Amino acids

Figure 2.16 Proportion of amino acid carbon derived from the adult diet in eggs of the hawkmoth Amphion floridensis, measured using stable isotopes.

Note: Data are for eggs laid on day 12, when carbon isotopic composition has stabilized (see O'Brien et al. 2000). All essential amino acids are within measurement error of zero, indicating their exclusive origin in the larval diet.

Source: O'Brien et al. (2002). Proceedings of the National Academy of Sciences of the USA 99, 4413-4418. © 2002 National Academy of Sciences, U.S.A.

reared gypsy moth larvae, Lymantria dispar (Lymantriidae) through several instars with differing access to two artificial diets, and found that an initial preference for high protein content shifted to one for high lipid content, especially in male larvae. Males need lipid for flight fuel, but female moths do not fly. Neither sex feeds as adults and there is no need to search for adult food plants. Moths eclose with mature eggs (1300 per female under laboratory conditions) which contain 50 per cent of the nitrogen assimilated by the larvae (Montgomery 1982). Incidentally, it is Lepidoptera with this type of life history that are most likely to reach outbreak densities in homogeneous food plant environments (Miller 1996). Spring-feeding forest Lepidoptera in the Geometridae and Lymantriidae exhibit a high incidence of wing reduction in females, although Hunter's (1995) phylogenetic analysis showed no statistically significant increase in fecundity.

Flight polymorphism

Polyphenisms or developmental switches are irreversible changes in phenotype in response to environmental information during a critical phase of development; as in the castes of social insects or the wet and dry seasonal phenotypes of some butterflies. Aphids exhibit a complex sequence of generations with different phenotypes, and it is commonly accepted that the development of winged aphids is a result of poor nutritional quality of their host plants, although this hypothesis is only partially supported by the accumulated evidence (Muller etal. 2001). All insect polyphenisms are likely to be controlled by changes in endocrine physiology (Nijhout 1999), and the best evidence for endocrine control comes from wing polymorphism in crickets. This arises from a combination of genetic and environmental variation, and is controlled by elevated titres of juvenile hormone which block the development of wings and flight muscle during a critical period of development (Zera and Denno 1997). The term polymorphism is often used when there is a genetic component to the morphological differences. However, the terms polymorphism, polyphenism, and pheno-typic plasticity are sometimes not carefully distinguished (see Section 5.2.1 for discussion of terminology).

Wing polymorphism is a commonly studied dispersal polymorphism because it involves discontinuous variation in flight capability, and wing morphs are easily recognized (reviewed by Zera and Denno 1997). The winged morph usually has fully developed, functional flight muscles and lipid stores for flight fuel, while the flightless morph has short wings, non-functional flight muscles and reduced lipid stores. In some species a second flightless morph is derived from long-winged adults by histolysis of flight muscles (although this morph was not distinguished from flight-capable morphs in earlier studies). Flightless females normally show increased fecundity, and histolysis of flight muscles coincides with ovarian growth in long-winged female crickets. These correlations have been interpreted as demonstrating a fitness trade-off between flight ability and reproduction, but are not sufficient to prove a causal relationship. However, recent nutritional studies provide unequivocal evidence for this fitness trade-off. Gravimetric feeding trials on Gryllus species have demonstrated that ovarian growth in flightless morphs (either natural or hormonally engineered) may be due either to increased food consumption or to relative allocation of the same quantity of absorbed nutrients, depending on the species. Only the latter situation represents a trade-off (Zera and Harshman 2001). Thus, reduced nutrient input can magnify a trade-off, whereas an increase in nutrients can eliminate it. This has been emphasized by measuring nutritional indices for three morphs of G. firmus (long-winged, short-winged, and flightless morphs with histolysed flight muscles). Values of ECD were significantly elevated in both types of flightless morph: compared to the flight-capable morph, flightless morphs converted a greater proportion of absorbed nutrients into body mass, mainly ovarian mass, and allocated a smaller proportion to respiration. Low-nutrient diets increased the discrepancy in ECD values, indicating that the trade-off between respiration and early reproduction was magnified (Zera and Brink 2000). Lipid accumulation in the first few days of adult life results in triglyceride reserves which are 30-40 per cent greater in the flight-capable morphs of G. firmus, and the magnitude of this difference suggests that limited space in the abdomen could also be a factor in the trade-off between lipid accumulation and ovarian growth (Zera and Larsen 2001). Newly emerged male and female dragonflies, Plathemis lydia (Libellulidae), are similar in mass and the mass of individual body parts, but the abdomens of females then increase fivefold in mass owing to ovarian development, and the thoraxes of males increase 2.5-fold in mass as a result of flight muscle growth (Marden 1989). Such a high investment in the thorax carries a cost in that gut mass and body fat content are minimal in territorial male dragonflies.

