Physical gills prevent drowning of many wetland insects, spiders and plants

Abstract

Summary Insects, spiders and plants risk drowning in their wetland habitats. The slow diffusion of O2 can cause asphyxiation when underwater, as O2 supply cannot meet respiratory demands. Some animals and plants have found a common solution to the major challenge: how to breathe underwater with respiratory systems evolved for use in air? Hydrophobic surfaces on their bodies possess gas films that act as a ‘physical gill’ to collect O2 when underwater and thus sustain respiration. In aquatic insects, this feature/process has been termed ‘plastron respiration’. Here, we demonstrate the similarities in function between underwater respiration of insect (Aphelocheirus aestivalis) plastrons and gas films on leaves of wetland plants (Phalaris arundinacea) and also show the importance of these physical gills by the resulting changes upon their removal. The gas films provide an enlarged gas–water interface to enhance O2 uptake underwater that is above that if only spiracles (insects) or stomata (plants) provided the gas-phase contact with the water. Body-surface gas films contribute to the survival of many insects, spiders and plants in aquatic and flood-prone environments.

Physical gills in diving insects and spiders: theory and experiment

“…Thus the total pressure under the plastron is less than the atmospheric plus hydrostatic pressure. Physical gills of insects and spiders aligns well with observations of the 20min duration of underwater foraging of raft spiders, Dolomedes fimbriatus (Araneae, Pisauridae), which have similar abdominal air-films (Pedersen and Colmer, 2012).…”

“…They also occur among the Arachnida, including some true spiders (Araneae) and whip spiders (Amblypygi) that forage underwater or at least survive submersion (Hebets and Chapman, 2000;Pedersen and Colmer, 2012). However, the only completely aquatic spider is Argyroneta aquatica (Cybaeidae), which lives in a 'diving bell' made from a bubble of air held by an underwater web (Seymour and Hetz, 2011).…”

Metabolic recovery from drowning by insect pupae

“…1). In our experiments, O 2 levels in the surrounding water did not affect survival rates, indicating that pupae did not absorb O 2 across their cuticles or spiracles or exchange gases via cryptic cuticular air films (Pedersen and Colmer, 2012). Rather, immersed pupae accumulated high levels of lactate, indicating that they relied on anaerobic metabolism; we have no information on other possible anaerobic end products.…”

“…For the pupa, an underground lifestyle raises the risk of flooding. The pupal chamber does not exclude water and therefore does not act as a physical gill (see Kolesnikov et al, 2012;Seymour and Matthews, 2013; J. C. Sprague and H.A.W., unpublished observations), nor do pupae trap air films on the cuticle as do many semi-aquatic insects (Hutchinson, 1981;Pedersen and Colmer, 2012). In nature, the risk of flooding may be high for pupae because larval host plants often occur in disturbed areas, such as along stream beds.…”

Respiratory function of the plastron in the aquatic bug,Aphelocheirus aestivalis(Hemiptera, Aphelocheiridae)

“…Therefore, resting bugs could withstand P O2 levels in stagnant water at approximately half of air-saturation. Even if the insects find themselves in more severely O 2 -depleted stagnant water, they can survive by moving, either to reduce the boundary layer, to enter water near the surface with higher P O2 or to obtain O 2 from the surface of aquatic vegetation (Pedersen and Colmer, 2012). If O 2 becomes very low, A. aestivalis moves near the surface and can even voluntarily emerge from the water (Thorpe, 1950).…”