae. It’s not a parasite as such, and its habits are positively tame compared to the creatures that often feature on this blog. It simply waits for its host to die of natural causes, and then eats the microbes that grow on its carcass.

But first, it has to get into a beetle. At some point during its early days, P.pacificus pauses its growth and becomes a dauer—an especially tough larva that’s adapted to survive through harsh conditions. The dauers stand on their tails and wave their body about in the hopes of latching onto passing beetles.

But Sider Penkov and Akira Ogawa from the Max Planck Institutes found that groups of P.pacificus can merge to form a single waving “dauer tower”, composed of up to a thousand individuals.

Each individual worm is just a quarter of a millimetre long but the towers can grow up to a centimetre. Some are so big that you can see them with the naked eye and photograph them with a macro lens, even though their members are all microscopic.

Such teamwork! Such togetherness! Such low odds of ever appearing on a motivational poster!

Other nematodes like C.elegans—that darling of biologists—also form dauer towers, but these constructions are small and fall apart easily. By contrast, P.pacificus’s towers are incredibly strong. Penkov and Ogawa tried prodding them with a metal wire, and they didn’t fall apart. They stuck the towers in water and the larvae started to swim, but they still kept together as a cohesive mass. The only thing that worked was a dash of detergent. When they added that to the water, and the towers disintegrate into a mass of individual larvae.

The team reasoned that the worms must be sticking together with a fatty or waxy chemical that repels water but can be dissolved by detergent. Indeed, they saw that the worms exuded small droplets over their skins, soon after they transformed into dauers. The droplets contained a huge wax molecule (C60H100O2N), one of the longest found in any animal or plant. The team called it nematoil.

Nematoil is the glue that gives the dauer tower its power. When the team synthesised the chemical and applied it to C.elegans, they found that even this nematode could unite into a sturdy spire.

Penkov and Ogawa suspect that the tower’s height gives its constituent larvae better odds of hitching onto a beetle. Once one of them snags some cuticle, the entire tower can get pulled along for the ride, held together by their nematoil secretions.

But their discovery raises many more questions. What brings the worms together in the first place? How do they coordinate their movements to produce a cohesive wave? And are there cheats?

P.pacificus reminds me of another microscopic creature called Dictyostelium discoideum, or Dicty for short. It’s not an animal but a slime mould. It mostly spends its time as single-celled amoebae, but these can merge into a many-celled slug. The slug slowly stretches skywards, forming a spore capsule atop a long stalk. Any amoebae that form the spores will survive, but those that create the stalk go nowhere and eventually die. This leads to conflict. Some amoebae are cheats, which make more than their fair share of spores and are rarely contribute to the stalk.

Does the same apply to P.pacificus? Do the nematodes at the base of the stalk perhaps get left behind? Do some of them secrete less nematoil (which, after all, takes a lot of energy to make), relying instead on their neighbours’ glue?

Reference: Penkov, Ogawa, Schmidt, Tate, Zagoriy, Boland, Gruner, Vorkel, Verbavatz, Sommer, Knolker, Kurzchalia. 2014.  A wax ester promotes collective host finding in the nematode Pristionchus pacificus. Nature Chemical Biology http://dx.doi.org/10.1038/nchembio.1460

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Can Moths Explain Why Sloths Poo On the Ground?

Here’s a memorable encounter between David Attenborough and a three-toed sloth, as shown in Life of Mammals. Sloths normally spend their lives hanging from high branches, but this one ambles down to the ground at the 1:10 mark. “It wants to defecate,” says Attenborough, “and the only place it’s happy doing that, oddly enough, is down on the ground.”

This happens once a week. The sloth climbs down, digs a small bowl in the ground with its tail, and poos.  It covers up its latrine with leaves before climbing back up.

This behaviour is bizarre. Sloths not only burn 8 percent of their daily calories on these laborious descents and climbs, but they are incredibly easy prey on the ground. Look at the video—Attenborough only has to slowly lean forward to scrag the animal. In fact, more than half of all sloth deaths are due to predators killing them while travelling to and fro their low latrines. If a sloth s**ts in the woods, predators seem to know.

So why do it? Surely, there must be some advantage. Otherwise, why waste energy and risk death, when they could just defecate from high branches and let gravity carry their poo away? Some people think that the sloths are fertilising their favourite trees, while others have suggested that they communicate with other sloths using the latrines.

But Jonathan Pauli from the University of Wisconsin-Madison has a different explanation. It involves thinking of a sloth as less of an individual, and more of a mobile ecosystem.

In their fur, sloths host a diverse community of fungi, algae, insects, mites and ticks. (In one case, scientists found 980 beetles in the fur of a single animal). Many of these residents are found nowhere else. To them, the sloth is the only world they know. The three-toed sloth even has adaptations that help it cultivate these partners. For example, its hair contains cracks that collect rainwater, and acts as miniature hydroponic gardens for growing algae.

The fur also contains moths. Cryptoses moths live exclusively on sloths, probably feeding on their skin secretions or algae. There can be up to 120 of them in one individual.

The moths are entirely dependent on the sloths, and specifically on their daring defecation descents. While the sloths do their thing, the female moths fly off and lay eggs in the fresh dung. The larvae eat nothing else. Surrounded by a banquet of delectable sloth faeces, they slowly transform into adults, before flying into the canopy and colonising more sloths. Beautiful.

So Pauli wondered: do the sloths also depend on the moths? Is that why they risk the dangers of terra firma, even though a squatting sloth is a sitting duck?

To find out, his team compared two types of sloth in Costa Rica—the brown-throated three-toed sloth, which always defecates on the ground, and Hoffmann’s two-toed sloth, which only sometimes does so. They cut locks of hair from the animals, sucked up all the moths using an “invertebrate vacuum”, and analysed the chemical composition of the remaining fur and algae.

