Many social insects have soldiers, but only one bee does – and Jatai bee soldiers are unlike any other soldier caste biologists have ever seen

   On the campus of the University of Sao Paulo, Brazil, some trees buzz more than others – which is exactly what behavioural ecologist Francisca Segers had hoped for.
She approaches one buzzing tree. There is a short wax tube extending from a hole in the trunk. Hovering around the opening are half a dozen small yellow-and-brown bees, the source of the gentle buzz.
   Next, Segers reaches into a box she is carrying and takes out a tiny black lump. It is the crushed head of a robber bee (Lestrimelitta limao), freshly killed that morning. She gingerly places the robber bee head on the tube opening, and watches as it slowly rolls down the tube into the tree.
In an instant, a cloud of the tiny yellow-and-brown bees bursts from the tube. "It was just six bees flying at the entrance… then suddenly there were two hundred," says Segers.
   These are no ordinary bees, though. Colonies of Tetragonisca angustula, known locally as "Jatai bees", are particularly adept at seeing off enemies. That is because Jatai bees, uniquely, have developed a soldier caste.

Jatai bees built heavily fortified nests (Credit: Christoph Grüter)

   Christoph Grüter at the University of Mainz and his colleagues first announced in 2012 that Jatai bees have soldiers. Their suggestion stirred up quite a buzz.
   Of course, we already know that a number of other social animals have evolved a soldier caste: ants, termites, and even some less socially-complex animals like aphids, snapping shrimps and flatworms. Yet until Grüter and his colleagues made their announcement, nobody had found bee soldiers. That fed a general assumption that bees cannot evolve such a class.
   One reason why Jatai soldiers went unnoticed for so long is because of the diminutive size of this particular bee.
   "It is very difficult to spot the size differences in Jatai bees because they are so small," says Martin Kaercher, who examined the defensive behaviours of Jatai guards for his PhD at the University of Sussex. "I had also not expected size differences in bees."
   Kaercher was not alone. Over the years, many researchers have examined the 5mm-long Jatai bees up close, without noticing that certain individuals are subtly, but consistently, larger. Size differences at such scale are almost impossible to spot; at least, without very good vision. Fortunately, Grüter's colleague, Cristiano Menezes at the University of Sao Paulo has an eye for detail.

An army ant (Eciton hamatum) soldier bites (Credit: Visuals Unlimited/naturepl.com)

"We were running a study where we introduced workers from one Jatai bee colony to the nest entrance of another," says Grüter. "Eventually, Cristiano noticed that the guards seemed larger than the workers we introduced."
Meticulous measurement of more than 300 bees confirmed Menezes's observation: Jatai bees guarding the entrance are 30% heavier than the rest. They also have larger hind legs.
"I was amazed and delighted [to know of Jatai bee soldiers], since we only knew about caste differences in ants and termites," says Kaercher of Grüter's 2012 discovery.
   Why might Jatai bees have developed a class of soldiers while other bees apparently have not?
   There is no definitive answer, but clues might come from Segers's experiments with the decapitated heads of robber bees. Because it turns out that robber bees pose a very real threat to Jatai colonies.

Jatai bees are the only species known to have soldiers (Credit: Christoph Grüter)

   Robber bees are pirates on wings. They plunder the colonies of other bees – like the Jatai – and raid their stores.
   If one robber bee encounters a Jatai colony and returns to its own colony to recruit more robbers for an attack, the result can be devastating, says Segers. "We have lost colonies to robber bees."
   This is why it is in the Jatai bees' best interests to attack a robber scout before it can relay its message. As Segers's experiment shows, the mere whiff of a robber bee's presence is enough to alert the Jatai soldiers. They rush out of the nest and charge at the intruder, flying close enough to lock on to the robber bee with their powerful jaws.
"Ideally, the Jatai bee grabs the wings of the robber bee and doesn't let go," says Grüter, who has witnessed many such fights. Both bees fall out of the sky, the robber grounded by the soldier. They grapple with each other as the robber bee tries to tear away its tenacious attacker.
Eventually, the much larger robber bee usually succeeds in killing the Jatai soldier, often decapitating it in the process. But the dead bee's relentless jaws clamp on to its killer, preventing the robber from flying away.
"The Jatai bees commit suicidal defence, lying on the ground with the robber bee until maybe an ant comes along and [takes] them away," says Grüter.

