When experimentally displaced in geomagnetic space, spiny lobsters act as if to make their way home. This is a fascinating case of navigation by an invertebrate using a magnetic map sense.
Sometimes an idea is so irresistible that it is revisited over and over again. One such is the notion that Earth's magnetic field provides guidance for animal orientation and even true navigation. This topic has a long history, and on page 60 of this issue Boles and Lohmann1 present the latest turn of events. From the results of elegant displacement experiments in both geographical and geomagnetic space, they conclude that the impressive homing capacity of spiny lobsters is probably based on a map sense involving geomagnetic cues. This is the first time that such true navigational capability has been plausibly ascribed to an invertebrate.
During the first half of the nineteenth century, great advances in the understanding of magnetism were made in basic physics and through expeditions to the north and south magnetic poles. Duly inspired, in 1855 Middendorff2 suggested that migrating birds behave like compass needles, unfailingly heading towards magnetic north in spring, guided by an inner magnetic sense caused (he conjectured) by induced electric currents in their bodies. Debate about the homing instinct in this journal in 1873 and 1874 included Darwin's crucial point3 that a compass sense alone is not enough to explain the spectacular navigation feats among animals: “Even if we grant to animals a sense of the points of the compass, of which there is no evidence, how can we account, for instance, for the turtles ... on the shores of the Isle of Ascension, finding their way to that speck of land in the midst of the Atlantic Ocean?”
Influenced by this debate, Viguier4, a French zoologist working in Algeria, proposed in 1882 that the geomagnetic field is not only the basis of a compass sense but also furnishes animals with information about their position. He believed that the coordinates provided by magnetic inclination (dip angle), field intensity and/or declination would be sufficient for possession of a complete map sense (Fig. 1). This hypothesis was revived several times in the twentieth century5,6,7, one version7 invoking coordinate information input from the Coriolis force as well. But each time the idea met with ephemeral support.
Only much later, by about 1970, did behavioural experiments with migratory birds and homing pigeons provide compelling evidence of the existence of a compass sense based on magnetoreception8. Since then, such a sense has been demonstrated in a wide range of animals — molluscs, crustaceans, insects, fishes, amphibians, reptiles and mammals8 — and there has been the discovery of biogenic magnetite as a possible basis for magnetoreception9. Hence the recent revival of interest in the topic.
All of which brings us to the spiny lobster, Panulirus argus, which lives in coastal waters in the Gulf of Mexico and the Caribbean. It undertakes seasonal migrations of up to 200 km, and has a remarkable capacity for homing even if displaced to deep waters. Some years ago, experiments carried out by Lohmann and colleagues10, employing underwater magnetic coils, showed that the lobsters have a magnetic compass sense that allows them to walk on the sea floor, in darkness and without hydrodynamic cues, along a constant course determined by the horizontal component of the geomagnetic field.
Boles and Lohmann1 have now turned to analysis of the lobsters' homing capacity, carrying out a series of experiments in which lobsters were displaced 12–37 km from their capture site. The lobsters were deprived of visual or chemical cues (and probably also lacked inertial cues) during transport from the capture site to the test site. They were likewise denied such cues during the tests themselves. But they nonetheless showed an impressive ability to start walking in the direction of the capture site — that is, back home. This held true even when magnets were used during transport to the test site to disrupt magnetic compass information. Apparently the lobsters have a sense of position relative to home that is based on information picked up at the test site.
The final step in Boles and Lohmann's study was to keep the lobsters at the same geographical position, but to displace them in geomagnetic space by exposing them to magnetic conditions of inclination and field intensity that simulated positions to the north or the south of the capture site (Fig. 2). The lobsters responded as one would expect if they were determining their position from a geomagnetic map.
There is increasing experimental evidence of magnetic positioning and navigation in birds8,11, sea turtles12 and newts13. This study with the spiny lobster adds the first invertebrate to that list. But plenty of questions remain. Here are four.
First, does the geomagnetic field provide a basis for uni- or bicoordinate navigation — that is, does it allow positioning in only one dimension or (if two parameters form a useful grid) in two dimensions? Second, the lines of equal dip angle and field intensity run almost (but not exactly) parallel east–west in the spiny lobster's range (Fig. 2), and one would think that this circumstance would make magnetic navigation more difficult along this axis than latitudinally. But the lobsters showed no difficulty in detecting east–west natural displacements. Do they use geomagnetic cues in this situation and, if so, what geomagnetic elements might be involved?
Third, does the magnetic landscape in the study area (the local pattern of different magnetic gradients) satisfy the requirements for unambiguous determination of position? Fine-scale charting of the magnetic field will be needed to infer how magnetic navigation might work over such short distances. And fourth, the magnetic field is slowly changing in a way that corresponds to several kilometres of annual displacement of magnetic parameters in the study region: how do the lobsters keep their magnetic map information up to date?
Finally there is the more general question of the sensory mechanisms that underlie the magnetic compass and navigational abilities. Progress has been made in studies of magnetoreceptor systems based on both light-dependent chemical (radical pair) processes and magnetite14. But all of the mechanisms that have been proposed remain hypothetical — this, above all, is the matter to which we would like to see some answers.
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