Anaerobic pathways and environmental hypoxia

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Insects generally do not have well developed anaerobic metabolic capabilities. Nonetheless, the majority of species show a remarkable ability to recover from either hypoxia or anoxia, and at least some taxa are capable of surviving, being active, and reproducing under conditions of profound hypoxia. While high altitude insects (such as those found in the high Himalayas) experience prolonged hypoxia and hypobaria, hypoxia or anoxia is also characteristic of several other environments. These include hypoxic water and anoxic mud in aquatic systems (Gade 1985), and hypoxic burrows, dung, carrion, and decomposing wood, and anoxic flooded and ice-covered ground in the terrestrial environment (Conradi-Larson and Somme 1973; Hoback and Stanley 2001). For example, larvae of Orthosoma brunneum (Coleoptera, Cerambycidae) inhabit wood where oxygen levels are as low as 2 per cent and CO2 levels reach 15 per cent (Paim and Beckel 1963). Moreover, adult females seek CO2 concentrations of 90 per cent in which to lay their eggs (Paim and Beckel 1964). Likewise, several species of insects (mostly beetles) that inhabit wet dung pats in Denmark encounter and can tolerate, over the short term, O2 levels as low as 1-2 per cent and CO2 levels as high as 25-30 per cent, although generally they seek out regions of the dung pats that have conditions closer to ambient levels (Holter 1991; Holter and Spangenberg 1997).

Functional anaerobiosis in insects, such as that induced by exhaustive activity, does not contribute substantially to the total energy budget, with lactate production accounting for as little as 7 per cent of total ATP production in grasshoppers (Harrison et al. 1991). By contrast, under conditions of environmental hypoxia or anoxia, anaerobic metabolism can be of considerable importance as a source of ATP. For example, under low oxygen conditions and after their haemoglobin O2 supply is exhausted, aquatic Chironomus midge larvae switch to anaerobic metabolism with glycogen as the primary substrate and ethanol as the end product (Gade 1985). Likewise, Chaoborus phantom midge larvae use anaerobic metabolism for energy production (primarily from malate with succinate and alanine as the end products) when they rest in anoxic mud during the day.

Most terrestrial insects are metabolic regulators. With declining pO2, oxygen consumption remains constant until a critical oxygen tension of about 5-10 kPa (generally lower in adults) (Loudon 1988). Thereafter, metabolic rate declines precipitously, and ATP levels are generally not defended while concentrations of ADP, AMP, and IMP increase (Hoback and Stanley 2001; Kolsch et al. 2002). At least some energy is made available via anaerobic metabolism with lactate and alanine forming the major end-products. In species that are regularly exposed to anoxia, such as the tiger beetle Cicindela togata, metabolism is rapidly downregulated and ATP levels are defended for at least 24 h. Thereafter anaerobic metabolism is responsible for energy provision (Hoback et al. 2000). Survival of long-term anoxia in the Arctic carabid beetle Pelophila borealis (Carabidae) is associated with metabolic downregulation and with provision of small amounts of energy via a lactate pathway (Conradi-Larson and Somme 1973).

Metabolic downregulation or arrest plays a major role in the response of insects to pronounced hypoxia, and downregulation of ion channel activity is thought to be an important component of the response allowing survival of low oxygen conditions. In Locusta migratoria (Orthoptera, Acrididae), anoxic conditions result in a reduction in outward K+ currents in neurons, and possibly also an inhibition of Na+ currents (Wu et al. 2002). Thus, ATP demand is reduced and membrane-

related changes that lead to cellular damage are presumably prevented (Zhou et al. 2001). These responses are in keeping with some of those found in vertebrates (Hochachka et al. 1996).

Short-term experiments indicating that insects can remain active and maintain virtually unchanged metabolic rates down to even fairly low pO2 levels (e.g. Holter and Spangenberg 1997) suggest that insects are largely unaffected by hypoxia. By contrast, longer-term rearing under hypoxic conditions reveals a rather different picture. Under these conditions, initial metabolic rate declines are often reversed (depending on pO2), and growth and development can take place. However, especially at low pO2, growth and development is reduced, leading to longer development times, to the addition of instars (in species where this is possible), and to a reduction in final body size (Fig. 3.1), especially if instar number is constrained (Loudon 1988; Frazier et al. 2001; Zhou et al. 2001). Reductions in body size often have a direct effect on fecundity, whereas increases in larval duration expose animals to greater risk of predation. Moreover, at pO2 levels which seem to have little short-term effect, mortality can be very high, even if exposures are not permanent, but take place on a regular basis (Loudon 1988).

Hypoxia is also likely to have a pronounced effect on the short-term performance of active

Body Mass Insects Reared Oxygen

15 20 25 30

Temperature (°C)

Figure 3.1 Change in body mass of Drosophila melanogaster females reared at a variety of temperatures in either 10% or 40% O2 relative to individuals reared under normoxic conditions.

15 20 25 30

Temperature (°C)

Figure 3.1 Change in body mass of Drosophila melanogaster females reared at a variety of temperatures in either 10% or 40% O2 relative to individuals reared under normoxic conditions.

Note: Although size declines with temperature under normoxic conditions this is not shown.

Source: Physiological and Biochemical Zoology, Frazier et al, 74, 641-650. © 2001 by The University of Chicago. All rights reserved. 1522-2152/2001/7405-01011S03.00.

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  • Jayden
    Does insects perform anaerobic?
    3 years ago

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