• Climate change;
  • insect development;
  • insect herbivory;
  • Lepidoptera


  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

1. Pedunculate Oak trees were grown in ambient and elevated temperatures and CO2. Leaves were fed to Winter Moth caterpillars reared either in constant conditions or with the trees (caged or on-tree).

2. Caterpillars in constant conditions ate the same mass and produced the same mass of faeces whether fed elevated or ambient temperature leaves. However, less was assimilated from elevated leaves, resulting in lighter pupae and fewer, lighter eggs.

3. Caterpillars in constant conditions ate more and produced more faeces when fed elevated CO2 leaves than when fed ambient CO2 leaves, but the mass assimilated and pupal mass were unchanged.

4. Caged caterpillars reared with the trees from which they were fed had constant pupal mass in all treatments, but pupated earlier at elevated temperature. Pupal mass was also unaffected when caterpillars fed on the trees.

5. Nitrogen was reduced in both elevated temperature and elevated CO2 leaves. Increased fibre in the former prevented increased consumption and resulted in reduced pupal mass and fecundity. Reduced fibre in the latter allowed increased consumption, resulting in pupae of normal mass.

6. Despite the clear effect of nutrient quality, experiments rearing caterpillars and trees together suggest that anticipated climatic change will have no nutritional effect on Winter Moth development.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Current predictions suggest that global levels of atmospheric carbon dioxide will increase to about 500 ppmv (from about 358 ppmv) by the year 2100, with a consequent global temperature increase of about 2 °C (IPCC 1996). Such change is unlikely to affect the essential synchrony between egg hatch of Winter Moth (Operophtera brumata L.) and budburst of Pedunculate Oak (Quercus robur L.), as the timing of both is equally affected (Buse & Good 1996). In elevated CO2, plant growth is generally stimulated, resulting in reduced nitrogen (Hilbert, Larigauderie & Reynolds 1991) and increased phenolics (Lambers 1993), although a few species have negligible responses (Woodward 1992; Rogers, Runion & Krupa 1994). Consequently, insect herbivores tend to grow more slowly, consume more plant material, take longer to develop and suffer heavier mortality (Watt et al. 1995). Elevated temperature also reduces foliar nitrogen concentration and increases condensed tannin content (Dury et al. 1998), thus impoverishing foliar quality for larval development (Scriber & Slansky 1981).

Under normal conditions, leaf quality is continually changing because of the seasonal and temperature-related decline in water and nitrogen content and increase in fibre, lignins, tannins and leaf toughness (Scriber 1984). However, the effect of these changes on insects varies. For example, the inhibitive effect of tannins is less if an insect normally feeds on tannin-rich species (Bernays 1981; Bernays, Driver & Bilgener 1989). Because digestibility and nutritional value vary with both plant and insect, House (1969) emphasized the importance of feeding tests in determining differences in food quality as ‘the animal concerned is the final judge’. Such tests show that, although high CO2 foliage normally results in slower larval growth and higher mortality than low CO2 foliage (Fajer, Bowers & Bazzaz 1989), CO2 had no effect on survival rate if plants were fertilized with nitrogen-based fertilizer (Osbrink, Trumble & Wagner 1987). They also show that some insects respond to diluted foliar nitrogen (owing to increased carbohydrates in elevated CO2) by increased consumption and little change in growth, whereas others have little change in consumption and decreased growth (Lincoln 1993).

Temperature and CO2 levels can also have direct effects on larval feeding performance. For example, reduced temperature (20 °C compared with 30 °C) depressed the amount of food eaten, amount of faeces produced, and consumption and growth rates and increased the non-feeding period in the caterpillar Spilosoma congrua (Stamp & Bowers 1994). In general, increasing temperature above a developmental null point increases the rate of development up to an optimum (Precht, Laudien & Havsteen 1973); this is why most models of arthropod development are temperature-based (Wagner, Olson & Willers 1991; Hilbert 1995). The only reported direct effect of elevated CO2 is more frequent spiracular opening (Hoyle 1960; Burkett & Schneiderman 1974), but the potential effect on the insect’s water balance has not been found (Lincoln 1993).

The interactive effects of temperature, CO2 and plant nutrition on larvae may differ from their independent effects. For example, nutritional requirements reflect metabolism and are therefore related to temperature. However, increased temperature does not always increase the rate of growth and development, because the effect of a particular balance of nutrients in the diet varies with temperature (House 1969). Thus, insect development is a function of nutrition as well as temperature (Hilbert 1995), although in some species temperature is the more important determinant of growth rate whereas in others food quality overrides the temperature effect (Scriber & Slansky 1981).

