Figure 6.1: The earth’s magnetic field lines and the angle of inclination.
BORN IN Toronto, Canada, in 1912, Fred Urquhart went to a school that bordered a cat-tail marsh. There he spent endless hours observing the insects, particularly the butterflies that populated the reed beds. His favorite time of the year was the early summer, when the marsh saw the arrivals of thousands of monarchs, those iconic North American butterflies with their familiar orange-and-black wing pattern. Monarchs would remain for the summer, feeding on the native milkweeds, before flying off again in the autumn. And the question that particularly intrigued Fred was: Where do the butterflies go?
As St. Paul is reputed to have said, adults generally put away their childish things. Not Fred, however, who continued, as he grew up, to wonder where the monarchs spent the winter. After studying zoology at the University of Toronto and eventually becoming a professor in the subject, he returned to his childhood question. By this time he had married Norah Patterson, a fellow zoologist and butterfly-lover.
Using the classic animal tagging techniques, Fred and Norah now attempted to discover the secret of the monarchs’ disappearance. This wasn’t easy. While tags tied to the feet of robins, or pinned to the fins of whales, work fine, attaching a tag to the delicate membranous wings of a butterfly presents a wholly different challenge. The husband-and-wife team experimented with sticky labels and gluing tags onto the insects’ wings; but either the tags fell off or the tagged butterflies had trouble flying. It wasn’t until 1940 that they hit upon the solution: a tiny adhesive label similar to those that are so difficult to scrape off newly bought glassware. Armed with this device, they began tagging and releasing hundreds of monarch butterflies, each with an identifying number and the instructions that, if it were found, the finder should “Send to Zoology, University of Toronto.”
But there were millions of monarchs in America and only two butterfly-loving Urquharts. So the couple took to recruiting volunteers, and by the 1950s had marshalled a network of thousands of butterfly enthusiasts who in turn had tagged, released, captured and recorded hundreds of thousands of butterflies. As Fred and Norah constantly updated a map that tracked these capture and release locations, a pattern gradually emerged. The butterflies setting off from the Toronto area tended to be captured along a diagonal flight path traveling southward that crossed the United States from the northeast to the southwest, passing through Texas. But despite numerous field trips, the Urquharts could not identify the final destination of these wintering butterflies in the southern US states.
Eventually, the Urquharts turned their eyes farther south, and in 1972 a frustrated Norah wrote about their project to newspapers in Mexico, asking for volunteers to report any sightings and to help with the tagging. In February 1973 a letter arrived from a Kenneth C. Brugger of Mexico City offering to help. With his dog, Kola, Ken took up the quest, driving his camper van into the Mexican countryside in the late evenings in search of butterflies. Over a year later, in April 1974, he reported having seen large numbers of monarchs in the Sierra Madre mountain range of central Mexico. Then, late that year, Ken reported spotting the bodies of many tattered and dead butterflies along roads in the Sierras. Norah and Fred wrote back that they believed that flocks of birds must have been feeding on large swarms of passing monarchs.
On the evening of January 9, 1975, Ken telephoned the Urquharts in some excitement with the news that he had “found the colony! … millions of monarchs—in evergreens beside a mountain clearing.” Ken told them that he had received a tip-off from Mexican woodcutters who claimed to have seen swarms of red butterflies as they trailed across the mountain with their laden donkeys. With the support of the National Geographical Society, Norah and Fred then put together an expedition to find and record the elusive wintering home of the monarchs, arriving in Mexico in January 1976. The following day they drove out to a village from which they set off to hike up the “Mountain of the Butterflies,” an ascent of ten thousand feet. Such an arduous climb at altitude was not a trivial undertaking for a couple now in their senior years (Fred was sixty-four), and they were quite concerned about whether they could make it to the top. Nevertheless, with pounding hearts and memories of brightly colored butterflies fluttering in the Toronto sunshine, they reached the summit, a plateau sparsely forested with juniper and holly. There were no butterflies. Disappointed and exhausted, they climbed down into a clearing filled with oyamel, a type of fir tree native to the mountains of central Mexico—and it was here that Fred and Norah finally found what they had sought for half a lifetime: “Masses of butterflies—everywhere. In the quietness of semi-dormancy, they festooned the tree branches, they enveloped the oyamel trunks, they carpeted the ground in their tremendous legions.” As they stood gaping at the incredible spectacle, a tree branch broke off and there, among the debris of dislodged butterflies Fred spotted the familiar white tag with its instruction: “Send to Zoology, University of Toronto.” That particular butterfly had been tagged by a volunteer named Jim Gilbert in Chaska, Minnesota, more than two thousand miles away!1
The voyage of the monarch butterfly is now recognized as one of the great animal migrations of the world. Between September and November every year, millions of monarchs in southeast Canada head southwest on a journey of several thousand miles that will take them across desert, prairie, fields and mountains, on the way threading through the geographical needle’s eye of a fifty-mile-wide gap of cool river valleys between Eagle Pass and Del Rio in Texas, eventually to roost on the peaks of only a dozen or so high mountains in central Mexico. And then, after overwintering on the cool Mexican mountaintops, the monarchs undertake the reverse journey in the spring to return to their summer feeding grounds. Most remarkably, no single butterfly makes the entire journey. Instead, they breed en route so that the butterflies that return to Toronto are the grandchildren of the monarchs that first left Canada.
How do these insects navigate with such accuracy that they can reach a tiny target thousands of miles from their origin, one that only their ancestors had previously visited? This is another of those huge mysteries of nature that is only now beginning to be unraveled. Like all migrating animals, the butterfly uses a variety of senses involving sight and smell, including a sun compass that can correct for the moving position of the sun during the day via its circadian clock, the biochemical process in all animals and plants that oscillates within a 24-hour period, tracking the day–night cycle.
Circadian clocks are familiar to us as the source of our feeling tired at night and wakeful in the morning; and of our suffering jet lag when their rhythms are disturbed by long-distance air travel. The last couple of decades or so has seen a succession of fascinating discoveries about how they work. One of the most surprising is the finding that subjects who are kept in isolation in constant light conditions still manage to maintain a roughly 24-hour cycle of activity and rest despite having no external cues. It seems that our body clock, our circadian clock, is hardwired. This built-in clock, the body’s “pacemaker” or circadian sense, is located in the hypothalamus gland buried inside the brain. But although subjects kept in constant light conditions still maintain a roughly 24-hour cycle, their circadian clock gradually drifts away from the actual times of the day, so their periods of wakefulness and sleep will not be in synch with those of people outside the study. Yet once exposed to natural light, the subject’s body clock soon recalibrates to the actual light–dark cycle in a process known as entrainment.
