Nutritional physiology and ecology

An understanding of insect ecology has been nutritional physiology.

Diverse insect diets are associated with entirely different constraints: liquid diets come with a weight or volume problem, solid diets require mechanical breakdown without damage to the gut, plant diets are poor in nutrients, and animal meals are unpredictable in time and space (Dow 1986). Most species of holometabolous insect could be represented in Fig. 2.1 by two linked circles, as a result of vastly different diets in the larval and adult stages. Folivory necessitates an increase in mass of the gut and its contents, with longer retention time, which is incompatible with flight (Dudley and Vermeij 1992). Although this applies to relatively sessile caterpillars, they metamorphose into nectar-feeding adults. About half of known insects are phytophagous, and among these some feeding guilds have been relatively well studied, in particular the leaf-chewers, which are mostly larvae. The nutritional ecology of immature insects was the subject of a classic review by Scriber and Slansky (1981). The present chapter is inevitably biased towards grasshoppers and caterpillars and, to a lesser extent, cockroaches and various fluid feeders. Recent technical advances and the advent of molecular biology have made it possible to study in some depth the nutrition of aphids, another group of agricultural pests, and their simpler diet means that synthetic diets are closer to the real thing. We consider the physiological constraints on feeding behaviour and the physiology of digestion and absorption, before turning to the difficulties of plant feeding and the longer-term consequences of feeding for hampered by an inadequate knowledge of Scriber and Slansky (1981)

growth, development, and the life histories of insects.

A major theme of this chapter is compensatory feeding. In spite of the enormous variation in the quality of plant food, insects obtain their requirements by means of flexible feeding behaviour and nutrient utilization (Slansky 1993). There are three basic categories of compensatory responses shown by phytophagous insects (Simpson and Simpson 1990): increased consumption in order to obtain more of a limiting nutrient such as nitrogen, dietary selection of a different food to complement a limiting nutrient, or increased digestive efficiency to make the best use of a nutrient. The mechanisms of compensatory feeding have been studied in some detail for the major nutrients, proteins and carbohydrates. To avoid difficulties in interpreting experiments, the use of artificial diets is essential, in spite of their ecological limitations (Simpson and Simpson 1990). Another pervasive theme is nitrogen limitation. Insect herbivores tend to be limited by nitrogen because their C : N ratio is so much lower than that of the plants they eat (Mattson 1980).

It is feeding that makes insects into agricultural pests and disease vectors, although the choice of species and problems for research has often been very selective as a result (Stoffolano 1995). Knowledge of food consumption and utilization is of great importance in managing problem insects, and consequently there is an enormous literature on basic and applied insect nutrition and nutritional ecology. As examples of major reviews, the more

Plant Animal

Solid

Liquid

Plant Animal

Solid

Liquid

Figure 2.1 Classification of insect diets according to Dow (1986), based on plant/animal and liquid/solid dichotomies.

Note: Many insects can be placed in borderline positions, for example, adult female mosquitoes which feed on both nectar and blood.

Source: Reprinted from Advances in Insect Physiology, 19, Dow, 187-328. © 1986, with permission from Elsevier.

Figure 2.1 Classification of insect diets according to Dow (1986), based on plant/animal and liquid/solid dichotomies.

Note: Many insects can be placed in borderline positions, for example, adult female mosquitoes which feed on both nectar and blood.

Source: Reprinted from Advances in Insect Physiology, 19, Dow, 187-328. © 1986, with permission from Elsevier.

mechanistic aspects are covered in nine chapters of volume 4 in the 1985 series Comprehensive Insect Physiology, Biochemistry, and Pharmacology (Kerkut and Gilbert 1985), regulation of insect feeding behaviour by Chapman and de Boer (1995), and the ecological context is represented in the 1000-page text of Slansky and Rodriguez (1987), with emphasis on feeding guilds, and by a substantial book on caterpillar foraging (Stamp and Casey 1993). Schoonhoven et al. (1998) list two pages of books and symposium proceedings devoted to insect-plant interactions. The treatment that follows is necessarily extremely selective.

Two areas of research in particular are providing new opportunities and motivation to investigate the effects of plant quality on insect herbivores (Awmack and Leather 2002). These are global climate change, a long-term experimental system involving gradual changes in host plant quality, and the development, since the mid-1990s, of transgenic plants expressing genes for insect resistance (first Bacillus thuringiensis toxin, then antinutrient proteins). Transgenic plants expressing antinutrient proteins permit direct measurement of the costs and benefits of plant defences. Very recently, the emerging field of elemental stoichi-ometry (Sterner and Elser 2002) is adding a new dimension to insect nutritional ecology. Fagan et al. (2002) have shown that insect predators contain on average 15 per cent more nitrogen than herbivores, even after correction for phylogeny, allometry, and gut contents (which could dilute the body nitrogen content of herbivorous species). There is also a phylogenetic trend towards decreasing nitrogen content, with the more derived Lepidoptera and Diptera showing significantly lower nitrogen values than the Coleoptera and Hemiptera.

