Sky Compass Orientation in Desert Locusts-Evidence from Field and Laboratory Studies

Abstract

Locusts are long-range migratory insects. At high population density, immature animals form marching hopper bands while adults take off and form huge swarms of millions of animals. At low population densities animals are solitarious, but likewise migrate, mostly during the night. Numerous studies aimed at predicting locust infestations showed that migrations both as hopper bands and as adults are largely downwind following seasonal shifts of the tropical convergence zone taking the animals to areas of rainfall. Only a few studies provided evidence for active orientation mechanisms, including the involvement of a sun compass. This scarcity of evidence stands in contrast to recent neurobiological data showing sophisticated neuronal adaptations suited for sky compass navigation. These include a special dorsal eye region with photoreceptors suited to analyze the polarization pattern of the sky and a system of topographically arranged sky compass neurons in the central complex of the brain. Laboratory experiments, moreover, demonstrated polarotaxis in tethered flying animals. The discrepancy of these findings call for more rigorous field studies on active orientation mechanisms in locusts. It remains to be shown how locusts use their internal sky compass during mass migrations and what role it plays to guide solitarious locusts in their natural habitat.

Keywords: animal migration; desert locust; insect brain; polarization vision; sky compass orientation.

Figure 1

(A–C) Seasonal breeding areas (shaded gray) and major movements of desert locust (Schistocerca gregaria) swarms (arrows). Adapted from Roffey and Magor (2003) with kind permission.

Figure 2

Seasonal movements of different generations of desert locust populations in West Africa in relation to seasonal shifts in the Intertropical Convergence Zone (ITCZ), monsoons and winter rains. Note that migratory directions from January—March (lower right) are against the prevailing wind directions. Data are largely based on migrations of individuals rather than swarms. Adapted from Farrow (1990) after Popov (1965) with kind permission.

Figure 3

(A) The celestial polarization pattern at a solar elevation of 50°. E-vectors of plane polarized light are arranged tangentially to concentric circles around the sun. The degree of polarization (bar thickness) is maximal at 90° from the sun. (B,D) Polarotaxis of the desert locust. (B) Experimental setup. The animal is mounted on a vertical rod attached to a yaw-torque meter. Tethered flight is initiated by laminar frontal wind (blue arrows). Yaw torque is measured while the animal is stimulated with white light from above passing through a rotating polarizer. (C) Averaged data of four 360° rotations of the polarizer reveals periodic changes in yaw torque corresponding with the periodicity of the polarizer. (D) When the dorsal rim areas of both eyes (arrowheads in C) are covered with black paint, yaw torque becomes irregular and no longer corresponds to the position of the polarizer. (A) from Pfeiffer and Homberg (2014) with kind permission; (B) from Backasch (2009) with kind permission; (C,D) from Homberg (2004).

Figure 4

Central processing of polarized light signals from zenithal directions in the locust brain. (A) Polarization vision pathways in the brain of the desert locust. Processing stages for polarization analysis include dorsal rim areas in the lamina and medulla (LADRA, MEDRA), a ventral layer in the anterior lobe of the lobula (ALO), the anterior optic tubercle (AOTU), the lateral and medial bulbs of the lateral complex (LBU, MBU), the central body (CB) and the protocerebral bridge (PB). In a second pathway, the accessory medulla (AME) is connected to the PB via the posterior optic tubercle (POTU). Inputs to the central complex are shown in blue, outputs in red. AL, antennal lobe; CA, calyx of the mushroom body. (B) Idealized compass-like representation of E-vector tunings (double arrows) in columnar neurons of the PB and upper division of the central body (CBU). LAL, lateral accessory lobe. (C,D) Morphology (C) and polarized light sensitivity (D) of a tangential neuron of the lower division of the central body (CBL). When the animal is illuminated from above through a rotating polarizer, spike frequency is modulated as a function of E-vector orientation. Maximum (Φ_max) and minimum spiking activity (Φ_min) occurs at orthogonal E-vectors. (A,B) adapted from Pfeiffer and Homberg (2014); (C,D) from Heinze et al. (2009) with kind permission.