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Evolution and Biodiversity

Category: aid

Amputation saves ant lives

9 July 2024 /

Florida carpenter ant workers treat leg wounds effectively

Workers of Florida carpenter ant amputate legs when useful

Injured leg? In the Florida carpenter ant, Camponotus floridanus, nestmates treat the patient to prevent lethal infections. If it is useful, they amputate the leg, Erik Frank and colleagues write.

With a wound on a leg, a worker of the Florida carpenter ant, Camponotus floridanus, would have only a small chance to survive if it were not for her nest mates that come to the rescue. To prevent infection, they lick the wound clean and often amputate the leg, significantly increasing the survival chance, Erik Frank and colleagues show. This care is frequently needed because colonies of this ant species fight each other intensively.

The researchers tested the ants’ medical skills by making a small cut in the leg of workers. They then injected a saline solution containing a deadly bacterium, Pseudomonas aeruginosa, into the wound. Infected ants were placed either in isolation or in a nest where two hundred workers were available.

Bitten off

Most of the ants that sat alone after infection succumbed to the injuries. But when placed in a nest, most ants did survive thanks to the care of nest mates. What care they provided turned out to depend on where the wound was.

If the infected wound was on the upper leg, usually one of the nest mates intervened drastically and bit off the leg at the top. If the wound was on the lower leg, this did not happen; instead, workers licked the wound thoroughly clean. In both cases, helpers chose the treatment that was most effective, as became clear in experiments with infected wounds in which the researchers amputated the affected leg.

Bacterial load

If they amputated a leg of an ant with a wound on the upper part, then her chance to survive was as high as it was in the case of amputation by nestmates. But if they removed a leg with an injury on the lower part, it did not help: most patients died. The treatment that the ants apply in that case, extensive cleaning, is much more effective.

Why is amputation only helpful for an infection in the upper leg?

Whether an ant will survive an infection depends on how quickly the bacteria are able to spread through the body: the higher the bacterial load, the higher the mortality. The bacteria spread via the hemolymph, the insect version of blood, which flows through the legs in channels.

In the upper leg, these channels are narrower than in the lower leg, so that bacteria are less likely to enter the hemolymph. Also, the upper leg has much more muscle mass than the lower leg, and blood is pumped around by muscle movements. If the upper leg is affected, circulation is slowed down much more than if the lower leg is affected, impeding the spread of bacteria.

Time enough

Consequently, when the upper leg is affected, ants have enough time to perform an amputation, which takes forty minutes at least, before the bacteria have spread. But timely amputation is unfeasible with an infection in the lower leg. Then cleaning is the best way to help a victim.

The ants also amputated the leg if the researchers injured the upper leg but injected a sterile saline solution instead of a solution with bacteria. That makes sense, because under natural conditions, in the ants’ nest, such a wound is most likely to become infected. The workers err on the side of caution.

The Florida carpenter ant is the only animal species known to apply amputation to treat conspecifics in case of injury.

The researchers previously discovered that also workers of the Matabele ant from Africa, Megaponera analis, treat infected wounds of nestmates. They do so by administering antibiotics from glands on their backs that produce a mix of antimicrobial substances. The Florida carpenter ant does not have such a built-in pharmacy. For this ant, cleaning and amputation are good alternatives.

Willy van Strien

Illustration: ©Hanna Haring

See also: the Matabele ant fights infections with self-made antibiotics

Source:
Frank, E.T., D. Buffat, J. Liberti, L. Aibekova, E.P. Economo & L. Keller, 2024. Wound-dependent leg amputations to combat infections in an ant society. Current Biology, 2 July online. Doi: 10.1016/j.cub.2024.06.021

Coordinated rolling

22 January 2024 /

Dung ball roller female helps male when things get difficult

Dung ball roller Sisyphus schaefferi: male pulling and female pushing dung ball

Together, a male and female dung ball roller are able to transport a dung ball over a path with obstacles. He leads, she moves along and assists where necessary, Claudia Tocco and colleagues show.

Dung ball rollers (Sisyphus species) have a striking habit. The dung beetles form pairs, take a piece of mammal droppings, construct a ball larger than themselves and roll it away in a straight line to make sure not to collide with other pairs that have taken a part of the same dung pile. When, often after demanding work, they arrive at a suitable place, they bury their ball in the soil together with an egg. The larva that will hatch from the egg is surrounded by excellent food.

