Origin and adaptive value of the DGC

Discontinuous gas exchange cycles have long been thought to represent a water-saving adaptation in insects (Chapter 4). The main reasons for this idea are that spiracles are kept closed for a portion of the DGC, thus reducing respiratory water loss to zero, and a largely convective F-period restricts outward movement of water (Kestler 1985; Lighton 1996). If the spiracles are artificially held open, water loss increases considerably (Loveridge 1968), and by calculation it can also be shown that a continuous O-period would lead to large increases in overall water loss (Lighton 1990; Lighton et al.1993a,b).

Indeed, the ideas that the DGC is an adaptation to conserve water, and that changes in various characteristics reflect additional selection for water economy permeate the modern literature (Siama and Coquillaud 1992; Lighton 1996; Duncan et al. 2002a). Clearly, an invaginated gas exchange surface does lead to a reduction in water loss (Kestler 1985). This can, perhaps, be seen most clearly in the pronounced trend in isopods towards an internalized lung system with spiracles in highly terrestrial species, from the original surface-borne lung system on the pleopodite exopods, which is found in species occupying moister habitats (Schmidt and Wagele 2001). However, whether the DGC itself and modifications thereof represent adaptations for restricting water loss is more controversial, although recent work has once again come out in favour of this idea (Chown and Davis 2003).

F-period gas exchange

One of the more controversial aspects of the water-saving (or hygric genesis) hypothesis for the origin and subsequent maintenance of the DGC is the nature of F-period gas exchange (Lighton 1996). If gas exchange is predominantly by convection, then the outward diffusion of water will be minimized and both a DGC, and increases in the duration of the F-period, will lead to enhanced water conservation (Kestler 1985). On the other hand, if gas exchange during the F-period takes place predominantly by diffusion, then there is unlikely to be any benefit to water economy in either possession of such a period, or regulation thereof. It is clear that at least in lepidopteran pupae (Brockway and Schneiderman 1967), the ant C. bicolor (Lighton et al. 1993a), and P. americana (Kestler 1985), the F-period is characterized by largely convective gas exchange. However, diffusion seems to predominate in the tenebrionid beetle P. striatus (Lighton 1988b) and in C. vicinus (Hy-menoptera, Formicidae).

In experiments to determine the nature of gas exchange in the latter species, Lighton and Garrigan (1995) manipulated external oxygen concentrations to investigate the nature of F-period gas exchange, and made several predictions. Because ambient oxygen concentration determines the amount of oxygen available at the start of the C-period, a reduction in ambient oxygen concentration should result in a decline in C-period duration. Declining ambient oxygen concentrations should also prevent the generation of a substantial negative endo-tracheal pressure. Thus, if F-period gas exchange is predominantly by convection, F-period duration should decline owing to reduced gas exchange capabilities due to the lower Ap (equation 2). Alternatively, if F-period gas exchange is dominated by diffusion, then metabolic requirements during declining ambient oxygen concentrations could be met by increasing spiracular opening (the area term in equation 1). If this is done, the time taken to reach the hypercapnic setpoint that usually triggers O-period spiracular opening will increase, resulting in an increase in F-period duration. In C. vicinus, F-period increased with declining oxygen concentration suggesting that gas exchange takes place mostly by diffusion (it cannot be solely by diffusion— see Kestler 1985). By contrast, in H. cecropia, declining external pO2 results in a reduction in F-period duration (Schneiderman 1960), as might be expected from a species in which changes in endotracheal pressure in the direction predicted by convective gas exchange take place (Brockway and Schneiderman 1967). A similar response to declining external pO2 was found in the dung beetle Aphodius fossor (Fig. 3.13), suggesting that in this species the F-phase is also predominantly convective (Chown and Holter 2000).

Based on the partial pressure gradients for both CO2 and O2, it has also been suggested that respiratory exchange ratios should be in the region of 0.2 during the F-period if gas exchange takes place primarily by diffusion. Calculated F-period RERs are not significantly different from this value in P. striatus (Lighton 1988b), and in C. vicinus (Lighton and Garrigan 1995), which has led Lighton (1996) to conclude that diffusion is the predominant form of gas exchange during the F-period in many insect species. However, RERs can be notoriously difficult to calculate owing to limitations of flow-through oxygen analysers (Kestler 1985).

Because only a small number of species have been investigated it is not possible to determine whether diffusion or convection is the predominant form of F-period gas exchange in insects. Moreover,

Figure 3.13 Gas exchange in the dung beetle Aphodius fossor showing a decline in F-period duration with declining ambient pO2, and the absence of a C-period at the lowest oxygen concentrations. Source: Chown and Holter (2000).