They found that the number of moths, the amount of algae, and the nitrogen content of the fur were all connected. If an individual has more moths, it also has more algae and more nitrogen. And three-toed sloths have more of all the above than the two-toeds.

Pauli believes that the moths seed the sloth’s fur with nutrients that spur the growth of the algae. Maybe they’re transporting nitrogen-rich waste from the dung pile into the fur. Maybe they die in the fur and release nitrogen when they’re decomposed by fungi. Either way, they seem to fertilise the algae.

This matters because, according to Pauli, the algae are an important food source for the sloths. His team mixed the sloth fur with bacteria from a cow’s stomach and showed that the algae within can be easily digested. They also analysed the chemical make-up of the algae and found that it has as much carbohydrate and protein as the leaves that the sloths normally eat, but three to five times more fat. (It’s possible that the algae, by painting the sloths green, help to camouflage them from predators like harpy eagles.)

So, the moths help to fertilise the sloths’ algal gardens, which gives the sloths a valuable energy boost to supplement their otherwise poor diets. The sloths, in turn, defecate on the ground to help their partners-in-gardening to complete their life cycle. They may die, but that’s a risk they have to take. They are locked into this partnership.

The sloth-moth cycle. Credit: Pauli et al, 2013. Royal Society.
The sloth-moth cycle. Credit: Pauli et al, 2013. Royal Society.
This would explain why the three-toed sloth always defecates on the ground while its two-toed cousin will often do it from the trees. The two-toed forages on a wider range of food so, as Pauli found, it isn’t so reliant on the moths or the algae.

But there are still a few loose threads. For example, the team haven’t calculated how much energy the algae could hypothetically provide, and whether that makes up for the cost of travelling to the ground once a week.

And Brazilian researcher Adriano Chiarello points out an even bigger problem with the hypothesis. He and his students have spent more than 1,000 hours watching maned sloths in the wild. “We never saw sloths behaving in a way that might suggest or indicate that they were somehow extracting algae or other nutrients from their fur,” he says. They’re not like cats; they clean their fur with their front paws rather than their mouths. “I don’t remember ever seeing a sloth licking or lapping its fur.”

So, how exactly are they eating the supposedly nutritious algae? “Perhaps sloths do this secretly, or solely at night when such behaviour would be even more difficult to witness,” says Chiarello. Or, perhaps they’re absorbing the nutrients directly through their skin. He’s not convinced by either possibility and, either way, “the smoking gun is missing”.

Still, Chiarello says the study is a strong piece of work. “Testing hypothesis with sloths is not easy as they are difficult to capture and observe in their natural environment,” he says. “The authors are making their best with available data.” He hopes that more will come.

Reference: Pauli, Mendoza, Steffan, Carey, Weimer & Peery. 2014. A syndrome of mutualism reinforces the lifestyle of a sloth. Proc Roy Soc B http://dx.doi.org/10.1098/rspb.2013.3006

More on sloths: Portable brain activity-recorder shows that sloths aren’t all that sleepy

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Bird Cheaters Target Teams, But Teamwork Beats Cheats

The common cuckoo is famed for its knack for mooching off the parental instincts of other birds. It lays its eggs in the nests of at least 100 other species, turning them into inadvertent foster parents for its greedy chicks. For this reason, it’s called a brood parasite.

It’s not alone. Among the birds, the full list of brood parasites includes more than 50 members of the cuckoo family, cowbirds, honeyguides, several finches, and at least one duck.

Now, William Feeney from the Australian National University has found that brand of reproductive cheating goes hand in hand with its polar opposite: cooperative breeding, where birds raise their young with help from siblings or offspring, often at the cost of the helpers’ own reproductive success.

The two strategies couldn’t be more different but Feeney found that each drives the evolution of the other. In places where one is common, the other is too. Exploitation goes hand-in-hand with cooperation.

Biologists have been exploring the origins of cooperative breeding for almost 140 years. “What I liked about the new paper is that is presents convincing evidence for an idea that wasn’t even really on the table—it is beneficial because groups reduce the risk of brood parasitism,” says Bruce Lyon from the University of California, Santa Cruz.

Similarly, scientists who study brood parasites have mostly focused on defences like spotting a cuckoo’s eggs. “For some reason the social system of the hosts was not really considered,” says Lyon.

The seeds of the discovery were planted in Australia, where Feeney’s group were studying the aptly named superb fairy-wren. It gets parasitised by Horsfield’s bronze cuckoo, but not without a fight. The team noticed that the fairy-wrens attacked incoming cuckoos with extreme prejudice, and that larger groups almost never got parasitised. They wondered if the two behaviours—cooperative breeding and brood parasitism—were connected in other parts of the world.

The answer was a resounding yes. Look at the maps below. The top one shows the global spread of cooperatively breeding passerines—the small perching birds that are the most frequent target of brood parasites. Red areas are rich in cooperative species, while white areas are devoid of them. The bottom map shows the spread of brood parasites. There’s a very strong match between the two. Even if you account for the total richness of species in a given area, places with lots of cooperative breeders also have lots of brood parasites. Africa and Australasia are particularly rich in both.

Credit: Feeney et al, 2013. Science.
Credit: Feeney et al, 2013. Science.

Of course, this connection could be due to some unrelated factor. For example, extreme parenting styles might just be more common in Africa and Australia, because these continents have harsh, variable environments. If the two strategies really are connected, then you’d expect that connection to hold within regions as well as between them.

That’s exactly what Feeney found. Even within Africa and southern Australia, brood parasites are much more likely to target cooperative breeders than other birds.

Here’s a family tree showing all the birds from southern Africa. The orange circles denote species that are cuckoo hosts, and the blue circles are the cooperative breeders. Around 28 percent of the hosts help each other out in the nest, compared to just 8 percent of the non-hosts.

