Long-distance Navigation and magnetoreception in migratory animals

The excerpt note is about twenty important mechanistic questions related to long-distance animal navigation from Mouritsen, H. (2018).

Mouritsen, H. (2018). Long-distance navigation and magnetoreception in migratory animals. Nature, 558(7708), 50.

Abstract: For centuries, humans have been fascinated by how migratory animals find their way over thousands of kilometers. Here, the author reviews the mechanisms used in animal orientation and navigation with a particular focus on long-distance migrants and magnetoreception. He contends that any long-distance navigational task consists of three phases and that no single cue or mechanism will enable animals to navigate with pinpoint accuracy over thousands of kilometers. Multiscale and multisensory cue integration in the brain is needed. He concludes by raising twenty important mechanistic questions related to long-distance animal navigation that should be solved over the next twenty years.

a, European robin (Erithacus rubecula). b, Bar-tailed godwit (Limosa lapponica). c, Wandering albatross (Diomedea exulans). d, Monarch butterfly (Danaus plexippus). e, Bogong moth (Agrotis infusa). f, Sea turtle (Eretmochelys imbricata). g, Salmon (Oncorhynchus kisutch). Photographs by H.M. (a, b, d); E. Dunens (c); A. Narendra (e); Adam (f); and the Bureau of Land Management Oregon and Washington (g). (c, f, g: https://creativecommons.org/licenses/by/2.0/).

Each year, billions of small songbirds, with ‘birdbrains’ weighing only a few grams, leave their Arctic and temperate breeding areas to overwinter in the tropics and subtropics. Most migrate at night, and young birds do so without regular contact with experienced individuals. Thus, their navigational capabilities must be innate or learned before their first departure. After having completed one round trip, many adult birds are able to navigate with an ultimate precision of centimetres over distances of 5000 km or more. Other impressive navigational tasks mastered by birds include bar-tailed godwits migrating from Alaska to New Zealand in a single not-stop flight lasting 7-9 days and nights, arctic terns breeding around the North Pole and wintering around the South Pole, and seabirds flying more than 100000km per year to return to tiny islands in the middle of vast oceans to breed.

Even insects with much simpler brains than birds are capable of performing impressive navigational tasks. In autumn, monarch butterflies migrate from the USA and Canada to very specific overwintering trees in Mexico, up to 3000 km away. A year later, the third-to-fifth-generation descendants of the previous year’s autumn migrants return to the exact same trees in Mexico. A similarly impressive return migration – but involving only a single generation – occurs in Southeast Australia, where millions of Bogong moths fill the night skies on their way to and from their yearly aestivation caves in the Snowy Mountains. Recently, Chapman et al. demonstrated that directed long-distance return migrations are also widespread among high-flying insects. These movements of trillions of individual insects are critical for understanding both natural and manmade ecosystems.

In the ocean, Salmonid fish and sea turtles, for instance, return to their natal streams or beaches over thousands of kilometres and many dispersing coral reef fish larvae relocate their natal reefs after being at the mercy of sea currents for weeks.

To complete their long voyages, migratory animals have developed elaborate abilities to detect a variety of sensory cues, to integrate these signals within nervous systems, and to use them as part of highly efficient navigational strategies. Navigation skills are also vitally important to non-migratory animals of almost any class. However, this review focuses primarily on long-distance navigation and homing. The author discusses how animals use, detect and process the main types of navigation relevant cue. He considers magnetic cues in more detail than other cues because the sensory mechanisms that underlie sight, olfaction and hearing are generally understood. By contrast, even though a lot of progress has been made recently, the mechanisms by which animals sense the geomagnetic field remains one of the most fundamentally important questions in sensory biology. He also highlights twenty of the most important outstanding mechanistic questions that remain to be answered.

The questions listed below represent some of the most important open mechanistic questions for the next two decades of long-distance navigation and magnetoreception research.

1. How do the magnetic senses work on the biophysical, biochemical, and molecular levels?

2. Does quantum biology exist (that is, is magnetic sensing truly quantum in at least some animals)?

3. What are the explanation for and ecological consequences of the extraordinary sensitivity of the bird’s magnetic compass to disruptive anthropogenic electromagnetic fields?

4. How does the light-dependent magnetoreception mechanism distinguish between changes in light intensity and magnetic direction, and how does it collect enough reaction statistics to detect magnetic direction s under low light conditions?

5. Do some animals use electromagnetic induction to detect the geomagnetic field?

6. Do magnetic particles exist inside cells at consistent and specific locations in many individuals of any migratory animal, and are the particles associated with the nervous system?

7. How, if at all, can slow-moving animal distinguish the spatial magnetic signal from temporal geomagnetic field variation to allow for a magnetic map with a resolution below 10-30 km?

8. Where and how is magnetic information sensed and processed?

9. Where in the brain, and how, is multisensory navigational information integrated and weighted?

10. How do processing strategies in the nervous system transition between the different phases?

11. How does the brain deal with conflicting and / or incomplete information, and does this depend on the ecological conditions and / or the navigational phase?

12. Do place and grid cell equivalents exist as neural correlates of the map over scales of kilometres or even thousands of kilometres, and, if yes, which cues contribute to their establishment?

13. Do equivalents of head direction cells exist that code for celestial and / or magnetic compass direction on a regional or global scale?

14. How is the very slow rotation of the stars detected?

15. How do small animals moving in air or water detect the direction of flow even though they are embedded in the flowing medium themselves?

16. Which genes trigger migration behaviour and /or code for migratory direction and distance?

17. Exactly what cues signal to an animal that it should start migrating or that it has reached its destination and should terminate migration?

18. What determines when an animal switches from one navigational phase to the next?

19. How is longitude (east-west) position determined on a regional or even global scale?

20. How does the pinpointing-the-gal phase work in a monarch butterfly or Bogong moth, which can pinpoint their very specific wintering locations even though they have never been there before?

Neural representations of map and compass

The rodent hippocampus contains place cells, which define a specific location within a small arena, and head direction cells, which represent the animal’s current heading. Furthermore, the entorhinal cortex contains grid cells, which fire at node-points in a repetitive triangular array covering the entire available surface. Grid cells might define distances. These fascinating cell types are highly likely to be neural representations of location and direction during the pin-pointing-the-goal phase, as these cell types are established relative to prominent local landmarks. In contrast to the extensive knowledge about short-distance navigation in rats, mice, and fruit bats, very little is known about long-distance navigation mechanisms in mammals. Do similar cell types exist that define direction (compass information) and location (map information) during the homing and long-distance phases of a navigational task? If so, their responses would need to be established relative to global cues such as celestial bodies or the geomagnetic field, because long-distance migrants and homing animals can determine direction and location in unfamiliar places. Furthermore, during the pinpointing-the-goal phase, the spatial coding cells of many animals will need to define in three-dimensional space were found in flying Egyptian fruit bats. Compass neurons also exist in the central complex of migratory insects. Map concepts – let alone map neurons – are very controversial among insect researchers.

For further info on Nature

Mouritsen, H. (2018). Long-distance navigation and magnetoreception in migratory animals. Nature, 558(7708), 50.