Why Ask for Directions? (A Guest Post)

A reposting of an original article by Anna Schneider on Feburary 8, 2016.

For the iconic monarch butterfly, the shorter days in fall mean it’s time to pack up and head south to a warmer climate! Just like clockwork, the Eastern population of monarch butterflies makes a 2000 mile journey to their winter paradise roosts in central Mexico. The journey in itself is one of the greatest migrations among all animals.

But here’s the catch: none of these butterflies has made this trip before. Several generations of monarchs have come and gone over the course of a summer, but the generation born in late August and early September are genetically prepared for months of survival without feeding or breeding. But their predecessors didn’t exactly leave them with a map. How do they know where to go? Do they have a map and compass inside their heads? The answer: yes! Well, sort of…

Think about this: if you were lost in the woods and needed to find south, what would you do? Here’s a hint: look up! The sun can be a great resource when you’re lost, and I’m not talking about just asking it for directions. As the Earth rotates on its axis throughout the day, the sun appears to travel overhead. By knowing approximately what time of day it is, you can determine the cardinal directions. Monarchs use specialized cells or organs called photoreceptors that respond to light to establish the position of the sun.

Representation of time compensated sun compass orientation used by monarchs;
Image created by Anna Schneider.

Until recently, it was thought that monarchs simply used the photoreceptors on the top portion of their compound eyes, called the dorsal rim. Past studies have shown that the signals are passed from the photoreceptors on to the “sun compass” region in their brains and the butterflies change direction based on that information. Like most animals, it was assumed that their internal clock was located inside their brains. However, recent research has demonstrated that individuals whose antennae have been painted or removed altogether become disoriented when placed in flight simulators. These monarchs do not adjust for the time of day when trying to fly south. When those same antennae that were removed were placed in a petri dish, they continued to respond to light and showed signs that they continued the pattern of time. This indicates that antennae and the brain are both needed for the monarchs to correctly determine their direction.

Diagram of features on the head of a monarch butterfly; Image created by Anna Schneider.

Now, estimating which way is South might be fine and dandy on a bright sunny day, but what happens when it’s cloudy? Not a problem for these super-insects! In another recent study, researchers tethered monarchs to flight simulators and altered the magnetic field conditions to see what would happen. When the magnetic field was reversed so magnetic North was in the opposite direction, the butterflies altered their bearings and flew exactly opposite as well. This suggests that monarchs could have some sort of way to detect the earth’s magnetic field, called magnetoreception, which could enhance the photoreception capabilities.

Many of the mechanisms behind the migration of these incredible creatures are yet to be discovered, but much progress has been made in the past decade. So next time you see a monarch butterfly, take a second look. There is more than meets the eye.

Sources:

Gegear, R., Foley, L., Casselman, A., & Reppert, S. (2010). Animal cryptochromes mediate magnetoreception by an unconventional photochemical mechanism Nature, 463 (7282), 804-807 DOI: 10.1038/nature08719

Guerra, P., Gegear, R., & Reppert, S. (2014). A magnetic compass aids monarch butterfly migration Nature Communications, 5 DOI: 10.1038/ncomms5164

Merlin, C., Gegear, R., & Reppert, S. (2009). Antennal Circadian Clocks Coordinate Sun Compass Orientation in Migratory Monarch Butterflies Science, 325 (5948), 1700-1704 DOI: 10.1126/science.1176221

Steven M. Reppert. The Reppert Lab: Migration. University of Massachusetts Medical School: Department of Neurobiology.

Why Ask for Directions? (A Guest Post)

by Anna Schneider

For the iconic monarch butterfly, the shorter days in fall mean it’s time to pack up and head south to a warmer climate! Just like clockwork, the Eastern population of monarch butterflies makes a 2000 mile journey to their winter paradise roosts in central Mexico. The journey in itself is one of the greatest migrations among all animals.