Claudia Tocco and colleagues wanted to know more about the harmonious cooperation that male and female exhibit. They investigated how partners divide tasks in two species: Sisyphus fasciculatus from South Africa and Sisyphus schaefferi, that lives in North Africa, Southern Europe, and Asia Minor. In an outdoor test setup, they offered cow dung to groups of dung ball rollers. The beetles formed pairs, constructed a dung ball and started rolling.

Backwards

The male, which is slightly larger than the female, is always the one driving the dung ball transport, as the researchers saw. He determines the course. He walks backwards and pulls the dung ball with his front legs. His partner walks on the other side, also backwards, with her head down and her hind legs on the ball. On flat terrain, she contributes nothing. If the male stops rolling, she also stops. So, you never see a female dragging a dung ball by herself. Conversely: if she stops, he goes on alone, rolling the dung ball as quickly and staying on course as well as a couple.

Mostly, she does move along, maintaining contact with the ball. Consequently, she can help immediately when things get difficult. And they do, because Sisyphus fasciculatus and Sisyphus schaefferi live in woodlands and forests, with all kinds of objects lying on the ground. A couple of dung ball rollers often encounters obstacles. The researchers conducted experiments to simulate these situations to see how the pair cleared them.

First, they placed two 2.6 centimeter high obstacles one behind the other on the path. That is quite a challenge, because a dung ball roller is less than a centimeter long. At these obstacles, the female no longer followed passively, as it turned out, but assisted by pushing or steering, and as a result, a pair cleared the double obstacle faster than a male working alone. Moreover, a male alone often gave up.

Climbing

In a next series of experiments, the beetles were challenged with a wall of 3.9, 6.5 or 9.1 centimeters high. The higher the wall, the less likely a pair was to climb over it with the ball and the less likely it was to succeed if it tried. A male alone declined more often than a pair, but if he tried to clamber over the wall, he usually succeeded.

A couple could get over a high obstacle faster than a male alone, mainly because the female helped at the start. When the male pulled himself up along the wall and lifted the dung ball from the ground, she stabilized the ball with her hind legs and pushed it, in a headstand position. Then he worked his way up, while she hung on the ball. Despite that extra burden for the male, a pair climbed as quickly as a male alone. If he was in danger of falling, she would provide support. Once she got to the top, she became active and pushed the ball over the edge with her head. The beetles then fell down and continued their path.

Punishment

Dung ball rollers manage to get their ball over difficult obstacles. Unlike the Greek mythical king Sisyphus, after whom the beetles are named. Because of his brutality towards the gods, he was punished by having to push a boulder up a slope in the underworld for eternity, while the boulder kept falling back. He could not do it alone and he did not have a partner to lend a hand.

Willy van Strien

Photo: Sisyphus schaefferi couple with dung ball, male at left side, female at right side. Daniel Ballmer (Wikimedia Commons, Creative Commons, CC BY-SA 4.0)

Watch the dung beetles’ behaviour on YouTube

Sources:
Tocco, C., M. Byrne, Y. Gagnon, E. Dirlik & M. Dacke, 2024. Spider dung beetles: coordinated cooperative transport without a predefined destination. Proceedings of the Royal Society B 291: 20232621. Doi: 10.1098/rspb.2023.2621
Dacke, M., E. Baird, B. el Jundi, E.J. Warrant & M. Byrne, 2021. How dung beetles steer straight. Annual Review of Entomology 66: 243-256. Doi: 10.1146/annurev-ento-042020-102149

Pharmacy on back

11 January 2024 /

Matabele ant heals infection of injured conspecifics

Matabele ant with a mouthful of termites

Workers of the Matabele ant treat infected wounds of nest mates with self-made antibiotics, Erik Frank and colleagues saw. That saves the lives of those nest mates.

Groups of Matabele ants (Megaponera analis) hunt termites, which fight back fiercely. Consequently, foraging trips cause many casualties. An ant colony would perish if it were not for the fact that ‘slightly’ injured specimens, for instance ants that lost one or two legs, are picked up and carried back to the nest. Thanks to the care they receive there, most of them recover from their injuries; without help, they would be dead within 24 hours in all probability.

Erik Frank and colleagues previously discovered that workers lick and groom the wounds immediately after arrival in the nest. Now, it appears that they also treat the wounds medically. The Matabele ant lives in Africa south of Sahara; the research was done in Ivory Coast.

