How Migrating Birds Use Quantum Effects to Navigate
New
research hints at the biophysical underpinnings of their ability to use
Earth’s magnetic field lines to find their way to their breeding and
wintering grounds
By Peter J. Hore, Henrik Mouritsen | e
Imagine
you are a young Bar-tailed Godwit, a large, leggy shorebird with a
long, probing bill hatched on the tundra of Alaska. As the days become
shorter and the icy winter looms, you feel the urge to embark on one of
the most impressive migrations on Earth: a nonstop transequatorial flight lasting
at least seven days and nights across the Pacific Ocean to New Zealand
12,000 kilometers away. It’s do or die. Every year tens of thousands of
Bar-tailed Godwits complete this journey successfully. Billions of other
young birds,
including warblers and flycatchers, terns and sandpipers, set out on
similarly spectacular and dangerous migrations every spring, skillfully
navigating the night skies without any help from more experienced birds.
People
have long puzzled over the seasonal appearances and disappearances of
birds. Aristotle thought that some birds such as swallows hibernated in
the colder months and that others transformed into different
species—redstarts turned into robins for the winter, he proposed. Only
in the past century or so, with the advent of bird banding,
satellite tracking and more widespread field studies, have researchers
been able to connect bird populations that winter in one area and nest
in another and show that some travel vast distances between
the two locales every year. Remarkably, even juvenile long-haul
travelers know where to go, and birds often take the same routes year
after year. How do they find their way?
Migrating birds use
celestial cues to navigate, much as sailors of yore used the sun and
stars to guide them. But unlike humans, birds also detect the magnetic
field generated by Earth’s molten core and use it to determine their
position and direction. Despite more than 50 years of research into magnetoreception in birds,
scientists have been unable to work out exactly how they use this
information to stay on course. Recently we and others have made inroads
into this enduring mystery. Our experimental evidence suggests something
extraordinary: a bird’s compass relies on subtle, fundamentally quantum
effects in short-lived molecular fragments, known as radical pairs,
formed photochemically in its eyes. That is, the creatures appear to be
able to “see” Earth’s magnetic field lines and use that information to
chart a course between their breeding and wintering grounds.
A MYSTERIOUS SENSE
Migratory birds have an internal clock with an annual rhythm that tells them, among other things, when to migrate.
They also inherit from their parents the directions in which they need
to fly in the autumn and spring, and if the parents each have different
genetically encoded directions, their offspring will end up with an
intermediate direction. For example, if a southwest-migrating bird is
crossed with a southeast-migrating bird, their offspring will head south
when the time comes. But how do the young birds know which direction is
southwest or south or southeast? They have at least three different
compasses at their disposal: one allows them to extract information from
the position of the sun in the sky, another uses the patterns of the
stars at night, and the third is based on Earth’s ever present magnetic field.
In
their first autumn, young birds follow inherited instructions such as
“fly southwest for three weeks and then south-southeast for two weeks.”
If they make a mistake or are blown off course, they are generally
unable to recover because they do not yet have a functioning map that
would tell them where they are. This is one of the reasons why only 30
percent of small songbirds survive their first migrations to their
wintering grounds and back again. During its first migration a bird
builds up a map in its brain that, on subsequent journeys, will enable
it to navigate with an ultimate precision of centimeters over thousands
of kilometers. Some birds breed in the same nest box and sleep on the
same perch in their wintering range year after year. Equipped with this
map, about 50 percent of adult songbirds make it back to their nesting
site to breed every year.
Migratory
birds’ navigational input comes from several senses—mainly sight, smell
and magnetoreception. By observing the apparent nighttime rotation of
the stars around the North Star, the birds learn to locate north before
they embark on their first migration, and an internal 24-hour clock
allows them to calibrate their sun compass. Characteristic smells can
help birds recognize places they have visited before. Scientists know a
great deal about the detailed biophysical mechanisms of the birds’
senses of sight and smell. But the inner workings of their magnetic
compass have proved harder to understand.
The
magnetic direction sense in small songbirds that migrate at night is
remarkable in several important respects. First, observations of caged
birds exposed to carefully controlled magnetic fields show that their
compass does not behave like the magnetized needle in a ship’s compass. A
bird detects the axis of the magnetic field and the angle it makes with
Earth’s surface, the so-called inclination compass. In laboratory
experiments, inverting the magnetic field’s direction so that it points
in exactly the opposite direction has no effect on the bird’s ability to
orient correctly. Second, a bird’s perception of Earth’s magnetic field can be disrupted by
extraordinarily weak magnetic fields that reverse their direction
several million times per second. Last, even though songbirds fly at
night under the dim light of the stars, their magnetic compass is
light-dependent, hinting at a link between vision and magnetic sensing.