Credit: Feeney et al, 2013. Science.
Credit: Feeney et al, 2013. Science.

And here are all the passerines in Australia. Again: an obvious connection. Around 53 percent of the hosts help each other out in the nest, compared to just 12 percent of the non-hosts.

Credit: Feeney et al, 2013. Science.
Credit: Feeney et al, 2013. Science.
Credit: Feeney et al, 2013. Science.

There are two possible reasons for this correlation. Brood parasites might selectively target cooperative breeders because they’d provide the best care. Alternatively, birds might resort to teamwork because they can better defend their nest against parasites.

Feeney found that both answers are right.

His team returned to the superb fairy-wren—a bird where some parents get help in the nest, but others don’t. By comparing different nests over 6 years, they showed that cuckoo chicks grow faster and survive better if they’re raised by larger groups of fairy-wrens. So cooperative breeding can foster the rise of brood parasitism.

But cuckoos rarely get to realise this benefit, because larger groups of fairy-wrens are also better at fending them off. Collectively, they’re more vigilant around the nest. If one of them spots a cuckoo, it makes a cuckoo-specific alarm call and the entire group mobs the intruder. The larger the group, the more persistently they attack. So the presence of brood parasites fosters can foster the rise of cooperative breeding.

Naomi Langmore, who led the study, thinks that the relative strength of these two effects probably changes over time. Cuckoos and other brood parasites often switch hosts. When this happens, it’s initially easier for them to reap the benefits of a larger surrogate family because the new hosts have evolved to detect or repel their infiltrators. Over time, as such defences emerge, the balance shifts. For the fairy-wrens and bronze cuckoos, “cooperation protecting against parasitism is the stronger force,” says Langmore.

Of course, there are many reasons for species to evolve cooperative breeding, and the threat of parasites is just one of them. If there aren’t enough territories to go around, or if predators are particularly rampant, it will also benefit youngsters to stay near their families rather than strike out on their own.  “Brood parasitism is not exclusive of other factors but may simply help tip the balance in favour of helping over dispersing,” says Lyon.

“The relative importance of brood parasitism in selecting for cooperative breeding is likely to vary from species to species,” says Langmore, “but our evidence suggests that, overall, it is one of the major selective forces favouring the evolution of cooperation.”

She’s not just talking about birds, either. There are also many brood parasites among the insects, including a group of over 3,000 cuckoo wasps. Many lay their eggs in the nests of other wasps, and their grubs devour the hosts’ own eggs and larvae. “The hosts of cuckoo wasps also mount highly aggressive colony attacks on the parasites,” says Langmore, “and hosts from parasitized populations have actually evolved larger bodies so they are better able to drive off the parasites.”

Reference: Feeney, Medina, Somveille, Heinsohn, Hall, Mulder, Stein, Kilner & Langmore. 2013. Brood Parasitism and the Evolution of Cooperative Breeding in Birds. Science http://dx.doi.org/10.1126/science.1240039

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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

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Mercenary Ants Protect Farmers With Chemical Weapons

Humans have a long history of bolstering their armies by paying mercenaries to fight on their behalf. Now, Rachelle Adams from the University of Copenhagen has found that some ants do the same.

Some ants defend their colonies with special soldiers, which are bigger and wield more formidable weapons. But others lack a proper army. Sericomyrmex ants, for example, are fungus-farmers. They bring bits of vegetation back to their nests and use these to nourish a fungus, which they then eat. They are poorly defended, and a sitting target for raiders and pirates. That’s why they rely on other ants to fight for them.

Another ant called Megalomyrmex symmetochus forms its own colonies, complete with queen and workers, inside those of Sericomyrmex colonies. This guest is present in over 80 percent of the farmers’ nests and, at first glance, it looks like a parasite. It eats the fungus that the farmers so assiduously grow, without contributing any labour of its own. Worse still, it eats some of the farmers’ larvae and clips the wings of their young queens, so they contribute to the gardening rather than flying off to start their own colonies.

But M.symmetochus doesn’t just freeload off its hosts. In some cases, it can be their salvation.

Megalomyrmex mercenary (top right) defends a fungus garden from a Gnamptogenys raider (bottom). Credit: Rachelle Adams
Megalomyrmex mercenary (top right) defends a fungus garden from a Gnamptogenys raider (bottom). Credit: Anders Illum

Sericomyrmex nests are often attacked by a third ant called Gnamptogenys hartmani—a sort of six-legged pirate. It raids the colonies of farming species, drives them out, usurps their nests and gardens, and eats any remaining larvae.

The farmers can do very little against these raiders, since they lack specialised soldiers and have mostly lost their stings. Their powerful jaws can deliver a strong bite, but at such close quarters, they risk getting stung and bitten themselves. When attacked, they’re much more likely to feign death or flee. That is, unless there’s a M.symmetochus colony living in their nests.

Back in 2011, Adams let some raiders loose upon a colony of Sericomyrmex farmers, which was already being parasitized by M.symmetochus. “To our surprise, the hosts hid and the parasites rose to the top of the garden to confront and kill the invaders,” she says.

Unlike their hosts, the parasitic ants are far from defenceless. They raise their stings and release a powerful venom directly into the air—an airborne chemical weapon that kills the raiders and befuddles any survivors. “Rather than uniting as an efficient infiltration squad they turn on each other and attack, sometimes killing their own kin,” says Adams.

M.symmetochus behaves like a colony of mercenaries. They can cause problems for the farmers during peace-time, but they provide an invaluable defence when an invading force arrives.

By pitting the three types of ants against each other, first in one-to-one battles and then in more realistic groups, Adams’ team showed that the mercenaries are much better at subduing the raiders than the farmers. It takes just two of them to overpower a single raider, while the same task requires at least eight farmers. On average, a pair of raiders can kill 70 percent of farmers in an unprotected nest, but just 10 percent of them if there are six mercenaries around.