An unidentified termite soldier (Credit: Kim Taylor/naturepl.com)

   Jatai soldiers hover around the nest, expanding the defence perimeter and intercepting robber bee scouts before they reach the colony. In addition, Jatai bees seal their nests at night, and use wax and resin on complex nest tunnels to entangle enemies.
It is a surprisingly comprehensive system, which Grüter has described as "one of the most sophisticated defences among social bees".
"I've read that Jatai bees and robber bees overlap greatly in their distribution," says Grüter. "If so, this would mean a long history of co-evolution and arms race between the bees."
Recently, however, Grüter and his colleagues reported that Jatai bee soldiers are quite unlike any other animal soldiers we know.

This turtle ant (Cephalotes rohweri) soldier has a huge head (Credit: Visuals Unlimited/naturepl.com)

   While ant or termite soldiers do little else but fight enemies, Jatai bee soldiers also partake in civilian duties. They build and clean the nest, nurse the larvae and dry the wax.
   Even more surprising is that in the first half of their month-long lives, Jatai bee soldiers outwork the workers. On average, each Jatai bee soldier performs ten different behaviours to the worker's eight, and each soldier does between 30 and 40% more work than the workers. Most of this work involved nest maintenance.
"We do not know of any other case where soldiers show more diverse behaviours than workers," says Grüter. "In ants, soldiers are specialists that work very little and have a relatively narrow set of behaviours.
"What we see in Jatai bee soldiers is counterintuitive. It goes against the theory of caste evolution that increasing specialisation leads to narrowing behaviour sets."
For now, Grüter and his colleagues can only speculate why Jatai bee soldiers are so versatile and hard-working.
   Perhaps Jatai bees have evolved their specialised soldier caste far more recently than other social animals, so the soldiers have not yet evolved to focus all their efforts on fighting.
   Or perhaps Jatai soldiers can work like workers do because they are not starkly different in size and shape. The soldiers in colonies of army ants or leafcutter ants dwarf the worker ants like tigers to cats. Jatai soldiers, in contrast, stand next to Jatai workers like horses to donkeys.
"Maybe there are developmental limits that make it impossible for Jatai bees to evolve extreme soldier types," Grüter says.
   Those limits might be set by the design of their nests.

Worker and soldier ants (Pheidole rhea) (Credit: Visuals Unlimited/naturepl.com)

   All Jatai bees are born in rigid cells of brood combs in the hive centre. Worker bees regurgitate food into each cell, the queen adds an egg, and the worker seals the cell. The egg hatches and the larva eats the provisioned food, developing in the cell until it emerges as an adult.
   Segers found that Jatai soldiers are reared in specific cells right in the centre of the brood. There the cells are a little larger and receive more food, giving rise to larger and heavier bees. But the size difference is still constrained by the need for the cells in the brood combs to tessellate.
In contrast, ant and termite larvae grow in open space and are fed continuously by their carers, which allows individuals destined to be soldiers to grow much larger.
   Scientists call the larger Jatai bees "majors" and the rest of the smaller workers "minors". Jatai bee majors make up less than 6% of the workers. Most end up as soldiers.
   But that does not happen until the end of their lives.

An African driver ant (Dorylus sp.) soldier (Credit: Martin Dohrn/naturepl.com)

   Newly-emerged majors and minors alike start work in the brood, deep in the hive. As the workers age, they move further from the hive's centre and switch occupations, dealing with waste, wax and resin. At this stage, majors work a lot more and have a couple more tasks in their repertoire than minors.
   But by the third week of their short lives, when their workplace moves to the periphery of the hive, minors and majors wear completely different uniforms. Minors forage for food while majors guard the hive, most becoming the soldiers that Grüter and Segers study.
"In a way, soldiers are really just hard-working workers until they reach the entrance," says Grüter. "It makes sense to call them majors, and refer to them as soldiers only when they pick up the defence at the end of their lives."
   Majors seem to be an asset to the hive. They outwork minors early in their life, and then later they help defend the hive. But they make up less than one-tenth of the workforce of the hive. So why does a Jatai bee colony not produce more majors?

