У Джо позиция мне симпатична: применяя принцип бритвы Оккама, зачем изобретать две системы, если можно все объяснить одной, основанной на магнетите? Да, но вот эксперименты в нашей лабе (статьи должна выйти в следующем году) показывают, что птицы могут ориентироваться и с перерезанным тройничным нервом, а именно в нем нашли нечто похожее на магниторецептивный орган с частицами магнетита (это конечно не исключает возможности существования другого магнититосодержащего органа в организме птицы, но тогда Джо попадает в свою же ловушку - множет сущности без потребности). В общем, сложно все.
Kenneth Kragh Jensen started the discussion with the following
Very well, I have two points that I would like to discuss:
1) A prerequisite for a light dependent compass is a well ordered arrays of light sensitive molecules. Are there any evidence that this is the case with chryptochromes in vertebrates? In insects/Drosophila?
2) Is there a size limit below which a magnetite based mechanism cannot work optimally and thus a selection towards a light sensitive mechanisms? Is Drosophila below this limit?
I suspect the optical and rf effects on magnetoreception -- if real and reproducible -- are at best a side effect of an inhibitory circuit which evolved to allow animals to calibrate their magnetite-based compasses against the Sun compass at sunrise and sunset, when the natural light is red and animals usually don't need a compass. I'm attaching a cartoon of such an inhibitory circuit here (from my RIN talk).
Note that one of the main drivers for considering an optically-pumped mechanism way back in the 1970's was the apparent axial-symmetry of the avian compass -- replacing the field vector, B, with -B, yielded no change in compass response. Although Gould and I (1981) explained this easily with magnetite, it is always cited as an argument for something like optical pumping, which ought to be axial symmetric. However, Wiltschko et al. (2008, HFSP J. v.1, p.41-48) have now demonstrated that there is a polar compass effect in birds (which they call a 'fixed direction response') that is polar, not axial. That response cannot be based on optical pumping. Either birds evolved two separate mechanisms for doing essentially the same thing (orienting wrt a magnetic field), or there is one polar compass (based on magnetite) with a more complex behavioral circuit involving cryptochromes operating in an inhibitory mode under red light conditions.
Given the thermodynamic problems with the optical compass, the magnetite-based compass hypothesis makes MUCH more sense, and is far, far, far simpler.
Joseph L. Kirschvink, PhD
Nico and Marilyn Van Wingen Professor of Geobiology
Division of Geological & Planetary Sciences
California Institute of Technology 170-25
1200 E. California Blvd., Pasadena, CA 91125
email@example.com; 626-395-6136(o); 626-437-0398(cell); FAX 626-568-0935
Please could you share with us the details of the calculations that demonstrate that cryptochrome cannot form the basis of a chemical compass?
P J Hore
Department of Chemistry, Oxford University
Physical and Theoretical Chemistry Laboratory
South Parks Road, Oxford OX1 3QZ
Tel: +44 1865 275415 Fax: +44 1865 275410
Joe Kirschvink's claim that alignment responses [fixed direction, non-goal oriented] are the same as compass responses [goal directed--either innate (migratory birds) or learned (newts)] is misleading and represents a fundamental mirepresentation of the literature. For anyone who is unclear on the distinction between these two types of responses, there is a literature on comparable (alignment vs. compass) responses to polarized light in invertebrates.
Magnetic alignment responses (e.g., in migratory birds, newts, and possibly mole rats) could be involved in extracting map (or timing) information from the magnetic field. The biophysical mechanism responsible for magnetic alignment responses may or may not have anything to do with the magnetic compass--the available evidence suggests that the two types of responses exhibit distinct functional properties, distinct sensory structures, and distinct biophysical mechanisms.
Mole rats are a particularly interesting case because they exhibit a fixed alignment response, with all the properties of the fixed alignment responses in birds and newts, and yet this is generally referred to as a compass response. It is worth considering that without regular access to the daily light cycle, molerats are an especially good candidate for a magnetic zeitgeber and could be aligning themselves to facilitate measurement of daily variation in the geomagnetic field.