But here’s the catch: none of these butterflies has made this trip before. Several generations of monarchs have come and gone over the course of a summer, but the generation born in late August and early September are genetically prepared for months of survival without feeding or breeding. But their predecessors didn’t exactly leave them with a map. How do they know where to go? Do they have a map and compass inside their heads? The answer: yes! Well, sort of…

Think about this: if you were lost in the woods and needed to find south, what would you do? Here’s a hint: look up! The sun can be a great resource when you’re lost, and I’m not talking about just asking it for directions. As the Earth rotates on its axis throughout the day, the sun appears to travel overhead. By knowing approximately what time of day it is, you can determine the cardinal directions. Monarchs use specialized cells or organs called photoreceptors that respond to light to establish the position of the sun.

Representation of time compensated sun compass orientation used by monarchs;
Image created by Anna Schneider.

Until recently, it was thought that monarchs simply used the photoreceptors on the top portion of their compound eyes, called the dorsal rim. Past studies have shown that the signals are passed from the photoreceptors on to the “sun compass” region in their brains and the butterflies change direction based on that information. Like most animals, it was assumed that their internal clock was located inside their brains. However, recent research has demonstrated that individuals whose antennae have been painted or removed altogether become disoriented when placed in flight simulators. These monarchs do not adjust for the time of day when trying to fly south. When those same antennae that were removed were placed in a petri dish, they continued to respond to light and showed signs that they continued the pattern of time. This indicates that antennae and the brain are both needed for the monarchs to correctly determine their direction.

Diagram of features on the head of a monarch butterfly; Image created by Anna Schneider.

Now, estimating which way is South might be fine and dandy on a bright sunny day, but what happens when it’s cloudy? Not a problem for these super-insects! In another recent study, researchers tethered monarchs to flight simulators and altered the magnetic field conditions to see what would happen. When the magnetic field was reversed so magnetic North was in the opposite direction, the butterflies altered their bearings and flew exactly opposite as well. This suggests that monarchs could have some sort of way to detect the earth’s magnetic field, called magnetoreception, which could enhance the photoreception capabilities.

Many of the mechanisms behind the migration of these incredible creatures are yet to be discovered, but much progress has been made in the past decade. So next time you see a monarch butterfly, take a second look. There is more than meets the eye.

Sources:

Gegear, R., Foley, L., Casselman, A., & Reppert, S. (2010). Animal cryptochromes mediate magnetoreception by an unconventional photochemical mechanism Nature, 463 (7282), 804-807 DOI: 10.1038/nature08719

Guerra, P., Gegear, R., & Reppert, S. (2014). A magnetic compass aids monarch butterfly migration Nature Communications, 5 DOI: 10.1038/ncomms5164

Merlin, C., Gegear, R., & Reppert, S. (2009). Antennal Circadian Clocks Coordinate Sun Compass Orientation in Migratory Monarch Butterflies Science, 325 (5948), 1700-1704 DOI: 10.1126/science.1176221

Steven M. Reppert. The Reppert Lab: Migration. University of Massachusetts Medical School: Department of Neurobiology.

Magnetoreception is Not a Party For a Supervillain

The majority of the more than 650 species of North American birds migrate. In search of food and nesting sites, some birds travel short distances and others (like Arctic terns) travel up to 12,000 miles each way. But all of them have to figure out where they are going, and much of how they do this is still unknown.

This is a magnetite rock. Scientists think
many animals have magnetite in their brains
to detect magnetic fields! For real?! Photo by
Rob Lavinsky at irocks.com and Wikimedia.

Last week, we learned that many birds get disoriented if the magnetic field around them is messed up by sunspots, magnetic rocks, or researchers gluing magnets to their heads. So they must sense magnetic fields, but how?

Sensation, whether by vision, touch, hearing, smell, taste or even magnetoreception (the sensation of magnetic fields) requires a stimulus to be transformed into an electrical signal that then must reach the brain. In the first five senses I listed, which we know considerably more about, this process occurs when sensory neurons (a type of cell in the brain and nervous system) convert the chemical or physical energy of the stimulus into an electrical signal. The sensory neurons then transmit the electrical signal to the brain, where it is processed and interpreted. So it is reasonable to think that magnetoreception works the same way too, right?