Winter Moth and Pedunculate Oak were chosen for this experimental study because of the long-term work at Wytham Wood near Oxford (e.g. Varley, Gradwell & Hassell 1973), particularly on the moth’s role as food for birds (Perrins 1965, 1991), and because of concurrent field studies on this species in the wood. Winter Moth larvae feed from the time of budburst, apparently to avoid the later toughening of the leaves (Feeny 1970), increased fibres (Pandey 1992) and increased condensed tannins which reduce larval growth rate and pupal mass (Feeny 1968, 1970). They thus take advantage of the high nitrogen and water content of the leaves, which then rapidly decline (Scriber & Slansky 1981; Dury et al. 1998). This study investigates whether elevated temperature or CO2 has an effect on larval development and thus on pupal mass and, consequently, fecundity, either via a change in nutrient quality of the leaf, or in the relative timing of leaf and larval development. It might be expected that elevated temperature, within the range of normal year-to-year variability, would have little effect because both leaves and caterpillars would develop faster. However, the effect of elevated CO2 outside the levels normally encountered is less predictable. Although any consequent change in nutrient quality of the leaves is unlikely to be matched by a change in larval physiology, and elevated CO2 might also have a direct effect on the larvae, it is possible that caterpillars, because they normally eat leaves of varying quality, might be able to compensate for low food quality.

The hypothesis that elevated temperature would have no effect on the relationship between leaf nutritional quality and larval development, whereas elevated CO2 would, was tested in two main experiments. In the first, the indirect effects of elevated CO2 and temperature through effects on the nutritional quality of the food were examined by feeding leaves taken from oaks grown under varying conditions to caterpillars maintained under constant environmental conditions (similar to the approach of Lincoln, Sionit & Strain 1984). In the second experiment, the direct effect of elevated CO2 or temperature on the interaction between host and larva was tested by maintaining both trees and larvae in the same environmental conditions (similar to the approach of Kirsten & Topp 1991). Chemical analyses of the leaves complemented the insect data.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References


The oak trees were maintained in a series of eight hemispherical glasshouses (Solardomes), each with a ground area of 10 m2. These provided two replicates of a 22 factorial combination of ambient and elevated temperature (elevated tracked 3 °C above varying ambient) and ambient and elevated CO2 (elevated tracked 340 ppm above ambient). This facility, at the Institute of Terrestrial Ecology in Bangor, was unusual in that true ambient temperatures in the domes were achieved by cooling the flow of incoming air (Rafarel, Ashenden & Roberts 1995). The controls were the two ambient temperature/ambient CO2 Solardomes. A replicated outdoor ‘control’ under a ‘normal’ CO2/temperature regime was added for comparison with the Solardome control treatment. These were exposed to wind chill and normal rainfall and so could not be directly compared with the entire range of Solardome treatments. There were thus five replicated treatments (10 groups of trees) in all. Nine 3-year-old trees, raised from a single seed source (Forest of Dean, UK), were randomly allocated and introduced into each of the treatments in March 1993 in readiness for the experiment in 1994. Their position in each group was re-randomized weekly to compensate for intra-Solardome variability. Each tree was in a 25-cm diameter by 25-cm deep plastic pot, containing 7 l of soil from Wytham Wood and standing in a 2-cm deep saucer, kept constantly filled with water to prevent drought stress. The trees were fed twice during 1993 with 15:30:15 nitrogen:phosphorus:potassium liquid fertilizer to provide an adequate nutrient supply. They were not fed during the spring experimental period in 1994 because the differing rates of tree development in the various treatments made consistent nutrition difficult. However, available soil nitrogen is high in spring (Reynolds & Edwards 1995), so a nitrogen deficit was unlikely.

Two-year-old trees, for use in the 1995 experiments, were introduced into the treatments early in 1994 and treated similarly.

Leaf development on the trees in the various treatments was monitored visually on a scale from closed bud, through new leaves protruding and young leaves completely free of scales, to full-size leaf (Aussenac 1975; Buse & Good 1996) to synchronize egg hatch with budburst and to standardize leaf collection for chemical analysis. Measurements were made of total nitrogen, total phenolics, condensed tannins, total carbon and leaf toughness, as outlined in Dury et al. (1998).


In spring 1994, leaves from the various treatments were fed to caterpillars in a controlled environment cabinet at 15 °C, 75% RH, ambient CO2 (the same as outdoors, i.e. about 340 ppm) and 16:8 h light:dark. The indirect effect of elevated temperature and CO2 on larval growth, through foliar quality, was thus separated from the direct effect on the caterpillars.

