The inner compass / Davida Castelvecki

Animals do have a magnetic sense. Scientists are beginning to understand how it works

For six months that seemed like an eternity in 2007, Sabine Begel, a zoologist at the University of Duisburg-Essen in Germany, spent the evenings in front of the computer, staring at pictures of cows in a pasture. She downloaded a satellite image of a pasture from Google Earth, tagged the cows one by one, then downloaded the next image. With the help of her colleagues, Begel discovered, in the end, that the migration rates of these low-spirited people were up to something. On average, they seemed to be positioned with a slight preference towards the north-south axis. But they did not turn towards the true north, which they could locate with the help of the sun. Instead, they somehow knew to turn in the direction of the magnetic north pole, located in northern Canada, hundreds of kilometers south of the geographic pole.

 

Follow-up research turned up more evidence that large animals, such as cows, can respond to the Earth's magnetic field: the alignment of cows with respect to north disappeared near high-voltage power lines that overpowered the relatively subtle signals originating from the Earth.

A few decades ago, studies like Begel's would have been met with ridicule. Everyone knew that organic matter does not respond to weak magnetic fields like the Earth's, and that animals are not equipped with magnets like those used in compasses. In the 18th century, Franz Anton Mesmer believed in "animal magnetism", that is, that breathing creatures contain magnetic fluids in their bodies, but this belief has long since been banished to the realms of charlatanism.

Today the scientific community recognizes that there are animals that read magnetic fields and respond to them, and that for many of them this ability gives them a survival advantage. But why cows would want to orient themselves according to the magnetic field remains a mystery. In fact, magnetic sense has been well-documented in dozens of species, from birds like the robins and butterflies like the royal damselfly that make seasonal migrations to expert navigators like homing pigeons and sea turtles; From invertebrates like lobsters, honey bees and ants to mammals like rats and elephant seals; From tiny bacteria to large whales.

What no one knows for sure is how exactly all creatures do this except the bacteria. Magnetism is "the sense we know the least about," says Steven M. Reppert, a neurobiologist at the University of Massachusetts Medical School in Worcester.

However, collaborations between biologists, earth scientists and physicists in the last decade have begun to yield possible mechanisms and to identify anatomical structures that serve as a basis for these mechanisms. None of these ideas has yet gained the support of the entire scientific community, but the experimental evidence that has been discovered so far is certainly intriguing. There are even animals with more than one magnetic organ. Some of the biological sensors that sense magnetic fields work like a normal magnet, while others may use more subtle quantum effects.

The issue continues to stir up controversy. But the growing interest in magnetic sensing and the rapid progress in experimental methods may prompt researchers to solve the mystery of the unusual sense in the coming years.

A voice calls to wander

The first modern hints that magnetic fields sometimes guide animal behavior emerged about half a century ago. In the 50s, researchers noticed that European red-breasted birds in cages were trying to escape south in the fall, where they are supposed to migrate in the wild, even if they have no visual cues as to where south is. And in the mid-60s, Wolfgang Wilczko, a biology student at Goethe University in Frankfurt, showed that electromagnetic coils wrapped around bird cages could confuse them and make them try to escape in the wrong direction. These were probably the first evidences of a magnetic sense, and the reaction was predictably skeptical. "When I discovered that a magnetic field plays a role in the spatial orientation of red-breasted animals, in fact no one believed me," says Wilcheko, who recently retired from his position at Goethe.

Shortly after the discovery, Vilchako met his future wife and research partner, Rovezlata. Since then, the pair have studied the magnetic sense in birds, working primarily with red-breasted redbreasts caught in nets near their laboratories. The Wilchekos began to publish the results of their joint research in 1972, when they discovered that red-breasted animals are sensitive not only to the geographic direction of magnetic north but also to the angle of inclination of the Earth's magnetic field relative to the horizon.

The inclination of the Earth's magnetic field changes continuously from pole to pole. At the south magnetic pole, the field points straight up, while at the north magnetic pole it points down. About halfway, along the "magnetic equator", the field is horizontal. In a simple compass, the needle is always balanced horizontally, so the compass cannot measure the angle of inclination of the field but only the horizontal component. But it turns out that birds and other animals can actually use this information to roughly estimate the distance from the magnetic poles.

