Experimental evidence for magnetic field sensitivity has been reported in insects belonging to various orders, including Isoptera (termites), Diptera (flies), Coleoptera (beetles), Hymenoptera (ants and bees), and Lepidoptera (moths and butterflies). There is evidence that a few insect species obtain directional information from geomagnetic fields for compass orientation. Two alternative properties of the local geomagnetic vector could serve this purpose. Like a number of birds, animals either make use of the direction in which the dip angle points (“inclination compass”) regardless of the field’s polarity or sense the local declination and polarity (“polarity compass”). Which of these alternatives pertains to insects has been investigated in only one species, the yellow mealworm (Tenebrio molitor) (Coleoptera), which makes use of the polarity compass. The sensory system that mediates magnetoreception in insects has not been identified definitively, though one favored hypothesis is based on the detection of magnetic fields using particles of magnetite.
Magnetic compass orientation can be useful for insects in the context of home range (topographic) orientation and during long-distance migration, especially in the absence of visual compass cues. Both honey bees building combs in darkness and blind termites building oriented mounds appear to use magnetoreception for aligning their structures. On the other hand, it is difficult to imagine how an insect could make adaptive use of sensing the absolute strength of the local geomagnetic field.
MAGNETIC COMPASS ORIENTATION
Multiple directional orientation or compass orientation to artificially induced magnetic fields has been shown in several species. The insects always responded to changes in the magnetic field’s declination, which implies sensing of magnetic polarity. In contrast, a geomagnetic inclination compass, as used by some migrating birds, has not been demonstrated for any insect.
Home Range Orientation in Social Insects
The magnetic sense of insects and its adaptive importance have been most thoroughly investigated in social insects such as ants,bees, and termites that require highly developed orientation skills to find and then communicate to their nestmates the location of resources within their home ranges. Much is known about how ants and bees use visual cues such as the sun, polarized light, the moon, and landmarks for spatial orientation. For most navigating insects, the primacy of visual cues must be taken into account in experiments designed to investigate magnetic field orientation. Indeed, an insect’s competence in magnetic field orientation may be hidden if more salient cues such as light are present. However, termite workers and soldiers, which have poor vision at best, rely more on nonvisual cues.
THE GEOMAGNETIC FIELD AS A BACKUP CUE FOR
ANTS Experiments with naturally foraging weaver ants, Oecophylla smaragdina, revealed that their sense of direction is stronger and more accurate under clear skies than under overcast skies. In addition, when ants were tested for orientation indoors after displacement from their outdoor foraging trail, those exposed to overcast conditions maintained the correct trail heading but others exposed to clear skies did not. The difference in response indicated the ants’ use of a nonvisual cue that is overridden by celestial cues if they are present. Support for this hypothesis came with further experiments showing that ants trailing in dim, diffuse light reversed their heading when exposed to an artificially induced magnetic field with polarity opposite that of the geomagnetic field. Wood ants, Formica rufa, have also been shown to use magnetic field orientation when directional light cues are unavailable. These experiments with two species of ants suggest a hierarchically organized orientation system designed so that the primary light compass is more efficient than the magnetic compass, which serves as a backup when directional light cues are absent.
MAGNETIC DIRECTION AS A REFERENCE FOR
LANDMARK LEARNING IN HONEY BEES
In flight, the honey bee, Apis mellifera, also uses a magnetic compass in home range orientation. Foraging bees approaching the vicinity of their “target” learn the precise location of resources with respect to surrounding landmarks so they can return to the same place in the future. The most popular hypothesis assumes fast “snapshot”-like recall of near-target constellations of landmarks. The returning bee finds the target location by matching the current perception of landmarks with the “snapshot memories” of them. While learning the spatial relations of landmarks, bees face in a preferred compass direction, using directional light and the geomagnetic field. Honey bees trained in an artificial field with polarity reversed to the geomagnetic field face landmarks in the opposite direction. Hence, their magnetic compass may provide directional information as a frame of reference for the memorized landmarks.
A MAGNETIC CUE FOR HOMING TERMITES
All termites are social insects that have evolved a different set of adaptations for home range orientation. Termites are specialized for foraging underground and in enclosed spaces. The eyesight of workers and soldiers either has regressed or has been lost completely. All foraging termites depend heavily on pheromone trails for finding their way back home. However, as in ants, such trails do not provide any cue that helps to discriminate between the outward and homeward direction. The geomagnetic field could provide such a cue. This has indeed been demonstrated in the blind African grass-harvesting Trinervitermes geminatus (Termitidae: Nasutitermitinae) which, unlike the majority of termite species, is an open-air forager. Homing orientation in returning workers is substantially disturbed by distortions of the geomagnetic field due to weak bar magnets. Whether geomagnetic field orientation is widespread among termites is still an open question.