The monarch butterfly’s sun compass works by comparing the height of the sun with the time of day—a relationship that varies with both latitude and longitude. It must also have a body clock that, like our own, is similarly automatically entrained by light, to compensate for the changing times of sunrise and sunset during its long migration. But where does the monarch house its circadian sense?
As the Urquharts discovered, butterflies are not the easiest animals to work with; the fruit fly, Drosophila, which we encountered in the last chapter sniffing its way through a maze, is a much more convenient laboratory insect as it breeds very rapidly and can easily mutate. Like us, fruit flies adjust their circadian rhythms to the cycles of light and dark. In 1998, geneticists found a fruit-fly mutant whose circadian rhythm could not be affected by exposure to light.2 They discovered that the mutation was in a gene encoding an eye protein called cryptochrome. Rather like protein scaffolds in the photosynthetic complexes that hold chlorophyll molecules together (as we saw in chapter 4), the cryptochrome protein is wrapped around a pigment molecule called FAD (flavin adenine dinucleotide) that absorbs blue light. Just like in photosynthesis, the light absorption knocks an electron out of the pigment, which leads to the generation of a signal that travels to the fly’s brain to keep its body’s clock in synch with the daily light–dark cycle. The mutant flies discovered in 1998 had lost this protein, so their body clocks were no longer adjusting to the cyclical change between light and dark: they had lost their circadian sense.
Similar cryptochrome pigments were later found in the eyes of many other animals, including humans, and even in plants and photosynthetic microbes, where they help to predict the time of day best suited for photosynthesis. They may represent a very ancient light-detection sense that evolved in microbes billions of years ago to synchronize cell activities with diurnal rhythms.
Cryptochrome is also found in monarch butterflies’ antennae. This was initially puzzling: What was an eye pigment doing in antennae? But insect antennae are truly amazing organs that house multiple senses, including those for smell and hearing, the detection of air pressure and even of gravity. Could they also house the insect’s circadian sense? To test this hypothesis, scientists painted some butterfly antennae black, thereby preventing them from receiving light signals. What they discovered was that the butterflies with blackened antennae could no longer entrain their sun compass with the cycle of night and day: they had lost their circadian sense. So the butterfly’s antennae seemed to house its biological clock. Remarkably, the clock in the butterfly’s antennae could be entrained by light even when removed from the rest of the insect’s body.
Was cryptochrome responsible for the monarch’s light entrainment? Unfortunately, it isn’t as easy to mutate butterfly genes as it is those of the fruit fly, so in 2008 Steven Reppert and colleagues from the University of Massachusetts did the next best thing. The team replaced the defective cryptochrome gene in mutant fruit flies with the monarch butterfly’s healthy gene and showed that it restored the fly’s ability to entrain its circadian rhythms with light.3 If the butterfly cryptochrome managed to keep fruit flies on time, then it was very likely to be doing the job of setting the monarch’s all-important body clock so that it could fly all the way from Toronto to Mexico without getting lost.
But what has any of this to do with quantum mechanics? The answer has to do with another aspect of animal migration, namely the sense we call “magnetoreception”—the ability to detect the earth’s magnetic field. As we saw in chapter 1, it has been known for a while that many creatures, including fruit flies and butterflies, possess this capability, and magnetoreception, particularly in robins, has become the poster child of quantum biology. By 2008 it was clear that the robin’s magnetic sense involved light (more on this later), but the nature of the light receptor was elusive. Steven Reppert wondered whether the cryptochrome that provided flies with the light sensitivity that helped to entrain their circadian rhythms could also be involved in their magnetoreception sense. To test the theory he performed the kind of flume choice experiment that Gabriele Gerlach had used to demonstrate olfactory navigation in clownfish (chapter 5), in which the test animal is forced to use sensory cues to choose between two routes to its food.
The researchers found that the flies could be trained to associate a sugar reward with the presence of a magnetic field. When given the option to fly down either the magnetized or the nonmagnetized arm of a maze (without food, so without olfactory cues), they chose the magnetized path. The flies must sense the magnetic field. So was cryptochrome involved? The researchers found that mutant fruit flies genetically engineered to lack cryptochrome were equally likely to fly down either arm of the maze, demonstrating that cryptochrome was essential for their magnetic sense.
In their 2010 paper, Reppert’s group also demonstrated that the flies kept their magnetic sense when their cryptochrome gene was replaced by the gene encoding cryptochrome from monarch butterflies4—showing that the monarch butterfly may well also use cryptochrome to detect the earth’s magnetic field. In fact, a paper from the same group in 2014 demonstrated that, like the European robin we met in chapter 1, the monarch butterfly possesses a light-dependent inclination compass that it uses to find its way from the Great Lakes to a Mexican mountaintop; and, as expected, it appears to be housed in its antennae.5
But how does a light pigment also detect an invisible magnetic field? To answer that question we have to return to our friend the European robin.
As we pointed out in chapter 1, our planet is a giant magnet, with a magnetic field of influence that extends from its inner core all the way out into space for thousands of miles. This magnetized bubble, the “magnetosphere,” protects all life on earth, because without it the solar wind—the stream of energetic particles emitted from the sun—would have long ago eroded our atmosphere. And, unlike the magnetism of a typical bar magnet, the earth’s field changes over time, because it has its origins inside the earth’s molten iron core. The precise origin of this magnetism is complicated, but it is thought to be due to what is known as a geo-dynamo effect, whereby electric currents are generated by the circulation of liquid metals in the earth’s core, which in turn generates a magnetic field.
So, life on earth owes its existence to this protective magnetic shield. But its usefulness to living creatures doesn’t end there; scientists have known for over a century that many species have evolved ingenious ways of making use of it. Just as human sailors have used the earth’s magnetic field for thousands of years to navigate the oceans, so many of earth’s other creatures, including marine and terrestrial mammals, birds (such as our robin) and insects, have evolved over millions of years a sense that detects the earth’s magnetic field and uses it to navigate.