The widespread occurrence of flightlessness and wing polymorphism in insects suggests that flight carries substantial fitness costs in the construction, maintenance, or operation of wings and flight muscles. This is borne out by differences in respiration rate between the pink flight muscle of fully winged G. firmus and the white muscle of the short-winged adults or of long-winged adults after flight muscle histolysis (Zera et al. 1997). The flying insects surveyed by Reinhold (1999) had resting metabolic rates which were about three times those of non-flying insects. Wing polymorphism is a type of dispersal polymorphism, and Roff (1990), in reviewing the ecology and evolution of flightless-ness in insects, concluded that secondary loss of wings is more frequent among females because of the trade-off with fecundity and is most likely in stable environments. Males remain mobile to find mates, and habitat fragmentation may select for rapid evolutionary change in flight-related morphology in both sexes, seen in an increased investment in the thorax as habitat area declines (Thomas et al. 1998).

2.6 Temperature and growth

2.6.1 Thermal effects on feeding and growth

In ectotherms, higher temperatures increase growth rates and decrease development times, and generally result in smaller adult body sizes (Atkinson 1994; Atkinson and Sibly 1997). In Drosophila, small body size resulting from development at high temperatures is due mainly to decreases in cell size (Partridge et al. 1994), although changes in cell number can also be involved (reviewed in Chown and Gaston 1999). The selective advantage of smaller size at higher temperatures, or larger size at lower temperatures, has long been considered obscure (Berrigan and Charnov 1994). Indeed, several authors have considered larger size at low temperatures an epiphenomenon of differences in the responses of growth and of differentiation to temperature, and therefore not adaptive at all (Chapter 7). Likewise, Frazier et al. (2001) have recently demonstrated interactive effects of hypoxia and high temperature on the development of D. melanogaster, and a discrepancy between oxygen delivery and oxygen demands is a possible explanation for smaller body size in ectotherms developing at high temperatures. Alternatively, other studies have suggested advantages to large size at lower temperatures, but not necessarily to small size at higher temperatures (e.g. McCabe and Partridge 1997; Fischer et al. 2003; see also Chapter 7). Given substantial variation in final body size relative to environmental temperature in the field (Chown and Gaston 1999), and that mechanisms of temperature-related size variation have yet to be resolved (Berrigan and Charnov 1994; Blanckenhorn and Hellriegel 2002), this field remains interesting and productive. Recently, stoichiometric work has started providing additional insights into the implications of temperature-related body size variation. Chemical analyses of Drosophila species show substantial variation in nitrogen and phosphorus contents, with the N and P contents of individual species being positively correlated with each other and with the N and P composition of the breeding sites (Jaenike and Markow 2003). Moreover, a variety of cold-acclimated organisms, including Drosophila species, exhibit substantially increased levels of N and P, as a result of both concentration changes and larger body sizes at low temperatures (Woods et al. 2003). It might, therefore, be useful for herbivores to forage on plants growing in cool microenvironments.

There is an extensive literature on the temperature dependence of larval growth rates in insects (Ayres 1993; Casey 1993; Stamp 1993). Most laboratory studies have been carried out under constant temperatures, but growth may be stimulated or inhibited in a fluctuating temperature regime, which better resembles field conditions (Ratte 1985). As an example of differing thermal response curves, Knapp and Casey (1986) compared the temperature sensitivity of growth rates in two caterpillar species. Eastern tent caterpillars Malacosoma americanum (Lasiocampidae), which hatch early and behaviourally thermoregulate, grow at rates that are highly dependent on temperature. By contrast, those of gypsy moth caterpillars L. dispar (Lymantriidae), which hatch later and are thermal conformers, are independent of temperature at ecologically relevant temperatures of 25-30°C. The

African armyworm Spodoptera exempta (Noctuidae) shows a density-dependent polymorphism resembling that of migratory locusts, and the gregaria phase develops much faster than the solitaria phase (Simmonds and Blaney 1986). Casey (1993) suggested that solitaria caterpillars are thermal con-formers, switching to a thermoregulating strategy in the gregaria phase. However, Klok and Chown (1998a) found no evidence of behavioural thermoregulation in gregaria in the field and concluded that different development rates recorded in several studies most likely result from differences in utilization of food.