The entrance to a Jatai bee nest (Credit: Christoph Grüter)

   For one thing, majors are expensive. A juvenile major eats 20% more food than a juvenile minor, and as adults they likely eat more food too. Yet majors do not collect food for the nest.
   Furthermore, Jatai bee majors may work more than minors, but nobody has compared their efficiency. "If majors are less efficient, they might not be worth the extra cost," says Grüter.
   For a better sense of the value a Jatai colony places on its majors, we simply have to look at the way colonies respond to limited food and threats. In one experiment, Segers moved Jatai bee colonies into areas where competition for food was intense. Five months later, the colonies had adapted by producing smaller soldiers – but minors remained the same size.
   In areas where enemy robber bees are rare, meanwhile, Jatai bee colonies deploy fewer soldiers. But when scientists jack up the threat for several weeks, or give the impression of a greater threat by rolling robber bee heads into the nest, Jatai bee colonies build up their army of soldiers.
In other words, it appears that Jatai bees can tune their production of majors and minors according to their needs. Majors – soldiers – are valued most when robber bees are lurking.

Jatai soldiers guard the nest entrance (Credit: Christoph Grüter)

   This makes sense to Paul Cunningham, an insect behavioural ecologist at the Queensland University of Technology in Brisbane, Australia, who has documented a four-month-long war between Australian stingless bees. He thinks that enemies play a key role in shaping the evolution of a defence system.
"If your enemy are larger bees and you are more likely to overpower them with individual strength, then having strong soldiers is an advantage," says Cunningham. "This is the case with Jatai bees against robber bees."
   On the other hand, if both sides are similarly matched in strength, then the colony with the most workers wins. "Having stronger fighters isn't always the best strategy."
Next, Grüter and his team will scrutinise other bee species for soldiers. If they discover soldiers in other bees, they could better understand how species of bees evolve soldiers.
The diverse behaviours of Jatai bee soldiers "draw a big question mark", says Grüter. "[It's] not just about the evolution of soldiers in this species but also in general about the evolution of physical caste in social insects."
   Perhaps other bees have also evolved hard-working soldiers that juggle many tasks. But that is not going to bother the Jatai bees – they are concerned only with robber bees and honey. As new cohorts of Jatai bee majors emerge from brood cells, they will live as all of the previous generations of soldiers did: work harder than the rest and die guarding the nest.

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The quantum origin of time

   In our experience the past is the past and the future is the future, but sometimes the two can cross over

Science has a habit of asking stupid questions. Stupid, that is, by the standards of common sense. But time and time again we have found that common sense is a poor guide to what really goes on in the world.

So if your response to the question "Why does time always go forwards, not backwards?" is that this is a daft thing to ask, just be patient.

Surely we can just say that the future does not affect the past because (duh!) it has not happened yet? Not really, for the question of where time's arrow comes from is more subtle and complicated than it seems.

What's more, that statement might not even be true. Some scientists and philosophers think the future might indeed affect the past – although we would only find out when the future arrives. And it may be able to due to an emergent property of quantum mechanics.

To all intents and purposes, time seems to have a direction.

Our everyday experience insists that things only happen one way. Cups of coffee always get colder, never warmer, when left to stand. If they are knocked to the floor, the cup becomes shards and the coffee goes everywhere, but shards and splashes never spontaneously reassemble into a cup of coffee.

Yet none of this one-way flow of time is apparent when you look at the fundamental laws of physics: the laws, say, that describe how atoms bounce off each other.

Those laws of motion make no distinction about the direction of time. If you watched a video of two billiard balls colliding and bouncing away, you would be unable to tell if it was being run forwards or backwards.

The same time symmetry is found in the equations of quantum mechanics, which govern the behaviour of tiny things like atoms. So where does time's arrow come into the picture?

There is a long-standing answer to this, which says that the arrow only enters once you start thinking about lots and lots of particles.

The process of two atoms colliding looks perfectly reversible. But when there are lots of atoms, their interactions lead inevitably to an increase in randomness – simply because that is by far the most likely thing to happen.

Say you have a gas of nitrogen molecules in one half of a box and oxygen molecules in the other, separated by a partition. If you take away the partition, the random movements of the molecules will quickly mix the two gases completely.

There is nothing in the laws of physics to prevent the reverse. A mixture of the two gases could spontaneously separate into oxygen in one half of the box and nitrogen in the other, just by chance.

But this is never likely to happen in practice, because the chance of all those billions of molecules just happening to move this way in concert is tiny. You would have to wait for longer than the age of the Universe for spontaneous separation to occur.

This inexorable growth of randomness is enshrined in the second law of thermodynamics. The amount of randomness is measured by a quantity called entropy, and the second law says that, in any process, the total entropy of the Universe always increases.

Of course, we can decrease the entropy of a group of molecules, say by sorting them one from another. But doing that work inevitably releases heat, which creates more disorder – more entropy – somewhere else. Ordinarily, there is no getting around this.

