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UBC Theses and Dissertations

On the respiratory consequences of the air-to-water transition in insects Lee, Daniel Jingyu

Abstract

Numerous terrestrial insect lineages have independently adapted to an aquatic existence to live and breathe underwater. Despite their success, these groups retained the same air-filled tracheal system used by their terrestrial ancestors. While the continued reliance on internal air to transport gases has numerous advantages, it also creates challenges that may hinder the insects' ability to thrive in water. This thesis investigates two potential consequences: reduced gas exchange efficiency in the tidally-ventilating dragonfly nymphs, and the tracheal system's susceptibility to pressure-induced failure. Testing the response of dragonfly nymphs to progressive hypoxia in Chapters 2 and 3 shows that they increase gill ventilation frequency while maintaining a constant metabolic rate. Calculating their oxygen (O₂) extraction efficiency (OEE) shows that it, while lower than that of unidirectional-breathers, is maintained even in severe hypoxia. Mathematical models indicate that this constant OEE cannot be explained solely by increased ventilation, and further experiments show that while the diffusion gradient is maintained in mild hypoxia due to a significant reduction in hemolymph PO₂, it steadily falls in severe hypoxia. Dragonfly nymphs compensate for this reduced gradient by increasing gill O₂ conductance, showing they employ both convective and diffusive methods to maintain O₂ uptake. Exposing water-breathing insects to increasing hydrostatic pressures in Chapter 4 shows that their tracheal systems collapse at depth and is associated with significant reductions in tracheal air volume. However, this tracheal collapse induced mortality only in mayflies and not in dragonflies and damselflies, potentially reflecting differences in their ability to ameliorate or tolerate the consequences of reduced tracheal gas transport. Comparing the tracheal wall morphology of the above insects with those of terrestrial species suggests that the former are thicker, likely as a consequence of living in an environment with higher external pressures. Overall, these findings indicate that the adaptation of the air-filled tracheal system in water-breathing insects is not perfect; while they are capable of extracting O₂ in hypoxia, they must also constantly contend with the risk of pressure-induced failure. Collectively, this thesis provides the starting point to a better understanding of how well insects have evolved to become secondary water-breathers.

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