Compressible gas gills of diving insects: Measurements and models

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Abstract

Many diving insects collect a bubble of air from the surface to supply their oxygen requirements while submerged. It has been theorised that these air bubbles may also act as compressible gas gills, as the low oxygen partial pressure (PO2) within the bubble caused by the insect's respiration creates a gradient capable of driving the diffusion of oxygen from the water into the bubble. Under these conditions nitrogen diffuses in the opposite direction, resulting in a situation where the volume of the bubble is continually shrinking while oxygen is obtained. This study measures changes in volume and PO2 within the gas gills held by a tethered water bug, Agraptocorixa eurynome. Both gill volume and PO2 drop rapidly at the beginning of a dive, but eventually the PO2 reaches an apparently stable level while volume continually declines at a slower rate. Active ventilation of the gill is crucial to maintaining oxygen uptake. These measurements are used to calculate oxygen flux into the gas gill and the oxygen consumption rate (V˙O2) of the bug. The effectiveness of a gas gill as a respiratory organ is also demonstrated by determining the critical PO2 of the water bug and comparing this with measured gas gill PO2 and calculated V˙O2.

Introduction

All terrestrial insects that have successfully colonised the aquatic environment have overcome the problem of adapting their air-filled respiratory system to function while submerged. Perhaps the simplest solution, used by many aquatic insects, is to continue to rely exclusively on atmospheric oxygen by using snorkels and siphons (Wigglesworth, 1972). At the other extreme, air-filled tracheal gills or an incompressible air bubble trapped beneath a dense layer of hydrophobic hairs (a plastron) can extract enough dissolved oxygen from the surrounding water to supply an insect's entire oxygen demand indefinitely (Kohnert et al., 2004, Thorpe and Crisp, 1947). But there is a middle ground occupied by many diving insects, especially bugs and beetles, which collect a bubble of air at the surface and hold it over their spiracles. The bubble not only supplies oxygen from itself, but also presents a gas exchange surface to the water, through which dissolved oxygen can enter the bubble. Because the volume of the bubble decreases due to removal of oxygen by the insect and diffusion of nitrogen into the water, this system is called a ‘compressible gas gill’.

The theory of compressible gas gill function was first established by Ege (1915). A bubble of atmospheric air containing oxygen, nitrogen and trace gases is held over the spiracles of an aquatic insect. When the air bubble is carried to depth during a dive, its total pressure, and therefore the partial pressures of nitrogen (PN2) and oxygen (PO2), increase due to the increase in hydrostatic pressure surrounding it. If the insect is in water equilibrated with atmospheric air, both oxygen and nitrogen now diffuse out of the bubble and into the water, down their respective partial pressure gradients. However, the insect's respiration simultaneously consumes the oxygen within the bubble, eventually causing its PO2 to drop below that in the surrounding water. Once this happens, the bubble becomes a gill, allowing the uptake of dissolved oxygen directly from the water. This effect extends the dive of the insect beyond that which would have been possible if only the initial oxygen content of the bubble were available. However, the decrease in PO2, together with the fact that CO2 from the insect quickly dissolves in the water, cause a complementary increase in PN2, as the sum of the partial pressures must remain equal to the atmospheric pressure plus the hydrostatic pressure. This results in continual shrinkage of the gas gill due to nitrogen loss and oxygen uptake, and the bubble eventually has to be renewed at the surface.

While there is evidence that bubbles of air can act as gills and so extend the dive duration of the insects that carry them (De Ruiter et al., 1951, Vlasblom, 1970), there is still debate over how the partial pressures of oxygen and nitrogen in the gas gill change during a dive, and whether different dive parameters alter the amount of oxygen obtained. The dispute centres on the conflicting models of Rahn and Paganelli (1968) and Chaui-Berlinck and Bicudo (1993), that describe gas exchange between a bubble held by a submerged insect and the surrounding water. Both models are based on Fick's first law, where the rate of diffusion (V˙) of a gas between a bubble and water is given byV˙=KAX(ΔP)where A is the surface area of the gill, X the thickness of a boundary layer of still water, ΔP the partial pressure difference of the gas across the boundary layer, and K is Krogh's diffusion constant for the gas in water. The same values for gas gill volume, surface area, metabolic rate and boundary layer thickness, obtained from the literature, are also common to both. Variations of these starting conditions are incorporated into the models which calculate, second by second, gas bubble PO2, PN2, PCO2 and the rates of O2 uptake and N2 loss. Thus both modelling approaches sought to draw conclusions about the effects of these parameters on dive time and ‘oxygen gain’ (i.e., the ratio of total oxygen consumed during a dive to the initial oxygen content of the gill).