And the raiders seem to know it. When the team gave them a choice between two nests, only one of which was defended by mercenaries, they were more likely to attack the unprotected nest. In the experiment, a wire mesh prevented the raiders from actually touching the colonies, so they were probably put off by the smell of the mercenaries’ chemical weapons. Just by living in the same colonies, the mercenaries protect the farmers by cloaking them in a defensive miasma.

The thing that clinches this incredible relationship is probably Megalomyrmex’s life cycle. They form a life-long bond with a single colony of farmers, and won’t leave to seek out a different host. They exploit their hosts but they don’t overexploit them, and if raiders attack, they mount a defence rather than abandoning the farmers to their fates.

Next, the team wants to study how this alliance varies over time and space. For example, it should be easier to find the mercenaries in the farmers’ nests in places where the raiders are more common. Similarly, a different farmer called Trachymyrmex zeteki should be relatively unbothered by raiders, since it also hosts a parasitic mercenary but in fewer than 6 percent of its nests.

For now, they very astutely compare the mercenary ants to a human disease called sickle cell anaemia. It’s an inherited genetic disease that warps the shape of red blood cells and causes a gradual building illness. The mutated gene behind the disease is common in Africa because two copies might cause sickle-cell anaemia, but one copy protects a person against malaria. Similarly, M.symmetochus is like a mild chronic disease that exerts a toll upon its host, while protecting it from an acute and more destructive infection—the Gnamptogenys raiders.

Reference: Adams, Liberti, Illum, Jones, Nasha & Boomsma. 2013. Chemically armed mercenary ants protect fungus-farming societies. PNAS http://dx.doi.org/10.1073/pnas.1311654110

Experimental manipulation of the tendon of the large jumping muscle of one hindleg

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How To Terraform A Squid

Terraforming—the act of transforming an inhospitable world into one that we can live on—has been a staple of science-fiction for decades. But some living things have been carrying out their own version of the practice for far longer.

The bacterium Vibrio fischeri is a squid terraformer. Although it can live independently in seawater, it also colonises the body of the adorable Hawaiian bobtail squid. The squid nourishes the bacteria with nutrients and the bacteria, in turn, act as an invisibility cloak. They produce a dim light that matches the moonlight shining down from above, masking the squid’s silhouette from predators watching from below. With its light-emitting microbes, the squid becomes less visible.

Margaret McFall-Ngai from the University of Wisconsin has been studying this partnership for almost 25 years and her team, led by postdoc Natacha Kremer, have now uncovered its very first moments. They’ve shown how the incoming bacteria activate the squid’s genes to create a world that’s more suitable for their kind. And remarkably, it takes just five of these microbial pioneers to start the terraforming (teuthoforming?) process.

Inside its egg, an embryonic squid is sheltered in a sterile bubble. When it hatches, it starts pumping seawater into its body, bringing a flood of bacteria into contact with a special light organ. Among these teeming hordes is V.fischeri. It gathers in the layer of mucus on the light organ’s surface, squeezes through six tiny pores, and multiplies to fill the various nooks and crannies within.

To understand the first moments of this partnership, Kremer raised baby squid in either normal Hawaiian seawater, or water that contained all the usual bacteria except for V.fischeri. By comparing the two groups, she could “eavesdrop into the very first conversations of an animal host with its coevolved partner”.

She found that the light organs can sense the presence of just five V.fischeri cells among millions of other bacteria. These microbes touch just two or three of the squid’s own cells at most, but that’s enough to change the activity of 84 genes across the whole light organ.

Several of these genes are involved in the squid’s immune system. The team suspects that they may activate antimicrobial chemicals in the mucus, to create an environment that’s inhospitable for other bacteria besides V.fischeri. This might explain why the light organ is exposed to hundreds of bacterial species, but only V.fischeri can colonise it.

Kremer also showed that V.fischeri switches on a squid gene that breaks down chitin, a large molecule found in the mucus around the light organ. The chitin is converted into a smaller molecule called chitobiose, which the bacteria can sense. And once they detect chitobiose, they become attracted to it.

So, when V.fischeri reaches the light organ, it starts destroying chitin and making chitobiose. Chitin is especially abundant near the pores and internal ducts, so these areas eventually teem with chitobiose. And that produces an alluring signal that draws other V.fischeri towards the pores and into the light organ itself. The first few bacteria that go down this route lay down a chemical trail that many more follow.

All of this happens in the hours after hatching. By tweaking the genome of their hosts, a few bacteria can make the squid more attractive to their peers and less conducive to their competitors.

Studies like this aren’t just relevant to squid. We are also colonised by trillions of bacteria in our first moments of life. The squid gets its bacteria from the surrounding water, and we get ours from our mothers—from her vagina if we’re born naturally, or from her skin if we’re born through C-section. Our microbes might not glow or hide us like the squid’s partners, but they do change the properties of our guts, help to control our immune system, and might even shape our behaviour as we grow up. Perhaps by studying the squid, we’ll learn more about how our own terraformers shape our bodies to their needs.

Reference: Kremer, Philipp, Carpentier, Brennan, Kraemer, Altura, Augustin, Hasler, Heath-Heckman, Peyer, Schwartzman, Rader, Ruby, Rosenstiel & McFall-Ngai. 2013. Initial Symbiont Contact Orchestrates Host-Organ-wide Transcriptional Changes that Prime Tissue Colonization. Cell Host and Microbe http://dx.doi.org/10.1016/j.chom.2013.07.006

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When Our Microbes Chat, Dangerous Germs Are Eavesdropping

In Africa, a superb starling has just spotted an eagle and gives off an alarm call. Any starling within earshot goes on high alert, but so do nearby vervet monkeys. They have learned to eavesdrop on the starling’s calls to gain extra intelligence about incoming threats.