Changes in the angle of inclination from one pole to another are not the only changes in the Earth's magnetic field. It is possible to find local anomalies in both the direction and strength of magnetic minerals in the Earth's crust. Certain animals, especially sea turtles, treasure a map of these anomalies in their memory, and it helps them not only to find the north but also to know where they are in relation to their destination. Kenneth J. Lohmann of the University of North Carolina at Chapel Hill and his colleagues found that captured sea turtles tend to respond to artificial magnetic fields that simulate conditions at various landmarks along their migration routes. The turtles try to swim in the direction that would lead them to their destination if they started from these landmarks. For animals to have such a sense of magnetic mapping, it is likely that they should be sensitive not only to deviations in the angle of inclination of the magnetic field but also to changes in its strength.

Some researchers believe that birds also have a magnetic mapping sense in addition to the normal ability of magnetic orientation, but Anna Galliardo, an expert on the sense of smell in birds at the University of Pisa in Italy, says that the evidence for the existence of such a sense is weak. In her opinion, birds probably find their way around effectively using other senses. "Forty years of experiments," she says, "and no magnetic manipulation was found that prevented mail pigeons from returning home." But birds do get lost if their sense of smell is destroyed by cutting the nasal nerves, she adds. Moreover, carrier pigeons raised in cages that only open upwards, so that the birds are unable to distinguish the directions of smells from the environment, are unable to navigate. So while the evidence that birds can distinguish between magnetic north and south is pretty solid, Galliardo says, she doubts that their magnetic sense can distinguish more details.

However, many other experts now believe that birds have two separate magnetic senses, each for different purposes. One is the compass sense for the directions of the magnetic field, and the other is a "magnetometer" that senses the strength of the field. Others claim that there is evidence of the existence of each of the senses separately, but not of both in one biological species. One reason for the controversy is that the behavioral effects of magnetism are particularly difficult to characterize, in part because birds and other animals use a variety of other cues for orientation and navigation. They use the sun, stars and moon. They can recognize land landmarks and the general direction of waves at sea, and they remember smells. Animals always navigate based on several senses, says Michael Winkelhofer, a geophysicist at Ludwig Maximilian University in Munich. "They use every possible clue. And whenever any clue is not reliable enough, they switch to more reliable information."

Unfortunately, even the most solid results obtained from well-designed experiments are open to several interpretations. One of the Wilchkos' key observations was that the red-breasted compass sense does not work in the dark. To operate, it needs light that contains a blue component, that is, a component with a short wavelength. Their findings were obtained under laboratory conditions, which indeed help to isolate clues from each other, but on the other hand are somewhat artificial. However, in a 2004 study that was a landmark in the field, Henrik Mortisen from the University of Oldenburg in Germany and his colleagues discovered convincing evidence of mutual activity between light and compass in nature as well. They showed that night-flying thrushes recalibrate their magnetic sense daily at sunset.

For the purpose of the experiment, Mortisen's group captured dozens of thrushes in central Illinois, and attached radio transmitters to them. At sunset, the researchers exposed 18 birds to a magnetic field that resembled Earth's, but pointed east instead of north. After dark, they opened the cages and released the birds. The investigators followed the birds in a 1982 Oldsmobile model car that was equipped with a large antenna that protruded from the roof and often attracted the attention of police cars that stopped them for inspection. While the control group continued their migration north toward Wisconsin, the 18 birds exposed to the fake geomagnetic field headed west toward Iowa or Missouri. In the following nights, these birds corrected their course and headed north again.

Although the results suggest that the birds recalibrate magnetic north at dusk, there are differing interpretations of the role of light in the process. One possibility is that birds have an internal compass that works only in the presence of light, as the Wilczkos concluded. But another explanation seems equally possible: the birds simply used the sun as a reference point to calibrate a compass that does not need light to operate. In fact, they may have continued to use the compass all night.

If so, it is clear that behavioral experiments are not enough to decide these questions. Ultimately, the sense organs must be located and explored directly.