Figure 3.13 Gas exchange in the dung beetle Aphodius fossor showing a decline in F-period duration with declining ambient pO2, and the absence of a C-period at the lowest oxygen concentrations. Source: Chown and Holter (2000).

in at least some species of desert-dwelling tenebrionid beetles the F-period has been modified such that gas exchange is reduced to a number of small bursts which are accompanied, at least in some species, by ventilatory movements, suggesting that the F-period might be modified in several other ways (Lighton 1991a; Duncan et al. 2002a). In addition, in C. bicolor, there is temporal partitioning of the F-period such that F-period gas exchange initially takes place via the small, abdominal spiracles and then via the larger thoracic spiracles. Lighton et al. (1993a) suggested that the limited diffusive capability of the abdominal spiracles might assist water retention during the initial part of the F-period when the pressure gradient is large, but that as this pressure gradient diminishes the larger thoracic spiracles supply O2 via diffusion owing to their larger cross-sectional area (see also Byrne and Duncan 2003). Therefore, a definitive conclusion regarding the role of the F-phase in water economy and the likely adaptive nature of the DGC from this perspective cannot be provided for the insects as a whole.

Alternative hypotheses

It is not only the nature of F-period gas exchange that has raised doubts regarding the contribution of the DGC to water balance in insects (see Chapter 4). The small contribution of respiratory transpiration to total water loss has also raised doubts about the extent to which modulation of gas exchange patterns might affect water balance (see

Hadley and Quinlan 1993; Shelton and Appel 2001a, and review in Chown 2002). Moreover, many insects seem to abandon the DGC just when water economy is required most—when desiccated or at high temperatures (Hadley and Quinlan 1993; Chappell and Rogowitz 2000), presumably because haemolymph buffering of CO2 cannot take place (Lighton 1998). For example, worker ants, which spend much time above ground exposed to hot, dry conditions, should show DGCs, whereas female alates, which spend the larger part of their lives underground in a humid environment should not. In Messor harvester ants exactly the opposite pattern is found, and this has lead Lighton and Berrigan (1995) to propose the chthonic (= underworld) genesis hypothesis for the origin of the DGC. They argued that female alates are likely to spend much time in environments that are profoundly hypoxic and hypercapnic, especially during their claustral phase when the burrow entrance is sealed. Under these conditions, in insects that rely predominantly on diffusion (as ants apparently do), gas exchange can be promoted either by increasing the area term (spiracular opening) or by increasing the partial pressure difference between the endotracheal space and the environment (equation 1). Opening the spiracles fully, as would be required in the former case, would result in elevated water loss, and presumably fairly rapid dehydration unless the surrounding air were completely saturated. However, alteration of the partial pressure gradients would not incur a water loss penalty, but would require that endotracheal gas concentrations are significantly hypoxic and hypercapnic relative to the environment. One way of ensuring this is would be to adopt discontinuous gas exchange, during which pCO2 is enhanced and pO2 depleted relative to the environment. In worker ants, this extreme form of gas exchange, which carries penalties in terms of internal homeostasis, would not be required because of the large amount of time they spend above ground (Lighton and Berrigan 1995).

Based on a qualitative review of gas exchange patterns in various species, Lighton (1996, 1998) has suggested that the chthonic genesis hypothesis better explains the absence of the DGC in some species (largely above-ground dwellers) and its presence in others (psammophilous and subterranean species), and is therefore more likely an explanation for the origin of this gas exchange pattern than the pure hygric genesis hypothesis. Since then, two direct tests of this hypothesis have been undertaken. In the first, it was found that the dung beetle A. fossor, which encounters profoundly hypoxic and hypercapnic environmental conditions in wet dung (Holter 1991), abandons the DGC as conditions become more hypoxic (Chown and Holter 2000) (Fig. 3.13). This suggests that DGCs, which are highly characteristic of the species at rest, do not serve to enhance gas exchange under hypoxic and hypercapnic conditions. Rather, under hypoxic conditions, this species increases spiracular conductance to meet its largely unchanging metabolic requirements, which is unlikely to carry a biologically significant water loss penalty because cuticular transpiration in this species is high and because it lives in a habitat where water is plentiful. In the second test, Gibbs and Johnson (2004) found that in the harvester ant Pogonomyrmex barbatus, which shows several different gas exchange patterns, the molar ratio of water loss to CO2 excretion does not vary with gas exchange pattern. Therefore, they concluded that the DGC does not serve to improve gas exchange while reducing water loss. Several other authors have argued that the chthonic genesis hypothesis cannot explain the origin and maintenance of the DGC, based mostly on the grounds of habitat selection and the presence or absence of DGCs in the species they have investigated (Vogt and Appel 1999; Duncan et al. 2002a). In particular, Duncan et al. (2002a) pointed out that subsurface conditions in sand are unlikely to become severely hypoxic and hypercapnic (Louw et al. 1986), highlighting the need for additional information on environmental gas concentrations (Section 3.2.2).

A second, alternative adaptive explanation for the origin of the DGC is the oxidative damage hypothesis proposed by Bradley (2000). He suggested that because oxygen is toxic to cells, DGCs might serve to reduce the supply to cells when metabolic demand is low. Although this is an interesting alternative hypothesis, it does not explain the absence of DGCs in many insects, nor does it account for the fact that oxidative damage might be limited more readily by alteration of fluid levels in the tracheoles (Kestler 1985).