The earliest evidence of this capability was provided by a Russian zoologist, Aleksandr von Middendorf (1815–94), who recorded the places and dates of arrival of several species of migratory birds. On the basis of these data he drew a number of curves on a map, which he referred to as isepipteses (lines of simultaneous arrival). From these, which reflected the directions of arrival of the birds, he deduced that there was “a general convergence northward” toward the magnetic north pole. When he published his findings in the 1850s he proposed that migratory birds orientate themselves by the earth’s magnetic field, referring to them as “sailors of the air” that can navigate “in spite of wind, weather, night or cloud.”6
Most other nineteenth-century zoologists remained skeptical. Paradoxically, even those scientists who were prepared to accept more outlandish pseudoscientific notions like paranormal activity—and there were many prominent scientific names in the late nineteenth century who did so—could not believe that magnetic fields could influence life. Joseph Jastrow, for example, an American psychologist and psychic researcher, in July 1886 published a letter in the journal Science entitled “The existence of a magnetic sense.” He described experiments he had carried out to test whether humans could be in any way affected by a magnetic field, but had to report that he found no sensitivity whatsoever.
Yet if you fast-forward from Jastrow into the twentieth century you encounter the work of Henry Yeagley, an American physicist who carried out research for the US Army Signal Corps during the Second World War. Avian navigation was of interest to the military because homing pigeons were still being used to carry messages and aviation engineers hoped to learn from their navigational capabilities. Yet how the birds managed to find their way home so unerringly remained a mystery. Yeagley developed a theory that homing pigeons could sense both the earth’s rotation and its magnetic field. This, he claimed, would create a “navigational grid work” in the bird’s brain, giving it both longitude and latitude coordinates. He even tested his theory by attaching small magnets to the wings of ten pigeons and nonmagnetic strips of copper of the same weight to ten others. Eight of the ten birds with copper strips attached to their wings found their way home, but only one of the ten pigeons with magnets attached to their wings managed to reach their nest. Yeagley concluded that the birds utilize a magnetic navigational sense to navigate, which could be disrupted by magnetic strips.7
Although Yeagley’s experimental results were initially dismissed as far-fetched, several researchers have since established beyond reasonable doubt that a wide range of animals have an inbuilt sensitivity to the earth’s magnetic field, giving them an acute sense of direction. Sea turtles, for example, are able to return to the same breeding beach, thousands of kilometers away from their ocean feeding grounds, without any visual landmarks; and researchers have shown that their navigational sense is impaired if powerful magnets are attached to their heads. In 1997, a team at the University of Auckland in New Zealand published research in Nature suggesting that the rainbow trout uses magnetoreceptor cells located in its nose.8 If proved correct, this would be the first example of a species that is able to smell the direction of the earth’s magnetic field! Microbes use the earth’s magnetic field to help navigate through murky water; and even organisms that don’t migrate, such as plants, appear to retain a magnetoreception sense.
The ability of animals to detect the earth’s magnetic field is no longer in doubt. The mystery is how they do it, not least because the earth’s magnetic field is extraordinarily weak and would not normally be expected to influence any chemical reactions in the body. There are two principal theories, and both are likely to be involved in different animal species. The first is that the sense functions like a conventional magnetic compass, while the second is that magnetoreception is conferred by a chemical compass.
This first idea, that a form of conventional compass mechanism resides somewhere in an animal’s body, was bolstered by the discovery of tiny crystals of magnetite, the naturally occurring magnetic iron oxide mineral, in many of the animals and microbes that seemed to possess a magnetic sense. For example, the bacteria that utilize a magnetic sense to orientate themselves in muddy marine sediments are often filled with bullet-shaped crystals of magnetite.
By the late 1970s, magnetite had been detected in the bodies of various animal species known to navigate with the help of the earth’s magnetic field. Notably, it seemed to have been found inside neurons within the upper beaks of the most famous of avian navigators, homing pigeons,9 suggesting that their neurons were responding to magnetic signals picked up by the magnetite crystals and then sending a signal to the animal’s brain. More recent research showed that pigeons became disorientated and lost their ability to track the geomagnetic field when small magnets were attached to their upper beaks, where those magnetite-filled neurons were apparently located.10 It seemed that the origin of a magnetoreceptive sense had finally been located.
However, it was back to the drawing boards in 2012 when yet another paper appeared in Nature describing a detailed 3-D study of the pigeon’s beak using an MRI scanner, which concluded that those magnetite-containing cells in the pigeon’s beak almost certainly had nothing to do with magnetoreception at all but were in fact iron-rich cells called macrophages that are involved in immunity to pathogens, not, as far as is known, sensory perception.11
It’s at this point that we should rewind the clock and return to that remarkable German ornithologist, Wolfgang Wiltschko, whom we first met in chapter 1. Wiltschko’s interest in bird navigation began in 1958 when he joined a Frankfurt-based research group run by the ornithologist Fritz Merkel. Merkel was one of the few scientists at the time studying the magnetic sense of animals. One of his students, Hans Fromme, had already shown that some birds could orientate themselves inside featureless closed rooms, which demonstrated that their navigational capability was not based on visual clues. Fromme had proposed two possible mechanisms: either the birds were receiving some sort of radio signals from the stars or they could sense the earth’s magnetic field. Wolfgang Wiltschko suspected the latter.
In the autumn of 1963, Wiltschko began conducting experiments with European robins, which as you may remember normally migrate between northern Europe and North Africa. He placed robins, captured in mid-migration, inside magnetically shielded chambers and then exposed the birds to a weak, artificial, static magnetic field generated by a device called a Helmholtz coil that can mimic the earth’s geomagnetic field but whose strength and orientation can be changed. What he found was that those birds captured during migration in the autumn or the spring became restless and would cluster on the side of the chamber that coincided with their migratory direction relative to the artificial field. After two years of painstaking effort he published findings in 1965 demonstrating that the birds were sensitive to the direction of the applied field and so, he surmised, could similarly detect the earth’s magnetic field.
These experiments conferred a degree of respectability on the idea of avian magnetoreception and sparked further research. But, at the time, no one had the faintest idea how this sense worked—how the extremely weak magnetic field of the earth could actually influence the bodies of animals. Scientists couldn’t even agree where in an animal’s body the magnetoreception sensory organ was situated. Even after magnetite crystals were found in several animal species, implying a conventional magnetic compass mechanism, the robin’s navigational capability remained a mystery because no magnetite could be detected in the bird’s body. The robin’s sense also displayed several puzzling features that didn’t fit with a magnetic compass, not least because the birds lost their ability when they were blindfolded, indicating that they need to “see” the earth’s magnetic field. But how does any animal see a magnetic field?