They’re not alone. Mongooses listen in on the calls of hornbills, black-capped chickadees act as inadvertent sentries for up to 50 species of birds, and lemurs tune into the soundtracks produced by forest birds. Eavesdroppers, it seems, are everywhere. They’re even found inside your bowels.

Your guts are home to tens of trillions of microbes, which help to digest your food, control your immune system, and protect you from invasions by disease-causing germs. They also communicate with each other, but through chemicals rather than sound.

For example, when threatened by antibiotics, the gut bacteria Escherichia coli release a substance called indole, which toughens them up. It prompts them to mass-produce molecular pumps that can evict any drugs that get inside them. They start building slimy cities called biofilms to fortify themselves against incoming antibiotics. And perhaps most importantly, some of them enter a dormant, inactive state. Since all of our antibiotics are designed to kill growing bacteria, these sleeper cells slip right under their radar. They’re called  persisters, are they’re extremely hard to kill.

Nicole Vega from Boston University discovered the link between indole and persistence last year. Now, she has shown that another bacterium—Salmonella typhimurium, a major cause of food-related illness—can eavesdrop on E.coli’s indole signals.

It doesn’t make any indole of its own, but it responds to the chemical in the same way as E.coli. Vega, with help from Amanda Samuels, showed that S.typhimurium becomes over three times more tolerant of certain antibiotics when grown alongside E.coli. And they only gained this advantage when Vega seeded the cultures with tryptophan—the substance that E.coli needs to make indole.

These experiments were done in glass flasks, but the team also challenged the bacteria in a more realistic environment—the guts of a nematode worm. Vega loaded the worms with S.typhimurium, and either normal E.coli or a mutant strain that couldn’t make indole. When she then added an antibiotic, she found that S.typhimurium tolerated the drug more easily if it sat alongside indole-making E.coli, rather than the mutant strain.

Like the vervets and lemurs, S.typhimurium intercepts signals used by a different species to ensure its own survival. Such eavesdropping might be very common. Indole is a widespread signal among bacteria, and might help different species to communicate with each other. Indeed, both E.coli and S.typhimurium do so by activating the same set of genes, which suggest that even species that have lost the ability to make indole have kept the machinery they need to respond to it. And that could spell trouble for us, allowing harmful bacteria to fortify themselves against our medicines by listening in on the chemical chatter of our microbial allies.

Reference: Vega, Allison, Samuels, Klempnerd & Collins. 2013. Salmonella typhimurium intercepts Escherichia coli signaling to enhance antibiotic tolerance. PNAS http://dx.doi.org/10.1073/pnas.1308085110


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How the World’s Smallest Farmers Turned Chemists Into Food

Wild grasses, like wheat, rice and barley, have long stalks that shatter to spread their seeds over the surrounding soil. But this doesn’t always work. A small number of genetic changes (mutations) can lead to shatter-proof stalks, whose seeds stay in place. These mutations are bad for the plant, but they’re spectacularly convenient for humans because they concentrate seeds in one easy-to-harvest place.

When our ancestors collected these mutant grains, they spilled some on the way back to camp, or excreted the seeds on their latrines. They might even have planted some deliberately. Either way, those shatterproof mutations—typically, one per crop—became some of the most critical in human history. They allowed us to domesticate the plants that fuelled the agricultural revolution, and that still feed the majority of the world today.

But this wasn’t the first or only time that small genetic changes gave rise to agriculture.

A social amoeba called Dictyostelium discoideum—let’s call it Dicty—carries bacteria inside it, which provide it with useful chemicals. But with just one mutation, these bacteria start making a different set of substances that make them more edible. Through one little change, these chemists turned into food, and the amoebas became the world’s smallest farmers.

Dicty spends most of its life as a single amoeba-like cell that feeds on bacteria. When their food runs out, many of these cells ooze towards each other and merge into a many-celled slug. When the slug gets big enough, it stretches skywards into a long stalk, tipped with a spore-filled capsule. The capsule eventually breaks and scatters its spores to the wind. When these land, they hatch into new amoebas, and the cycle starts anew.

In 2011, a team of scientists including postdoc Debbie Brock, now at Washington University in St Louis, discovered that Dicty is also a farmer. Many of the amoebas carry edible bacteria inside them. When they land in a new spot, they seed their environment with this livestock, starting their new lives with a ready supply of food.

But Dicty only eats half of these bacteria. The rest are apparently inedible. Why would the amoebas carry such passengers?

Brock, together with postdoc Pierre Stallforth, have now discovered the answer. The inedible bacteria produce at least two beneficial chemicals that the edible ones don’t. The first—pyrrolnitrin—kills soil-living fungi, including those that cause disease. The second—a newly discovered substance called chromene—helps Dicty to make more spores.

But Stallforth and Brock also found that these inedible bacteria are virtually identical to the edible ones—they’re both different strains of the same species, Pseudomonas fluorescens. The only thing that separates them is a single mutation that’s found in the edible bacteria, which disables a gene called GacA. When the team deleted the gene from the inedible strains, they stopped producing pyrrolnitrin and chromene, and they started serving as food.

The team think that this lone GacA mutation radically changed the nature of P.flourescens’s partnership with Dicty, changing it from a purveyor of helpful chemicals into a food source. It’s not clear why it suddenly became edible, but GacA supervises many other genes and perhaps some of these are responsible.

Whatever the reason, it’s certainly a bizarre situation—some strains of P.flourescens have actually evolved to be more easily eaten by their host. That’s probably because Dicty carries their clone siblings to new locations. Sure, some cells may die, but the rest can prosper in their new homes. It’s the same story for rice and wheat. Their shatter-proof mutations made them easier food for humans but also catalysed their success, as we started planting them all over the world.

