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Figure 2.9 Rates of proline transport by posterior midguts of Manduca sexta caterpillars (fifth instar) reared on high or low protein diets and then transferred to high or low protein diets for 24 h. Mean ± SE of 6-7 midguts.

Note: The four high traces are fluxes from lumen to haemolymph, and the four low traces are fluxes in the other direction. Lower values at 15 min are due to equilibration of labelled proline. There was no effect of rearing or test diets.

Source: Reprinted from Journal of Insect Physiology 45, Woods and Chamberlin, 735-741. © 1999, with permission from Elsevier.

15 30 45 60

Time (min)

Figure 2.9 Rates of proline transport by posterior midguts of Manduca sexta caterpillars (fifth instar) reared on high or low protein diets and then transferred to high or low protein diets for 24 h. Mean ± SE of 6-7 midguts.

Note: The four high traces are fluxes from lumen to haemolymph, and the four low traces are fluxes in the other direction. Lower values at 15 min are due to equilibration of labelled proline. There was no effect of rearing or test diets.

Source: Reprinted from Journal of Insect Physiology 45, Woods and Chamberlin, 735-741. © 1999, with permission from Elsevier.

of monosaccharides in insect midgut is less likely to be modulated in response to dietary change. Whether the paracellular route is involved in nutrient absorption in insects has apparently not been considered.

2.4 Overcoming problems with plant feeding

Half of all insect species feed on living plants. Although few orders have overcome the evolutionary hurdles of plant feeding, those few (especially Orthoptera, Hemiptera, and Lepidoptera) have been extremely successful (Southwood 1972; Farrell 1998). Apart from mechanical obstacles to feeding, herbivores must contend with indigestible cellulose, nutrient deficiencies (especially low nitrogen), and allelochemicals. Often, maximizing nutrient intake while minimizing secondary compound intake requires complex foraging decisions and can prevent the insect from reaching its intake target (Behmer et al. 2002). Many of the solutions involve interactions with microorganisms. There is a vast literature in this area and our treatment is highly selective.

2.4.1 Cellulose digestion: endogenous or microbial?

Caterpillars and most other insect folivores are unable to use the huge proportion of plant energy locked up in cellulose. Martin (1991), in reviewing the evolutionary ecology of cellulose digestion, suggests that it is rare because insect herbivores are usually limited by nitrogen or water and not by carbon, so they would derive no particular benefit from exploiting the energy in cellulose. Cellulose digestion is much more likely in wood-feeding (xylophagous) insects or omnivorous scavengers with nutritionally poor diets, especially those whose guts are colonized by microorganisms. The best known cellulose-digesting insects are termites and the closely related cockroaches.

The traditional assumption is that cellulose-digesting enzymes are derived from protozoa or bacteria residing in the hindgut, or fungi ingested with the diet; this assumption is consistent with the independent evolution of the capacity in different taxa (Martin 1991). However, the contribution of endogenous enzymes has been strongly debated (Slaytor 1992). Because insects are almost universally associated with microorganisms, it has been difficult to refute the long-standing hypothesis of derived enzymes, even though most symbionts are located in the hindgut, endogenous cellulase is present in salivary glands and midgut, and cockroaches have far smaller symbiont populations than do termites. Lower termites appear to utilize both endogenous and protozoal cellulases; their specialized hindgut has chambers containing large populations of protozoa, which break down cellulose to glucose and ferment it to short-chain fatty acids, mainly acetate, propionate and butyrate. Higher termites (the majority of termite species) lack hindgut protozoa and appear to utilize endogenous enzymes, except for fungus-growing species in the subfamily Macrotermitinae which acquire additional cellulases from the fungus (Termitomyces sp.) that they cultivate and consume.

Cellulase is an enzyme complex capable of converting crystalline cellulose to glucose (Slaytor 1992). In termites and cockroaches its main components are endo-b-1,4-glucanases, which cleave glucosidic bonds along a cellulose chain, and b-1,4-glucosidases, which hydrolyse cellobiose to glucose. Insects apparently lack an exoglucanase active against crystalline cellulose (Martin 1991), but their endoglucanases possess some exoglucanase activity and can be present in large quantities, as in Panesthia cribrata (Blattaria, Blaberidae), which feeds on rotting wood (Scrivenor and Slaytor 1994). An endogenous insect cellulase, endo-b-1, 4-glucanase from the lower termite Reticulitermes speratus (Rhinotermitidae), was identified by Watanabe et al. (1998). It is secreted in the salivary glands, along with a b-glucosidase, and produces glucose from crystalline cellulose. Unhydrolysed cellulose is then fermented to acetate by hindgut protozoa, and this double action could account for the high efficiencies of cellulose digestion mentioned by Martin (1991).

The Macrotermitinae cultivate symbiotic fungi on combs constructed from undigested faeces, and consume fungus nodules and older comb. Besides enzymes, they acquire concentrated nitrogen, because fungi contain reduced quantities of structural carbohydrates (Mattson 1980). The fungus comb in newly founded termite colonies is inoculated with spores carried by alates or collected by foragers (Johnson et al. 1981). Genetic techniques have recently been applied to the evolutionary histories of fungus-farming in ants, termites, and beetles (see Mueller and Gerado 2002). Fungiculture has evolved several times independently: multiple origins are evident in certain beetles such as cerambycid larvae, but only a single origin each in ants and termites. This sophisticated form of cellulose digestion has enabled leaf-cutting ants and the Macrotermitinae to become dominant herbivores and detritivores in tropical ecosystems, and fungus-growing beetles are major forestry pests. The emphasis in the literature has been on cellulose digestion, but this is still in dispute where leaf-cutting ants are concerned (Abril and Bucher 2002). Other polysaccharides may be important: leaf-cutting ants and their symbiotic fungi together possess the enzymes necessary to degrade the xylan and laminarin of hemicellulose (D'Ettorre et al. 2002). Workers of Atta sexdens obtain a large proportion of their nutritional needs from the extracellular degradation of starch and xylan by enzymes of fungal origin (Silva et al. 2003).

Scarabaeid dung beetles are extraordinarily successful on a food resource that is patchy and ephemeral, but also rich: dung, especially from ruminants, contains substantial nitrogen (Hanski 1987). Although both larvae and adults feed on dung of mammalian herbivores, only larvae digest cellulose, with the help of bacteria in a hindgut fermentation chamber, and reingestion of faeces. This ensures maximum utilization of the strictly limited amount of food in the brood ball (Cambefort 1991). Larger particles in fresh dung are indigestible plant fragments, which may be macerated by larvae. By contrast, adults have filtering mouthparts that reject such coarse particles. Recently, latex balls of various diameters, manufactured for calibration of Coulter Counter® instruments, were mixed with the preferred dung of 15 species of adult Scarabaeinae (size range 0.05-7.4 g) to determine the maximum size of ingested particles (Fig. 2.10): the range was only 8-50 mm (Holter et al. 2002). These very small particles have higher nutritional value because their large surface area to volume ratios promote microbial activity. Fine particles (<20 mm) have a much lower C: N ratio than coarse particles (>100 mm) or bulk dung, and the value for fine particles resembles the C : N ratio for bacteria (P. Holter and C.H. Scholtz, unpublished). Thus,

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