Manduca larvae survive drowning

Abstract

Dragonfly larvae are perfectly equipped for a life of total immersion in their pond homes prior to emergence for their final metamorphosis. However, other species may be less well prepared for soggy starts in life. Art Woods from the University of Montana, USA, explains that although the larvae and pupae of other insects spend some portion of their lives buried in dry soil, their conditions can change rapidly when the weather turns. Whether it's the onset of the monsoon or a rapid thaw, dry soil in river beds and desiccated flood plains can flood quickly, submerging larvae as the soil saturates. ‘Anoxia can be highly stressful, even in highly anoxia-tolerant individuals’, says Woods, who was intrigued by how well Manduca sexta moth pupae survive drowning.Graduate student Steven Lane submerged pupae for up to a fortnight and plucked the insects from the water on alternate days (from day 1 to 13) to find out whether they survived and, if so, how long it took them to recover from total immersion. Impressively, all of the pupae that were removed from the water after submersion for 5 days survived; however, the partially drowned pupae took 7 days longer to emerge as adults than pupae that had remained dry, and extending the immersion by 2 days proved fatal. ‘Survival times of pupal M. sexta in immersion (anoxia) are impressive but not unprecedented’, says Woods, adding that other species that suffer flooding are capable of surviving similar periods. And when Lane measured the amount of lactic acid produced by the submerged insects, the pupae that had been submerged for longest had the largest amount and it took 2 days to dissipate; the insects had switched from aerobic to anaerobic respiration while submerged.Recording the pupae's respiration patterns as they recovered, it was clear to Lane that they initially opened their spiracles for an extended period to release large amounts of CO2. However, once the CO2 levels had fallen sufficiently, individual spiracles began to close, possibly because the pH of the body tissues had increased as the CO2 seeped out. And then the CO2 emission pattern switched again, rising and falling every 0.8–2.2 min, suggesting either that the pupa was opening and closing its spiracles rapidly or that the insect was pumping its abdomen while holding its spiracles open to expel the accumulated CO2. It was also clear that the recovering insect's metabolic rate was 50–75% higher than that of pupae that had not been submerged. As the spiracle opening patterns that produce intermittent breathing patterns in insects in other circumstances are regulated by the interplay between CO2 and O2 levels in the spiracles and adjacent tissues, Woods explains that only one scenario – where spiracle opening and closing are triggered by the acidity of the surrounding tissue – seemed likely to produce the conditions that could trigger some, but not all, aspects of the recovering pupae's unusual high-frequency breathing pattern.So, the pupae of species that occasionally suffer flooding and are at risk of drowning are capable of recovering after several days of submersion, and Woods says, ‘Pupae of Manduca would make a good model system for further studies linking immersion, anoxia tolerance and the mechanisms underlying patterns of gas exchange in insects’.