Antibiotics

Video recordings in artificial nests in the lab show that workers groom victims’ wounds again after 10 to 12 hours, and then often apply a substance after cleaning that they take from glands on the back, the metapleural glands. They use their own glandular product or that of the wounded individual. They mainly treat ants with wounds that have become infected, for example with the deadly bacterium Pseudomonas aeruginosa.

The glands of the Matabele ant form a well-supplied pharmacy. They turn out to produce more than a hundred compounds, many of which have an antimicrobial or healing effect. Tests show that the antibiotic mix suppresses the growth of the bacteria. Most other ant species also have metapleural glands, but with a less extensive arsenal of substances.

Unique

How do nursing workers know whether a wound is infected or not? Probably because the composition of the outer layer that ants have – a waxy layer of hydrocarbons – changes during infection. Colony mates can smell that.

Conclusion: Matabele ant workers can effectively treat wounds of conspecifics with self-made antibiotics. This ability is unique among insects and other invertebrates.

Willy van Strien

Photo: Matabele ant worker with termites. ETF89 (Wikimedia Commons, Creative Commons CC BY-SA 4.0)

Former research on Matabele ant

Source:
Frank, E.T., L. Kesner, J. Liberti, Q. Helleu, A.C. LeBoeuf, A. Dascalu, D.B. Sponsler, F. Azuma, E.P. Economo, P. Waridel, P. Engel, T. Schmitt & L. Keller, 2023. Targeted treatment of injured nestmates with antimicrobial compounds in an ant society. Nature Communications 14: 8446. Doi: 10.1038/s41467-023-43885-w

Purple-crowned fairywren assists dear breeders

23 November 2023 /

Subordinate works not always equally hard

purple-crowned faiywren helps parent and potential partner

Purple-crowned fairywrens living with breeding parents often help raise offspring. A subordinate works hardest when father or mother has a new, valuable partner, Niki Teunissen and colleagues show.

The number of territories available is limited for purple-crowned fairywren, a small passerine bird that lives in northern Australia in dense vegetation along rivers and creeks. The territories are linearly aligned, are kept all year round and are all occupied. Out of necessity, young birds often stay with their parents for a few years; most breeding pairs have a few male and female subordinates around them. Purple-crowned fairywrens, Malurus coronatus, eat insects; males have a beautiful purple crown during the breeding season.

Subordinates can assist the breeding pair during the busiest time, the two weeks when the young need to be provisioned. But not all of them offer help, and not all helpers work equally hard. Group members that don’t help are still allowed to stay in the group. Niki Teunissen and colleagues investigated under which circumstances group members do or do not help well. They show that a purple-crowned fairywren subordinate ‘knows’ precisely when it pays to be helpful.

The researchers provided birds with colour rings to make them individually recognizable and of each bird, they knew its parents and its brothers and sisters. They observed the behaviour of fifty groups during three breeding seasons.

Brothers and sisters

If young in the nest have the same parents as a subordinate, or share one parent with it, that subordinate will help feed them. And that is worth the effort. Because with help, more young fledge per clutch on average. A helper shares in this greater success, because those young are full siblings or half-siblings. But in the few years that children stick around, both parents may have died or disappeared and been replaced. And sometimes young birds do not join their parents, but another couple. In such cases, the young are unrelated and a subordinate will not help raise them.

Kinship with the young does not fully explain the willingness to help, though, because, on average, group members work harder for a clutch of half-brothers and half-sisters than for a clutch of full brothers and sisters. That seems enigmatic, but something else is going on. Whether a subordinate will support a breeding pair and how hard it will work, also depends on the value that the pair itself has.

Main prize

When both the breeding male and female are not its parents, it is not going to help feed the young, as we already saw. If both are its parents, it will help; the young are then full siblings. Thanks to this help, the parents reduce their workload. Their chance of survival increases, and so does the chance that a new clutch of brothers and sisters will be produced. This is also a win for the helper.

Things get interesting, the researchers discovered, when one parent is gone and the other parent has a new partner. How hard a resident purple-crowned fairywren will work now depends on which parent is left: the same-sex parent or the other one.

