Innate visual attraction before, during and after escape from adverse substrates in carpenter ants

Abstract

Many animals exhibit an innate attraction to dark areas or objects, driving orientation behaviours such as beacon aiming. In ants, some species do not appear to display beacon aiming. Here, we show that in one such species, Camponotus japonicus, the behaviour is triggered when crossing liquid-covered surfaces, regardless of locomotor pattern and the presence of water in the liquid. Once initiated, beacon aiming persisted even after the ants transitioned from water to dry substrates, as evidenced by their reorientation towards a displaced beacon. Beacon aiming could be observed before the ants fully transitioned from a dry substrate to a liquid-covered surface: when the ants were isolated on a water-surrounded platform, attraction to a beacon emerged while they were contacting the water, before finally deciding to swim towards the beacon. Adverse substrate conditions in general appear to be a factor triggering beacon aiming as we also identified one condition (so far) in which even liquid immersion was not required for beacon aiming, namely upside-down walking. These results indicate that beacon aiming in C. japonicus is performed before, during and after escape from adverse substrates. Evidence that substrate conditions can alter seemingly hardwired responses suggests that insects may adjust even simple behaviours in response to environmental conditions in a more sensitive way than commonly assumed.

Keywords: Innate behaviour; Landmark; Substrate conditions; Swimming; Visual orientation; Walking.

Fig. 1.

Experimental setup. All experiments were conducted in an arena with a black beacon (height: 45 deg, width: 20 deg, measured from the effective centre of the floor) placed against the wall. Arrows and crosses represent the overall orientation trend. (A) Basic arena used for land walking. (B) Arena filled with water for swimming (water swimming) or with shallow water for wading (water wading). (C) Arena (same as in A) with a transparent dish filled with either an 80% (v/v) glycerol and 20% (v/v) 2-propanol mixture (glycerol swimming) or a 1.0% (w/w) Tylose aqueous solution (Tylose swimming). (D) Arena with an inverted walking surface (upside-down walking) and chamber to introduce ants such that they transitioned from upside-up (on plastic) to upside-down walking (on sandpaper, brown) by themselves. The black bar indicates the beacon. The camera and illumination were positioned below the arena. (E) Arena fitted with extruded polystyrene foam inserts for transition from swimming in water to walking on a dry substrate. The insert contained a central pool filled with water (for the beacon-fixed and beacon-displaced condition). In controls, an insert of the same thickness but without the centre pool was used for identical dry walking surface conditions (for the walking-without-transition condition). The final beacon position after displacement (for the beacon-displaced condition) is shown as a dashed outline. (F) Arena (as in B) with a central platform surrounded by water (island).

Fig. 2.

Beacon aiming during walking and upside-down walking on a dry substrate, as well as during swimming and wading. (A–F) Trajectories of all N trials and circular box-and-whisker plots of final bearings are shown for: (A) land walking (N=57); (B) water swimming (N=57); (C) water wading (N=57); (D) glycerol swimming (N=47); (E) Tylose swimming (N=59); and (F) upside-down walking (N=45). The beacon range is represented as a black arc segment on the left side of each plot. Circular box-and-whisker plots show median, first quartile, third quartile (coloured interquartile range), minimum and maximum (whiskers), and outliers (black-filled circles) of the final bearing distributions.

Fig. 3.

Persistence of attraction to the beacon after water-to-land transition. (A–C) Trajectories of all N trials and circular box-and-whisker plots of final bearings are shown for: (A) the walking-without-transition condition, until ants reached the arena edge (N=33); (B) the beacon-fixed condition, with an enlarged view of the central pool area [‘before walking’: until ants reached the central water-filled pool edge (dashed circle) swimming; N=33]; and (C) as for B but for the beacon-displaced condition, with an enlarged view of the central pool area (N=33). For the beacon-displaced condition (C), the arrow indicates the direction of the 60 deg beacon position shift. The initial beacon range is shown in grey, and the final range after displacement is shown in black.

Fig. 4.

Gradual emergence of attraction to the beacon around the land-to-water transition. Walking on a water-surrounded platform (island, dashed centre circle) to swimming transition. (A) Representative frame images capturing key moments: first contact, first immersion, start of swimming and end of swimming. (B) Initial phase: walking trajectories on the island for this phase (until first water contact). One representative trajectory in magenta, its end point at first water contact (yellow star) displayed with a circular box-and-whisker plot of the distribution of the directions of the first water contact for all trials (N=33). (C) Contact phase: circular box-and-whisker plot of the distribution of directions of all water contacts (N=282) between first water contact and first water immersion for all trials. (D) Contact phase: conventions as in B with a circular box-and-whisker plot indicating the direction of first immersion (N=33). Representative trajectory in magenta, with its water contact positions (yellow stars) and its first water immersion position (blue star). (E) Immersion phase: conventions as in C, but for all water immersions (N=1250) until the start of swimming for all trials. (F) Immersion phase: conventions as in B, a circular box-and-whisker plot indicating the direction of swimming initiation position (N=33). Representative trajectory (magenta), with its immersion positions (blue stars) and its swimming initiation position (green star). (G) Swimming phase: conventions as in B but for swimming, circular box-and-whisker plot representing the direction of final swimming bearing (N=33). Representative trajectory (magenta), with its swimming initiation position (green star) and its final arrival position at the arena edge (purple star).