However, the entropic arrow of time gets less well-defined at smaller scales. For example, the chances of three oxygen and two nitrogen molecules briefly "un-mixing" are pretty good.

This was illustrated by a 2015 study. Researchers studying single molecules found evidence that the growth of entropy is a good measure of how far the system was from being reversible in time.

This argument about entropy, which was worked out in the late 19th Century by the Austrian scientist Ludwig Boltzmann, is often seen as a complete and satisfying answer to the puzzle of time's arrow.

But it turns out the Universe holds deeper secrets. When you start looking at very small things, Boltzmann's neat story gets increasingly muddled.

In Boltzmann's picture, it takes a while for the arrow of time to find its direction. In the tiny fractions of a second after the partition between the two gases is removed, before any of the molecules have really moved anywhere, there is nothing to show which direction of time is forwards.

Entropy increases when collisions between atoms even out their energies, as for example when the heat of hot coffee spreads out into the surrounding air. This process, which washes away reservoirs of energy, is called dissipation.

Until dissipation starts to happen, a process looks much the same backwards or forwards in time. It does not really have a thermodynamic arrow.

But there is a one-way process in quantum mechanics that happens much faster. It is called decoherence.

At the quantum scale, particles behave as if they were waves. This has peculiar consequences.

For example, if you shoot individual electrons or whole atoms through two closely spaced slits in a screen , they will interfere with each other as if they were waves. But this does not happen with ordinary-sized objects. If you throw two coffee cups through two open windows, they do not interfere with each other.

Decoherence explains why objects on the everyday scale of coffee cups do not show the wave-like behaviour of quantum objects.

It arises because quantum particles can be coordinated in their quantum waviness, but if there are lots of them – like the countless atoms in a coffee cup – they rapidly lose any coordination. This means the object they constitute cannot show quantum behaviour.

Decoherence happens because of interactions between the objects and their environment: for example, the impact of air molecules on the cup. Quantum theory shows that these interactions rapidly cause a large object's quantumness to "leak" into its environment.

This means the object takes on unique characteristics. Quantum theory tells us that objects can show one of many possible properties when they are measured, but in our everyday world objects only have a single well-defined position, speed and so on. Decoherence is thought to be how this "choice" is enforced.

Quantum decoherence is incredibly fast, because interactions between particles are extremely efficient at dispersing quantum coherence.

For a dust grain one-thousandth of a centimetre across, floating in air, the collisions of other air molecules will destroy any quantum behaviour in around 0.0000000000000000000000000000001 seconds. That is a trillionth of the time it takes for light to cross the face of a single hydrogen atom.

This is much faster than the time it takes for heat in a dust grain to get redistributed in the environment. In other words, decoherence is faster than dissipation – and it seems to only work one way. That means decoherence reveals the arrow of time faster than dissipation.

This implies that the arrow of time really comes from quantum mechanics, not thermodynamics as Boltzmann thought.

In a sense it has to, because everything is made of atoms, and quantum mechanics is the right theory to use for atoms. "The thermodynamic arrow of time must emerge from the quantum one," says George Ellis of the University of Cape Town in South Africa.

Yet in the end, the quantum and thermodynamic explanations amount to the same thing: the scrambling of information.

It is easy to see that the mixing of two types of gas molecule is a kind of scrambling, a destruction of orderliness.

But decoherence involves scrambling too: of the coordination between the "waves" that describe quantum objects. In effect, decoherence comes from the way interactions with atoms, photons and so on in an object's environment carry away information about the object and scatter it around. This is, in fact, a quantum version of entropy.

In both the classical and the quantum cases, then, time's arrow comes from a loss of information.

This offers a better way to think about time's arrow. It points in the direction in which information is lost and can never be retrieved.

A process is only truly irreversible when the information about the change is lost, so that you cannot retrace your steps. If you could keep track of the movement of every single particle, then in principle you could reverse it and get back to exactly where you started. But once you have lost some of that information, there is no return.

"The loss of information is a key aspect," says Ellis. "At the macroscopic scale this gives the second law."

It is still not entirely clear when, in the quantum world, the information is truly lost.

Some researchers think that decoherence alone is enough. But others say that the information, although smeared and dispersed in the environment, is still recoverable in principle. They think an additional, rather mysterious process called "collapse of the wave function" – in which the quantum waviness is irreversibly lost – takes place. Only then, they say, does the arrow of time point unambiguously in one direction.

In either case, in quantum physics we can only really say that an event has happened if we have lost the option of making it "unhappen".