All the larvae used were the progeny of one female. Eggs were maintained at about 6 °C and hatched to coincide with budburst in a particular treatment by transferring them to room temperature about 10 days before budburst was anticipated. Ten larvae were allocated to each group of trees, i.e. 100 in total. In each experiment, one newly hatched larva was introduced into a 95-mm Petri dish with lid, containing a weighed, freshly excised leaf on filter paper moistened with 1 ml water. As far as possible, the leaves used for the 10 larvae were from the same tree. For each group of trees, four similar leaves from the same tree(s) were individually weighed, dried at 60 °C for 24 h and reweighed to estimate the dry mass of the experimental leaves. Every second day, each caterpillar was transferred to a new, similarly prepared dish. Preliminary tests showed no visible drying out of the leaf during these 2 days. The uneaten portion of each leaf and the faeces were transferred to individual small paper envelopes, dried at 60 °C and weighed. Dry mass was used in preference to wet mass, in which water loss from control leaves is measured (e.g. Kerslake et al. 1996), because it is more consistent. This process was repeated for the 100 larvae, the instar and date being recorded at each feed.

During the fifth instar, the caterpillar was weighed at each feed. The resultant pupa was also weighed and its sex determined. The fibre content (% Modified Acid Detergent Fibre; Clancey & Wilson 1986) of the faeces from the fifth instar caterpillars was measured.

Each pupa was maintained in moistened Vermiculite in a 50-ml plastic tube, closed with a cotton-wool ball, at a constant temperature of 10 °C. On emerging in the autumn, each adult female was mated with a male from the same treatment and allowed to lay eggs, which were counted and weighed. After dying, each female was dissected and any unlaid eggs counted. Losses as pupae and about 50% of pupae being female resulted in only 16 females producing eggs in the Solardome treatments. There were insufficient females from the outdoor treatment for comparison.


These experiments examined the interaction between tree and caterpillar when both received the same treatment. The on-tree experiment was more natural, but the mass of leaf eaten and the mass of individual caterpillars could not be monitored. The caged experiment allowed this closer examination.

Caged experiment

In 1995, caterpillars and the trees providing the leaves fed to them were reared in the same Solardome. The experimental procedures were as for the 1994 experiment, except that individual caterpillars were kept in 50-mm high by 12-mm diameter glass tubes, containing a strip of moistened filter paper and closed with a cotton-wool ball. In this ‘caged’ experiment, as previously, a new leaf, leaf remains and faeces were weighed at 2-day intervals and the current instar recorded; pupal mass was recorded at the end of the experiment. The leaves were from a group of trees that were 3 years old and had been exposed to the various treatments since January 1994. The duration of leaf development, from budburst to full-size, but not toughened, was also determined.

On-tree experiment

At the start of this experiment in 1995, newly hatched caterpillars from one mother were divided among the 10 tree groups and fed, in Petri dishes, with leaves from the trees in their group. On reaching instar 3, 10 caterpillars were transferred to each of three sleeved trees in each of the 10 groups. The 0·15-mm mesh sleeving covered the entire tree and surface of the soil, above which was a 250-mm layer of Vermiculite. In this experiment, the caterpillars were left to feed undisturbed, and the resultant pupae were retrieved and weighed.


ANOVA, in the MINITAB statistics package, was used to compare the treatment effects. In the experiment conducted in a constant environment chamber, individual values were used as the basis of the comparisons. For the experiments in the Solardomes, means were used to avoid pseudoreplication. Temperature comparisons were either between the elevated and ambient (control) dome treatments or between the ambient dome treatment and the outdoor treatment. The effects of CO2 treatments can only be compared among the Solardomes.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References


Nutrient quality of leaves fed to caterpillars

The effect of elevated temperature and CO2 treatments on the nutrient quality of oak leaves during growth, the time at which they were fed to caterpillars, has been reported by Dury et al. (1998) and is summarized in Table 1. At elevated temperature, total nitrogen was reduced, condensed tannins accumulated faster and the leaf became tougher. The increased fibre was shown indirectly by its increase in caterpillar faeces (Table 2). In elevated CO2, total nitrogen was again reduced, total phenolics were increased and the leaf was softer than normal. The duration of leaf development was reduced at elevated temperature, but elevated CO2 had no effect (Table 2).