Migration in Moths and Butterflies
Long-distance compass migration has evolved in relatively few species of insects as an adaptation for dispersal and for coping with seasonal climatic changes. Examples are found among dragonflies (Anisoptera), true bugs (Heteroptera: e.g., the large milkweed bug Oncopeltus fasciatus), and moths and butterflies (Lepidoptera). The implied geographic orientation mechanism could, plausibly, make use of magnetic compass orientation, especially during nocturnal migration and migration under dense overcast.
The most spectacular example of geographic orientation in insects is the massive annual fall migration of the monarch butterfly, Danaus plexippus. Eastern North American populations of mon-archs migrate over 3000 km to winter in the mountains of Mexico. Experimental evidence substantiates their use of a sun compass for geographic orientation, and some experiments suggest their use of a magnetic compass as well.
For years entomologists have speculated about magnetic compass orientation in migrating monarch butterflies. The first supportive evidence came in field experiments: migratory butterflies were exposed to a brief pulse of an induced magnetic field 15,000 times the intensity of the geomagnetic field, whereupon the treated butterflies were released and tracked to determine their direction of flight. Two control groups of butterflies were also tested. One of the control groups received the same treatment as the experimental group except for the magnetic pulse. The other group received no treatment and was composed of naturally occurring butterflies migrating through the test area. Both control groups of butterflies kept their normal migratory flight direction to the southwest, but directional headings of the magnetically treated group were randomly distributed, indicating disorientation. Because these experiments were conducted on clear days, however, the sun was also available as a cue. Thus conflicting information from the butterflies’ sun and magnetic compasses may have caused the insects’ disorientation.
OTHER EFFECTS OF MAGNETIC FIELDS ON
THE ORIENTATION BEHAVIOR OF INSECTS
Some of the earliest and most detailed studies of magnetic field sensitivity were also conducted with social insects. Once again the honey bee was the focus of intense research, but this time the investigators studied its communication behavior. To recruit and guide nestmates to a newly discovered resource, a honey bee performs a dance indicating to her followers the direction and distance of the resource from the hive. The dance is usually performed in darkness on a comb’s vertical surface. The flight direction to the resource in reference to the sun is transposed by the bee to the direction of her dance with respect to gravity on the comb. If the resource is in the direction of the sun, the dance is directed upward; if away from the sun, downward; and if in other locations, at various angles to the vertical. Small systematic errors in the directional component of this dance are correlated with daily fluctuations in intensity of the geomagnetic field. These errors disappear when the bees dance in an artificial magnetic field that compensates for the earth’s field.
When honey bees are forced to dance on a horizontal surface in the dark, their dances become aligned with the cardinal and intercar-dinal axes of the geomagnetic field. This response intensifies when the magnetic field is artificially enhanced and disappears when the field is canceled.
Evidence also suggests that honey bees use magnetic fields in nest construction. Bees that are transferred to a new hive construct combs that are oriented in approximately the same magnetic direction as those in their old hive. In one study, bees built abnormal combs when they were exposed to magnets during construction.
Among the most spectacular and magnificent termite mounds are those of Amitermes meridionalis (Termitidae: Amitermitinae) in tropical Australia near the town of Darwin (Fig. 1). These massive tombstone-like black structures reach up to 4 m in height, and their long horizontal axes align near perfectly north—south. Similar but less perfectly oriented and shaped mounds are constructed by A. lauren-sis on the Cape York Peninsula of Australia. It is more than tempting to refer to these mound builders as “magnetic termites.”
FIGURE 1 Giant (2.3-m high) mound of the Australian “magnetic” termite Amitermes meridionalis. On the left is the east—west aspect and on the right the north— south aspect.
Indeed some good evidence supports this label. If a strong, permanent magnet is buried underground where a new colony starts to build, the resulting structure is misshapen and lacks clear orientation.
In addition to nest alignment, numerous studies have identified insects that align the body axis to magnetic fields. Resting termites, flies, and honey bees adopt positions aligned with the cardinal axes of a magnetic field.
Finally, orientation transfer sometimes occurs from light orientation to magnetic compass orientation. When a yellow mealworm moves away from a light source, it remembers its current magnetic compass bearing. If the directional light is turned off, the course direction is maintained with the help of the remembered magnetic compass bearing.
POSSIBLE SENSORY MECHANISMS
Several hypotheses have been proposed to explain how animals sense magnetic fields. There is circumstantial but no definitive evidence in insects for two such sensory mechanisms. One type of mechanism could be based on the magnetic sensitivity of some chemical or photochemical reactions. If such reactions are linked to light reception in the eye, then changing the wavelength of ambient visible light could alter the directional orientation to the geomagnetic field. Such effects have been obtained in male Drosophila melanogaster (Diptera) as well as in some birds. A second mechanism could be based on the interaction between the geomagnetic field and intracellular, submicroscopic magnetite particles that have been found in some insects, including ants, honey bees, and monarch butterflies.