Behavioural thermoregulation (see Chapter 6) has physiological consequences for feeding, growth and reproduction, exemplified in field and laboratory studies of acridid grasshoppers. Populations of Xanthippus corallipes at different altitudes maintain similar metabolic rates, because smaller body mass at high elevations, which leads to relatively higher mass-specific metabolic rates, is offset by lower Tb in the field. Stabilization of field metabolic rate enhances total egg production, assessed by counting corpora lutea of females at the end of the reproductive season (Ashby 1998). During sunny days, Melanoplus bivittatus regulates its body temperature (Tb) between 32-38°C and has an essentially non-functional digestive system during the night (Harrison and Fewell 1995). The rate of digestive throughput is strongly limiting at low temperatures but this process has a high Q10 so growth is fast at high temperatures. Variables such as food consumption and faecal production are more temperature-sensitive (have a higher Q10) than variables reflecting chewing and crop-filling rates. Within the range of preferred Tb, ingestion and processing rates are well matched. Faster growth at high temperatures is more an effect of faster consumption than of increased efficiency, and this is also true of caterpillars. In general, thermoregulating caterpillars and grasshoppers have higher Q10 values for feeding and growth than thermoconformers, which must be able to grow over wide temperature fluctuations in the field. Note that endothermic insects will also experience intermittent digestive benefits.

Social caterpillars in the family Lasiocampidae (tent caterpillars) show highly synchronized bouts of foraging activity, alternating with digestive phases when they rest in or on their tent, and these activity patterns can be electronically recorded under field conditions (Fitzgerald et al. 1988; Ruf and Fiedler 2002). The duration of both foraging bouts and digestive phases is inversely related to temperature in Eriogaster lanestris, which has an opportunistic feeding pattern in relation to thermal conditions. In contrast, another lasio-campid, the eastern tent caterpillar M. americanum, forages only three times a day, possibly because predation risk may outweigh the need for feeding efficiency. The effects of temperature on caterpillar foraging and growth are reviewed by Casey (1993) and Stamp (1993), but generalizations are difficult because such effects are intimately connected with the natural history of a species (which includes constraints due to predators and parasites).

The majority of caterpillar species are solitary, palatable, and cryptic and do not have the option of thermoregulation. Kingsolver (2000) measured peak consumption and growth rates around 35°C in fourth instar Pieris brassicae in the laboratory, and integrated these with the operative temperatures of physical models placed under leaves in a collard garden to demonstrate that infrequent high temperatures can make disproportionate contributions to caterpillar growth—because growth rates are so much faster at higher temperatures. In M. sexta, another thermoconformer (Casey 1976a), short-term consumption and growth rates show similar shallow thermal response curves, with Q10 values less than 2.0 for temperatures up to 34°C (Kingsolver and Woods 1997). When the thermal sensitivity of growth and its component processes in M. sexta was compared by measuring growth rate, consumption rate, protein digestion, methionine uptake, and respiration rate over the range 14-42°C, the thermal performance curve for growth rate was most similar to that for consumption rate, and declining growth above 38°C could not be ascribed to decreased digestion or absorption rates or increased respiration rates (Fig. 2.17). Reynolds and Nottingham (1985) similarly found that nutritional indices in M. sexta were unaffected by temperature, although chronic exposure resulted in smaller size at high temperatures.

2.6.2 Interactions with food quality

Caterpillars of M. sexta have again been used as a model system in examining nutritional interactions between temperature and dietary protein levels. Although low temperatures reduce rates of consumption and growth, low protein levels lead to increased consumption rates through compensatory feeding but may not affect growth rates. In short-term experiments (4 h), fifth-instar larvae of M. sexta failed to compensate for low protein levels at the most extreme temperatures of 14 and 42°C, but long-term experiments (duration of the fifth stadium) over a narrower temperature range showed little evidence of interactions between temperature and dietary protein (Kingsolver and Woods 1998). These authors suggest that compensatory feeding responses may be less effective in diurnally fluctuating temperatures than in the constant temperatures in which they are commonly examined. This study was extended by examining interactive effects on instars 1-3, 4, and 5 separately, and there were some striking differences between instars (Petersen et al. 2000). Mean growth rate was highest at 34°C during the first three instars but highest at 26°C during the fifth instar (the latter is the temperature at which laboratory colonies of M. sexta are maintained). Fifth instar caterpillars were surprisingly sensitive to high temperatures, which is significant in view of the fact that most studies of caterpillar nutritional ecology use this instar (Petersen et al. 2000). The gypsy moth is a spring-feeding forest insect which develops during a period of declining leaf nitrogen and increasing ambient temperatures. Lindroth et al. (1997) found interactive effects of temperature and dietary nitrogen on several performance parameters measured through the fourth instar, but there were no interactions over the larval period as a whole. The combination of poor quality food and low temperature can result in exceptionally slow growth and long life cycles, as in the Arctic caterpillar Gynaephora groenlandica (Lymantriidae) which has a development time of 7 years in spite of well developed basking behaviour (Kukal and Dawson 1989).

Temperature's effects become even more complex when allelochemicals or other trophic levels are

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