Humans and Dicty aren’t the only farmers around. Leafcutter ants grow gardens of fungi using sliced-up leaves. They also harbour antibiotic-secreting bacteria on their bodies, which they use to protect their crops from diseases. Meanwhile, ambrosia beetles sow gardens of fungi on trees, and also defend their crops using bacterial pesticides.

Dicty does something very similar. Like the ants and beetles, it also partners with an edible crop and an antibiotic-producer. But in its case, these partners are virtually the same—two strains of the same microbe, separated by the tiniest of differences.

Reference: Stallforth, Brock, Cantley, Tian, Queller, Strassmann & Clardy. 2013. A bacterial symbiont is converted from an inedible producer of beneficial molecules into food by a single mutation in the gacA gene. PNAS http://dx.doi.org/10.1073/pnas.1308199110

Update: I originally credited the initial discovering of Dicty farming to Jon Clardy, who only became involved in this latest study. Apologies to Dr Brock.

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Ant Bodyguards Get Exclusive Contract from Trees

If animals and plants can’t defend themselves, they often form partnerships with bodyguards. Wasps use zombified caterpillars. Corals recruit goby fish. And acacia trees hire ants. The ants defend the trees against hungry mouths by biting and stinging any invading plant-eaters. Some are so ferocious that they can deter elephants. In return, the trees pay their bodyguards by providing shelter in the form of swollen thorns, and food in the form of nectar or nutritious parcels called “food bodies”.

This alliance between ants and acacias is a staple of textbooks, but it’s even more intimate than anyone suspected. Some acacias don’t just supply their ants with any old food. They offer the biological equivalent of a cheque—a reward that only the ants can cash.

Every partnership is vulnerable to thieves. The acacia’s bright, nutritious food bodies could easily be pilfered by any insect quick enough to avoid the patrolling ants. But insects that steal them are in for a poor and possibly dangerous meal.

Domancar Orona-Tamayo from CINVESTAV-Irapuato in Mexico and Natalie Wielsch from the Max Planck Institute for Chemical Ecology in Germany found that the food bodies of two acacia species are loaded with molecules called protease inhibitors. As their name suggests, these block enzymes called proteases, which animals use to digest the protein in their food.

These acacia enzymes were extremely good at neutralising the proteases of two species of seed-eating beetles, slashing their protein-busting abilities by more than 98 percent.

Pseudomyrmex ferruginea—one of the ants that guards the acacia—has no such problems. Its guts are dominated by a special protease called chymotrypsin-1, which the acacia’s protease inhibitors do not inhibit. When these bodyguards eat the food bodies, they get a nutritious reward. When beetles try to do the same, they get indigestion.

The protease inhibitors aren’t found throughout the acacia, just in the food bodies. They are security measures that protect the tree’s rewards by harming would-be thieves. Only the ants can bypass these defences, and only the right ants at that.

Pseudomyrmex ferrugineus, by April Nobile. Via AntWeb
Pseudomyrmex ferrugineus, by April Nobile. Via AntWeb

Orona-Tamayo and Wielsch found that Pseudomyrmex gracilis—a species that exploits the acacia’s rewards without ever lifting a mandible to defend it—isn’t quite as well-equipped as the P.ferrugineus. It has some chymotrypsin-1, but also plenty of other proteases that are inactivated by the acacia’s neutralising enzymes.  It gets something out of the food bodies, but not as much as the tree’s true partner.

There are other examples in the natural world of alliances where partners lock each other into exclusive contracts. Some do it physically. Many flowers hide their nectar at the bottom of long tubes that only the right pollinators can reach them, whether they’re long-billed hummingbirds or long-tongued flies.

In these cases, it’s clear that the flowers and their pollinators evolved alongside one another. As nectar tubes got longer, so did bills and tongues, until both fit together like locks and keys. Is the same true for the acacia and the ant? It’s possible, but the team suspects that both partners came prepared for exclusivity.

The acacia uses the same protease inhibitors as many other related plants, and many ants and spiders* have chymotrypsin-1 in their guts. The tree eventually concentrated its inhibitors into its food bodies, while its ant partners emphasised chymotrypsin-1 and downplayed other proteases. They were already a good match from the start. They just became closer over time.

*This might be why the world’s only vegetarian spider, Bagheera kiplingi­­, can get away with eating acacia food bodies.

Reference: Orona-Tamayo, Wielsch, Blanco-Labra, Svatos, Farias-Rodriguez & Heil. 2013. Exclusive rewards in mutualisms: ant proteases and plant protease inhibitors create a lock–key system to protect Acacia food bodies from exploitation. Molecular Ecology http://dx.doi.org/10.1111/mec.12320

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Groupers Use Gestures to Recruit Morays For Hunting Team-Ups

The giant moray eel can grow to three metres in length and bites its prey with two sets of jaws—the obvious ones and a second set in its throat that can be launched forward like Hollywood’s Alien. It’s not a creature to be trifled with. But the coral grouper not only seeks out giant morays, but actively rouses them by vigorously shaking its body. The move is a call to arms that tells the moray to join the grouper in a hunt.

The two fish cooperate to flush out their prey. The grouper’s bursts of speed make it deadly in open water, while the moray’s sinuous body can flush out prey in cracks and crevices. When they hunt at the same time, prey fish have nowhere to flee.

Redouan Bshary from the University of Neuchatel in Switzerland discovered this partnership in 2006. He usually studies cleaner wrasse, which pick parasites off larger fish. When tracking groupers to see if they patronised several cleaners, Bshary noticed one of them rousing a moray. They also team up with the humphead wrasse—a huge human-sized fish whose extensible jaws can suck prey out from cracks. It too complements the grouper’s open-water skills.

Bshary was fastidious in recording his grouper observations—all 187 hours of them. He also took several films and when Alexander Vail from the University of Cambridge watched them, he noticed something Bshary had missed. The groupers always summoned the wrasses and morays with a vigorous shimmy, but they also used a second, much rarer signal—a headstand, combined with head-shaking. Vail thinks it was a signal, one that said: “The prey’s in here, guys!”