Proposing that the same biophysical mechanism may be responsible for both alignment and compass responses, or for both map and compass responses, is a useful contribution to the field, but stating this as a conclusion and ignoring evidence to the contrary is not. A good example of how unproven assumptions can limit consideration of legitimate alternative hypotheses is the recent paper claiming that bats have a magnetite-based compass--perhaps a topic for future discussion.
John B. Phillips, Professor
Department of Biological Sciences
Blacksburg, VA 24061-0406
540-231-7669 (behavioral testing facility)
The question at hand is in the domain of the biophysics of neurophysiology – concerning the transduction mechanisms that animals may use to detect the geomagnetic field. I don’t want to get involved in a fruitless hair-splitting argument about what you call a fixed-direction vs. a compass response – that obscures the underlying biophysics.
A fundamental theorem of neurobiology is that all information about environmental stimuli that an animal has comes from cells specialized for transducing the stimuli, and in animals these are conveyed via a coded stream of action potentials to the rest of the nervous system (see Steve Block’s (1) excellent review on this). This sensory processing is then used to influence the behavior. Unfortunately, in studying magnetoreception we most often are looking at some behavioral response that is a complex assemblage of many competing factors, and must try inferring the properties of the underlying biophysical transduction mechanisms from the behavioral mess.
Now, let’s assume that Wiltschko’s birds (and your newts and many other animals) are put in a testing funnel, cage or whatever, and display some consistent response to a magnetic direction. If the direction of the field is rotated, and the animal adjusts its position in response, then this fundamental theorem of neurobiology states that there are specialized receptor cells somewhere in the organism that are providing information about the magnetic direction to the animal. Something that obtains directional information from the magnetic field is called a ‘magnetic compass’, a definition that goes back at least to the 12th Century AD, clearly pre-dating any definition that psychologists or ethologists have devised since then. Biophysically, we are fully justified in calling a behavioral response that fits this definition (adjustment of a behavioral outcome in response to the magnetic direction) a magnetic compass response.
If you then look at the classic bird experiments demonstrating the axial (inclination) magnetic compass, and ask what neurological inputs are needed to make that behavior, you immediately realize it cannot be a pure, simple input from any one sensory system – the behavior involves both a magnetic input AND a gravitational input. (Inclination is measured with respect to the vertical!).
So where do we stand? At the minimum, the bird’s axial compass is derived from the neurological processing of two sensory systems – something measuring magnetism, and gravity. Why not three? Throw in a cryptochrome visual inhibition to prevent using the magnetic compass when only red light is present (and the setting/rising Sun gives a better direction reference, anyway), and you can explain a lot more of the observed behavior, including radio-frequency EMF effects.
And now we see that birds treated in a slightly different fashion display a polarity sensitive ‘fixed direction’ magnetic compass that simply cannot be explained by a magnetic compass based on free radical effects, from cryptochrome or anything else. It fits the biophysical definition of a magnetic compass behavior because the animals will shift their orientation/behavior to follow the magnetic field. As it doesn’t seem to be influenced either by gravity or the EMFs that disrupt the cryptochromes, it may be a simpler, perhaps more primitive (‘ancestral’) behavioral program. It could tell us more about the underlying biophysics of actual magnetic compass receptor cells.
Note that the SAME underlying magnetic sensory cells can provide the necessary information about the magnetic field for both your 'fixed direction, non-goal oriented' and 'goal-directed' magnetic compass responses.
Behaviors evolve very rapidly, far more rapidly than basic physiological structures like new sensory receptor systems. Parsimony suggests that we do not need to invoke a brand new sensory transduction mechanism each time we observe a new flavor of behavior, particularly when simple combinations of sensory systems will suffice.
Very good questions.
I give my answers below, also considering the statements by Joe
Kirschvink. Just my general take in the beginning: For any biological
sensory mechanism (smell, vision, hearing), biophysicists were initially
baffled and sometimes still are baffled by the extreme sensitivity
revealed. Why should it be different for magnetic sensing? Rather than
using physics considerations as a weapon to prematurely reject hypotheses,
I feel we should use them as a guide to understand how nature achieves its
remarkable feats and what to look for.
Best wishes, Thorsten
1) A prerequisite for a light dependent compass is a well ordered arrays of
light sensitive molecules. Are there any evidence that this is the case with
chryptochromes in vertebrates? In insects/Drosophila?
