Discontinuous gas exchange cycles

Discontinuous gas exchange cycles (DGCs) are one of the most striking gas exchange patterns shown by insects. Discontinuous gas exchange was originally described in adult insects (Punt et al. 1957; Wilkins 1960), but it was the investigation of DGCs in diapausing saturniid pupae by Schneiderman and his colleagues (e.g. Schneiderman 1960; Levy and Schneiderman 1966a,b; Schneiderman and

Schechter 1966) that resulted in a comprehensive understanding both of the pattern and the mechanisms underlying it. Subsequently, discontinuous gas exchange has been documented in a wide variety of both adult and pupal insects, although the patterns and control thereof show considerable variation among species. To date, discontinuous gas exchange has been found in cockroaches (Kestler 1985; Marais and Chown 2003), grasshoppers (Harrison 1997; Rourke 2000), hemipterans (Punt 1950), beetles of several families (Lighton 1991a; Davis et al. 1999; Bosch et al. 2000; Chappell and Rogowitz 2000), lepidopterans (Levy and Schneiderman 1966b), robber flies (Lighton 1998), wasps (Lighton 1998), and ants (Lighton 1996; Vogt and Appel 2000). Similar patterns have been found in a variety of other insects including thy-sanurans, termites (Shelton and Appel 2001a,b) and Drosophila (Williams et al. 1997), but these patterns are not considered DGCs because they deviate somewhat from the standard, three-period cycles. Nonetheless, the considerable variation that is characteristic of DGCs means that the distinction between this gas exchange pattern and other forms of cyclic gas exchange is often difficult to make. Moreover, convergence in pattern does not necessarily mean that the same underlying mechanism is responsible for it (Lighton 1998; Lighton and Joos 2002).

Discontinuous gas exchange cycles have variously been referred to as discontinuous ventilation, discontinuous ventilatory cycles, and discontinuous respiration. Obviously, cellular respiration is not discontinuous, making that title inappropriate. Likewise, gas exchange is not always by ventilation, making that term inappropriate as a general descriptor too. In consequence, discontinuous gas exchange remains the most appropriate broad descriptive name for the gas exchange pattern described below, and if the pattern is repeated then the outcome can be referred to as 'discontinuous gas cycles'. Discontinuous gas exchange cycles are characterized by the repetition of three major periods, during which the exchange of CO2 and O2 is partially separated (Fig. 3.10). In terms of spiracular behaviour, these periods are an open (O) period when the spiracles are fully open, a closed (C) period during which the spiracles are tightly shut, and a

Gaseous Exchange Cycle

Time (min)

Figure 3.10 Discontinuous gas exchange in Psammodes striatus (Coleoptera, Tenebrionidae), indicating the Closed (C), Flutter (F), and Open (O) periods.

Note: Oxygen (thin line) and carbon dioxide (thick line) are partially separated in time.

Source: Reprinted from Journal of Insect Physiology, 34, Lighton, 361-367, © 1988, with permission from Elsevier.

Time (min)

Figure 3.10 Discontinuous gas exchange in Psammodes striatus (Coleoptera, Tenebrionidae), indicating the Closed (C), Flutter (F), and Open (O) periods.

Note: Oxygen (thin line) and carbon dioxide (thick line) are partially separated in time.

Source: Reprinted from Journal of Insect Physiology, 34, Lighton, 361-367, © 1988, with permission from Elsevier.

flutter (F) period during which the spiracles open and shut by means of reduced fluttering movements. Although this spiracular behaviour has been confirmed for both lepidopteran pupae (Schneiderman 1960), and adult ants (Lighton et al. 1993a), it is generally assumed to be characteristic of other insects showing DGCs on the basis of the gas exchange (especially CO2 output) trace recorded during an investigation. Likewise, the majority of the work on the control of the DGC has been conducted on lepidopteran (usually saturniid) pupae, and mostly assumed to apply more generally to adult insects. However, there is considerable variation in control of the DGC, and it cannot be assumed that it is necessarily the same across all insects, irrespective of the taxon or stage (Harrison et al. 1995). Nonetheless, the patterns and control mechanisms are sufficiently similar in those insect species that have been investigated for them to be dealt with as a whole here.

