Gas exchange via the tracheae
The general morphology and functioning of the tracheal system and the spiracles has long been known and has now been well described for many species (Snodgrass 1935; Miller 1974; Nation 1985). Typically, gas exchange is thought to proceed as follows. Oxygen moves along a pathway from the spiracles through the main tracheal tubes (via convection or diffusion—see Section 3.3.2) to the tracheoles where it diffuses to the mitochondria (Buck 1962; Kestler 1985). Diffusion from the large tracheae to the surrounding tissues or haemo-lymph is thought to be negligible because of the small partial pressure difference (ApO2) between the tracheal lumen and the surrounding tissues compared to the ApO2 between the metabolically active tissues and the tracheoles. Carbon dioxide does not follow the same route in the opposite direction. Rather, it is thought to enter the tracheal system at all points from the tissues and haemolymph where it is buffered as bicarbonate (Bridges and Scheid 1982). One of the reasons for the difference in routes followed by O2 and CO2 might be the much larger Krogh's constant (K) for CO2 than O2 in water, and the somewhat lower K in air for CO2 than O2 (Kestler 1985).
Stereological morphometrics of the entire tracheal system of Carausius morosus (Phasmatodea, Lonchodidae) have both confirmed and modified this paradigm (Schmitz and Perry 1999). These methods, which have now been applied to several arthropod groups (Schmitz and Perry 2001, 2002), allow systematic examinations of wall thickness and tracheal surface area of the entire tracheal system. Moreover, they also enable the whole tracheal volume, the volumes of different tracheal classes and the volumes of other organs to be determined (Schmitz and Perry 1999). In C. morosus, class I tracheae (or the tracheoles) account for 70 per cent of the oxygen diffusing capacity of the system, while larger classes II and III tubes account, respectively, for 17 and 7 per cent of this capacity, and may thus be important for gas exchange. Diffusion through larger tracheae could therefore be an effective way of providing all tissues with O2, especially following spiracular closure, although this clearly depends on metabolic demand (ApO2) (Schmitz and Perry 1999). The morphometric analyses also showed that the lateral diffusing capacity for the tracheal walls is much higher for CO2 than for O2. Thus, tracheal classes I and II contribute 85 per cent to diffusing capacity, and classes III and IV the remaining 15 per cent, indicating that the entire tracheal system plays a large role in the elimination of CO2.
Recently, it has also become clear that gas exchange does not take place only via direct dif fusion from the gaseous phase in the tracheal and tracheolar lumen to the tissues and mitochondria. Although the aeriferous tracheae, which serve organs such as the ovaries in Calliphora blowflies and other insects, have been known for some time, Locke (1998) has recently demonstrated that an entirely different oxygen delivery system is used for the haemocytes. These cells are the only insect tissues that are not tracheated, and their tolerance of anoxia has led to the assumption that they either obtain oxygen from the haemolymph or live under anoxic conditions. In contrast, Locke (1998) has shown that in the larvae of Calpodes ethlius (Lepidoptera, Hesperiidae) some tracheae leading away from the spiracles of the 8th segment form profusely branching tufts suspended in the haemo-lymph, and also have branches extending to the tokus compartment at the tip of the abdomen (Fig. 3.4). Not only are haemocytes abundant among the tufts, but also anoxia causes an increase in the number of circulating haemocytes, with many moving to the tufts themselves. Moreover, haemocytes among the tufts in anoxic larvae show none of the signs of anoxic stress typical of haemocytes distributed elsewhere throughout the body. A similar situation is found in the tokus compartment, where haemocytes attach themselves to the basal lamina of the tracheae. The tracheal
Source: Reprinted from Journal of Insect Physiology, 44, Locke, 1-20, © 1998, with permission from Elsevier.
tufts (or aerating tracheae) and tokus compartment, therefore, form a lung for haemocytes in this caterpillar, and a similar arrangement has been found in several other species from a variety of lepidopteran families (Locke 1998).
Owing to the presence of the tracheal system, it has also been assumed that, with a few well known exceptions (Chironomus (Diptera, Chironomidae) and Gasterophilus (Diptera, Gasterophilidae) larvae, and adult Notonectidae (Hemiptera) in the genera Anisops and Buenoa), respiratory pigments (specifically haemoglobin, Hb) are absent in insects (Weber and Vinogradov 2001; Nation 2002). However, Burmester and Hankeln (1999) recently identified the presence and expression of a haemoglobin-like gene in D. melanogaster by comparing Chironomus globin protein sequences with anonymous cDNA sequences of the former species. Further investigation revealed a haemoglobin similar to that of other insect globins in terms of its ligand binding properties and expression patterns (Hankeln et al. 2002). As is the case in other insects with more pronounced Hb expression (Weber and Vinogradov 2001), the Drosophila Hb is synthesized in the fat body and tracheal system. Similarity between the oxygen affinity and tissue distribution of the Drosophila Hb and those in other insects suggests that its role is the transport and storage of oxygen even under normoxic conditions. Hb in the tracheoles might facilitate the movement of oxygen from the tracheolar space into the tissues, and might be associated with storage of oxygen in the fat body surrounding metabolically active tissues such as the brain (Hankeln et al. 2002). Haemoglobin may also function to enhance tolerance of anoxia or might serve as an oxygen sensor involved in the regulation of tracheal growth. In the latter case, Hb could serve as a source of oxygen for nitric oxide synthase needed for nitric oxide synthesis, which is in turn involved in a signalling pathway that is thought to stimulate tracheal growth under hypoxia (Wingrove and O'Farrell 1999). Alternatively, it might also be involved in oxygen signalling of tracheal growth via the Branchless Fibroblast Growth Factor (Jarecki et al. 1999). Whatever the actual role of Drosophila Hb, its discovery suggests that oxygen supply in insects is likely to be more complex than previously thought, and may depend on some form of haemoglobin-mediation or storage. Nonetheless, the restriction of Hb to the tracheoles and terminal cells of the tracheal system, and to fat body cells, suggests that the supply of oxygen to the tissues is still largely fulfilled by the tracheae. Recently, a haemocyanin has been found in the stonefly Perla marginata (Hagner-Holler et al. 2004).
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