In
1978, in an attempt to make sense of these features of avian
magnetoreception, Klaus Schulten, then at the Max Planck Institute for
Biophysical Chemistry in Göttingen, Germany, put forth a remarkable
idea: that the compass relies on magnetically sensitive chemical transformations.
At first glance, this proposal seems preposterous because the energy
available from Earth’s magnetic field is millions of times too small to
break, or even significantly weaken, the bonds between atoms in
molecules. But Schulten was inspired by the discovery 10 years
previously that short-lived chemical intermediates known as radical
pairs have unique properties that make their chemistry sensitive to
feeble magnetic interactions. Over the past 40 years researchers have
conducted hundreds of lab studies of radical-pair reactions that are
affected by the application of magnetic fields.
To appreciate why radical pairs are so special, we need to talk about a quantum-mechanical property of the electron known as spin angular momentum, or “spin” for
short. Spin is a vector with a direction as well as a magnitude, and it
is often represented by an arrow, ↑ or ↓, for example. Particles with
spin have magnetic moments, which is to say they behave like microscopic
magnets. Most molecules have an even number of electrons arranged in
pairs with opposed spins (⇅), which therefore cancel each other out.
Radicals are molecules that have lost or gained an electron, meaning
that they contain an odd, unpaired, electron and hence have a spin and a
magnetic moment. When two radicals are created simultaneously by a
chemical reaction (this is what we mean by radical pair), the two
unpaired electrons, one in each radical, can have either antiparallel
spins (⇅) or parallel spins (↑↑), arrangements known as singlet and
triplet states, respectively.
Immediately
after a radical pair is created in a singlet state, internal magnetic
fields cause the two electronic spins to undergo a complex quantum
“waltz” in which singlet turns into triplet and triplet turns back into
singlet millions of times per second for periods of up to a few
microseconds. Crucially, under the right conditions, this dance can be
influenced by external magnetic fields. Schulten suggested that this
subtle quantum effect could form the basis of a magnetic compass sense
that might respond to environmental stimuli a million times weaker than
would normally be thought possible. Research that we and others have
carried out in recent years has generated fresh support for this
hypothesis.
To
be useful, hypotheses need to explain known facts and make testable
predictions. Two aspects of Schulten’s proposed compass mechanism are
consistent with what is known about the birds’ compass: radical pairs
are indifferent to exact external magnetic field reversals, and radical
pairs are often formed when molecules absorb light. Given that the
birds’ magnetic compass is light-dependent, a prediction of Schulten’s
hypothesis is that their eyes play a part in the magnetic sensory
system. About 10 years ago the research group of one of us (Mouritsen)
at the University of Oldenburg in Germany found that a brain region
called Cluster N,
which receives and processes visual information, is by far the most
active part of the brain when certain night-migrating birds are using
their magnetic compass. If Cluster N is dysfunctional, research in
migratory European Robins showed, the birds can still use their sun and
star compasses, but they are incapable of orienting using
Earth’s magnetic field. From experiments such as these, it is clear
that the magnetic compass sensors are located in the birds’ retinas.
One
early objection to the radical-pair hypothesis was that no one had ever
shown that magnetic fields as tiny as Earth’s, which are 10 to 100
times weaker than a fridge magnet, could affect a chemical reaction. To
address this point, Christiane Timmel of the University of Oxford and
her colleagues chose a molecule chemically unlike anything one would
find inside a bird: one that contained an electron donor molecule linked
to an electron acceptor molecule via a molecular bridge. Exposing the
molecules to green light caused an electron to jump from the donor to
the acceptor over a distance of about four nanometers. The radical pair
that formed from this reaction was extremely sensitive to weak magnetic
interactions, proving that it is indeed possible for a radical-pair
reaction to be influenced by the presence of—and, more important, the
direction of—an Earth-strength magnetic field.
Schulten’s
hypothesis also predicts that there must be sensory molecules
(magnetoreceptors) in the retina in which magnetically sensitive radical
pairs can be created using the wavelengths birds need for their compass
to operate, which another line of research had identified as light
centered in the blue region of the spectrum. In 2000 he suggested that
the necessary photochemistry could take place in a then recently
discovered protein called cryptochrome.