Table 1.  . The effect of elevated temperature and CO2 treatments on the nutrient quality of oak leaves during leaf growth, the time at which they are eaten by Winter Moth larvae (Dury et al. 1998) (leaf toughness was measured outside this period) Thumbnail image of
Table 2.  . Comparison (ANOVA) of the duration of leaf development and fibre content of leaves grown in contrasting temperature and CO2 treatments. Leaf development is from budburst to full-size leaf (but not toughened); fibre content (% MADF, Modified Acid Detergent Fibre) is in the faeces of fifth instar caterpillars (as an indication of leaf fibre). [] = probability for elevated and ambient temperature comparison only.= SD of mean Thumbnail image of
Effects on caterpillar growth and development

Caterpillars fed leaves grown at elevated temperature ate the same total mass of food and produced the same total mass of faeces as those fed on ambient temperature leaves, although a lesser mass was assimilated (Table 3). The masses of instar 5 larvae were not significantly different between temperature treatments, although they differed from those fed leaves from the outdoor treatment. However, the resultant pupae were lighter when fed on elevated temperature leaves and feeding duration was slightly less. Also, significantly fewer and lighter eggs were laid.

Table 3.  . Comparison (ANOVA) of the effect on caterpillar development and fecundity in a constant environment when fed oak leaves grown at ambient or elevated temperature and CO2, or outdoors. Value = mean = SD of mean [] = probability for the elevated and ambient temperature comparison only. Egg data are means for 16 females. Thumbnail image of

More food was eaten and more faeces produced when caterpillars were fed on leaves from the elevated CO2 treatments than from the ambient treatments (Table 3). However, in this case, the mass assimilated and the pupal masses were the same at both CO2 levels and the duration of feeding was unaffected. There was no effect on egg production or mass.


Caged experiment

No difference in pupal mass was found between the ambient and elevated temperature or CO2 treatments when caterpillars, in cages, and trees were maintained under the same conditions (Table 4). There was, however, a reduction in the duration of feeding at elevated in comparison with ambient temperature, but no difference between CO2 levels.

Table 4.  . Comparison (ANOVA) of pupal mass of caterpillars reared under the same temperature and CO2 treatments as the host plant: (a) in cages and (b) on the trees. In (a) insufficient larvae survived in the outdoor treatment for comparison with the ambient temperature treatment. = SD of mean Thumbnail image of
On-tree experiment

Because caterpillars were allowed to feed ‘naturally’ on the trees, final pupal mass was the only parameter which could be measured. There was no significant difference for either temperature or CO2 comparisons (Table 4). There was also no significant difference in pupal mass when fed in the ambient domes or outdoors.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Plant nitrogen levels have a major influence on insect herbivores (Mattson 1980), although individual benefits may be lost at population level because of similar benefits to predators and parasitoids (Kytö, Niemelä & Larsson 1996). Following successful synchrony between budburst and Winter Moth egg hatch, which is unaffected by elevated temperature or CO2 (Buse & Good 1996), caterpillars must feed before foliage nitrogen declines or leaves toughen, both accelerated by elevated temperature (Tables 1 and 2). Eating elevated temperature leaves resulted in reduced assimilation, reduced instar 5 and pupal masses and fewer, lighter eggs (Table 3), although the mass consumed was unaffected. As the duration of feeding remains virtually the same, increased leaf fibre appears to prevent increased feeding to augment nitrogen input; larvae are feeding too early during leaf development (Dury et al. 1998) for the condensed tannins of older leaves (Feeny 1970) to inhibit their growth. Species that do feed longer to compensate for decreased nitrogen (Slansky 1993) may become more vulnerable to natural enemies (Hochuli 1996). Thus, as in gypsy moth (Rossiter, Coxfoster & Briggs 1993), feeding on elevated temperature leaves reduces the mother’s performance and, consequently, the fitness of her offspring and local population dynamics.

In contrast, reduced leaf nitrogen in the elevated CO2 leaves (Table 1) had no effect on the normal masses of instar 5 larva and the pupa or the number and mass of the eggs (Table 3); the less fibrous leaves allowed more food to be ingested and more faeces produced, enabling ‘normal’ amounts of nitrogen to be obtained. In general, the effect of CO2 treatment on foliar quality varies among plant species (Woodward 1992) and is particularly dependent on soil nutrient status (Lloyd & Farquhar 1996). Similarly, the response of insects to enhanced CO2 host plants is variable. For example, on high CO2 oak (Quercus rubra) the performance of Gypsy Moth (Lymantria dispar) is improved and that of Forest Tent Caterpillar (Malacosoma disstria) is unaffected, whereas on maple (Acer saccharum), the former is unaffected, but the latter grows less (Lindroth, Kinney & Platz 1993). Similarly, birch species affect the outcome of the influence of elevated CO2 on larval performance (Traw, Lindroth & Bazzaz 1996).

