Virtual migration in tethered flying monarch butterflies reveals their orientation mechanisms

Abstract

A newly developed flight simulator allows monarch butterflies to fly actively for up to several hours in any horizontal direction while their fall migratory flight direction can be continuously recorded. From these data, long segments of virtual flight paths of tethered, flying, migratory monarch butterflies were reconstructed, and by advancing or retarding the butterflies' circadian clocks, we have shown that they possess a time-compensated sun compass. Control monarchs on local time fly approximately southwest, those 6-h time-advanced fly southeast, and 6-h time-delayed butterflies fly in northwesterly directions. Moreover, butterflies flown in the same apparatus under simulated overcast in natural magnetic fields were randomly oriented and did not change direction when magnetic fields were rotated. Therefore, these experiments do not provide any evidence that monarch butterflies use a magnetic compass during migration.

Figure 1

(A) Schematic drawing of the flight simulator, the details of which are described in Materials and Methods. The translucent Plexiglas sky was used only in indoor experiments to simulate complete cloud cover. For clarity reasons, the overcast simulation is drawn higher above the apparatus than it was actually placed. (B–D) Examples of how the time resolution in our simulator data can be used to recreate the virtual path flown by the butterfly, compared with normal circular histograms of the same data. All virtual flight paths start in the center of the diagram and are directed toward the periphery. North is up. Units ≈1 m (1/5 s at speed 18 km/h). See text for details. Circular histograms show the orientation data accumulated from the periphery of the circle toward the center represented in the appropriate compass direction (north at top).

Figure 2

Monarch orientation in a flight simulator. (A) Under natural sunny skies (control), monarchs oriented toward southwest (n = 17, α = 225°, r = 0.83), consistent with the location of their Mexican wintering quarter. Butterflies clock-shifted −6 h (B) shifted their orientation toward southeast (n = 13, α = 136°, r = 0.62), and those clock-shifted +6 h (C) oriented northwest (n = 11, α = 335°, r = 0.80). These results are consistent with monarchs' use of a time-compensated sun compass. Butterflies tested under simulated overcast conditions (translucent Plexiglas cover) (D) were not significantly oriented (n = 18, r = 0.21, P = 0.46), suggesting that they were unable to use the natural magnetic field for orientation (see also Fig. 3). (Upper) The circular diagrams show the mean orientations for individuals and group mean vectors. ●, Mean orientation of each actively flapping individual. ○, Mean orientation of the four gliding individuals. ↑, The sample mean vector. The length of the sample mean vectors, r, indicates the angular concentration of the samples. Dashed circles indicate required length of the sample mean vectors to obtain significance at 0.05 and 0.01 levels (Rayleigh test). (Lower) The diagrams show the virtual path flown by each butterfly under the assumption of constant speed. (They all start in the center of the diagram and travel toward the periphery.) Distances have been normalized.

Figure 3

Normalized virtual tracks of 11 different butterflies tested under simulated overcast conditions in a Helmholtz coil system. The tracks are drawn so that the overall mean direction of each track is from left to right; i.e., the butterflies start at the left and end at the right side. Blue traces show the virtual path flown in the unchanged geomagnetic field, whereas the red traces show the same butterfly's orientation with magnetic north turned 120° clockwise to southeast.