“Well-ordered” is a qualitative term. If you want a compass with an
accuracy of 0.1 degrees, “well-ordered” means something very different
than if you are happy with 10 degrees accuracy, which appears closer to
the animal’s compass accuracy. Averaging over many molecules in a cell can
give directional signals, even if individual molecules point in many
different directions. If you conduct signal-to-noise ration calculations
as done in Weaver et al, Nature, 405, 707 (2000) you will find that the
light-sensitive mechanism is rather insensitive to the arrangement of
molecules. Of course, if all molecules are perfectly randomised, you
cannot have a compass. But even if molecules are distributed with as much
as 50 degrees variation from an average angle, there is no fundamental
problem with a light-sensitive compass in a single cell that operates with
about 10 degrees accuracy. I am currently preparing a manuscript on this.
Most people would not call a group of molecules with 50 degree angular
variation a “well-ordered” array, but this is well-ordered enough for a
To Joe’s other objection regarding the role of thermal fluctuations:
Assume a protein with a rotational diffusion coefficient D_r of 10^7/s
(very reasonable, if not high for cryptochrome). According to Fick’s law
(theta^2 = 4 D_r x t), this leads to an angular motion of (on average)
about 6-7 degrees in a microsec or 20 degrees in 10 microsec. Not a
problem for a compass operating on these timescales as the light-dependent
compass does. I have heard Joe claim otherwise a few times, but he has yet
to reveal his calculations substantiating this claim.
2) Is there a size limit below which a magnetite based mechanism cannot work
optimally and thus a selection towards a light sensitive mechanisms? Is
Drosophila below this limit?
Of course there is a size limit for both magnetite and light-dependent
mechanisms. For magnetite, the challenge I see is force generation. Take a
typical magnetosome in magnetotactic bacteria with a particle size of
50x50 nanometers and magnetization M of 5x10^5 A/m. The force generated by
a 50 microT field (according to F=M x V x H / L, where V is volume, L is
length, and H is magnetic flux density) is about 50 femtoNewtons. Is this
enough to initiate signal transduction? That depends on the sensitivity of
the mechanoreceptor to which the magnetite particle is presumably linked
and the sources of noise. For a 100 nanoT field, the force is 0.1
femtoNewtons. I am not aware of any biological mechanoreceptor capable of
detecting such small forces, yet there are several reports of sensitivity
to 100 nanoT fields in the literature.
Interestingly, there is no trivial way of increasing the force with
magnetite-based sensors, because of the physics of soft magnetic materials
such as magnetite. Note that the bird magnetite system in the beak, whose
structure has been rather well characterized, does not look at all like
the one-cell magnetosomes in bacteria. To name only the most obvious one:
the bird system has dimensions well beyond those of a micrometer-sized
cell. In keeping with my opening statement, it would be interesting to
understand why nature chose to build a very different magnetite-based
system in birds than in bacteria. Your question as to what the optimal
range of each mechanism is, is just the right one to lead us towards such
understanding. I would not be surprized to find multiple specialized
magnetosensors, depending on the task at hand. It would be nice to see
rigorous signal-to-noise calculations on magnetite-systems, showing their
respective optimal ranges, to lead us in our search for understanding.
Thorsten Ritz, UC Irvine
Dr. Michael Winklhofer
thank you for your contribution to this discussion. No offense,
just a brief comment on your closing remarks about the
magnetite-based sensor: In the last paragraph, you wrote
"Interestingly, there is no trivial way of increasing the force
with magnetite-based sensors, because of the physics of soft
I am afraid I have to object to this view, not so much because
"the physics of soft magnetic materials" is not the right argument
to make this claim (see further below), but simply because there
appears to be a trivial way of increasing the force, namely by
increasing the number of magnetite particles per cell and by
increasing the number of magnetite-containing cells. It would be
less trivial if the system had to comply with the constraint that a
certain force has to be achieved with as little material as possible.
But is it sensible at all to impose such a constraint, given that
iron is not a rare element? In order that the magnetic-field
sensory system is viable, we require it to be - first and foremost –
effective, but not necessarily to be efficient (in terms of its effectiveness
relative to the amount of material used).