Where might such magnetoreception sensory neurons be? Bob Beason at State University of New York and Peter Semm at the Goethe University Frankfurt in Germany conducted a series of experiments to test whether the trigeminal nerve, a major nerve that provides sensation to the face, might play a role in magnetoreception. The trigeminal nerve has three major branches: the ophthalmic nerve, the maxillary nerve and the mandibular nerve. These nerves are each a bundle of sensory neuron fibers that send electrical signals to communicate to the brain what the head and face is sensing… a good place to look.

This illustration, titled Bubbling Bob the Bobolink,
was created by Louis Agassiz Fuentes in 1919.
Image at Wikimedia.

Bob and Peter exposed bobolinks, migratory birds that use magnetic fields to navigate, to a set of coils that could produce both vertical and horizontal magnetic fields. They then recorded the electrical activity of individual sensory neurons in the trigeminal nerve while exposing the birds to different magnetic fields. They found that many of these trigeminal sensory neurons, especially in the ophthalmic nerve branch, responded to the magnetic fields either by increasing or decreasing their electrical activity. Horizontal and vertical magnetic fields elicited different responses from different sensory neurons. Also, some sensory neurons responded to increases in magnetic strength and others responded to decreases in magnetic strength. The pattern of neuron activity could be a way that the nervous system could communicate the direction, and change in direction, of the magnetic field to the brain during navigation.

In order to test whether the ophthalmic nerve branch carries magnetic information to the brain, Bob and Peter tested another group of bobolinks that were preparing for migration. For each bird, they first tested what direction it preferred to go (for a control). Then, they magnetized the birds such that if their beak were iron, the tip of it would attract the south end of a compass. They figured that this process would send a confusing magnetic signal to the birds’ brains. Then they tested the birds’ preferred flying directions again (as expected, they got confused and went the wrong way). Finally, they numbed the ophthalmic nerve by putting a drop of Lidocaine on it and tested their preferred direction again. They found that although magnetizing the birds made them go the wrong direction, when their ophthalmic nerve was numbed, they ignored this incorrect magnetic information and went the right way again. Clearly, the ophthalmic nerve is sending magnetic information to the brain.

But how does a sensory neuron in the ophthalmic nerve respond to a magnetic force? For magnetoreception to work, magnetic forces need to affect receptors of some kind. Gerta Fleissner, Branko Stahl, Peter Thalau, Gerald Falkenberg, and Günther Fleissner at the Goethe University Frankfurt were the first scientists to systematically seek out such magnetoreceptors. They examined the skin lining the upper beak of homing pigeons with fancy microscope and X-ray techniques that could identify iron compounds in the skin.

These researchers found two different types of iron, magnetite and maghemite, in dendrites, the receiving ends of sensory neurons. Not only do these dendrites have both metals, but the metals are arranged in a particular way. This particular arrangement could cause the dendrite to physically respond to a magnetic field that is oriented in a particular way, perhaps by changing shape and stretching the membrane of the cell (remember, a sensory neuron is a cell). This physical pull on the membrane could cause the neuron to send an electric pulse, in much the same way as a hearing cell does.


Researchers discovered two magnetic metals, magnetite and maghemite, in the receiving
ends of sensory neurons. These two metals were arranged in such a way that if a magnetic
force were to align with the neuron in a particular direction, the metals would likely move and
stretch the membrane, which could activate the neuron, sending a signal to the brain. Figure
from Fleissner, Stahl, Thalau, Falkenberg, and Fleissner's 2007 paper in Naturwissenschaften.

Furthermore, the skin lining the pigeon beak has six separate iron-containing patches. In each of these patches, there is a different prevailing direction of how the iron-containing dendrites are aligned. This means that different nerve endings could be activated by different directions of magnetic field, potentially providing the bird with a complex perception of the magnetic field as it turns its head.