The fundamental difference between the two models lies in their treatment of gill area (A). The inevitable outward diffusion of N2 causes a bubble's volume to decrease during a dive, and, depending on the bubble's geometry, this could potentially cause its surface area to decrease. Rahn and Paganelli (1968) numerically modelled two gas gills: one where the gill's surface area decreased with volume, and one where area remained constant but gill height decreased. Their decreasing area model shows a constantly dropping oxygen partial pressure, but the constant area model shows the development of stable oxygen and nitrogen partial pressures that persist for the duration of a dive, with both gases becoming exhausted simultaneously. Considering only the constant area model, they concluded that oxygen gain of a gas gill is dependent on the initial ratio of oxygen and nitrogen in the gill and their relative diffusivities, i.e., for every unit of nitrogen lost to the water a fixed amount of oxygen would be obtained, independent of metabolic rate, gill area, initial gas volume and boundary layer thickness. With this model, the oxygen gain was 8, that is, 7 times the amount of oxygen originally in the bubble diffused across the gas gill, thus lengthening the maximum dive time 8-fold.

Chaui-Berlinck and Bicudo (1993), on the other hand, considered a shrinking gill area to be unavoidable, and based their numerical model on this assumption. Their model predicted that during a dive, the PO2 in the gill would decrease constantly, because the shrinking area available for diffusion would always prevent equilibrium between the rate at which the insect's respiration consumed oxygen and the rate that the PO2 gradient would drive its uptake. Their model defined the end of a dive as occurring when either intolerable hypoxia (given as <2.7 kPa) was reached or the gas gill's volume was too small to guarantee positive buoyancy.

The behaviour of numerical models is necessarily determined by the values of the parameters used. However, Chaui-Berlinck et al. (2001) used an analytical model to evaluate the conclusions drawn from Rahn and Paganelli's (1968) constant area gill model. Through mathematical argument it was concluded that, even with a constant gill area, a fixed oxygen gain was an impossibility as “this would imply a PO2 inside the bubble different from the one occurring as a result of physical constraints of the gas exchange process” (Chaui-Berlinck et al., 2001).

While these papers are interesting from a theoretical point of view, they remain pure conjecture without experimental validation. To assess the applicability of gas gill models, this study directly measures changes in PO2 and volume occurring within the gas gills of water bugs. These data are then used to derive the rate of oxygen uptake (V˙O2) by the insect and the partitioning of oxygen uptake from the initial bubble and from the water, to calculate the oxygen gain of the gas gill. Furthermore, this study evaluates two parameters central to understanding gas gill function: the role of ventilatory movements in maintaining diffusion between the gill and surrounding water and the hypoxia tolerance of an active water bug.

Section snippets

Insects

Aquatic water boatmen (Agraptocorixa eurynome, Kirkaldy 1897) were collected from rivers and ponds around Adelaide during the winter and spring of 2005–2008. They were collected from the River Torrens, Nelumbo Pond at the Adelaide Botanic gardens, and ponds at the Waite Campus of the University of Adelaide. They were transported to the laboratory in plastic buckets containing water and organic debris and housed within a constant temperature (CT) room set to 20 °C and with a 12:12 h light:dark

Gas gill morphology

The mean ventral gill area of A. eurynome was 20.55 ± 1.17 mm2 and body width measured behind the head was 2.85 ± 0.10 mm (n = 10). These dimensions were regressed against their body mass. The equations describing these relationships are:A=403.82Mb+7.5482(R2=0.912)W=33.725Mb+1.7632(R2=0.935)where A is gill area (mm2), W is the ventral body width behind the head (mm) and Mb is body mass (g). These dimensions correlate significantly with mass (ANOVA p < 0.0001).

Changes in the surface of the gas gill

Discussion

These experiments demonstrate that an equilibrium state, characterised by a stable PO2 and steadily decreasing volume, can occur in the gas gill of a submerged insect (Fig. 5, Fig. 6). Like the constant gill area model of Rahn and Paganelli (1968), the gas composition within a submerged gas gill reaches this equilibrium condition following an initial transient drop in PO2. This pattern does not match the constant decline in gill PO2 predicted from decreasing gill area models (Chaui-Berlinck and

Conclusion

This study presents new data on the functioning of compressible gas gills, particularly in relation to the issue of oxygen gain. Models of gas gill function incorporating a stable gas gill surface area have variously concluded that oxygen gain is either fixed (Rahn and Paganelli, 1968) or a physical impossibility (Chaui-Berlinck et al., 2001). In the absence of empirical studies, these conflicting conclusions have remained untested. Here we show that the gas gills of water boatmen closely

Acknowledgements

This study was supported by an Australian Postgraduate Award and the Australian Research Council. We sincerely thank the two anonymous reviewers for their helpful comments and criticisms which greatly improved this paper.

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