2.1 Method and measurement

2.1.1 Artificial diets

Artificial diets are widely used in nutritional studies. Often they are semi-synthetic and contain crude fractions of natural diets; for example, the widely used diet for rearing Manduca sexta (Lepi-doptera, Sphingidae) larvae contains wheat germ, yeast, casein, and sucrose, together with salts, vitamins, and preservatives, combined with agar in water (Kingsolver and Woods 1998). For food specialists it may be necessary to include extracts of the host plant in the diet. The advantage of artificial diets is that single nutrients or allelochemicals can be omitted or their concentrations changed, and the effect on performance measured. An essential nutrient can be detected from the effects of its deletion on growth, development, or reproduction, but the determination of nutritional requirements tends to be laborious. Protein and carbohydrate are the major macronutrients, so lipids are generally minimal components of artificial diets, even those for wax moths (Dadd 1985). In compensatory feeding studies, animals may respond differently to diets diluted with water or indigestible agar (Timmins et al. 1988).

Artificial diets have certain limitations. They are based on purified proteins, such as the milk protein casein, which are probably easier to digest than plant proteins because they contain little secondary structure and are not protected by cell walls (Woods and Kingsolver 1999). Artificial diets are rich, and caterpillars raised on them have much higher fat contents than those fed on leaves (Ojeda-Avila et al. 2003). Laboratory selection experiments using Drosophila are influenced by the abundance of food, so that the responses of flies to various forms of selection have tended to involve energy storage rather than energy conservation

(Harshman and Hoffman 2000). These diets are also much softer than plant material, and this can lead to a reduction in the size of the head and chewing musculature in caterpillars (Bernays 1986a). Experiments using natural forage are ecologically more realistic, but are complicated by the fact that plant tissue is highly variable in chemical composition and levels of nitrogen, water, and allelochemicals tend to covary. Nitrogen and phosphorus also covary in plant tissue (Garten 1976). The use of excised leaves is not recommended in assays of herbivory, because induced plant defences may reduce their nutritional quality (Olckers and Hulley 1994).

2.1.2 Indices of food conversion efficiency

Standard methods have been extensively used for quantifying food consumption, utilization, and growth in insects, especially phytophagous larvae (Waldbauer 1968; Scriber and Slansky 1981). The efficiency of food utilization is assessed using various ratios based on energy budget equations. Waldbauer, in his classic paper, defined three nutritional indices:

Approximate digestibility (or assimilation efficiency) AD = (I — F)/I;

Efficiency of conversion of ingested food (or growth efficiency) ECI = B/I;

Efficiency of conversion of digested food (or metabolic efficiency) ECD = B/(I — F), where I — dry mass of food consumed, F — dry mass of faeces produced, and B — dry mass gain of the insect. Performance is expressed in terms of relative (i.e. g per g) rates of consumption (RCR) and growth (RGR). Various interconversions between nutritional indices and performance rates are possible, for example, RGR — RCR x AD x ECD — RCR x ECI. An insect may maintain its growth rate over various combinations of these parameters because there are trade-offs between rates and efficiencies, for example, a higher RCR lowers retention time and thus AD. Slansky and Scriber (1985) discussed the methodology and summarized an enormous amount of data on the nutritional performance of insects in different feeding guilds. Slansky (1993) recommended measuring food consumption based on fresh weight as well as dry weight, otherwise compensatory feeding (see below) may not be evident when the foods differ in water content. Errors resulting from inaccurate measurement of food water content (especially leaves) are common and potentially serious.

Dry mass measurements (most of the data) can be converted for calculation of energy or nitrogen budgets (Wightman and Rogers 1978). ECI and ECD of a phytophage will be higher when expressed in terms of energy content than when expressed in dry mass because insect tissue has a higher energy content than plant tissue (Waldbauer 1968).

2.1.3 Use of a geometric framework

Ratio analyses in ecophysiology are problematic (Packard and Boardman 1988; Raubenheimer 1995; Beaupre 1995), and statistical problems can be avoided by direct analysis of measured variables. This approach has been convincingly advocated over the past decade by Simpson and Raubenheimer (Simpson and Raubenheimer 1993a; Simpson et al. 1995; Raubenheimer and Simpson 1999) for nutritional analysis in insects at both ingestive and post-ingestive levels. Their geometric approach has been valuable for demonstrating how animals eating unbalanced or suboptimal foods compromise between intakes of different nutrients, and is briefly explained here.

The concept of an 'intake target' provides a new way of looking at the regulation of nutrient intake (Simpson and Raubenheimer 1993a). Intake targets, which vary with growth or reproduction, are defined as the optimal amount and balance of nutrients that must be ingested for post-ingestive processes to operate at minimal cost to fitness. In the simplest case of two nutrients (such as protein and carbohydrate), with each represented as an axis on a two-dimensional graph, an insect given a single food type consumes a fixed proportion of nutrients so that its intake lies on a line passing through the origin, termed a 'rail' to suggest movement in a fixed direction (Fig. 2.2). The insect will not be able to achieve its intake target for the two nutrients if the rail does not pass through the target. It may have to compromise by eating an

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