Magnetic dendrites (receiving ends of sensory neurons) were aligned in one of three
directions depending on where they were in the beak. This arrangement could allow birds
to know the direction of a magnetic field based on which neurons are activated. Figure from
Fleissner, Stahl, Thalau, Falkenberg, and Fleissner's 2007 paper in Naturwissenschaften.

Now, before you declare, “These birds have iron in them? What, are they some kind of superhero?” remember, we all (pretty much everyone except for our arthropod and mollusc friends) have iron in us… in our respiratory pigments (like hemoglobin). But this (new to us) use of iron does seem to give these birds super-human abilities.

Want to know more? Check these out:

1. Beason RC, & Semm P (1987). Magnetic responses of the trigeminal nerve system of the bobolink (Dolichonyx oryzivorus). Neuroscience letters, 80 (2), 229-34 PMID: 3683981

2. Semm P, & Beason RC (1990). Responses to small magnetic variations by the trigeminal system of the bobolink. Brain research bulletin, 25 (5), 735-40 PMID: 2289162

3. Beason R, & Semm P (1996). Does the avian ophthalmic nerve carry magnetic navigational information? The Journal of experimental biology, 199 (Pt 5), 1241-4 PMID: 9319100

4. Beason R, Dussourd N, & Deutschlander M (1995). Behavioural evidence for the use of magnetic material in magnetoreception by a migratory bird The Journal of experimental biology, 198 (Pt 1), 141-6 PMID: 9317510

5. Fleissner G, Stahl B, Thalau P, Falkenberg G, & Fleissner G (2007). A novel concept of Fe-mineral-based magnetoreception: histological and physicochemical data from the upper beak of homing pigeons. Die Naturwissenschaften, 94 (8), 631-42 PMID: 17361399

6. Cadiou H, & McNaughton PA (2010). Avian magnetite-based magnetoreception: a physiologist's perspective. Journal of the Royal Society, Interface / the Royal Society, 7 Suppl 2 PMID: 20106875

A Sixth Sense

Birds have long been known for their incredible navigational abilities. More than 4000 years ago, ancient Egyptians used carrier pigeons, the domesticated descendants of wild rock doves, to carry urgent messages to distant lands. They proved to be cheaper, faster and more efficient than human messengers and their use spread throughout the Mediterranean, central and northern Europe, and then throughout the world. Yet it wasn’t until the mid-1800s that scientists began to ask how they do it. To this day, how animals accurately navigate on long migrations is still one of biology’s great mysteries.

A modern day rock dove. Photo by Ingrid Taylar at Wikimedia.

That’s not to say science hasn’t made a lot of headway on this investigation. Scientists have found that some animals learn landmarks when they travel in one direction, and use those landmarks to find their way back. Some animals follow odor cues. But one of the more intriguing theories is that animals have an internal map and compass… but not a literal map and compass. The “map” is how the brain knows where things are in relation to each other and the “compass” is how the animal knows what direction it is facing with respect to where it wants to be.

How might such a compass work? One internal compass is a sun compass, in which an animal can use the position of the sun and the time of day to determine what direction it is facing. Some of the most convincing evidence supporting the existence of such a compass is that pigeons that are kept in a room with a time-shifted light cycle will fly in a predictably wrong direction on a sunny day. They will fly this wrong direction for long distances and even when they can see known landmarks. So pigeons clearly rely on the sun to achieve their great navigational feats… But what do they do on cloudy days… or at night?

A cartoon of the Earth's magnetic field by Zureks at
Wikimedia. In reality, the directions of magnetic pull
are not this straight and uniform, but you get the idea.

Maybe pigeons have another compass based on the Earth’s magnetic field. Over 30 years ago, researchers found that racing pigeons (the new profession of decedents of carrier pigeons after mailmen in trucks and airplanes took their previous jobs) arrive at their destinations a little bit later when there have been recent magnetic storms due to sunspots. Pigeons also get disoriented in places with magnetic anomalies, such as areas with lots of iron ore. But experiments in which researchers have placed magnets or magnetic coils on the backs, wings, necks, heads or legs of pigeons have not had consistent effects, particularly on sunny days (when the sun compass likely comes into play).