Rusty clues

The search for organs sensitive to a magnetic field is the greatest nightmare of anatomy researchers. The sensors may be single cells, scattered anywhere in the body. They may contain microscopic magnetic particles, the equivalent of a compass needle, and when studied they will be difficult to distinguish from impurities in the tissue samples. The mechanism will also have to meet strict requirements. In particular, it must be sensitive to weak magnetic fields like the Earth's, and it must distinguish the magnetic signal from the noise of natural molecular vibrations, a particularly difficult requirement for microscopic structures. So far, the only mechanism identified and clearly explained exists in bacteria.

At latitudes where the angle of inclination of the magnetic field is steep enough, certain bacteria use it as a substitute for gravity to "know" how to swim downward, towards the muddy sea floor, where they prefer to live. In the 70s, researchers showed that these bacteria contain strings of microscopic spherules of magnetite, a highly magnetic iron oxide structure, which align with each other and with respect to the magnetic field and in the process direct the entire organism in the right direction.

The bacteria thus served as a natural model with which one can learn about magnetic sensing in general. In the 80s, geobiologist Joseph L. Kirschwink, now at the California Institute of Technology, and others suggested that similar structures based on magnetite might exist throughout the animal kingdom. Scientists began looking for such particles in animals sensitive to magnetism.

In the early 2000s, a research group that included Winkelhofer, Wolfgang Wilczko and Greta, and Gunther Pleissner, another married couple from Goethe University, used advanced imaging methods to identify intriguing structures containing magnetic nanoparticles in postions. They discovered these structures in the skin of the birds' upper beaks. The magnetic particles were extremely small, only a few nanometers long, so any random movement of them is significant relative to their size. This means that the system is too noisy to detect the strength of a magnetic field, but in principle it is able to detect the direction of the field. "The response will not be very strong, but it can at least be used as a compass," says Winkelhofer. It is interesting to note that the areas where the structures were found are rich in nerve endings as expected from sensors supposed to be integrated into the nervous system.

Only a small part of the particles contained magnetite. The rest contained a similar material, known as maghemite, whose degree of magnetism is less. However, the researchers believed that this was the winning proof of the existence of a magnetic sense.

In a subsequent paper, the Pleisners and their colleagues proposed a model explaining how a structure containing mostly maghemite might act as a compass. They suggested that the maghemite structures might become temporarily more magnetic and therefore increase the geomagnetic field near them, channeling it into the magnetite particles.

But Winkelhofer stopped the collaboration with his colleagues and published a message with Kirschwink that they were retracting their findings. Both researchers presented evidence that the maghemite in the study was "amorphous", meaning without crystalline arrangement. Amorphous materials are extremely weak magnets, Winkelhofer says, too weak to perform the role intended for the particles discovered in the birds. Others also claim that it is not clear if the nerve endings are located exactly near the magnetic particles. It is possible that the structures discovered in the origin of mail ions have nothing to do with magnetic sensing at all, Winkelhofer concludes.

Another reason for caution is that magnetite and other magnetic particles are common in the environment. "Even dust from the laboratory contains magnetic materials," says Winkelhofer. Anatomists use ceramic scalpels to try to prevent metal particles from penetrating the tissues they remove from the animals. But if the particles have entered the body as pollutants, they may be picked up by white blood cells, which can be seen under a microscope as sensor cells.

Despite the difficulties that arose with the post ion magnetic sensor hypothesis, Winklehofer and Kirschwink remained enthusiastic supporters of the magnetite theory. They point to the best evidence, in their opinion, for the existence of such an organ: cells lining the nasal openings of the rainbow trout. Michael M. Walker of the University of Auckland in New Zealand and his colleagues have been studying the cells since they were first discovered in 1997. The researchers were able to show an electrophysiological response to magnetic fields, and the cells did send signals to the brain.

Kirschwink is now leading multi-year research in multiple laboratories to characterize the structure and behavior of these putative magnetic sensors. He suspects that the magnetic particles are contained within organelles that are directly attached to the membranes of unique nerve cells. Each such cell will serve as a microscopic magnetic sensor. When a magnetic field causes the organelles to rotate into a new configuration, they cause the release of ions that cause the nerve cells to fire and "tell" the brain which direction the fish should turn [see illustration on the previous page]. According to him, it is possible that researchers who were looking for sensors on the skin of the pigeons' beaks should learn from the fish and look in the guts of the birds.