It was in 1972 that the Wiltschkos (Wolfgang having by this time teamed up with his wife, Roswitha) discovered that the robin’s compass was unlike any that had been previously studied. A normal compass has a magnetized needle, one end of which (its south pole) is attracted toward the magnetic north pole of the earth, while the other end points toward the south pole. But there is a different kind of compass that doesn’t discriminate between the magnetic poles. This, you may remember from chapter 1, is called an inclination compass; and it points to whichever pole is nearest, so it can only tell you if you are heading either toward or away from that pole, whichever one it is. One way of providing this kind of information is to measure the angle of the earth’s magnetic field lines with respect to the surface of the earth (figure 6.1). This angle of inclination (hence the name for this kind of compass) is near-vertical (pointing into the ground) close to the poles, but parallel to the ground at the equator. Between the equator and the poles the magnetic field lines enter the earth at some angle less than 90° and that angle points toward the nearest pole. So any device that measures this angle can function as an inclination compass and provide directional information.
In their 1972 experiments the Wiltschkos trapped the test birds in a shielded chamber and subjected them to an artificial magnetic field. Crucially, reversing the polarity of the field, by turning the magnet around by 180°, had no effect on their behavior: the birds would orientate themselves in relation to the closest magnetic pole, whichever one it happened to be; so they didn’t possess a conventional magnetic compass. That 1972 paper established that the robins’ magnetoreceptor was indeed an inclination compass. But how it worked remained a mystery.
Then in 1974 Wolfgang and Roswitha were invited to Cornell University in the United States by the American bird migration expert Steve Emlen. In the 1960s he had developed with his father, John, also a highly respected ornithologist, a special bird chamber that became known as an Emlen funnel.*1 Shaped like an inverted cone, this funnel has an ink pad at the bottom and blotting paper on the interior sloping sides (figure 6.2). When a bird hops or flutters up the sloping walls it leaves telltale footprints that give information about the preferred direction in which it would fly if it could escape. The bird species the Wiltschkos studied at Cornell University was the indigo bunting, a small North American songbird that, like the European robin, migrates using some kind of internal compass. Their year-long study of this bird’s behavior inside the Emlen funnel was published in 1976,12 and established beyond doubt that the indigo bunting, like the robin, was able to detect the geomagnetic field. Wolfgang Wiltschko regards the publication of this first Cornell-based paper as the team’s breakthrough moment, for it established beyond doubt that migratory birds have a built-in magnetic compass and caught the attention of many of the world’s leading ornithologists.
Of course, no one in the mid-1970s had a clue how a biological magnetic compass might work. However, as we saw in chapter 1, in the same year that the Wiltschkos and Stephen Emlen published their work, the German chemist Klaus Schulten proposed a chemical mechanism that links light with magnetoreception. Schulten had recently graduated from Harvard with a PhD in chemical physics and returned to Europe, where he obtained a position at the Max Planck Institute for Biophysical Chemistry in Göttingen. There he became interested in the possibility that electrons generated in the fast triplet reaction by exposure to light could be quantum entangled. His calculations suggested that if entanglement was indeed involved in chemical reactions then the speed of these reactions should be affected by an external magnetic field, and he proposed a way of proving his theory.
As he talked freely about his idea, Schulten developed a reputation at the Max Planck Institute for being regarded as somewhat crazy. His problem was that he was a theoretical physicist who worked with paper, pen and computers, not a chemist; and certainly not an experimental chemist capable of donning a lab coat and performing the kind of experiment that would prove his ideas. Thus he was in the position of many theoreticians who come up with a neat idea but have then to find a friendly experimentalist willing to take time out of their busy lab schedule to test a theory that, more often than not, will prove to be wrong. Schulten had no luck in persuading any of his chemist colleagues to try out his idea, because none of them believed that his proposed experiment had any chance of success.
The source of all this skepticism, Schulten discovered, was the institute’s lab manager, Hubert Staerk. Eventually Schulten summoned up the courage to confront Staerk in his office, where he finally learned the reason for this entrenched skepticism: Staerk had already done the experiment and found no effect of magnetic fields. Schulten was thunderstruck. It seemed that his hypothesis was to suffer the fate described by the evolutionary biologist Thomas Huxley as just another “beautiful theory … killed by an ugly fact.”
After thanking Staerk for conducting the experiment, the dejected Schulten was about to leave his office, but then turned back and asked to see the disappointing data. When Staerk showed him the file, Schulten’s mood suddenly lifted. He noticed something that Staerk had missed: a small but significant blip in the data that he had perfectly predicted. He recalls that it was “exactly what I expected, and so I was very happy that I saw it. A disaster turned into a happy moment, because I knew what to look for. He didn’t.”13
Schulten immediately set to writing what he was sure would be a breakthrough scientific paper—but he was soon to get another shock. Sharing a drink at a conference with a colleague, Maria-Elisabeth Michel-Beyerle, from the Technical University of Munich, he discovered that Michel-Beyerle had done the exact same experiment. This put Schulten in an ethical quandary. He could reveal his discovery and potentially prompt Michel-Beyerle to rush back to Munich to write her own paper, which might scoop his own publication; or he could make his excuses and high-tail it back to Göttingen to write up his own results. But if he did flee without saying a word and then published first, Michel-Beyerle might later accuse him of stealing her idea. He recalls his thoughts: “If I don’t now tell what I know, she may say I went home to do the experiment.”14 In the end, Schulten came clean and admitted to Michel-Beyerle that he had done similar work. Both scientists stayed for the remainder of the conference and then returned to their respective homes to write their own papers (Schulten’s appeared just a little before Michel-Beyerle’s) describing the discovery that the weird property of quantum entanglement can indeed influence chemical reactions.
Schulten’s 1976 paper15 proposed that quantum entanglement was responsible for the speed of the exotic fast triplet reactions studied in the Max Planck laboratory; but his groundbreaking paper also presented Staerk’s experimental data, which clearly showed that the chemical reaction was sensitive to magnetic fields. With two big results “in the bag,” many scientists would have been content; but Schulten, not yet thirty, still possessed the recklessness of youth and was prepared to stick his neck out yet farther. Aware of the Wiltschkos’ robin migration work and the problem of finding a plausible chemical mechanism for a biological compass, he realized that his spinning electrons could provide such a mechanism; and in a 1978 paper he proposed that the avian compass depended on a quantum-entangled radical pair mechanism.