During the closed period, no gas exchange takes place through the tightly shut spiracles. Oxygen in the endotracheal space is depleted by respiration, but CO2 is buffered in the haemolymph, leading to a slow decline in endotracheal pressure, and to a steady decline in pO2, to c.5 kPa. A CNS-mediated O2 setpoint (see Section 3.4.1) then causes the spiracles to partially open and close in rapid succession, and the flutter period is initiated. At least in saturniid pupae, P. americana, and the ant C. bicolor, the negative endotracheal pressure is responsible for convective movement of air into the tracheae (Levy and Schneiderman 1966c; Kestler 1985; Lighton et al. 1993a), and this exchange of gases by means of inward convection has been termed passive suction ventilation (Miller 1974). Convective gas transport restricts outward movement of both CO2 and H2O and is thought to be one of the major ways in which the DGC is responsible for water conservation. However, in some species of ants and probably in the tenebrionid beetle Psammodes striatus, it appears that gas exchange during the F-period is primarily by means of diffusion (Lighton 1988b; Lighton and Garrigan 1995), thus reducing its water saving potential (see below).

During the F-period in saturniid pupae, endo-tracheal pressure increases rapidly towards ambient in a series of steps caused by spiracular opening and closing. During the open periods, gas exchange takes place predominantly by diffusion, whereas when the spiracles are more constricted convective gas exchange predominates (Levy and Schneiderman 1966b,c; Brockway and Schneiderman 1967, see also Lighton 1988b). According to Brockway and Schneiderman (1967) spiracle filters in saturniid pupae impede inward air flow and prolong the period during which convective gas exchange takes place, thus enhancing water conservation. A similar role has been ascribed to sieve plates in scarab beetles (Duncan and Byrne 2002), although these plates might also serve to exclude parasites which can have a substantial effect on performance (Brockway and Schneiderman 1967; Miller 1974; Harrison et al. 2001). In saturniid pupae, when endotracheal pressure reaches ambient values, the F-period continues, with microcycles of decreasing and increasing pressure associated with spiracular fluttering. During this time, pO2 remains at c.5 kPa and the partial pressure gradient is sufficient to ensure that tissue oxygen demand is met. In both P. americana and P. striatus, oxygen uptake during the F-period is modulated to match cellular demand. Although the F-period in saturniid pupae comprises two readily distinguishable parts, this division is not discernible in P. americana (Kestler 1985), and has not been sought in other species.

Carbon dioxide continues to accumulate during the F-period until pCO2 reaches an endotracheal value of approximately 3-6 kPa, depending on the species (Brockway and Schneiderman 1967; Burkett and Schneiderman 1974; Harrison et al. 1995; Lighton 1996). At this partial pressure, CO2 affects the spiracles both directly and indirectly (see Section 3.4.1), causing them to open widely, with concomitant egress of CO2 and H2O, and ingress of oxygen. During this O-period, gas exchange may take place either predominantly by diffusion (Levy and Schneiderman 1966a; Lighton 1994) or by ventilation as a consequence of active ventilatory movements (Lighton 1988b; Lighton and Lovegrove 1990; Harrison 1997). In P. americana, both forms of gas exchange can occur in the O-period, and Kestler (1985) referred to the former as CFO type and the latter as CFV type. Over the course of the O-period, pO2 increases to approximately 18 kPa, and pCO2 declines to initial values (approximately 3 kPa in saturniid pupae). In some species, such as ants and trogid beetles, the spiracles close shortly after pCO2 has declined to initial values, so producing a single spike representing the O-period (Fig. 3.7). However, in lepidopteran pupae (Brockway and Schneiderman 1967; Hetz et al. 1999), and in scarab and carabid beetles (Davis et al. 1999; Duncan and Byrne 2000; Duncan and Dickman 2001), the O-period is characterized by an initial rapid release of CO2 and then by several smaller bursts owing to repeated opening and restriction of the spiracles. These smaller bursts decline in amplitude until there is total constriction of the spiracles (Fig. 3.11), and in the beetle species these bursts are accompanied by abdominal pumping. It has been suggested that this alternative opening and closing of the spiracles during the O-period might be a mechanism to reduce water loss (Duncan and Byrne 2000; Duncan and Dickman 2001), although evidence for this idea is wanting. It also appears likely that in at least some cases these patterns might be a consequence of washout associated with slow flow rates in the experimental system (see Bartholomew et al. 1981; Lighton 1991b), although this is unlikely to account entirely for them.

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