The arrow of time seems to reflect a process of the Universe "committing itself" to something, rather than hedging its bets by allowing for many different outcomes. It is this "crystallising" of the classical present from the quantum past, says Ellis, that produces a direction in time.

This idea fits neatly with one of the most famous thought experiments in physics.

Do effects always come after their causes? (Credit: Blend Images/Alamy)

The second law of thermodynamics says that things tend to become more random, but only because randomness is so likely. In the late nineteenth century, the Scottish physicist James Clerk Maxwell came up with what looked like a way to get around this.

Maxwell imagined a tiny intelligent being that could observe the random motions of molecules. This "demon" could un-mix two gases, by opening and closing a door at just the right moments.

Maxwell's demon seems to violate the second law, but in fact it cannot. The reason is that the demon has to accumulate information in its brain as it observes the molecular motions. To keep this up, it has to delete the older information, and that increases the entropy.

It is the act of erasure, of forgetting, that guarantees the thermodynamic arrow of time. Once again, the key thing is loss of information.

However, the quantum-mechanical picture of time's arrow leads to something deeply peculiar. In some experiments, it looks as though influences can work backwards in time. The future can affect the past.

The double slit experiment (Credit: Victor de Schwanberg/Science Photo Library)

Take the double-slit experiment, in which a quantum particle such as a photon of light is fired at two narrow slits in a screen.

Suppose we do not measure which way the particle went, and so cannot tell which slit it went through. In this case, we see an interference pattern – a series of light and dark bands – when the particles emerge on the far side.

This reflects the wave-like character of quantum particles, because interference is a wave property. The interference even persists when the particles pass through the slits one at a time, which only "makes sense" intuitively if we imagine each particle passing, wave-like, through both slits at once.

However, now suppose we place a detector by the slits to reveal which one the particle passes through. In this case the interference pattern disappears, and the particles act more like sand grains being fired through holes. Measuring a particle's path destroys its waviness.

Here is the really strange thing. We can set up the experiment so that we only detect which slit a particle passed through after it has done so. And yet we still see no interference.

How does the particle "know" that it is going to be detected after passing through the screen, so that when it reaches the slits it "knows" whether to go through both slits or just one? How can the later measurement seem to affect the earlier behaviour?

This effect is called "retrocausality", and it seems to imply that the arrow of time is not as strictly one-way as it seems. But does it really?

Must time only flow one way? (Credit: Robin Treadwell/Science Photo Library)

Most physicists think that retrocausality in these delayed-choice experiments is an illusion created by the counterintuitive nature of quantum mechanics.

Detecting a particle "after" it has passed through the slits does not really influence the path it takes, they say. That is just the way we are forced to imagine what is happening when we try to apply our classical intuition to quantum events.

"Post-selection is like a parlour trick that makes it seem like there is backwards causation where there actually is none," says Todd Brun of the University of Southern California. "It's like the guy who shoots at the side of a barn and then goes and draws a target around the bullet hole."

However, others say that backwards effects in time are a perfectly valid way of interpreting such processes.

According to Ellis, we can regard retrocausality as a kind of fuzziness in the "crystallisation of the present". "Quantum physics appears to allow some degree of influence of the present on the past, as indicated by delayed-choice experiments," he says.

Ellis has argued that the past is not always fully defined at any instant. It is like a block of ice that contains little blobs of water that have not yet crystallized.

Even though the broad outline of events at a particular instant has been decided, some of the fine details remain fluid until a later time. Then, when this "fixing" of the details happens, it looks like they have retrospective consequences.

It is hard to find the right words to describe this situation.

Molecules tend to get jumbled up (Credit: Indigo Molecular Images/Science Photo Library)

Certainly we should not imagine a "force" reaching back through time and altering earlier events. Instead, those things are slow to acquire the true status of events – of stuff that has actually "happened" – at all.

Alternatively, perhaps those past events really did happen at the time, but the laws of quantum mechanics forbid us from seeing them until later. "If the future detector choice causes the particle to behave a certain way in the past, one should consider the past behavior 'real' when it originally happened," says Ken Wharton of San José State University in California.

Quantum retrocausality crops up quite naturally if, instead of trying to force an arrow of time onto quantum theory, we simply let quantum mechanics work equally well in both directions in time. Wharton's colleague Huw Price of the University of Cambridge in the UK has argued that such a theory really would allow backwards causation.Still, Wharton admits that such retrocausal theories are speculative.

Particles are always colliding (Credit: Harald Ritsch/Science Photo Library)

Only a handful of physicists and philosophers have embraced retrocausality. Most consider backwards causality "too high a price to swallow", says Wharton.