At the time, hardly anyone took this idea seriously. Schulten’s colleagues at the Max Planck Institute considered it to be just another of his crazy notions, and the editors of Science, the top scientific journal to which he first sent his paper, were similarly unimpressed, writing: “A less bold scientist may have designated this idea to the waste paper basket.”16 Schulten describes his response: “I scratched my head and thought, ‘This is either a great idea or entirely stupid.’ I decided it was a great idea and published it quickly in a German journal!”17 But at this juncture most scientists, if they knew about it at all, filed Schulten’s speculative theory away with pseudoscientific and paranormal explanations of magnetoreception.
Before we can see how Schulten’s and the Wiltschkos’ work might help to explain how birds find their way around the globe, we need to return to the mysterious quantum world and take a careful look at the phenomenon of entanglement, which we described briefly in the first chapter of this book. You may remember that entanglement is so strange that even Einstein insisted that it could not be correct. First, however, we need to introduce you to another peculiar property of the quantum world: “spin.”
Many popular science books on quantum mechanics use the concept of “quantum spin” to highlight the strangeness of the subatomic world. We’ve chosen not to do so here simply because it is probably the notion furthest removed from anything that we can conceptualize using everyday language. But we cannot put the task off any longer, so here goes.
Just as the earth spins on its axis as it orbits the sun, so electrons and other subatomic particles have a property called spin that is distinct from their normal motion. But, as we hinted in chapter 1, this “quantum spin” is unlike anything that we can visualize on the basis of our everyday experience of spinning objects like tennis balls or planets. For a start, it doesn’t really make sense to talk about the speed of an electron spinning, as its spin can only take on one of two possible values: it is quantized, just as energy is quantized at the quantum level. Electrons can only—in a loose sense—spin in either a clockwise or a counterclockwise direction, corresponding to what is usually referred to as spin “up” or spin “down” states. And because this is the quantum world, an electron can, when not being watched, spin in both directions at the same time. We say that their spin state is a superposition (i.e., combination or mixture) of spin-up and spin-down. In a sense, this may sound even weirder than saying that an electron can be in two locations at once—for how can a single electron spin both clockwise and counterclockwise at the same time?
And just to stress how counterintuitive this notion of quantum spin is, what we regard as a 360° rotation will not take an electron back to its original state; to do that, it needs to make two full rotations. This sounds strange because we still tend to think of an electron as a tiny sphere, maybe something like a very small tennis ball. But tennis balls are inhabitants of the macroscopic world, and electrons live in the subatomic quantum world where the rules are different. In fact, electrons are not only not tiny spheres, they cannot even be said to have a size at all. So, while quantum spin is just as “real” as the rotation of a tennis ball, it doesn’t have a counterpart in the familiar everyday world and cannot be pictured.
However, do not therefore think that this is just an abstract mathematical concept that exists only in textbooks and impenetrable physics lectures. Every electron in your body, and everywhere else in the universe, spins in this peculiar way. In fact, if they didn’t, the world as we know it, including us, just couldn’t exist, because quantum spin plays a key role in one of the most important ideas in science, namely the Pauli Exclusion Principle, which underpins the whole of chemistry.
One of the consequences of the Pauli Exclusion Principle is that if two electrons are paired up in an atom or molecule and have the same energy (remember from chapter 3 that the chemical bonds that hold molecules together are made up of electrons that are shared between atoms), then they have to have opposite spin. We can then think of their spins as canceling out, and we refer to them as being in a spin singlet state, since they can only inhabit a single state. This is the normal state of pairs of electrons in atoms and most molecules. However, when not paired together at the same energy level, two electrons can spin in the same direction, and this is called a spin triplet state,*2 as in the reaction that Schulten studied.*3
You may be familiar with highly dubious claims that identical twins are able to sense each other’s emotional states even when separated by vast distances. Somehow, the idea goes, twins are joined at a psychic level that science has yet to understand. Similar claims have been made to explain how a dog apparently senses when its owner is coming home. We should clarify that neither of these examples has any scientific merit, even though some people have mistakenly tried to ascribe to them a quantum mechanical basis. However, although such “instantaneous action at a distance” (as it is often described) is not found in our everyday classical world, it is a key feature of the quantum domain. Its technical name is nonlocality, or entanglement, and it refers to the idea that something happening “over here” can have an instantaneous effect “over there” no matter how far away “there” is.
Consider a pair of dice. The mathematical probability of throwing a double is easy to work out. For any given number that one of the dice lands on, there is a one in six chance that the other die will land on the same. For example, the probability of the first die being a four is 1/6, and the chances of a double four are one in thirty-six (since 1/6 × 1/6 = 1/36). So the chances of throwing any pair of numbers, a double, are of course one in six. And by multiplying 1/6 by 1/6 ten times, it is straightforward enough to calculate that the probability of throwing a double ten times in a row (regardless of what it is—for example, a double four, then a double one, and so on) is about one in sixty million! This means that if every person in Britain were to have a go at throwing a pair of dice ten times in succession then, statistically, only about one person will get all doubles every time.
But imagine that you were presented with a pair of dice that always lands on a double when thrown together. The actual number that they both land on appears to be random, usually changing at every throw, but both dice always end up rolling onto the same number. Clearly, you would assume some trickery. Perhaps these dice have some sophisticated internal mechanism that controls their motion, such that they land on numbers in an identical preprogrammed sequence? To test this theory you start by holding on to one of the dice while throwing the other, but thereafter throwing pairs of dice. Now any preprogrammed series will be out of step, so the trick shouldn’t work. But despite this stratagem, the dice persist in landing on the same number.
