A magnetic compass aids monarch butterfly migration

Abstract

Convincing evidence that migrant monarch butterflies (Danaus plexippus) use a magnetic compass to aid their fall migration has been lacking from the spectacular navigational capabilities of this species. Here we use flight simulator studies to show that migrants indeed possess an inclination magnetic compass to help direct their flight equatorward in the fall. The use of this inclination compass is light-dependent utilizing ultraviolet-A/blue light between 380 and 420 nm. Notably, the significance of light <420 nm for inclination compass function was not considered in previous monarch studies. The antennae are important for the inclination compass because they appear to contain light-sensitive magnetosensors. For migratory monarchs, the inclination compass may serve as an important orientation mechanism when directional daylight cues are unavailable and may also augment time-compensated sun compass orientation for appropriate directionality throughout the migration.

Figure 1. Fall migrant monarch butterflies can use a magnetic field to orient in the proper southerly fall migratory direction.

(a) Flight simulator and coil system used in magnetic compass trials. (b) Irradiance curve of lighting conditions during flight simulator trials. Light measurement was taken inside the flight simulator, with the flight encoder and diffuser in position, at the position of the head of the tethered monarch butterfly during trials. (c) Orientation of individual directional fall monarchs during the fall 2012 (n=18) and 2013 (n=27) migration seasons (red dots; both years pooled: n=45) in a generated field with a 45° inclination angle, at a 141 μT field intensity. For the circle diagram, arrow indicates mean group orientation, shaded area is 95% confidence interval, mN is magnetic north.

Figure 2. The inclination magnetic compass of fall migratory monarch butterflies.

(a) Fall migrant monarchs that oriented equatorwards during their initial flight (left; red; n=8), shifted their orientation towards magnetic North when tested a second time under similar generated field conditions (right; dark green; n=8), but with the inclination angle reversed (−45°). (b) Fall migrant monarchs that oriented equatorwards during their initial flight (left; red; n=7), each displayed flight with significantly reduced directionality (that is, Z score <500) when tested a second time under a horizontal field (0° inclination angle) with the same field intensity (n=7). For both a and b, bar graphs indicate the mean Z±s.e.m. score of animals for each group. Circular diagrams are the group orientation behaviour for each group in which each monarch plotted (dot) had a Z score >500. For each circular diagram, the arrow indicates mean group orientation, shaded area is 95% confidence interval, and mN is magnetic north.

Figure 3. The inclination magnetic compass uses ultraviolet-A/blue light.

(a) Irradiance curves of lighting conditions during flight simulator trials. Black line indicates full spectrum light, blue line denotes filtered light that provided wavelengths of light >420 nm only, and purple line designates filtered light where only wavelengths of light >380 nm were available. (b) Migrants that oriented equatorwards during their first flight when tested under full spectrum lighting conditions (left; red; n=5) had significantly less directional flight, that is, Z<500 (right; blue; n=5), when tested under light that contained wavelengths >420 nm. (c) In contrast, monarchs that oriented equatorwards under full spectrum light during their initial flight (left; red; n=5), maintained similar oriented flight that was equatorwards when tested under lighting conditions that included wavelengths >380 nm (right; purple; n=5). For all trials, the inclination angle was 45° and the field intensity was 141 μT. In both b and c, bar graphs indicate the mean Z±s.e.m. score of animals for each group. Circular diagrams consist of the group orientation behaviour for each group in which each monarch plotted (dot) had a Z score >500. In each circular diagram, arrow indicates mean group orientation, shaded area is 95% confidence interval, and mN is magnetic north.

Figure 4. The light-dependent magnetosensor involves the antennae.

(a) Fall migrants that were oriented equatorwards during their initial flight (left; red; n=5) had significantly less directional flight (that is, Z<500) when both antennae were painted black during their second flight (right; black; n=5). (b) In contrast, fall migrants that were directed towards magnetic South during their initial flight (left; red; n=5) shifted towards magnetic North when tested with clear-painted antennae under reversed inclination angle conditions (right; grey; n=5). For both a and b, monarchs (left diagrams; red) were tested in a generated field with a 45° inclination angle and an intensity of 141 μT. In contrast, monarchs (right diagrams; black for a and grey for b) were tested in a generated field that had the same intensity, but where the inclination angle was −45°. In both a and b, each bar graph indicates the mean Z±s.e.m. score of animals for each group. Each circular diagram consists of the group orientation behaviour for each group in which each monarch plotted (dot) had a Z score >500. For each circular diagram, the arrow indicates mean group orientation, shaded area is 95% confidence interval, and mN is magnetic north.

Figure 5. The inclination compass of monarchs functions at an Earth-strength field intensity.

(a) Orientation of individual directional monarchs (left; red; n=7) in a generated field with a 45° inclination angle, at a 141 μT field intensity. The orientation of individual directional monarchs (right; maroon; n=7) tested a second time (same monarchs from left circular diagram), but in a generated field with a 60° inclination angle, at a 57 μT field intensity. (b) Monarchs that flew towards magnetic South (left; maroon; n=5) in a field with a 60° inclination angle and a 57 μT intensity (second flight) reversed their flight orientation to magnetic North (right; green; n=5) in a generated field with a −60° inclination angle at a 57 μT field intensity, when tested a third time (same monarchs from left circular diagram). In both a and b, circular diagrams consist of the group orientation behaviour for each group in which each monarch plotted (dot) had a Z score >500. In each circular diagram, the arrow indicates mean group orientation, shaded area is 95% confidence interval, and mN is magnetic north. For both a and b, bar graphs indicate the mean Z±s.e.m. score of animals for each group.