When doing their headstands, the groupers always swam over the location of hidden prey that they had failed to catch. They only used the move when a moray or wrasse was nearby, continued to do so until one arrived, and stopped as soon as one did.

Most morays and all wrasses headed towards the grouper’s location when they saw the signal, causing the prey to break their cover. (The fact that the prey didn’t abandon their hiding spots beforehand shows that the headstand itself isn’t a hunting tactic.) And when the morays ignored the headstand, the groupers actually swum after their partner and either performed their “recruitment shimmy” or forcibly tried to push the eels in the right direction.

To Vail, the headstand has all the hallmarks of an attention-grabbing “referential gesture”, like a human pointing at an object. It’s directed at a ‘listener’, draws attention to an object of interest, triggers a response, and has no other purpose beyond being a signal. It also seems like something the grouper intends to do, rather than a random movement that coincidentally summons a moray—after all, if the signal doesn’t work, the grouper gives up and attracts the eel through other means.

The team also found that another reef fish—the coral trout—uses the same signal to team up with octopuses! The partners have the same set of complementary skills as the grouper and moray—the trout chases exposed prey and the octopus grabs hidden ones.

If this really is a referential gesture, that’s an important discovery. Such gestures are part and parcel of human life, but the only animals that seem to use them are intelligent ones, like chimps and other great apes, ravens, dolphins, and domestic dogs. In fact, the discovery of gestures in ravens was taken as further evidence of their impressive mental abilities.

But Vail and Bshary believe that intelligence is a red herring. The grouper and trout use gestures, and while they may be more intelligent than we give them credit for, it’s very unlikely that they rival apes. Instead, they evolved to use gestures simply because they benefit from coordinated cooperation with other species. Their gestures are driven by needs not smarts. They remind us once again that complex behaviour doesn’t necessarily imply complex minds.

Reference: Vail, Manica & Bshary. 2013. Referential gestures in fish collaborative hunting. Nature Communications. http://dx.doi.org/10.1038/ncomms2781

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Do chimpanzees care about fairness? The jury’s out

A stranger gets a pot of money and offers you a share of it. If you accept the offer, both of you walk away with your proposed shares. If you reject, you both leave with nothing.

This is the ultimatum game—a classic psychological experiment used to study fair play. If both players behave completely selfishly, the proposer might offer as little as possible, while the responder should accept any offer as long as it’s not zero. That way, both of them walk away with something. In practice, responders typically reject any offers less than 20 percent. They care enough about fairness to do themselves out of money in order to punish unfair partners. Meanwhile, proposers from industrialised countries, who are wary of social norms and the potential for punishment, tend to offer between 40 and 50 percent of the pot.

But what about chimpanzees? Do our closest relatives also share our attitudes to equality? Darby Proctor from Georgia State University thinks so. She modified the ultimatum game so that chimps and human children could play it in the same way. In both cases, when proposers needed to cooperate with responders, they became more likely to offer an equal split, rather than trying to hog the rewards for themselves. The conclusion: “humans and chimpanzees show similar preferences regarding reward division, suggesting a long evolutionary history to the human sense of fairness.”

But her study has prompted stern criticism from scientists who have also tested chimps at the ultimatum game and found the opposite. In their studies, our fellow apes did not make fair offers and accepted anything as long as it was greater than zero.

This debate reflects a growing divide between scientists who study chimpanzees, but it is more than an academic spat. It speaks to a fundamental question about our evolution: is our sense of fairness a uniquely human trait, or one that we share with our closest kin?

Old male chimp, by Prabir Kumar Bhattacharyya

The experiments

Keith Jensen, Josep Call and Michael Tomasello were the first to play the ultimatum game with chimps. In their experiments, two chimps sat in adjacent cages, facing a contraption with two sliding trays. Each tray contained one dish on the proposer’s side and another on the responder’s side, and the two dishes carried varying numbers of raisins. The proposer made an offer by using a rope to pull one of the two trays half-way over. The responder could accept this offer by pulling the tray the rest of the way, allowing them both to eat their respective raisins. Alternatively, they could reject the offer by doing nothing, leaving both animals unfed.

The team found that the proposers were likely to choose the tray that gave them the most raisins, and the responders tended to accept any offer, no matter how unbalanced. They wrote that “in this context, one of humans’ closest living relatives… does not share the human sensitivity to fairness.” And in a second study, the team found that our other close relatives—the bonobos—behaved in a similar way.

But Proctor was unimpressed by the team’s set-up. She felt that the “complex mechanical apparatus” was unlike anything that humans use when we play ultimatum games, and may have been too complicated for the chimps to understand. And while humans usually play for money, which is exchanged for other rewards, the chimps were playing for food, which is immediately rewarding.

In her version of the ultimatum game, two chimps play for tokens that are exchanged for six bananas laid out in front of them. A human experimenter offers two tokens to the proposer chimp, one signifying an equal banana split and the other signifying an unequal 5:1 divide. The proposer picks one token and passes it to a responder in an adjoining cage. They can drop the token to reject the offer, or pass it back to the experimenter to accept.

Proctor played the game with three pairs of chimps, one of which swapped roles as proposer and responder. She found that two of the proposers chose the equal-split token more often than expected by chance. And all four of them chose that token more often in the ultimatum game than in a straight preference test, when their choice dictated their reward irrespective of what a responder did. Proctor concluded that when chimps need to cooperate to get a reward—that is, when the proposer depends on the responder—they change their behaviour to favour the fairer option. Young children, aged two to seven, behaved in the same way.

Margot, an orphaned chimpanzee from a sanctuary in Cameroon. By Daniel Bergin

So what does that mean?