Another possible explanation is that the dice must somehow be able to resynchronize before each throw by exchanging a remote signal. While such a mechanism seems rather sophisticated, it is at least possible to imagine in principle. However, any such mechanism would be subject to a limitation imposed by Einstein’s theory of relativity, according to which no signal can travel faster than the speed of light. This provides you with a means of testing whether any signal is passing between the dice: all you need to do is ensure the dice are sufficiently far apart that there isn’t enough time for any synchronizing signal to be exchanged in between throws. So let’s imagine you try the same trick, as above, but somehow arrange for one die to be thrown on earth and the other to be thrown simultaneously on Mars. Even at its closest distance from earth, light takes four minutes to travel between the two planets, so you know that any synchronizing signal must suffer a similar delay. To beat it, you simply arrange for the two dice to be thrown at intervals more frequent than this. This should prevent any signal from synchronizing the dice between throws. If they continue to fall on matching numbers, then there would seem to have to be an intimate connection between them that ignores Einstein’s famous limitation.
Although the above experiment hasn’t been performed with interplanetary dice, analogous experiments have been performed with quantum-entangled particles on earth, and the results show that separated particles can perform the same kind of trick that we imagined for our dice: their state can remain correlated irrespective of the distance between them. This bizarre feature of the quantum world seems not to respect Einstein’s cosmic speed limit, for a particle in one place can instantaneously influence another, however far apart the two may be. The term “entanglement” to describe this phenomenon was coined by Schrödinger who, along with Einstein, was not a fan of what Einstein referred to as “spooky action at a distance.” But, despite their skepticism, quantum entanglement has been proved in many experiments and is one of the most fundamental ideas in quantum mechanics, with many applications and examples in physics and chemistry—and, as we shall see, possibly in biology too.
To understand how quantum entanglement gets tangled up with biology we have to combine two ideas. The first is this instantaneous connection between two particles across space: entanglement. The second is that ability of a single quantum particle to be in a superposition of two or more different states at once: for example, an electron could be spinning both ways at once, so we would say it was in a superposition of “spin up” and “spin down” states. We combine these two ideas by having two entangled electrons in an atom, each in a superposition of its two spin states. Although neither has a definite spin direction, whatever it is doing influences and is influenced by the spin of its partner. But remember that pairs of electrons in the same atom are always in a singlet state, which means that they have to have opposite spin at all times: one must be spin-up and the other must be spin-down. So although both electrons are in a superposition of being both up and down at the same time, in a peculiar quantum way they must, at all times, have opposite spin.
Now let’s separate the two entangled electrons so that they are no longer in the same atom. If we then decide to measure the spin state of one electron we will force it to choose which way it is spinning. Say we find that, after measurement, it is spin-up. Because the electrons were in an entangled singlet spin state, this means that the other electron must now be spin-down. But remember that, before measurement, both were in a superposition of spinning up and down. After measurement both have distinct states: one of them is up and the other is down. So the second electron has instantly and remotely changed its physical state from being in a superposition of spinning both ways at once to being spin-down—without being touched. All we have done is to measure the state of its partner. And in principle it doesn’t matter how far away this second electron is—it could be on the other side of the universe and the effect would be the same: measuring just one of an entangled pair immediately collapses the superposition of the other, irrespective of how far away it is.
Here is a useful analogy that may help you (just a little!). Imagine a pair of gloves, each in a sealed box, but separated by many miles. You have in your possession one of the boxes and, before opening it, you do not know whether yours is the left-handed or right-handed glove. Once you open the box and discover the right-handed glove you instantly know that the other glove in the unopened box is left-handed, no matter how far away the other box is. What is crucial here, however, is that all that has changed is your knowledge. The remote box had always contained the left-handed glove, irrespective of whether or not you chose to open your box.
Quantum entanglement is different. Before the measurement, neither electron has a definite spin direction. It is only the act of measurement (of either entangled particle) that forces both electrons to change their state from each being in a quantum superposition of both up and down to being in a definite state of up or down; whereas with the gloves it was only your ignorance of the pre-existing definite state of the gloves that was banished. Not only does quantum measurement of one electron force it to “choose” to spin either up or down; that “choice” instantaneously forces its twin to adopt the complementary state, no matter how far away it is.
There is one further subtlety that needs to be added. As we have already discussed, two electrons are in a combined singlet state when they are coupled together and spinning in opposite directions, and in a triplet state when they are spinning in the same direction. If one electron from a singlet pair sitting in the same atom jumps across into a neighboring atom, its spin can flip over so that it is now spinning in the same direction as the twin it left behind, creating a triplet spin state. However, despite now being in different atoms, the pair can still maintain their delicate entangled state in which they remain quantum mechanically coupled together.
But this is the quantum world, and just because the electron that jumped out of the atom can now flip its spin, this doesn’t mean that it definitely has. Each of the two electrons will still be in a superposition of spinning both ways at once, and as such the pair will exist in a superposition of being in a singlet and a triplet state simultaneously: spinning in the same direction and in opposite directions at the same time!
So now that you have been suitably primed, and probably confused, it is time to introduce you to the strangest and yet most celebrated idea in the field of quantum biology.
At the beginning of this chapter we discussed the problem of how something as weak as the earth’s magnetic field can provide sufficient energy to alter the outcome of a chemical reaction and thereby generate a biological signal that will, for example, tell a robin in which direction it needs to fly. The Oxford-based chemist Peter Hore has a very nice analogy of how such extreme sensitivity might be possible:
Imagine we have a block of granite weighing one kilogram and ask whether a fly could tip it over. Common sense says the answer is, surely, no. But suppose I were to poise the stone on one of its edges. Clearly it would not be stable in such a position and would tend to fall to the left or the right if left to its own devices. Now suppose that while the block is teetering in this way a fly were to land on its right hand side. Even though the energy imparted by the fly would be tiny, it could be enough to cause the block to fall to the right rather than the left.18
The moral is that tiny energies can have significant effects, but only if the system on which they operate is very finely balanced between two different outcomes. So, to detect the impact of the earth’s very weak magnetic field we need the chemical equivalent of a granite block in a finely balanced state, such that it could be dramatically affected by the slightest of external influences, such as a weak magnetic field.
And now we come back to Klaus Schulten’s fast triplet reaction. You may recall that electronic bonds between atoms are often formed by the sharing of a pair of electrons. This electron pair is always entangled and almost always in a singlet spin state: that is, the electrons have opposite spin. However, remarkably, the two electrons can remain entangled even after the bond between the atoms is broken. The separated atoms, which are now called free radicals, can drift apart, and it becomes possible for the spin of one of the electrons to flip over so that the entangled electrons—now on different atoms—find themselves in a superposition of both singlet and triplet states, as in Schulten’s fast triplet reaction.