Cryptochromes
are found in plants, insects, fish, birds and humans. They have a
variety of functions, including light-dependent control of plant growth
and regulation of circadian clocks. What makes them attractive as
potential compass sensors is that they are the only known naturally
occurring photoreceptors in any vertebrate that form radical pairs when
they absorb blue light. Six types of cryptochromes have been found in
the eyes of migratory birds, and no other type of candidate
magnetoreceptor molecule has emerged in the past 20 years.
Like
all other proteins, cryptochromes are composed of chains of amino acids
folded up into complex three-dimensional structures. Buried deep in the
center of many cryptochromes is a yellow molecule called flavin adenine
dinucleotide (FAD) that, unlike the rest of the protein, absorbs blue
light. Embedded among the 500 or so amino acids that make up a typical
cryptochrome is a roughly linear chain of three or four tryptophan amino acids stretching
from the FAD out to the surface of the protein. Immediately after the
FAD absorbs a blue photon, an electron from the nearest tryptophan hops
onto the flavin portion of the FAD. The first tryptophan then attracts
an electron from the second tryptophan and so on. In this way, the
tryptophan chain behaves like a molecular wire. The net result is a
radical pair made of a negatively charged FAD radical in the center of
the protein and, two nanometers away, a positively charged tryptophan
radical at the surface of the protein.
In 2012 one of us (Hore), working with colleagues at Oxford, carried out experiments to test the suitability of cryptochrome as a magnetic sensor. The study used cryptochrome-1, a protein found in Arabidopsis thaliana,
the plant in which cryptochromes had been discovered 20 years earlier.
Using short laser pulses to produce radical pairs inside the purified proteins,
we found that we could fine-tune their subsequent reactions by applying
magnetic fields. This was all very encouraging, but, of course, plants
don’t migrate.
We
had to wait almost a decade before we could make similar measurements
on a cryptochrome from a migratory bird. The first challenge was to
decide which of the six bird cryptochromes to look at. We chose
cryptochrome-4a (Cry4a), partly because it binds FAD much more strongly
than do some of its siblings, and if there is no FAD in the protein,
there will be no radical pairs and no magnetic sensitivity. Experiments
in Oldenburg also showed that the levels of Cry4a in migratory birds are
higher during the spring and autumn migratory seasons than they are
during winter and summer when the birds do not migrate. Computer
simulations performed by Ilia Solov’yov in Oldenburg showed that
European Robin Cry4a has a chain of four tryptophans—one more than the
Cry1 from Arabidopsis. Naturally, we wondered whether the extended chain had evolved to optimize magnetic sensing in migratory birds.
Our
next challenge was to get large amounts of highly pure robin Cry4a.
Jingjing Xu, a Ph.D. student in Mouritsen’s lab, solved it. After
optimizing the experimental conditions, she was able to use bacterial
cell cultures to produce samples of the protein with the FAD correctly
bound. She also prepared versions of the protein in which each of the
four tryptophans was replaced, one at a time, by a different amino acid
so as to block electron hopping at each of the four positions along the
chain. Working with these alternative versions of the protein would
allow us to test whether the electrons are really jumping all the way
along the tryptophan chain.
We
shipped these samples—the first purified cryptochromes from any
migratory animal—to Oxford, where Timmel and her husband, Stuart
Mackenzie, studied them using the sensitive laser-based techniques they
had developed specifically for that purpose. Their research groups found
that both the third and fourth tryptophan radicals at the end of the
chain are magnetically sensitive when paired with the FAD radical. We
suspect that the tryptophans work cooperatively for efficient magnetic
sensing, biochemical signaling and direction finding. We also speculate
that the presence of the fourth tryptophan might enhance the initial
steps of signal transduction, the process by which nerve impulses
encoding the magnetic field direction are generated and ultimately sent
along the optic nerve to the brain. We are currently conducting
experiments to identify the proteins that interact with Cry4a.
One
more cryptochrome finding deserves mention here. We compared robin
Cry4a with the extremely similar Cry4a proteins from two nonmigratory
birds, pigeons and chickens. The robin protein had the largest magnetic
sensitivity, hinting that evolution might have optimized robin Cry4a for navigation.
Although
these experiments confirm that Cry4a has some of the properties
required of a magnetoreceptor, we are still a long way from proving how
migratory birds perceive Earth’s magnetic field lines. One crucial next
step is to determine whether radical pairs actually form in the eyes of
migratory birds.
The
most promising way to test for radical pairs inside the birds’ eyes was
inspired by the work of chemists and physicists who, in the 1980s,
showed that fluctuating magnetic fields alter the way radical-pair
reactions respond to static magnetic fields. Their work predicted that a
weak radio-frequency electromagnetic field, fluctuating with the same
frequencies as the “singlet-triplet waltz,” might interfere with the
birds’ ability to use their magnetic compass. Thorsten Ritz of the
University of California, Irvine, and his colleagues were the first to confirm this prediction in 2004.
