Mechanisms of sustaining oxygen extraction efficiency in dragonfly nymphs during aquatic hypoxia

Abstract

Despite breathing water using their tidally ventilated rectal gills, dragonfly nymphs show a surprising ability to maintain oxygen (O2) extraction from the water during hypoxia. However, an increase in convective O2 transfer is insufficient to sustain aerobic demands by itself, which suggests that diffusive mechanisms must also be involved. This study examines the contributions of changing the O2 partial pressure gradient (PO2) and/or O2 conductance across the rectal gill in maintaining O2 extraction efficiency (OEE) of dragonfly nymphs during hypoxia. Data were collected using the same custom-designed respiro-spirometer described in a previous study with the addition of an implanted O2 sensor to measure hemolymph PO2. Results show that the implantation of the O2 sensor does not affect the respiratory and ventilatory response of nymphs to hypoxia. Hemolymph PO2 fell from 6.3 {+/-} 1.6 kPa at normoxia to 2.5 {+/-} 0.6 kPa at 16.0 kPa, which resulted in the PO2 diffusion gradient remaining statistically constant at these two water PO2s (17.5 {+/-} 1.7 and 15.4 {+/-} 0.7 kPa during normoxia and 16.0 kPa respectively). Beyond 16.0 kPa, a progressive reduction in hemolymph PO2 was unable to sustain the diffusion gradient. Mathematical modeling revealed that while the addition of hemolymph PO2 in tandem with ventilation frequency was able to elevate OEE during 16.0 kPa to that of normoxia, both were still insufficient during severe hypoxia and required an increase in O2 conductance. Estimating the change in whole-gill conductance showed that nymphs are indeed increasing their conductance as the water becomes hypoxic, demonstrating a reliance on both diffusion gradient and O2 conductance to enhance diffusive O2 transfer in conjunction with convective mechanisms to maintain O2 extraction during hypoxia.