An important feature of this quantum superposition is that it isn’t necessarily equally balanced: the probabilities of our catching the entangled pair of electrons in the singlet or triplet state are not equal. And, crucially, the balance between these two probabilities is sensitive to any external magnetic field. In fact, the angle of the magnetic field with respect to the orientation of the separated pair strongly influences the likelihood of catching it in a singlet or triplet state.
Radical pairs tend to be very unstable, so their electrons will often recombine to form the products of the chemical reaction. But the precise chemical nature of the products will then depend on this singlet–triplet balance, with all its sensitivity to magnetic fields. To understand how it works, we can think of the free radical intermediate stage of the reaction state as being like that metaphorical balanced granite block. In this state, the reaction is so delicately poised that even a weak magnetic field—taking the place of the fly—of less than 100 microtesla, such as the earth’s, is sufficient to influence the way that the singlet/triplet state coin toss falls to generate the products of the chemical reaction.19 Here at last was a mechanism by which magnetic fields could influence chemical reactions, and thereby, Schulten claimed, provide a magnetic compass for birds.
But Schulten had no idea where in the bird’s body this proposed radical pair reaction was taking place—presumably it would make most sense for it to be located in the brain. But for it to work, the radical pair had to be created in the first place (just as the granite block needs to be tipped onto its edge). He presented his work at Harvard in 1978, describing the experiments carried out by his group in Göttingen in which a laser pulse was used to create an entangled radical pair of electrons. In the audience was an eminent scientist named Dudley Herschbach, who would later go on to win a Nobel Prize in chemistry. At the end of the lecture Herschbach asked as a good-natured jibe: “But Klaus, where in the bird is the laser?” Under pressure to provide a sensible answer to such a senior professor, Schulten suggested that if indeed light was needed to activate the radical pair, then maybe that process took place within the bird’s eye.
In 1977, a year before Schulten’s radical pair paper, an Oxford physicist named Mike Leask had speculated in another Nature paper that the origin of the magnetic sense might indeed lie within photoreceptors in the eye.20 He had even suggested that the eye pigment molecule, rhodopsin, was responsible. When Wolfgang Wiltschko read Leask’s paper he was intrigued, although he had no experimental evidence to suggest that light played a role in avian magnetoreception. So he set out to test Leask’s idea.
At the time, Wiltschko had been conducting experiments on homing pigeons to see whether they gathered magnetic navigational information on their outward journey that they then used to find their way back home. He had found that subjecting the pigeons to a disrupting magnetic field while being transported away from their home messed up their ability to find their way back when released. Inspired by Leask’s theory, he decided to conduct the experiment again, this time without the magnetic field disturbance. Instead, he transported the pigeons in total darkness in a box on the roof of his Volkswagen bus. The birds then had difficulty finding their way home, demonstrating that they required light to help them plot out a magnetic map of their outward journey, which they would then use to track their way home.
The Wiltschkos finally met Klaus Schulten at a conference in the French Alps in 1986. They were by this time convinced that the robin’s magnetoreception relied on light entering its eye but, like almost everyone else interested in the biochemical effects of magnetic fields, they were not yet persuaded that the radical pair hypothesis was correct. Indeed, no one knew where in the eye the radical pair might form. Then, in 1998, the pigment protein cryptochrome was discovered in the eyes of fruit flies and, as we described earlier in the chapter, was shown to be responsible for the light-driven entrainment of their circadian rhythms. Crucially, cryptochrome was known to be the kind of protein capable of forming free radicals during its interaction with light. This was seized upon by Schulten and his coworkers to propose that cryptochrome was the elusive receptor for the avian chemical compass. Their work was published in 2000 and would become one of the classic papers of quantum biology.21 The lead author on that paper was of course Thorsten Ritz, whom we also met in chapter 1 and who at this point was working on his PhD with Klaus Schulten. Now at the physics department at the University of California, Irvine, Thorsten is today regarded as one of the world’s leading experts on magnetoreception.
The 2000 paper is important for two reasons. First, it proposed cryptochrome as the candidate molecule for the chemical compass; and second, it described in beautiful—albeit speculative—detail just how the bird’s orientation in the earth’s magnetic field might affect what it sees.
The first step in their scheme is the absorption of a photon of blue light by the light-sensitive pigment molecule, FAD, that sits within the cryptochrome protein, and which we met earlier in the chapter. As we described, the energy of this photon is used to eject an electron from one of the atoms within the FAD molecule, leaving behind an electron vacancy. This can be filled by another electron donated from an entangled pair of electrons in an amino acid called tryptophan within the cryptochrome protein. Crucially, however, the donated electron can remain entangled with its partner. The pair of entangled electrons can then form a superposition of singlet/triplet states, which is the chemical system that Klaus Schulten found to be so exquisitely sensitive to a magnetic field. Once again, the delicate balance between the singlet/triplet states is highly sensitive to the strength and angle of the earth’s magnetic field, so that the direction in which the bird flies makes a difference to the composition of the final chemical products that are generated by the chemical reaction. Somehow, in a mechanism that isn’t at all clear even now, this difference—which way the granite block tumbles—generates a signal that is sent to the bird’s brain to tell it where the nearest magnetic pole lies.
This radical pair mechanism proposed by Ritz and Schulten was certainly very elegant; but was it real? At the time there wasn’t even any evidence that cryptochrome can generate free radicals when exposed to light. However, in 2007 another German group, this time based at the University of Oldenburg and led by Henrik Mouritsen, was able to isolate cryptochrome molecules from the retina of the garden warbler and show that they did indeed produce long-lived radical pairs when exposed to blue light.22
We have no idea what this magnetic “seeing” looks like to birds, but since cryptochrome is an eye pigment that is potentially doing a similar job to the opsin and rhodopsin pigments that provide color vision, perhaps the birds’ view of the sky is imbued with an extra color invisible to the rest of us (just as some insects can see ultraviolet light) that maps onto the earth’s magnetic field.
