Abstract
Despite the remarkable evolutionary success of insects at colonizing every conceivable terrestrial and aquatic habitat, only five Halobates (Heteroptera: Gerridae) species (~0.0001% of all known insect species) have succeeded at colonizing the open ocean – the largest biome on Earth. This remarkable evolutionary achievement likely required unique adaptations for them to survive and thrive in the challenging oceanic environment. For the first time, we explore the morphology and behavior of an open-ocean Halobates germanus and a related coastal species H. hayanus to understand mechanisms of these adaptations. We provide direct experimental evidence based on high-speed videos which reveal that Halobates exploit their specialized and self-groomed body hair to achieve extreme water repellence, which facilitates rapid skating and plastron respiration under water. Moreover, the grooming behavior and presence of cuticular wax aids in the maintenance of superhydrophobicity. Further, reductions of their body mass and size enable them to achieve impressive accelerations (~400 ms−2) and reaction times (~12 ms) to escape approaching predators or environmental threats and are crucial to their survival under harsh marine conditions. These findings might also inspire rational strategies for developing liquid-repellent surfaces for drag reduction, water desalination, and preventing bio-fouling.
Highlights
The proliferation of invertebrate taxa in the ocean during the Cambrian explosion eventually led to their colonization on land, where insects first appeared ~479 million years (Myr) ago[1] to eventually dominate various terrestrial ecosystems[2,3]
For Halobates, which is restricted to oceanic life, the structure and arrangement of the characteristic mushroom-shaped microtrichia seems to be crucial in the formation of a more efficient plastron as compared to the peg-like microtrichia of a related stream-dwelling Ventidius sp[18,19]
The body hair of Halobates can prevent the insect from wetting by mist or rain, which could eventually lead to accidental submersion, and facilitate a plastron that enables them to resist and emerge from accidental underwater submersion (Movie S5)[18,21,22]
Summary
The proliferation of invertebrate taxa in the ocean during the Cambrian explosion eventually led to their colonization on land, where insects first appeared ~479 million years (Myr) ago[1] to eventually dominate various terrestrial ecosystems[2,3]. Several of the adaptations required for Halobates to thrive in the ocean, such as feeding, prey capture[10,12,14], reproduction[15,16], dispersal[16] osmotic regulation[14] and protection from high UV10,17, have been described in other Gerridae species, the fundamental question of how Halobates could survive storms without drowning, the key adaptation that enabled them to colonize the open ocean[18], has remained largely unresolved It has been postulated more than four decades ago[18] that the critical adaptation enabling Halobates to live on the open ocean could be attributed to its special microtrichia body covering, detailed studies of their biomechanical attributes and self-cleaning behaviors have not received much attention. We demonstrate, using a broad range of approaches, how these adaptations confer extreme water-repellence to allow their remarkable agility at the sea-air interface, thereby allowing them to cope with ocean turbulence and to avoid predation by fish from below and seabirds from above
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