Concerning soft magnetic materials: A stable single-domain (SSD)
particle of magnetite is magnetically quite hard, that is, its switching
field is much higher than an earth-strength field. At the other extreme,
a collective of superparamagnetic (SPM) magnetite crystals (say 5 nm
crystal size as in the pigeon beak) has no coercive force and therefore
is quite soft, that is, it can be magnetized easily. Thus, both soft and hard
magnetic particles can be realized with a material of given intrinsic magnetic
hardness (concerning the soft/hard issue, see also
http://arxiv.org/abs/0805.2249, point V therein) .
Therefore, I'd suggest to not use the word "magnet soft materials"
when talking about magnetite in general. Why not call a spade a
spade and use the word SSD particles when meaning SSD particles
and specifically use the word SPM instead of soft when referring to
SPM crystals. Note that a large multi-domain particle of magnetite
would also behave magnetically soft (if such particles were present
in the receptor cells), but would have otherwise different magnetic
characteristics than SPM particles, hence the word "soft" is not
very specific either. The specific usage of words will help to avoid
confusion, all the more so because SD and SP are established concepts
in the field, that is, concepts that also ethologists and neuroanatomists
are now familiar with.
Dr. Michael Winklhofer
Department of Earth and Environmental Science
Ludwig-Maximilians-University of Munich
Tel. +(1149) 89 2180 4207
Fax. +(1149) 89 2180 4205
Good reply to Thorsten. His reference to soft materials raised a flag for me also. After reading your reply, it appears to me that Thorsten was focussing on the Fleissner model. I would have thought, however, that he would have known that SSD magnetite in biological systems has only been observed as chains.
Dear Michael (Winklhofer),
Thank you for your thoughtful response. Thank you also, Mike Walker, for
your point well made. I felt that my contribution was long already and
reduced the discussion too much because of that. I stand corrected in my
sloppy use of "soft material" for magnetite.
I agree with you that the availability of magnetite is not a constraint.
The constraint I see is in the way magnetite chains can be linked to
signal transduction. The most straightforward solution that has been
suggested would be to link a magnetite chain to a membrane, so that the
pull or push of the chain leads to opening of mechanosensitive ion
channels. Opening of ion channels is a rather local effect. A single
magnetsome of 50 nm size already covers many mechanosensitive ion
channels. How, then, can one increase the force at one membrane patch?
1. You could use multiple magnetite chains, as you suggested. These would
then have to be tethered with some flexible linker to one membrane region.
There is going to be a limit to this solution, simply because of space
constraints. Once you tether more than a few magnetite chains to one
place, more and more tethers will be at different angles, leading to
reduced force increases with each new chain.
2. You could increase the size of the individual particles in the chain.
The problem with magnetite is that it becomes multi-domain once you
increase the particle size beyond that observed in magnetosomes of
bacteria. Other materials, e.g. cobalt-based ones might allow larger SD
particles, but are not used by nature. (This is what I was thinking about
when writing the original contribution).
3. You could increase the length of the chains. This does not increase the
force immediately, however, because force=torque/length.
Thus, it does not seem straightforward to me to increase the force at a
membrane patch beyond, say, a factor of 10 compared to that of a single
magnetite chain. Of course, nature can find non-trivial solutions, e.g.
use multi-cellular sensors, as you suggested. I do not say it cannot be
done and, in fact, I am convinced that there are animals that successfully
use magnetite-based sensors.
But I would like to see a concrete model as to how signal transduction is
achieved with serious biophysical estimates of the sensitivity limits. How
many tethered magnetosomes do you need in a single cell to achieve 100 nT
or 1 degree sensitivity? Is this number reasonable? If not, how else could
it be done?
I am prodding you a bit here, because your calculations have so far been
the most rigorous I have seen in the magnetite field. My hope is to see
more of them and less of simple conceptual pictures only.
This discussion may be too detailed for the listserver, so, may I invite
you (and anyone else who would like to join) to work towards a joint paper
on "Sensitivity limits of single-cell magnetoreceptors"? I will challenge
you on your assumptions and estimates for the magnetite mechanism (SSD or
otherwise) and will happily accept your challenges for the radical pair
mechanism. What say you?
Best wishes, Thorsten
Associate Professor, UC Irvine
Dept of Physics and Astronomy