But he feels that we only resist this idea because we are not used to seeing it in daily life.

"The view that the past does not depend on the future is largely anthropocentric," says Wharton. "We should take apparent backwards causation more seriously than we usually do. Our intuition has been wrong before, and this time symmetry on quantum scales is a reason to think we could be wrong again."

If time's arrow is not quite as one-way as it seems, that raises one last question: why do we perceive it as always pointing one way? Why should the "psychological arrow of time" be aligned with the physical ones?

Quantum particles behave counter-intuitively (Credit: Richard Kail/Science Photo Library)

Again, it might sound like an odd question. If the laws of physics dictate an arrow of time, surely our perception of it should follow quite naturally? But that is not as obvious as it sounds.

Suppose you have some particles moving around in a box according to physical laws. If you know all the exact positions and speeds of the particles right now, you can predict the future exactly.

In principle, there is nothing in the future that could not be known in the present. Why could that not be experienced as a "memory" of the future; a little like a master chess player seeing well in advance how the game will inevitably end?

This question is usually swept under the carpet. "Since biology rests on a foundation of chemistry, which rests in turn on foundations of quantum mechanics and thermodynamics, I think most people believe that the biological arrow of time is a consequence of the thermodynamic arrow," says Brun.

But this is not a foregone conclusion. Brun and his colleagueLeonard Mlodinow at the California Institute of Technology in Pasadena have argued that the psychological and thermodynamic arrows of time are actually independent. They only coincide because of how our memories work.

Particles can only stay "fuzzy" for so long (Credit: Richard Kail/Science Photo Library)

The first part of the argument was put forward by David Wolpert of the Santa Fe Institute in New Mexico. He said that, before you can remember something, you must initialize your memory in some standard starting state; like wiping your hard drive to make space for new data.

But as Maxwell's demon showed us, erasing information always increases entropy. This means initialization is an irreversible process, and so only works forward in time.

However, Mlodinow and Brun say that this argument is not quite complete. In principle, you can eliminate any need for erasure and initialization just by remembering everything. Then, recording information in the memory can be fully reversed, and has no arrow of time.

In this case, they argue that the psychological arrow of time is still preserved, by something they call "generality".

When atoms collide their statuses get fixed (Credit: Mike Agliolo/Science Photo Library)

The problem with remembering the future now is that there can always be "surprise" events that wreck the link between the system's state now and its state in the future. I can "remember" that my clock will show 11 o'clock in an hour's time – but if the battery runs out in ten minutes, my "memory" will be wrong.

A real memory cannot be contingent on the system behaving a certain way, Mlodinow and Brun say. It has to remain general, meaning it is true whatever happens. So even if memory is recorded in a reversible system, the requirement of generality imposes a directionality in time.

In this case, says Brun, the reason we cannot remember the future is not simply because it has not happened yet. Instead, it is because the "memory" would really only be a prediction, which might or might not be correct. And it is not a true memory unless it is correct.

In other words, a putative "future memory" is fine-tuned to a particular outcome, and must be readjusted if any slight change occurs between now and the appearance of the "remembered" future state. That means it is too fragile to count as a genuine memory.

Quantum mechanics is counter-intuitive (Credit: Pascal Goetgheluck/Science Photo Library)

Not everyone is convinced that Brun and Mlodinow have cracked the problem.

Some think their argument is circular. They had to put in the asymmetry of time by hand, making it possible for contingent events to intervene in the future but not the past – which some feel is a bit of a cheat.

All the same, simply by posing the question, Brun and Mlodinow have shown that the answer is not as obvious as we might suppose. Our perception of time may not have much to do with the actual passage of time.

What is clear is that the arrow of time, which seems like such a common-sense fact of life, is actually a profoundly tricky concept. The closer we look, the less we can be sure that the arrow is really always one-way.

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Meet the microbes that have made New York City their home

   Cities are home to uncounted millions of microorganisms, many of which are only there because we bring them. But the built environment is a uniquely challenging place for them to live

In the summer of 2013, several science students at Cornell University in New York found themselves tasked with an unusual project. They were asked to go into subway stations and trains, and swab surfaces for no less than three minutes.

Christopher Mason, the Weill Cornell Medicine geneticist who devised the study, points out that three minutes is a long time when you are in the middle of a public place, swabbing away at a subway pole. Some bemused looks and questions from commuters later, though, the team amassed a comprehensive collection of samples from 468 stations.