Cryptic signals

Magnetite is not the only front-runner in the competition. Many researchers support a mechanism based on quantum physics. Klaus Schulten, a theoretical biophysicist now working at the University of Illinois at Urbana-Champaign, discovered in the 70s that chemical reactions affected by magnetic fields could serve as a physical basis for magnetic sensing. These reactions begin when a photon of light hits the appropriate pigment molecules and causes the formation of free radicals. The need for a photon can explain the possible connection that biologists found between sunlight and the sense of the compass. But in those days the idea sounded wild, and Sultan did not explain how the signal would be transmitted to the brain.

Then, in the 90s, biochemists discovered a colored protein known as cryptochrome, first in plants and then in the retina of mammals, including humans, where it is found in several versions and helps mammals coordinate the day and night cycles. Schulten, along with his colleagues Sally Adam and Thorsten Ritz, a biophysicist now working at the University of California, Irvine, argued that cryptochrome has just the right properties to serve as a compass organ and that certain cells in the retina may use the free radical pairs it creates to detect the direction of the Earth's magnetic field.

Laboratory experiments have shown that when cryptochrome absorbs a photon of blue light, the energy of the photon causes an electron to move from one part of the molecule to another. In chemically stable molecules the electrons are arranged in pairs, but the excitation of the electrons in cryptochrome causes two electrons to move separately. Now, the two electrons, called a pair of free radicals, explode in a "dance in two" dictated by the spin of each electron. In quantum physics, spin is the analog of a magnetic axis of a bar magnet. The spin of each electron reacts to the geomagnetic field and the spins of the atomic nuclei, and all these interactions together cause the axis to oscillate (in a wobble, precession) like a top. In the radical pair, the spin of each electron is also affected by that of its partner.

Sometimes, during the "dance show" of the pair of electrons, their spins point more or less in the same direction, while at other times they point in opposite directions. The important thing is that an external magnetic field, such as that of the Earth, changes the relative amount of time that the electrons are in each of the arrangements. This is how an external field might affect the chemistry of cryptochrome: certain chemical reactions can only occur when the spins are parallel to each other. Therefore, if the field keeps the spins parallel for a longer time, the rate of these reactions will increase.

The rate of occurrence of a spin-sensitive chemical reaction can be used as a chemical signal that will cause a sensory nerve cell to fire, i.e. send an electrical signal and transmit the information along the nerve to a center in the brain responsible for the behavior dependent on the magnetic field. Unfortunately, although the general principle is well known, in the case of cryptochrome, no one knows what the relevant chemical reaction is supposed to be, and how changes in its rate will cause a nerve cell to fire. And yet, in the last decade, some circumstantial evidence has emerged.

The spin-locking phenomenon is sensitive not only to stable fields, but also to fields that change rapidly with time, such as radio waves. In 2004, Ritz teamed up with the Wilchekos and they showed that radio waves disrupt the internal compass of birds. The interference occurred only at certain wavelengths, as expected if the waves do interfere with the "dance" of the radical pairs. "From the point of view of physics, this is currently the best proof of the radical pair mechanism," says Ritz.

In 2009, a research group led by Murtissen discovered that birds with damage to the center of the brain associated with vision had difficulty locating themselves according to magnetic signals. And in 2010, a study by Christine Niesner of Goethe University on chickens and European robins showed that cryptochrome is produced in large quantities not just in the birds' retinas, but in particular in the cells that are sensitive to ultraviolet light, i.e. exactly where biologists would expect to see it, because the formation of the pair of radicals depends on light.

However, the investigation did not end. A significant part of the results have not yet been reproduced independently by other researchers. And as in the case of magnetite, some of the evidence is not as conclusive as it might be implied. For example, Ritz himself warns that radio waves produce electric fields that may interfere with biological processes in unexpected ways. For example, it is known that radio waves interfere with the receptors of neurotransmitters active in the pleasure centers of the brain, and therefore may indirectly confuse the birds without affecting their ability to sense magnetic fields.