Enter Cordula Mora and Michael Walker from the University of Aukland, New Zealand. Cordula and Michael reasoned that because the magnetic field gets weaker with distance and because we think that magnetoreception (the ability to perceive magnetic fields) occurs in or around the head, maybe these previous studies had inconsistent results because the magnets used were too far away and/or too weak to affect the receptors in a consistent way. So they did their own study with smaller, stronger magnets applied to pigeon beaks.

Cordula and Michael glued magnets to the cere of pigeons. The diagram on the left shows how they did it and the photo on the right is a pigeon showing off his new nosepiece. (Check out the rock dove image above to see what a naked cere looks like). Diagram and image from Mora and Walker 2012 Animal Behaviour paper.

Cordula and Michael glued either a magnet or a brass weight (as a control) to the cere (the fleshy upper-part of the beak that contains the nostrils) of experienced racing pigeons right before a flight. In one experiment, researchers released the pigeons 11 consecutive times from the same place (called Gernsheim), and alternated whether they had a magnet or a brass weight glued to their cere. In a second experiment, the researchers released every bird once from each of 25 different places, each time with either a magnet or a brass weight glued to their cere. The birds were always flying to the same place (their loft), but the direction and distance they needed to fly was different for each of the release sites. Thus, the first experiment provides the birds with an opportunity to learn and compensate for any effect of the magnet, while the second experiment does not. All of the flights were done on sunny days.

The places the researchers released the pigeons from were all
different directions and distances from their home loft (at the center).
Diagram from Mora and Walker 2012 Animal Behaviour paper.

For each flight, the researchers watched the bird through binoculars until it vanished from view, at which point they recorded the vanishing bearing (the direction the pigeon was flying before it vanished from view). They also timed how long it took the bird to return to the loft and recorded any instances in which the bird did not return to the loft.

The pigeons with magnets consistently flew just a little to the right of pigeons with brass weights. The effect was very small (ranging from 11° to 22°), but it almost always happened, regardless of the bird or the release site. The effect was also consistent over consecutive years, even in birds tested repeatedly from the same release site. However, although the vanishing bearing of birds with magnets was regularly to the right of the birds with brass weights, the magnets did not prevent the pigeons from finding their loft and did not even cause them to take longer to get home. This shows that some time after the vanishing distance, the pigeons with magnets compensated for their originally slightly-off bearing.

The fact that the pigeons with magnets almost always started off flying too-far right suggests that they do have and use a magnetic compass, or perhaps even a magnetic map. But the fact that they always got back to the loft just as fast as their brass weight carrying counterparts shows that they also rely on other mechanisms, like a sun compass and landmarks. Perhaps magnetoreception is only important to determine take-off direction. Or alternatively, maybe the birds learn to ignore the confusing signals of the magnets after awhile.

We still have a lot to learn about how animals use magnetic fields. And how does magnetoreception even work? How animals navigate over long distances is still a great mystery, but scientists are on the case.

Want to know more? Check these out:

1. Mora, C.V., & Walker, M.M. (2012). Consistent effect of an attached magnet on the initial orientation of homing pigeons, Columbia livia. Animal Behaviour, 84, 377-383 DOI: 10.1016/j.anbehav.2012.05.005

2. Wiltschko, R., & Wiltschko, W. (2003). Avian navigation: from historical to modern concepts. Animal Behaviour, 65, 257-272 DOI: 10.1006/anbe.2003.2054

3. Bingman, V. P., & Cheng, K. (2005). Mechanisms of animal global navigation: comparative perspectives and enduring challenges. Ethology Ecology & Evolution, 17, 295-318 DOI: 10.1080/08927014.2005.9522584

4. Winged Migration, a fantastic movie by Jacques Perrin