The point of the exercise? To investigate the microbes that share our environments, riding the same subway trains that millions of New Yorkers use daily. These microscopic urban commuters vastly outnumber humans but we still know little about them. The project is one of many now underway to explore the urban "microbiome" – the localised population of microorganisms – and its influence on human health.

The work is at an early stage. But the initial results suggest we might want to nurture the urban microbiome, rather than fight to remove the microbes from our cities.

Back in the lab, Mason and his colleagues analysed their subway samples for viral and bacterial DNA. A huge range of microbes showed up. For example, there was heaps ofPseudomonas stutzeri, which is quite common in soils, and lots of Acinetobacter radioresistens, a radiation-resistant bacterium found on human skin.

For instance, they seemed to lack many of the specific chunks of DNA that trigger human disease. And, obviously, people who ride the subway are not as a rule in a constant state of poor health.

"I'm extraordinarily confident in knowing that I can grab the pole and it's probably fine," says Mason. "I have more confidence [in that] than I did before, I would say."

The researchers also found that one subway station, which had been flooded during Hurricane Sandy the year before, still bore a microbial fingerprint of the event. The station's microbiome included ten species associated with marine life, likeShewanella putrefaciens. This suggested that, even a year later, microbes likely brought in by the weather had persisted there.

It is these sorts of studies that are finally revealing to us the microbes with which we share our city spaces.

The US recently launched a new initiative to better document these invisible species in our midst. Meanwhile, Mason and colleagues are now examining the microbiomes ofmass transit systems in many places around the world.

But our co-existence with urban microbes is not always a happy one.

Humans have a combative relationship with their microscopic neighbours. Even now, with increasing awareness that many microbes in the human body are "friendly" – or potentially beneficial to our health – Western societies are at war with the bacteria and viruses that occupy the environment.

Cleaning products boast about the 99.99% of bacteria to which they will lay waste, and entrepreneurs are even developing devices to extend this reach. For example, a start-up called Bio-Smart is hoping to market an ultraviolet light that will indiscriminately vaporise bacteria within its range. In general, we are paranoid about pathogens.

"The fear-mongering is not warranted, because most of the bugs that we encounter on a daily basis are either good in terms of immune development, or good in terms of the whole barrier effect," says Klas Udekwu, a microbiologist at Stockholm University in Sweden.

The barrier effect Udekwu mentions refers to the process by which microbes on and within our bodies are able to fend off would-be pathogens. For example, bacteriophages are viruses that live on us but are sometimes good for us – they can help toprevent infections by infecting and replicating inside bacteria.

Of course, this does not mean that all of the microbes we encounter in the built environment are beneficial – but neither are they all detrimental to our health. The research efforts of Mason and others aim to explore where the balance lies.

How dangerous are the potentially pathogenic strains? What locations and surfaces support microbes better than others? And, living in these urban jungles, are we missing out on helpful microbes more commonly found out in nature?

As far as that last question is concerned, there is certainly some evidence to show that the urban environment, by its very nature, is not always home-sweet-home to microbial life.

In a study published in April 2016, researchers placed tiles with swatches of plasterboard, ceiling tile and carpet on the floors, walls and ceilings of nine offices in three cities. Over a year, samples were collected every four to six weeks, and the DNA of collected microbes was later analysed.

Microbes were there, certainly, but the data seemed to show that they were largely the result of human presence and activity in the area, even though workers in the offices did not touch the experiment tiles during the study.

"Surface microbial communities may behave similarly to those found in the soils of the Atacama Desert, waiting for liquid water to become active," the paper notes.

Sean Gibbons at the Massachusetts Institute of Technology argues this paints a picture of office spaces as "microbial wastelands": microorganisms may be regularly deposited in buildings, but are not always able to thrive there.

Mason makes a similar point with regard to his research on the subway, which he describes as a "high traffic area". The next question, he says, is to find out which of the deposited microbes are able to do well over time.

There is evidence that, despite the harshness of our offices and homes, some special microbes do get along quite nicely.

In a study published in June 2016, Rob Dunn, a microbiologist at North Carolina State University, investigated the ability of some of these organisms to thrive in extreme conditions. Some microbe species seem quite happy in hot water heaters, dishwashers or even the bleach tanks of washing machines.

Some microbes could only handle certain kinds of extremes: for example, they survived extremely hot habitats but succumbed to high or low pH. But others, like the nitrogen-fixing bacteria Azospira, were found in places that had extremes of all three kinds.