A female purple-crowned fairywren living with her mother and her new partner works much harder than a subordinate in a group with both parents. That is because that new male partner is interesting. If her mother dies, the helper may inherit her place and her partner, become the owner of the territory and produce the next clutch. That’s the main prize!

With a father and a new partner, she has less to gain. That new female partner is of no use to her, in fact: she is a rival if a new male ever comes into play. So, she works less hard.

Likewise, a male fairywren puts in most effort in helping when living with a father with a new partner.

Sophisticated

And therefore, a subordinate purple-crowned fairywren works hardest when the breeding pair consists of a parent and a potential mate – which is very sophisticated. Such couple has great value to him or her. That is why he or she often helps provisioning a nest with half-siblings more intensively than a nest with full siblings.

In line with this, the researchers had previously shown that a young purple-crowned fairywren is less willing to join a group with a same-sex stepparent. Subordinates affiliate with parents and a potential mate. Also, when they help defend the nest against predators, it is to protect (half)siblings as well as parents and a potential mate.

Willy van Strien

Photo: Female (left) and male purple-crowned fairywren. P. Barden (Wikimedia Commons, Creative Commons CC BY 4.0)

Sources:
Teunissen, N., M. Fan, M.J. Roast, N. Hidalgo Aranzamendi, S.A. Kingma & A. Peters, 2023. Best of both worlds? Helpers in a cooperative fairy-wren assist most to breeding pairs that comprise a potential mate and a relative. Royal Society Open Science 10: 231342. Doi: 10.1098/rsos.231342
Teunissen, N., S.A. Kingma, M. Fan, M.J. Roast & A. Peters, 2021. Context-dependent social benefits drive cooperative predator defense in a bird. Current Biology 31: 4120-4126. Doi: 10.1016/j.cub.2021.06.070
Teunissen, N., S.A. Kingma, M.L. Hall, N. Hidalgo Aranzamendi, J. Komdeur & A. Peters, 2018. More than kin: subordinates foster strong bonds with relatives and potential mates in a social bird. Behavioral Ecology 29: 1316-1324. Doi: 10.1093/beheco/ary120
Kingma, S.A., M.L. Hall, E. Arriero & A. Peters, 2010. Multiple benefits of cooperative breeding in purple-crowned fairy-wrens: a consequence of fidelity? Journal of Animal Ecology 79: 757-768. Doi: 10.1111/j.1365-2656.2010.01697.x

Complex cooperation

15 November 2018 /

Weaver ant will rescue nestmate from spider web

a weaver ant on its nest

Floria Uy and colleagues show that workers of the weaver ant care about their nestmates: when an ant gets entangled in a spider’s web, others are willing to help it. The ants were already known for their ‘living sewing machine’.

The weaver ant or green tree ant, Oecophylla smaragdina, is common in the tropical parts of Asia and Australia. Its presence is clearly visible because of its nests, which stand out as balls of leaves in bushes and trees. The arboreal nests are the result of a special piece of group work, involving not only workers, but also larvae.

weaver ants building their nestTo construct a nest, the ants must glue the leaf edges together. Workers will line up, grasp the edges of two leaves (or two pieces of a long leaf) and draw them together. If the distance between the leaf edges is large, they grab each other and form living chains to bridge the gap. By then shortening the chain, they pull the leaf edges towards each other.

 

Living sewing machine

They then attach the edges firmly to each other with a ‘living moveable sewing machine’, as described by Ross Crozier. While many workers hold the leaf edges, others join with a mature larva between their jaws.weaver ants use larval silk to construct the nest The workers stimulate the larvae to spin a silk thread and move them zigzag between the leaf edges, stitching the leaves together.

In many ant species, larvae spin silk to make a cocoon in which they pupate. But in the weaver ant, their silk is used for nest construction.

A colony of weaver ants consists of multiple nests in several trees; many ants are running on trails between these nests. In peripheral nests of the colony, soldiers live that guard the boundaries of the territory and defend it against conspecific ants from foreign colonies. On average, a colony will live for eight years and can have as many as half a million inhabitants.

That is a lot, and you would be inclined to think that an ant’s life does not matter that much.

Yet, the ants are concerned when a nestmate that is in danger, Floria Uy and colleagues now show. They discovered a second example of complex cooperation within this species.

Ant in distress

If a weaver ant is trapped in a spider’s web, conspecifics may bite the threads of the web and free the victim, as Uy showed. But an alternative scenario is also possible: ants may attack a worker that is entangled in a spider’s web and kill it. When will the ants rescue a conspecific, and when will they kill it?

