A nocturnal bull ant, Myrmecia pyriformis, worker. Photo credit: Ajay Narendra.
Bull ants have a fearsome reputation, delivering vicious stings to anything that stumbles into their path. However, when it comes to living in harmony with other members of the bull ant family, the aggressive insects have evolved the ultimate timeshare solution: they take it in turns to come out. Some species specialise in daytime activity, while others roam at dusk and dawn, and others have opted for a nocturnal take on the day. However, it was not clear what locks each of these closely related species into their own unique schedule. ‘Competition and temperature tolerance did not explain this’, says Ajay Narendra, from Macquarie University, Australia. Puzzled by the ability of the close relatives to partition the day and knowing that some ant species have a pupil structure in the eye that can expand to admit more light in dim conditions, Narendra and colleagues from The Australian National University, Willi Ribi and Jochen Zeil, wondered whether bull ants with different activity patterns might have specially adapted eye designs that could account for their temporal segregation.
Narendra selected four species that live in close proximity – daytime active Myrmecia croslandi, dawn active M. tarsata, dusk active M. nigriceps and nocturnal M. pyriformis – and recalls that it was simply a matter of arriving at the nest just as the ants became active in order to collect them; ‘The activity schedule of these ants is so predictable’, he says. However, no one risked approaching the nests without protective gum boots, and Narendra adds that collecting the nocturnal species was particularly hazardous: ‘we armed ourselves with infrared cameras to spot the ants before they found us,’ he chuckles.
Back in the lab, Narendra, Ribi and Birgit Greiner exposed all four species to bright light and total darkness. Scrutinising how the eye structures responded, the team clearly saw a pupil structure that constricted when the light was bright in the eyes of the three species that are active in the darker conditions. The pupil was composed of pigment cells that encircled the crystalline cone, reducing the aperture through which light passes to 0.8 μm in the twilight and dawn active ants and 1.6 μm in nocturnal M. pyriformis. However, when all three species experienced 24 h of darkness, the pigment cells migrated away from the crystalline cone, expanding the aperture to over 5 μm in M. pyriformis. In contrast, there was no difference in the pupil diameter of the day active M. croslandi ants, which remained stable at 1.2 μm regardless of the light conditions. All three species that restricted their activity periods to times when light was low were capable of adapting their vision to bright light conditions, and Narendra says, ‘The properties of the compound eye do not restrict nocturnal ants to be active exclusively at night’.
Having confirmed that the ants’ vision was not responsible for their time-shifted lifestyles, the team investigated how the nocturnal ants control their sensitivity to bright light to find out whether the movement of the pupil pigment cells is triggered by the presence of light or the ants’ internal body clock. After exposing nocturnal M. pyriformis ants to light during the night and taking ants that had been kept in the dark during the day and exposing them to light, the team found that the ants can contract the pupil at any time of day, suggesting that pupil formation is controlled by light exposure. However, when the team exposed the ants to dark conditions during the day, the ants were unable to fully open the pupil, suggesting that the insect's body clock controls when the pupil aperture opens to some extent.