In contrast to the three adaptive hypotheses (hygric genesis, chthonic genesis, oxidative damage), Chown and Holter (2000) proposed that DGCs are not adaptive at all. They suggested that the cycles might arise as an inherent consequence of interactions between the neuronal systems that control spiracular opening and ventilation (see also Miller 1973). Under conditions of minimal demand, interacting feedback systems can show a variety of behaviours ranging from a single steady-state to ordered cyclic behaviour (May 1986; Kaufman 1993), and the periodic nature of several physiological phenomena is thought to be the consequence of such interactions (Glass and Mackey 1988). In the case of cyclical gas exchange patterns there are several reasons for considering this to be likely. First, the isolated CNS is capable of producing rhythms very similar to those of the DGC (Bustami and Hustert 2000; Bustami et al. 2002), and is characterized by neuronal feedback (Ramirez and Pearson 1989). Second, changes in pO2 have a marked influence on CO2 setpoints and vice versa, suggesting that considerable interaction is characteristic of the system (Levy and Schneiderman 1966a; Burkett and Schneiderman 1974). Third, although much of the recent literature suggests that DGCs are rather invariant in the species that have them, there is much evidence showing that gas exchange patterns vary considerably within species and within individuals (Miller 1973, 1981;

Lighton 1998; Chown 2001; Marais and Chown 2003; Gibbs and Johnson 2004). The latter is reminiscent of the kinds of variability characteristic of interacting feedback systems.

A consensus view?

By the mid-1970s the DGC story appeared to have been told: the cycles are characteristic especially of diapausing pupae in which there is likely to have been strong selection for reductions in water loss, resulting in a water-saving convective F-period and a C-period when the spiracles are entirely closed. Thirty years later, the situation is less clear. DGCs are characteristic of many adult and pupal insects (living in a variety of environments), show considerable variability, and are sometimes abandoned just when they seem to be needed most. None of the alternative adaptive hypotheses proposed to explain the origin and maintenance of the DGC appear to enjoy unequivocal support either, and recent work has once again highlighted the fact that metabolic rate and DGC patterns (specifically O-period and F-period durations) can be modulated to save water (Chown and Davis 2003). Moreover, it has also recently been suggested that DGCs might represent convergent patterns that have evolved along two entirely different routes. That is, DGCs might include CFO and CFV patterns of the kind that we have been most concerned with, but might also have convergently arisen from intermittent-convective gas exchange (Lighton 1998). Although there is little evidence for this idea, it does highlight the fact that similar patterns may not necessarily be the consequence of identical mechanisms.

The likely independent evolution of DGCs several times within the arthropods lends additional support to this idea. Discontinuous gas exchange cycles are also found in soliphuges (Lighton and Fielden 1996), ticks (Lighton et al. 1993c), pseudoscorpions (Lighton and Joos 2002) and centipedes (Klok et al. 2002), (but not in mites (Lighton and Duncan 1995) or harvestmen (Lighton 2002)) and have probably evolved independently at least four times in the arthropods (Fig. 3.3). Moreover, it appears that in pseudoscorpions (or at least the one that has been investigated) the O-period is triggered by hypoxia rather than by hypercapnia as is the case in the insects that have been investigated to date. Thus, there might be considerable variation in both the origins of and mechanisms underlying DGCs in arthropods, and given the patchy distribution of DGCs and their considerable variety among the insects, it seems likely that in this group they have also evolved independently several times.

Whether natural selection has been responsible for this evolution is a more difficult question to resolve. Arguably, there is a variety of circumstances that could impose selection for discontinuous gas exchange. These include drought, hypoxia, hypercapnia, and perhaps also the need for insects to reduce metabolic rates during dormancy (Lighton 1998), especially in long-lived adults that have to cope with unpredictably unfavourable environments (Chown 2002). In addition, these circumstances are probably not important in active insects that have ready access to food and water, and which can generally tolerate starvation and desiccation for periods that are much longer than those routinely encountered during the peak activity season (Chapter 4). Thus, the various environmental factors that promote the DGC are most likely to be important during dormancy, and probably also act in concert to promote both DGCs and low metabolic rates (to overcome the threat of starvation), making it difficult to distinguish between the major adaptive hypotheses solely by using experimental manipulations. One solution to this problem might be to combine experimental work with broad comparative studies within a strong inference framework (Huey et al. 1999). Another is to examine more broadly the extent to which variation in the DGC is partitioned within and among individuals. At the moment it appears that even in highly variable species most of the variation in the DGC and its characteristics is partitioned among individuals, and much less within individuals, so providing natural selection with much to work on (Marais and Chown 2003). If this is the case in most species then the adaptive hypotheses will be much more difficult to dismiss (Chown 2001), particularly because metabolic characteristics also respond to selection (Gibbs 1999).

Thus, it would seem prudent to conclude, based on the evidence of the current literature, that DGCs have evolved as adaptations to cope with unfavourable environmental conditions, and particularly limited water availability. However, the alternative, non-adaptive hypothesis—that cyclic gas exchange is a basal characteristic of all arthropods that have occludible spiracles, which results from interactions between the regulatory systems responsible for spiracular control and ventilation— has not been sufficiently well explored for it to be rejected. Indeed, cyclic gas exchange may well have had a non-adaptive origin, but subsequently found itself pressed into other forms of service.

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