Uy, who conducted experiments on the Solomon Islands, put a number of ants next to an ant trail after having wrapped them in spider’s silk; in some cases, the victim was a nestmate of the ants on the trail, in other cases it was from a foreign colony.

She found that ants will always help a nestmate in distress. But for ants from a different colony, the outcome is uncertain: some are rescued, others are killed. That some of them are killed is to be expected: to the residents on the trail, they are intruders and accordingly, they are treated aggressively. The fact that some non-nestmates in distress are helped instead is surprising.

It may be a mistake, the researchers hypothesize. In the study area, ants from neighbouring colonies have a greater chance of being rescued than ants from distant colonies. Ants recognize nestmates and colony mates by smell, and neighbouring colonies may have a rather similar odour.

Willy van Strien

Photos:
Large: weaver ant on nest. Rushen (via Flickr, CC BY-SA 2.0)
Small, middle: workers building the nest. Sean.hoyland (Wikimedia Commons, Public Domain)
Small, below: nest with weaver ants. Bernard DUPONT (via Flickr, CC BY-SA 2.0)

Watch weaver ants building a nest

Sources:
Uy, F.M.K., J.D. Adcock, S.F. Jeffries & E. Pepere, 2018. Intercolony distance predicts the decision to rescue or attack conspecifics in weaver ants. Insectes Sociaux, online Nov. 3. Doi: 10.1007/s00040-018-0674-z
Crozier, R.H., P.S. Newey, E.A. Schlüns & S.K.A. Robson, 2010. A masterpiece of evolution – Oecophylla weaver ants (Hymenoptera: Formicidae). Myrmecological News 13: 57-71

Helpers in the nest

16 March 2018 /

Thanks to helpers, cichlid mothers acquire more food

In Neolamprologus obscurus, young fis stay with their mother to help

When young of the cichlid species Neolamprologus obscurus have grown up, they are allowed to remain in the territory of their mother for a while because of their help. Hirokazu Tanaka and colleagues wanted to know why that help is important.

Neolamprologus obscurus, a cichlid fish that occurs in Lake Tanganyika in Africa, lives in groups in which each breeding female owns a territory along a steep bank, where she has dug out several cavities under stones. In those safe shelters, she spends almost all her time and she uses them for breeding. She guards her eggs and fry, and chases conspecifics out of her territory.

But her grown up young are allowed to stay. They help her defend the territory and maintain the shelters by removing sand that continuously enters from the edges.

Tiny prey

The removal of sand from the shelters is most beneficial to her, Hirokazu Tanaka and colleagues discovered. The shelters not only serve as a safe residence and as a breeding ground, but they are also a means to acquire food. The fish feed on small benthic invertebrates, especially shrimp. These tiny animals move up to the water surface at night to forage, but in the full light of the day they are not safe there and before dawn, they sink back to the bottom to hide in cracks and cavities – such as cavities in which Neolamprologus obscurus lives. The food comes to the fish by itself.

Tanaka shows that the larger a cavity is, the more benthic invertebrates immigrate at dawn. Because of this increased food abundance, it is desirable for a breeding female to have helpers that maintain the shelters and even enlarge them.

Content

Of course, helpers take some of the food that they acquire, so part of the gain is lost for the breeding female. But she still profits, because the more helpers are present to remove sand from the edges of the cavity, the longer those edges can be. And the area and content increase even more: with a double number of diggers, maintaining a cavity with a circumference that is twice as large, the area and the volume become four times larger, and as a consequence, more food is available per fish when more helpers are around.

But there is a limit to the number of helpers a female will tolerate; it will be no more than ten. So, when young fish have become larger, they will disappear from her territory to start for themselves.

