Lymantria dispar L. caterpillars have a decreased ability to assimilate protein from mature leaves of red oak (Quercus rubra) compared with young, expanding leaves. The present study determines whether the drop in protein assimilation efficiency (PAE) occurs during the rapid phase of leaf maturation. Several mechanisms that might account for decreased PAE are also examined: mature leaf tissues could resist being chewed efficiently, protein in mature leaf tissues could become difficult to extract, and other nutrients in mature leaves might become growth limiting. The entire seasonal decrease in PAE occurs rapidly (in less than 2 weeks), when the leaves finished expanding. The maturation process is characterized by increased levels of fibre and decreased levels of water but no significant changes in the levels of protein or carbohydrates. Despite increased fibre in mature leaves, they are not chewed into larger food particles than are immature leaves. Carbohydrate assimilation efficiencies remain high on mature leaves, and signs of limiting water levels in larvae of L. dispar on mature leaves are not observed. The most important finding in the present study is the decreased extractability of protein in food particles from mature leaves, which plays a major role in explaining the rapid decrease in PAE. It is hypothesized that structural changes in cell walls during the rapid process of leaf maturation decrease protein extractability, which, in turn, greatly decreases the nutritional quality of mature oak leaves for caterpillars. The results of the present study therefore suggest a general mechanism to help explain the widely documented decrease in the nutritional quality of the mature leaves of many tree species for herbivorous insects.

Sulfur amino acids [cysteine (Cys) and methionine (Met)] play two major roles during animal development: protein synthesis for growth and glutathione synthesis for defense. For caterpillars, the levels of sulfur amino acids found in foliar protein can be especially low relative to their nutritional needs. Previous work has measured concentrations of glutathione (GSH; containing Cys) in specific animal tissues, but has not examined whole-body levels to ascertain the costliness of this defense in terms of Cys allocation. This study examined whether the production of GSH varies between species and within individuals in accordance with an insect's need for antioxidant defense. Secondly, we quantified the allocation of total Cys (peptide-bound plus free Cys) to GSH in caterpillars as an estimate of its cost. Two contrasting species were compared: Lymantria dispar (Lymantriidae), a species that is highly defended, and Malacosoma disstria (Lasiocampidae), a species that is less defended. As expected, GSH levels were significantly higher in L. dispar than in M. disstria. Consistent with the function of the midgut as a first line of defense against ingested toxins, GSH levels were significantly higher in these tissues than in the whole bodies of both species. A major finding in this study was that a large fraction of total Cys is used to produce GSH: GSH in the midguts of L. dispar and M. disstria contained 23 and 21%, respectively, of the total Cys in these tissues, and the GSH in their remaining body tissues contained 19 and 17% of the total Cys in these tissues. Levels of total Cys in caterpillar tissues followed the same pattern of distribution as did GSH, producing a strong association between GSH and total Cys (R(2) = 0.794). We conclude that GSH is a costly defense, especially in generalist tree-feeding species such as L. dispar. These results further suggest that the large allocation of Cys to GSH in highly defended species might produce a tradeoff by limiting the amount of Cys available for rapid growth.

The growth rates of insect herbivores commonly decrease when they feed on mature leaves due to the combined effects of several nutritional and physiological mechanisms. Environmental stresses during leaf development may also decrease herbivore performance. The present study tests two main hypotheses to help clarify the importance of these factors for the nutrition and growth of an insect herbivore: (i) decreases in nutrient levels, consumption rates and nutrient assimilation efficiencies impact negatively on herbivores feeding on mature leaves and (ii) wind stress has a negative impact on herbivores feeding on mature leaves. The results show that mature poplar (Populus alba × Populus tremula) leaves have decreased levels of protein and increased levels of fibre, and that growth rates of gypsy moth (Lymantria dispar L.) are decreased on mature leaves in association with decreased consumption rates. However, in contrast to the first hypothesis, protein and carbohydrate are assimilated efficiently (74–82% and 84–87%, respectively) from immature and mature poplar leaves. The larvae are able to chew mature leaves as efficiently as immature leaves, potentially maximizing nutrient extraction. By contrast to the second hypothesis, wind‐stressed leaves have no significant detrimental effects on nutrient assimilation efficiencies, and the lower growth rates of L. dispar larvae feeding on mature wind‐stressed leaves can be explained by lower consumption rates. Therefore, the availability of nutrients to herbivores feeding on mature tree leaves is not necessarily impacted by lower assimilation efficiencies, even when leaves develop under wind stress. These results help explain some of the large variation between the nutritional qualities of trees for forest Lepidoptera.