In a 2015 study, Dunn and his colleagues analysed microbes found in the dust on the outside of around 1,200 homes across the US. There were geographic trends, but not such a stark difference between urban and rural locations. Dunn makes the point that people with dogs in their homes are more likely to come into contact with microbes found in soil, thanks to Rover's habit of garden hole-digging.

Besides environmental location and the presence of pets, there are all kinds of ways in which the introduction of microbes to our homes can vary. One of the most unexpected, for some, is tap water.

Although drinking water itself lacks certain nutrients, a wealth of microbes can be found there. Amy Pruden at Virginia Tech points out that our water pipes are not sterile inside. In fact, they have a thin biofilm into which nutrients – and microbes – can be deposited.

"I don't know if you've ever checked out your pipe when the plumber has come over, but it's kind of eye-opening to see how gross your pipes are," she says. "There's a lot of microbiology going on there."

In a 2015 study, Pruden and colleagues examined the microbiome of water systems. They developed a rig of pipes, which they installed at five water utility plants in the US. They found the plants contained potential pathogens likeMycobacterium and Legionella, which can cause Legionnaire's disease – although these particular strains of the bacteria will not necessarily trigger disease.

It was the way each utility processed its water that made the largest difference between the microbiomes. Two of the utilities even drew their water from the same source, but the microbiomes of the liquid they pumped out to homes were distinct – showing that it was their own process for treating the water that really mattered.

What effect could all of this be having on human health? Are there healthier microbiomes to live within?

Dunn says there is likely a "huge impact" on our wellbeing from the microbes we are exposed to. But he adds, "Do we understand which of these exposures matter? Not at all."

Still, there are interesting leads that deserve more research. In 2013, science journalist Ed Yong wrote about the work of Susan Lynch at the University of California, San Francisco. Lynch has shown how the extra microbial diversity of a home with a dog appeared to have a positive impact on health – at least in experiments using mice instead of humans.

Some of the mice ate dust from homes where dogs lived, and were then exposed to allergens. These mice had reduced asthma-associated inflammation in their lungs than mice exposed to dust from dog-free homes. One of the microbial species that had this effect was Lactobacillus johnsonii – one of many bacteria found in mothers' vaginas just before birth.

It is also possible that our modern ways of living hamper microbes that our bodies have evolved to support.

Another 2016 study by Dunn's team investigated the effect of antiperspirants and deodorants on armpit bacteria.

The armpits of volunteers were sampled during the course of an eight-day period. For the first day, participants kept to their normal hygiene habits, then spent five days not using odour-busting sprays at all. Finally, participants they began using them again on the last two days of the experiment.

The results showed that one genus of bacteria, Corynebacterium, had dramatically reduced levels when the aerosols were being used. In one sense this is desirable – for it isCorynebacterium that produce the unpleasant odours in a sweaty armpit. But what you might not know is that our armpits' apocrine glands seem to want them there.

"What they're really doing is not producing sweat, they're actually producing a sebaceous, liquid-like substance that appears to serve no function other than to feed microbes," says Dunn. "So basically it's a gland for feeding microbes."

Again, it is not yet clear how negative the effects of displacingCorynebacterium may be. But Dunn notes that knocking it out allows other microbes to thrive in our armpits, which could be disadvantageous for us.

Is there any way we could use all this information to improve the microbial diversity of our surroundings?

Increasingly, microbiologists are thinking about ways in which the introduction of favourable bacteria to urban environments may be more beneficial than approaches that seek to sterilise those places of all microbial life – not least because, thanks to microbes that favour extremes, those approaches seldom work as advertised.

Pruden suggests that one way of displacing harmful bacteria likeLegionella in water systems could be to encourage the growth of antagonistic bacteria. These bacteria produce chemicals that can inhibit the bloom of potentially pathogenic microbes. One such species is Bacillus subtilis, which can have an antagonistic effect on Legionella.

And then there is Jack Gilbert, a trail-blazing microbiologist who is hoping to develop materials for buildings that encourage the presence and persistence of microbes that can stop pathogens taking hold.

In the last few years alone, then, we have unearthed heaps of new knowledge about how rich our urban environment is with microbial life – but also how fragile an ecosystem it is, too. The microbes we need are sometimes hampered by the structures we have build around us, and it is still not clear exactly how our health may be affected as a result.

It seems certain, though, that as this understanding continues to evolve, we will become ever more cognizant of our microbial neighbours. We have long shared our cities with them. Perhaps it is time we thought about how to get along.

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