Willy van Strien

Photo: Neolamprologus obscurus, helper. ©Hirokazu Tanaka

Sources:
Tanaka, H., J.G. Frommen & M. Kohda, 2018. Helpers increase food abundance in the territory of a cooperatively breeding fish. Behavioral Ecology and Sociobiology 72: 51. Doi: 10.1007/s00265-018-2450-5
Tanaka, H., J.G. Frommen, L. Engqvist & M. Kohda, 2017. Task-dependent workload adjustment of female breeders in a cooperatively breeding fish. Behavioral Ecology 29: 221–229. Doi: 10.1093/beheco/arx149
Tanaka, H., D. Heg, H. Takeshima, T. Takeyama, S. Awata, M. Nishida & M. Kohda, 2015. Group composition, relatedness, and dispersal in the cooperatively breeding cichlid Neolamprologus obscurus. Behavioral Ecology and Sociobiology 69: 169–181. Doi: 10.1007/s00265-014-1830-8

First aid

27 February 2018 /

Hunting ant workers rescue lightly injured nest-mates

termite-hunting ant Megaponera analis rescues lightly-wounded nest-mates

Groups of the African ant Megaponera analis undertake hunting parties that are risky because of the fierce resistance of the termites that are attacked. Some ant workers get injured, but they are carried back to the nest and treated if possible, Erik Frank and colleagues report.

Workers of the large African ant Megaponera analis, also known as Matabele ant, face a heavy task. The ants prey on termites that they detect and overpower at their foraging sites. The ants approach the termites in a column formation consisting of hundreds of individuals. When the first ants reach a site, they wait until all participants have arrived and then they attack. The large individuals, the majors, break open the protective layer of earth that covers the termites’ foraging site; the small ants, the minors, then go inside to seize, kill, and pull out the termites.

Emergency signal

And that is a risky job, as Erik Frank and colleagues write. Termite soldiers with strong head and mandibles will fight fiercely. Some ants, almost all of them being minors, get injured; some ants are bitten off one or more legs or antennas, others are hindered by a termite that clings to them.

The ants limit losses by rescuing many injured nest-mates. After the fight, the ants gather before they jointly return to the nest, because an ant travelling alone easily falls prey to predators, for example spiders. Majors run over the place to pick up and carry dead termites and nest-mates that lag behind. If all ants have joined the column, they start walking. But ants that lost one or two legs and ants with a termite clinging to them are unable to keep up with the group, according to observations and experiments in the field and in the lab. By excreting certain substances they signal to others that they need help.

Majors that are not yet carrying anything will pick up these lightly-injured nest-mates, which tuck in their legs to facilitate transportation.

Ants who are severely injured and can no longer stand on their legs, don’t emit an emergency signal and they don’t let themselves to be picked up: they keep on twisting and turning. These unhappy ants are left behind, so that only victims that have a chance to recover are taken home. Almost all of them safely reach the nest, whereas without help many injured ants would not be able to complete the journey.

Care

As soon as the victims are brought into the nest, they are taken care of. A termites that clings to an ant mostly is pulled off successfully and the ant doesn’t suffer any long-term consequences of the adventure. An ant that lost a leg or antenna receives a thorough treatment: nest mates groom the open wound for a long time, cleaning it and probably also applying antimicrobial substances that they produce in special glands. Experiments show that an ant with an untreated open wound almost always dies, probably due to an infection. But when treated, it usually survives and it will learn to walk on four or five legs as fast as the others – and soon enough, it will join termite raiding parties again.

When heavily injured ants are brought in, which happens only infrequently, they will get no treatment, but are carried out of the nest instead. The ants only help injured nest mates that will survive.

The rescue behaviour in Megaponera analis is unique. It could develop in these ants because they conduct short and space-limited raids on a dangerous prey. There are many casualties, but the injuries are rarely fatal when the victims get help – and help is worth the effort. Without rescuing behaviour, the colony would be much smaller and fewer workers would be available to join a raiding party. To give an idea of the importance: the number of ants that are rescued on a day roughly equals the number that is born.

Willy van Strien

Photo: Megaponera analis: major carrying injured nest mate back to the nest. ETF89 (Wikimedia Commons, Creative Commons CC BY-SA 4.0)

Videos of Megaponera ants that carry and treat injured nest mates

Sources:
Frank, E.T., M. Wehrhahn & K.E. Linsenmair, 2018. Wound treatment and selective help in a termite-hunting ant. Proceedings of the Royal Society B 285: 20172457. Doi: 10.1098/rspb.2017.2457
Frank, E.T., T. Schmitt, T. Hovestadt, O. Mitesser, J. Stiegler, K.E. Linsenmair, 2017. Saving the injured: Rescue behavior in the termite-hunting ant Megaponera analis. Science Advances 3: e1602187. Doi: 10.1126/sciadv.1602187

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