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Cambridge University Science Magazine
Quantum entanglement is what one would associate with sophisticated machinery found in a laboratory. The migratory behaviour of a bird across oceans and continents, travelling thousands of kilometres with incredible precision is one of the most remarkable phenomena in ethology. These are not scientific ideas one would link together in the wildest of dreams, but in the search of the ‘sixth sense’ that guides birds on their migratory paths, sensory biologists have found increasing evidence that the quantum mechanical principles may be inextricably linked to what is regarded by many as the ‘holy grail’ of sensory biology: a definite theory for the mechanisms of magnetoreception.

The sixth sense: magnetoreception

It has long been shown that the migratory behaviour of a bird is genetically determined. That celestial patterns guide the birds in their migratory path is also well established. However, how the magnetic field of the Earth contributes to the accuracy with which birds journey is an elusive mystery that scientists have only recently made progress in unravelling. Although ethologists had observed throughout the 20th century that birds were indeed capable of extracting information from surrounding magnetic fields, the mechanism by which this incredible ‘sixth sense’ occurred was completely unknown.

Magnetoreception involves the ability to perceive and respond to magnetic fields. The Earth’s magnetic field comes from the motion of its conducting fluid core which is rich in iron. This field is a vector quantity which is considered to have three components; inclination, declination and an intensity. With these distinct geophysical parameters, scientists have proposed that each of these could be used as a navigation aid by migratory animals.

With the development of behavioural biology in the 1960s, Friedrich Merkel and Wolfgang Wiltschko used a migratory bird, the European robin (Erithacus rubecula) to reveal the magnetic field-dependent behaviour within migratory species. They applied artificial magnetic fields to modify the preferred direction of orientation during migratory restlessness within small circular arenas within controlled environmental conditions, providing behavioural evidence for how these migratory birds both possess and are able to use magnetic compasses. With further development in behavioural biology, more migratory species have been identified with a magnetic sense.

However, the Earth’s magnetic field is very weak, with a strength of 25000 - 65000 nanoteslas. For reference, that is more than four magnitudes weaker than the strength of a typical bar magnet at 0.01 teslas. The question is then evident: how exactly do birds make use of the minute force to guide their arduous journeys?

Enter the quantum: ‘The Radical Pair Hypothesis’

The first insight into the workings of magnetoreception in migratory birds came not from biological reasoning but physical. Klaus Schulten, a German theoretical physicist, first proposed the radical pair hypothesis for the phenomena of magnetoreception in birds in 1978. In his paper A Biomagnetic Sensory Mechanism Based on Magnetic Field Modulated Coherent Electron Spin Motion, Schulten suggested that a molecule produced by birds used the quantum entanglement of two special electrons called radical pairs. A radical, simply defined, is a molecule which has unpaired electrons. The very first introductory chemistry class one takes with quantum flavours almost always immediately introduces the idea that electrons are found in two spin states: spin up (↑) or spin down (↓). A radical pair is a very special type of radical species, with two unpaired electrons that are quantum entangled and created simultaneously. Quantum entanglement, in very reduced terms, refers to the property that two particles have quantum states which are dependent on the state of the other entangled particle. For electrons in a radical pair, this is critical as the spin of an electron specifies its spin angular momentum, which in turn is associated with a magnetic moment. A radical pair can be described in terms of its total angular momentum, with two possible states: the triplet state, in which the spin of the radical electrons are aligned with S = 1 and electrons both spin up (↑↑) or both spin down (↓↓) or the singlet state in which the spin of the radical electrons are antiparallel (↑↓) with S = 0.  However, the spin and magnetic moment of radical pairs alone is insufficient to generate a biological compass in birds. Further interactions between the spin of spin-active nuclei, such as the hydrogen nuclei of proton nuclear magnetic resonance spectroscopy fame, with the radical pair, termed ‘hyperfine interactions’ is necessary for magnetoreception in birds as dictated by the radical pair hypothesis. The coupling of the nuclei spin and the electron spin generates a large number of energy levels between which electrons oscillate from the singlet state to the triplet state and back. The application of an external magnetic field results in further interactions and a shift of the energy levels such that the oscillation between the singlet and triplet states alters. Due to the anisotropic nature of some hyperfine interactions, the directionality of the magnetic field also influences how exactly the oscillations between the spin states are altered. This directionality of magnetic interactions provides the quantum mechanical basis of the radical pair hypothesis.