Peter J. Hore, a physicist at the University of Oxford, adds that the apparent sensitivity of birds to radio waves is too good to be true: a magnetic field with a strength 2,000 times smaller than the Earth's geomagnetic field seems to be enough to disrupt their magnetic sense.

Similar confusion abounds over studies of cryptochrome in fruit flies. In 2008, Reffert and his colleagues showed that fruit flies could be trained to follow a magnetic field and direct them toward a sugary bait, but not mutant flies lacking the gene for cryptochrome, which are unable to produce the protein.

But the insects were exposed to fields 10 times stronger than the geomagnetic field. And because the experimenters knew when the artificial fields were turned on or off, they could have biased the results of the experiment without realizing it, warns Kirschwink.

In general, Hor says, despite the accumulation of evidence in favor of the idea of ​​the radical couple, "we have not yet reached the goal." Several pieces of the attachment are missing, first and foremost the details of the mechanism, "and this frustrates me a lot." Eventually researchers will have to show an electrophysiological response, that is nerve cells that send an electrical signal in response to a magnetic field, to prove that they have found the seat of the new sense. Electrophysiology is the decisive method in the biology of the senses, notes Ritz: "This is how we learned how the sense of sight works."

Interestingly, in June 2011 Reppert and his colleagues showed that fruit flies whose gene for cryptochrome was replaced with the human gene for this protein still retained the magnetic sensing ability. The discovery reignited the hypothesis that humans also have a magnetic sense, although the evidence for this is scant. Experiments conducted by Robin B. Baker of the University of Manchester in England in the late 70s apparently showed that people have some magnetic navigational ability, but attempts to reproduce the results failed.

put everything together

Most experts have abandoned alternative explanations for the magnetic sense, because they believe that at least one of the two leading hypotheses is plausible. The exception may be the magnetic sense of manta rays and sharks, which some argue is a byproduct of these creatures' extraordinary sensitivity to electric fields. In the skin of these fish there are microscopic channels, electrically conductive, which are used to sense weak voltage up to five billionths of a volt [see "The Electrical Sense of the Sharks", by R. Douglas Fields; Scientific American Israel, December 2007]. Because magnetic fields induce voltage on moving conductors, a fish can pick up the geomagnetic fields simply by moving left and right while swimming.

Even after the disputes are settled, we may not be able to explain the extraordinary feats of migratory animals, such as the fin whale, which is able to swim continuously for hundreds of kilometers in the open sea without deviating from its planned course by more than one degree.

However, many researchers hope that the magnetic sensing mechanism will be explained soon. Experimental methods have advanced enormously: technology now allows researchers to track even small birds, imaging methods of microscopic anatomical structures have become more accurate and scientists from several fields have begun to work together. When the mystery is solved, there will be those who will look back to this time with longing, Ritz says: "We don't often get the chance to discover a new sense."

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About the author

Davida Castelvecchi, science reporter living in Rome, editorial member of Scientific American.

And more on the subject

Structure and Function of the Vertebrate Magnetic Sense. Michael M. Walker et al. in Nature, Vol. 390, pages 371-376; November 27, 1997.

A Model for Photoreceptor-Based Magnetoreception in Birds. Thorsten Ritz, Salih Adem and Klaus Schulten in Biophysical Journal, Vol. 78, no. 2, pages 707-718; February 2000.

Migrating Songbirds Recalibrate Their Magnetic Compass Daily from Twilight Cues. William W. Cochran, Henrik Mouritsen and Martin Wikelski in Science, Vol. 304, pages 405-408; April 16, 2004.

Magnetic Alignment in Grazing and Resting Cattle and Deer. Sabine Begall, Jaroslav Červený, Julia Neef, Oldřich Vojtěch and Hynek Burda in Proceedings of the National Academy of Sciences USA, Vol. 105, no. 36, pages 13451-13455; September 9, 2008.

Magnetoreception. Single-theme supplement of Interface Focus: Journal of the Royal Society Interface, Vol. 7, no. 2; April 6, 2010.

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