When Thorsten Ritz proposed his theory in 2000 there was no evidence for cryptochrome being involved in magnetoreception; but now, thanks to the work of Steve Reppert and colleagues, the same pigment is known to be involved in how fruit flies and monarch butterflies detect external magnetic fields. In 2004, researchers found three types of cryptochrome molecules in eyes of robins; and then in 2013 a paper from the Wiltschkos (still as active as ever, even though Wolfgang has now retired) demonstrated that cryptochrome extracted from the eyes of chickens*4 absorbed light at the same frequencies as those they discovered were important for magnetoreception.23
But does the process definitely rely on quantum mechanics in order to work? In 2004, Thorsten Ritz went to work with the Wiltschkos to try to differentiate between a conventional magnetite compass and a chemical compass based on their free radical mechanism. Compasses can of course be disrupted by anything magnetic: hold a compass close to a magnet and it will point to the magnet’s north pole rather than the earth’s. A standard bar magnet produces what is called a static magnetic field, which means that it doesn’t change with time. However, it is also possible to generate an oscillating magnetic field—by, for example, rotating a bar magnet—and this is where it gets interesting. A conventional compass may still be disrupted by an oscillating magnetic field, but only if the oscillations are slow enough for the needle of the compass to track. If the oscillations are taking place very fast, say hundreds of times a second, then the needle of the compass can’t track them any more, and their influence averages to zero. So a conventional compass may be disrupted by magnetic fields oscillating at low frequencies but not at high frequencies.
But a chemical compass will have a very different response. You will remember that the chemical compass was proposed to depend on radical pairs being in a superposition of singlet and triplet states. Because the two states differ in their energy and energy is related to frequency, the system will be associated with a frequency that, considering the energies involved, would be expected to be in the millions of oscillations per second range. A classical way of thinking about what is going on that may be easier to imagine (though it is not strictly correct) is that the entangled pair of electrons is flipping between singlet and triplet state many millions of times a second. In this state, the system can interact with an oscillating magnetic field by the process of resonance, but only if the field is oscillating at the same frequency as the radical pair: only if, to use our previous musical analogy, they are in tune. The resonance will then pump energy into the system that will change that critical balance between singlet and triplet states on which the chemical compass depends—essentially, tipping over that metaphorical granite block before it has time to detect the earth’s magnetic field. So, in contrast to a conventional magnetite compass, a radical pair compass will be disrupted by magnetic fields that oscillate at very high frequencies.
The Ritz–Wiltschko team set up an experiment to test this very clear prediction of the radical pair theory using the European robin: Would its compass be sensitive to low- or high-oscillating magnetic fields? They waited until the autumn, when the birds would be getting impatient to migrate south, and then placed them inside Emlen funnel chambers. They applied oscillating fields from various directions and at various frequencies and waited to see whether the fields could disrupt the birds’ natural ability to orientate themselves.
The results were astonishing: a magnetic field tuned to 1.3 MHz (that is, oscillating at 1.3 million cycles per second), thousands of times weaker than even the earth’s field, could nevertheless disrupt the birds’ ability to orientate themselves. But increasing or decreasing the frequency of the field made it less effective. So the field appeared to be resonating with something vibrating at very high frequencies in the avian compass: clearly not a conventional magnetite-based compass, but something consistent with an entangled radical pair in a superposition of singlet and triplet states. This intriguing result24 also shows that, if it exists, the entangled pair must be able to survive in the face of decoherence for at least a microsecond (a millionth of a second), because otherwise its lifetime would be too short to experience the ups and downs of the applied oscillating magnetic field.
However, the significance of this result has recently been questioned. Henrik Mouritsen’s group at the University of Oldenburg showed that manmade electromagnetic noise, from a wide range of electronic devices, seeping through the walls of the unscreened wooden huts housing the birds at the university campus disrupted their magnetic compass orientation. But the capability returned once they were placed in aluminium-screened huts, which cut out about 99 percent of the urban electromagnetic noise. Crucially, their results suggest that the disruptive effect of radio-frequency electromagnetic fields may not be confined to a narrow frequency band after all.25
So there are still aspects of the system that remain mysterious; for example, why the robin’s compass should be so hypersensitive to oscillating magnetic fields, and how free radicals can remain entangled for long enough to make a biological difference. But in 2011, a paper from Vlatko Vedral’s laboratory in Oxford presented quantum theoretical calculations of the proposed radical pair compass and demonstrated that superposition and entanglement should be sustained for at least tens of microseconds, greatly exceeding the durations achieved in many comparable manmade molecular systems; and potentially long enough to tell a robin which way it needs to fly.26
These remarkable studies have sparked an explosion of interest in magnetoreception, which has now been demonstrated in a wide range of species including a whole host of bird species, spiny lobsters, stingrays, sharks, fin whales, dolphins, bees and even microbes. In most cases, the mechanisms involved haven’t yet been investigated, but cryptochrome-associated magnetoreception has now been discovered in a wide range of creatures from our doughty robin to the chickens and fruit flies we have already mentioned and several other organisms, including plants.27 A study published by a Czech group in 2009 demonstrated magnetoreception in the American cockroach and showed that, as with the European robin, it was disrupted by high-frequency oscillating magnetic fields.28 A follow-up study presented at a conference in 2011 showed that the cockroaches’ compass required functional cryptochrome.
The discovery of a capability and a shared mechanism so widely distributed in nature suggests that it has been inherited from a common ancestor. But the common ancestor of chickens, robins, fruit flies, plants and cockroaches lived way, way back: more than five hundred million years ago. So quantum compasses are probably ancient, and are likely to have provided navigational skills for the reptiles and dinosaurs that roamed the Cretaceous swamps alongside the T. rex we met in chapter 3 (remember that modern birds such as robins are descended from dinosaurs), the fish that swam the Permian seas, the ancient arthropods that crawled over or burrowed beneath the Cambrian oceans and maybe even the pre-Cambrian microbes that were the ancestors of all cellular life. It seems that Einstein’s spooky action at a distance may have been helping creatures to find their way around the globe for most of the history of our planet.
*1 Not to be confused with Emlen Tunnell, the great American football player of the 1950s.
*2 The term “triplet” here can be confusing to the nonexpert in quantum mechanics, especially since it refers to just a pair of electrons, so here is a very brief explanation: an electron is said to have a spin of ½. So, when a pair of electrons have opposite spin, these values cancel: ½−½ = 0. This is referred to as a spin singlet state. But when they have their spins pointing in the same direction, these values add up: ½ + ½ = 1. The term “triplet” refers to the fact that a combined spin of 1 can be pointing in three possible directions (up, down and sideways).
*3 The two unpaired electrons in an oxygen molecule that hold its two atoms together are normally in a spin triplet state.
*4 Chickens do not of course migrate, even in the wild. But they still appear to retain magnetoreception.