Schulten suggested that light-induced photoexcitation was responsible for generating these radical pairs in birds. Energy provided by photons at the correct frequency can excite a single electron in a species, creating unpaired electrons. The total energy of a system can then be lowered with another species donating an electron to the radical species which now has an electron hole, generating an unpaired electron in the donor species as well. This results in the formation of a radical pair in the singlet state. As charge is conserved, the spin state of a radical pair is also conserved. This means that only a radical pair in the singlet state can be formed from reactants with electrons in the singlet state, and products with electrons in the triplet state can only be formed from a radical pair intermediate in the triplet state. As the probability of being in the singlet or triplet state is affected by a magnetic field, the proportion of products and reactants is also dependent on the direction of the magnetic field if the hyperfine interactions in consideration are anisotropic. Even though the strength of the Earth’s magnetic field is extremely weak as mentioned above, the energy difference between the singlet and triplet state is so small that even the Earth’s magnetic field is able to considerably increase the favorability of one state over the other. Under the radical pair hypothesis then, the bird is able to sense the Earth’s magnetic field by some mechanism that relies on the equilibrium concentrations of products and reactants of a radical reaction that forms radical pairs through photoexcitation.

From theory to experimentation: Mouritsen and Hore

Theory is perfect for the abstract, but birds are real life creatures and so experimentation was needed to bring Schulten’s radical pair hypothesis from the quantum realm into the macroscopic world of birds. One class of molecule was of particular interest to sensory biologists: the cryptochrome. Cryptochromes are flavin-based proteins which serve roles in determining the circadian rhythms of both plants and animals. More importantly, the flavin moiety of cryptochromes makes them the only class of molecules in animals which are able to form radical pairs (in plants chlorophyll can also form radical pairs). In particular, the absorbance of blue light excites cryptochromes in the ground state to the radical pair intermediate state, which can then go on to generate the product signalling state from the triplet pair intermediate state. Sensory biologists have then hypothesised that the signalling state triggers a signal cascade that releases neurotransmitters, activating sensory nerves responsible for magnetoreception.

As the generation of the radical pair requires cryptochromes to absorb blue light, scientists naturally looked to find magnetically-sensitive cryptochrome molecules in the eye of magneto-receptive migratory birds. In 2016, Prof. Henrik Mouritsen of the University of Oldenburg was able to synthesise a particular cryptochrome, CRY4, which is typically found in the eye of European robins. Using ultra-sensitive detection equipment, Prof. Peter Hore of the University of Oxford was able to show that these CRY4 proteins were indeed magnetically sensitive in that when their flavin moiety absorbed blue light, radical pairs were formed and a very weak applied magnetic field with a strength similar to that of the Earth was able to significantly affect the concentration of activated CRY4 signalling state formed from the triplet state. Hore and Mouritsen were also able to show that the CRY4 counterparts found in non-migratory birds such as the household chicken exhibit significantly reduced magnetic sensitivity and that CRY4 concentrations rose considerably during migratory seasons, suggesting that CRY4 indeed serves some role in magnetoreception during migration for migratory birds. This collaboration between behavioural biology and physical chemistry has therefore shown birds do indeed possess molecules which satisfy the requirements dictated by Schulten’s radical pair hypothesis.

Laboratory to nature: the future

While Mouritsen and Hore’s experiments with CRY4 provide tremendous evidence in support of the radical pair hypothesis, the properties of molecules generated in isolation under laboratory conditions should not be directly translated to their biological analogues. Further experimentation under biological conditions is necessary to solidify the radical pair hypothesis. This next step is particularly challenging as the model organism used for Mouritsen and Hore’s experiment, the European robin, cannot be bred to exhibit migratory behaviours under experimental control. Although the radical pair hypothesis is one of the central ideas proposed to explain magnetoreception in migratory birds, other hypotheses such as the presence of ferrimagnetic magnetite crystals in bird beak which have magnetic moments responding to an external applied field, have also been suggested to decipher magnetoreception. These hypotheses are not necessarily in contradiction of one another, but instead cooperate in harmony to unravel the precise mechanisms of magnetoreception. As strange as combining quantum mechanical principles and ethological observations may seem at first, this interaction between biology, chemistry and physics is now rapidly becoming the dominant path by which modern research develops and further work on this mystical ‘sixth sense’ which guides birds on their journey across the globe will certainly continue to require the intersection of different fields of science.

Article by Andy Song and Yena Seo

Image credit: Andrea Stöckel

Image licence: CC0 1.0 Universal

The original image has been cropped