In 2007 Mouritsen began similar behavioral experiments in his lab in Oldenburg—with intriguingly different results. During the spring and fall, birds that travel between nesting and wintering grounds exhibit a behavior called Zugunruhe,
or migratory restlessness, as if they are anxious to get on their way.
When caged, these birds usually use their magnetic compass to
instinctively orient themselves in the direction in which they would fly
in the wild. Mouritsen found that European Robins tested in wooden huts
on his university’s campus were unable to orient using their magnetic
compass. He suspected that weak radio-frequency noise (sometimes called
electrosmog) generated by electrical equipment in the nearby labs was
interfering with the birds’ magnetic compass.
To
confirm that electrosmog was the source of the problem, Mouritsen and
his team lined the huts with aluminum sheets to block the stray radio
frequencies. On nights when the shields were grounded and functioned
properly, the birds oriented well in Earth’s magnetic field. On nights
when the grounding was disconnected, the birds jumped in random
directions. When tested in an unshielded wooden shelter typically used
for horses some kilometers outside the city and well away from
electrical equipment, the same birds had no trouble detecting the
direction of the magnetic field.
These
results are significant on several fronts. If the radio-frequency
fields affect the magnetic sensor and not, say, some component of the
signaling pathway that carries nerve impulses to the brain, then they
provide compelling evidence that a radical-pair mechanism underpins the
bird’s magnetic compass. The main competing hypothesis, for which there
is currently much less support, proposes that magnetic iron–containing
minerals are the sensors. Any such particles that were large enough to
align like a compass needle in Earth’s magnetic field would be far too
big to rotate in a much weaker field that reversed its direction
millions of times per second. Furthermore, the radio-frequency fields
that upset the birds’ magnetic orientation are astonishingly weak, and
we don’t yet understand exactly how they could corrupt the directional
information available from the much stronger magnetic field of Earth.
It is also remarkable that the birds in the Oldenburg lab were disoriented much more effectively by broadband radio-frequency noise (randomly
fluctuating magnetic fields with a range of frequencies) than by the
single-frequency fields mostly used by Ritz and his collaborators. We
hope that by subjecting migratory songbirds to bands of radio-frequency
noise with different frequencies we will be able to determine whether
the sensors really are FAD-tryptophan radical pairs or whether, as some
other investigators have suggested, another radical pair might be
involved.
Many
questions about the birds’ magnetic compass remain, including whether
the magnetic field effects on robin Cry4a observed in vitro also exist
in vivo. We also want to see whether migratory birds with genetically
suppressed Cry4a production are prevented from orienting using their
magnetic compass. If we can prove that a radical-pair mechanism is
behind the magnetic sense in vivo, then we will have shown that a
biological sensory system can respond to stimuli several million times
weaker than previously thought possible. This insight would enhance our
understanding of biological sensing and provide new ideas for artificial
sensors.
Working
to gain a full understanding of the inner navigation systems of
migratory birds is not merely an intellectual pursuit. One consequence
of the enormous distances migratory birds travel is that they face more
acute threats to their survival than most species that breed and
overwinter in the same place. It is more difficult to protect them from
the harmful effects of human activity, habitat destruction and climate
change. Relocating migratory individuals away from damaged habitats is
rarely successful because the birds tend to instinctively return to
those unlivable locales. We hope that by providing new and more
mechanistic insights into the ways in which these extraordinary
navigators find their way, conservationists will have a better chance of
“tricking” migrants into believing that a safer location really is
their new home.
When
you next see a small songbird, pause for a moment to consider that it
might recently have flown thousands of kilometers, navigating with great
skill using a brain weighing no more than a gram. The fact that quantum
spin dynamics may have played a crucial part in its journey only
compounds the awe and wonder with which we should regard these
extraordinary creatures.
This
article was originally published with the title "The Quantum Nature of
Bird Migration" in Scientific American 326, 4, 26-31 (April 2022)
doi:10.1038/scientificamerican0422-26
The Big Day. Kate Wong; October 2021.
Peter J. Hore is
a chemist at the University of Oxford. He works on the biophysical
chemistry of electron and nuclear spins and their effects on processes
such as the mechanisms of animal magnetoreception. Credit: Nick Higgins
Henrik Mouritsen is
a biologist at the University of Oldenburg in Germany. He studies the
mechanisms of orientation and navigation in many different animals with
an emphasis on night-migrating songbirds. Credit: Nick Higgins