The obvious criticism is that Proctor’s study only included six chimps, and only the two animals who played both roles offered the equal token more often than expected by chance. Proctor admits that the numbers were small, but says that these were the only chimps that passed her rigorous pre-tests and clearly understood the nature of the game.

But Jensen disputes Proctor’s claim. He is glad that another team tried to replicate his results, since “one can only conclude so much from one or two studies,” but says that Proctor’s experiment was no ultimatum game. The most important aspect of the ultimatum game is not what the proposer does, but how the responder reacts,” he says. The proposer’s offers are strategic rather than a sign of fairness—they’re a reaction to what the responder might do. It’s the responder’s ability to reject unequal offers that drives fairness in the game.

And among Proctor’s chimps, no responder ever refused an offer, even the many unfair ones. That’s even less rejection than in Jensen’s study. “Not rejecting unfair offers is puzzling if chimps are really playing the ultimatum game,” says Call. “I see that as a fatal flaw,” adds Jensen. At best, it confirms his original experiment by showing that the responders are insensitive to unfairness and only motivated by getting bananas. At worst, it shows that they didn’t understand the task.

Proctor counters that she did extensive tests to be as sure as possible that the chimps understood what the tokens meant. She admits that she did not explicitly train the chimps that they could refuse offers, but says, “This actually makes our results more striking. Without experiencing a refusal, proposers changed their behaviour to be more equitable. They may be responding to the potential for refusals as do adult humans.”

Jensen doesn’t buy it. “There isn’t the tiniest shred of evidence that proposers understood that responder could reject their offers, and no demonstration that responders understood anything of the possible consequences of their choices,” he says.

David Rand, a psychologist from Harvard University who has used the ultimatum game in human studies, agrees with Jensen’s criticisms. While Proctor’s set-up does look like an ultimatum game, “it looks like maybe the chimps didn’t understand the game structure,” he says.

Jensen thinks that this confusion arose because Proctor’s task is not as simple as she claims. Unlike human ultimatum games, where players interact with each other, Proctor’s chimps spent as much time exchanging tokens with humans. “Passing a token is just an intermediate step to getting food from experimenters, something they are highly trained to do,” says Jensen. He doubts that this set-up, which involved tokens exchanging hands three times, is truly simpler than his tray-pulling machine.

The verdict

As Proctor notes, there are many reasons to suspect that chimps care about equality. They help one another, share food, and cooperate extensively to hunt, fight, patrol, defend, and more. But it’s difficult to interpret wild anecdotal behaviour, which is why experiments are valuable.

None of the existing studies is perfect. In all the chimp ultimatum games, the animals could only reject offers passively, by not pulling a tray or not handing over a token; in human games, rejection is an active choice. In the chimp games, the animals could see each other, and played multiple rounds with the same partners; in human games, partners usually play single rounds anonymously to stop social dynamics and reputations from clouding the results.

Given these shared weaknesses, Proctor’s team is right that Jensen’s studies don’t prove that chimps are insensitive to fairness even though they support that hypothesis. After all, absence of evidence is not evidence for absence. But equally, the problems in Proctor’s study prevent it from confirming that chimps are sensitive to fairness. Until more research is done, we’re at an impasse.

Reference:  Proctor, Williamson, de Waal & Brosnan. 2013. Chimpanzees play the ultimatum game. PNAS http://dx.doi.org/10.1073/pnas.1220806110

Note: This study was “contributed” to PNAS by co-author Frans de Waal, a publishing route where members of the National Academy of Sciences can nominate their own peer-reviewers. I try to avoid papers that use this track but did most of the reporting before I noticed, so here’s the piece anyway.

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Corals Summon Gardening Gobies to Clean up Toxic Seaweed

For corals, gardening’s a matter of life and death. Corals compete with algal seaweeds for space, and many types of seaweed release chemicals that are toxic to corals, act as carriers for coral diseases and boost the growth of dangerous microbes. These dangers require close contact—the seaweed poisons won’t diffuse through the water, so they need to be applied to the corals directly. And that gives the corals an opportunity to save themselves. When they sense encroaching seaweed, they call for help.

Danielle Dixson and Mark Hay from the Georgia Institute of Technology have found that when Acropora corals detect the chemical signatures of seaweed, they release an odour that summons two gardeners – the broad-barred goby and redhead goby. These small fish save the corals by eating the toxic competitors. In return, one of them stores the seaweed poisons in its own flesh, becoming better defended against its own enemies.


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Not a hug hormone – fish version of oxytocin acts as social spotlight

If there’s any molecule that is consistently viewed through rose-tinted glasses, it’s oxytocin. This simple hormone has earned misleading but charmingly alliterative nicknames like “hug hormone”, “cuddle chemical” and “moral molecule”. Writers love to claim, to the point of absurdity, that oxytocin increases trust, generosity, cooperation and empathy, among a slew of other virtues.

But while these grandiose claims take centre-stage, a lot of careful science plods on in the background. And it shows that oxytocin affects our social interactions in both positive and negative ways, depending on the situation we’re in, or our personality and disposition. It can fuel conformity as well as trust, envy as well as generosity, and favouritism as well as cooperation. If we sniff the stuff, we might, for example, become more cooperative towards people we know, but less so towards strangers.

These lines of evidence might seem contradictory, but only if we hold the naive view that oxytocin is a chemical force for good. Instead, many scientists have suggested that, rather than some positive panacea, it’s more of a general social substance. It directs our attention towards socially relevant information – everything from facial expressions to posture – or drives us to seek out social interactions.

Now, Adam Reddon from McMaster University has found more evidence to support this idea by studying the daffodil cichlid, a beautiful African fish. When he injected them with isotocin – the fish version of oxytocin – he found that they became more responsive to social information. They were more sensitive to an opponent’s size before a fight, and they behaved more submissively when they themselves were challenged.