Neither elevated temperature nor elevated CO2 had an effect on final pupal mass when caterpillars were fed under the same conditions as the host plants (Table 4). However, the duration of feeding and leaf development (Table 2) decreased at elevated temperature. This agrees with the generalization that above or below an optimal temperature performance value (and thus the duration of feeding) declines, but assimilation efficiency remains the same (Scriber & Slansky 1981). Similarly, despite the reduced nitrogen content of high CO2 leaves, elevated CO2 had no effect. This response varies with both insect and plant species and plant nutrition levels. For example, the noctuid Trichoplusia ni (Hubner) had reduced pupal mass at low tree fertilization rates, irrespective of CO2 level, whereas, at high fertilization rates, pupal mass was less at elevated than ambient CO2 (Osbrink et al. 1987). As in our Winter Moth study, Kinney et al. (1997) found that Gypsy Moth fed on aspen compensated for reduced foliar nitrogen by increased consumption, thus maintaining final pupal mass. However, when fed maple, final mass decreased. In our study, contrary to the results of feeding treated leaves to caterpillars at constant temperature, neither elevated temperature nor CO2 had an effect on development or fecundity when Winter Moth and its tree host were reared together.

The difference in the effects of elevated temperature between the two experiments is due to differences in synchrony between the development of larvae and leaves, which were concurrent only when both were in the fluctuating Solardome temperatures. Then, maximum caterpillar food and, consequently, nitrogen intake was at the equivalent stage of leaf development whether at 25 days at elevated temperature or 40 days at ambient temperature. In contrast, maximum larval intake at a constant 15 °C (at about 20 days) coincided with greater nitrogen levels when fed from ambient than from elevated temperature treatments. Thus, a difference in pupal mass occurred. Carbon dioxide levels, however, did not affect synchrony between leaf and caterpillar development and, because of compensatory feeding, pupal mass, and thus fecundity, were also unaffected.

By hatching as oak buds open, Winter Moth caterpillars feed on developing leaves with the highest nitrogen content (Slansky & Wheeler 1992; Dury et al. 1998), required for protein building, and avoid the later increase in tannins and reduction in nutrients (Feeny 1970). It also allows the free amino acids available during leaf flushing to be accessible to these very young chewing insects that might have difficulty masticating or digesting more mature plant tissues (Cockfield 1988). Felton (1996) considered that adaptations, in this case synchrony of budburst and egg hatch, to optimize the acquisition of amino acids would be favoured. The high water content of early leaves is also beneficial for larval growth (Scriber 1984). We concluded that, because the duration of both larval and leaf development decreased equally at higher temperatures, the relationship between the caterpillars and the leaves was unlikely to be affected by climate change. However, the balance with factors unrelated to tree development, such as predators and parasites, might be affected (Feeny 1970). For example, whereas elevated temperature shortens the larval stage (Table 4), the duration of the nesting cycle of the Great Tit, which feeds caterpillars to its young, is relatively inflexible once laying has commenced (Noordwijk, McCleery & Perrins 1995). The reduced availability of caterpillars at higher temperatures results in smaller fledglings and poorer survival (Perrins 1991). This suggests that the effect of climatic change on Winter Moth development will have an adverse effect on tit populations.

The hypothesis that elevated temperature has no effect on the relationship between leaf nutritional quality and Winter Moth larval development is thus supported by the data. Although several studies show that caterpillars eating young leaves achieve greater body mass than those eating mature leaves (e.g. Schweitzer 1979), one of the few studies including the interaction of temperature (Stamp 1993) indicates that this response varies with the temperature at which the caterpillars are reared (Stamp & Bowers 1990). Our Solardome facilities allowed us to compare the effect of ‘real’, fluctuating ambient and elevated temperatures on the interaction among temperature, plant growth and caterpillar development as it evolved in spring. The differing results for caterpillars reared at constant and ‘normal’ temperatures demonstrate the importance of our approach when examining a univoltine species developing in tandem with its leaf food. The hypothesis that elevated CO2 would have an effect is not supported. We found no effect on pupal mass; a few studies show this is reduced, although most have been inconclusive (Watt et al. 1995). No other studies have examined how changes in plant phenological development at elevated CO2 affect the performance of insect herbivores (Watt et al. 1995). There was no evidence of a combined effect of temperature and CO2 which differed from the separate effects.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We thank our colleagues at the Institute of Terrestrial Ecology: C. R. Rafarel at Bangor for maintaining the Solardomes and controlled environment cabinets, and T. H. Sparks at Monks Wood for statistical advice and assistance. We also thank L. Houldcroft for assistance with the 1995 experiment.

This study is part of a project funded by the Natural Environment Research Council under its Terrestrial Initiative in Global Environmental Research (TIGER) programme (TIGER IV.2b: Species Interactions).


  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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