Intraspecific variation in aspen phytochemistry: effects on performance of gypsy moths and forest tent caterpillars

Individual quaking aspen trees vary greatly in foliar chemistry and susceptibility to defoliation by gypsy moths and forest tent caterpillars. To relate performance of these insects to differences in foliar chemistry, we reared larvac from egg hatch to pupation on leaves from different aspen trees and analyzed leaf samples for water, nitrogen, total nonstructural carbohydrates, phenolic glycosides, and condensed tannins. Larval performance varied markedly among trees. Pupal weights of both species were strongly and inversely related to phenolic glycoside concentrations. In addition, gypsy moth performance was positively related to condensed tannin concentrations, whereas forest tent caterpillar pupal weights were positively associated with leaf nitrogen concentrations. A subsequent study with larvae fed aspen leaves supplemented with the phenolic glycoside tremulacin confirmed that the compound reduces larval performance. Larvae exhibited increased stadium durations and decreased relative growth rates and food conversion efficiencies as dietary levels of tremulacin increased. Differences in performance were more pronounced for gypsy moths than for forest tent caterpillars. These results suggest that intraspecific variation in defensive chemistry may strongly mediate interactions between aspen, gypsy moths and forest tent caterpillars in the Great Lakes region, and may account for differential defoliation of aspen by these two insect species.     

Effects of phytochemical variation in quaking aspen Populus tremuloides clones on gypsy moth Lymantria dispar performance in the field and laboratory

1. This study investigated how phytochemical variation among clones of quaking aspen Populus tremuloides, growing in a common habitat, affects the growth and fecundity of a model herbivore. 2. Gypsy moth Lymantria dispar larvae were reared from egg hatch to pupation on 10 aspen clones in the field or on excised foliage in the laboratory. Foliage was collected from each clone, and concentrations of phenolic glycosides, condensed tannins, nitrogen, and water were determined. 3. Herbivore fitness parameters and aspen phytochemical concentrations varied significantly among clones. In both the field and laboratory, larvae reared on clones containing high concentrations of phenolic glycosides exhibited prolonged developmental times and reduced pupal weights and fecundity. Herbivore performance parameters were also related positively to foliar nitrogen concentrations in the laboratory. Food consumption, but neither growth nor reproductive parameters, were related positively to condensed tannin concentrations. 4. In this study, foliar concentrations of phenolic glycosides were implicated as a significant determinant of food quality for gypsy moths, consistent with results of previous laboratory experiments. Additionally, this study documents a case in which host plant variation at a local level influences the performance and possibly the distribution and abundance of an important herbivore.     

Plant-associated bacteria degrade defense chemicals and reduce their adverse effects on an insect defoliator

Phytophagous insects must contend with numerous secondary defense compounds that can adversely affect their growth and development. The gypsy moth (Lymantria dispar) is a polyphagous herbivore that encounters an extensive range of hosts and chemicals. We used this folivore and a primary component of aspen chemical defenses, namely, phenolic glycosides, to investigate if bacteria detoxify phytochemicals and benefit larvae. We conducted insect bioassays using bacteria enriched from environmental samples, analyses of the microbial community in the midguts of bioassay larvae, and in vitro phenolic glycoside metabolism assays. Inoculation with bacteria enhanced larval growth in the presence, but not absence, of phenolic glycosides in the artificial diet. This effect of bacteria on growth was observed only in larvae administered bacteria from aspen foliage. The resulting midgut community composition varied among the bacterial treatments. When phenolic glycosides were included in diet, the composition of midguts in larvae fed aspen bacteria was significantly altered. Phenolic glycosides increased population responses by bacteria that we found able to metabolize these compounds in liquid growth cultures. Several aspects of these results suggest that vectoring or pairwise symbiosis models are inadequate for understanding microbial mediation of plant–herbivore interactions in some systems. First, bacteria that most benefitted larvae were initially foliar residents, suggesting that toxin-degrading abilities of phyllosphere inhabitants indirectly benefit herbivores upon ingestion. Second, assays with single bacteria did not confer the benefits to larvae obtained with consortia, suggesting multi- and inter-microbial interactions are also involved. Our results show that bacteria mediate insect interactions with plant defenses but that these interactions are community specific and highly complex.     

Genotype and environment determine allocation to and costs of resistance in quaking aspen

Although genetic variability and resource availability both influence plant chemical composition, little is known about how these factors interact to modulate costs of resistance, expressed as negative correlations between growth and defense. We evaluated genotype × environment effects on foliar chemistry and growth of quaking aspen (Populus tremuloides) by growing multiple aspen genotypes under variable conditions of light and soil nutrient availability in a common garden. Foliage was analyzed for levels of nitrogen, phenolic glycosides and condensed tannins. Bioassays of leaf quality were conducted with fourth-stadium gypsy moth (Lymantria dispar) larvae. Results revealed strong effects of plant genotype, light availability and nutrient availability; the importance of each factor depended upon compound type. For example, tannin concentrations differed little among genotypes and across nutrient regimes under low light conditions, but markedly so under high light conditions. Phenolic glycoside concentrations, in contrast, were largely determined by genotype. Variation in phenolic glycoside concentrations among genotypes was the most important factor affecting gypsy moth performance. Gypsy moth biomass and development time were negatively and positively correlated, respectively, with phenolic glycoside levels. Allocation to phenolic glycosides appeared to be costly in terms of growth, but only under resource-limiting conditions. Context-dependent trade-offs help to explain why costs of allocation to resistance are often difficult to demonstrate.     

CO2-mediated changes in aspen chemistry: effects on gypsy moth performance and susceptibility to virus

We investigated the effects of long-term CO₂ enrichment on foliar chemistry of quaking aspen ( Populus tremuloides ) and the consequences of chemical changes for performance of the gypsy moth ( Lymantria dispar ) and susceptibility of the gypsy moth to a nucleopolyhedrosis virus (NPV). Foliage was collected from outdoor open-top chambers and fed to insects in a quarantine rearing facility. Under enriched CO₂, levels of leaf nitrogen declined marginally, levels of starch and phenolic glycosides did not change, and levels of condensed tannins increased. Long-term bioassays revealed reduced growth (especially females), prolonged development and increased consumption in larvae fed high-CO₂ foliage but no significant differences in final pupal weights or female fecundity. Short-term bioassays showed weaker, and sex-specific, effects of CO₂ treatment on larval performance. Correlation analyses revealed strong, negative associations between insect performance and phenolic glycoside concentrations, independent of CO₂ treatment. Larval susceptibility to NPV did not differ between CO₂ treatments, suggesting that effects of this natural enemy on gypsy moths are buffered from CO₂-induced changes in foliar chemistry. Our results emphasize that the impact of enriched CO₂ on plant–insect interactions will be determined not only by how concentrations of plant compounds are altered, but also by the relevance of particular compounds for insect fitness. This work also underscores the need for studies of genetic variation in plant responses to enriched CO₂ and long-term population-level responses of insects to CO₂-induced changes in host quality.     

Increased mortality of gypsy moth Lymantria dispar (L.) (Lepidoptera: Lymantriidae) exposed to gypsy moth nuclear polyhedrosis virus in combination with the phenolic gycoside salicin

Second instar gypsy moth, Lymantria dispar (L.) (Lepidoptera: Lymantriidae), larvae suffered significantly greater mortality from aerially applied gypsy moth nuclear polyhedrosis virus (Gypchek) when the virus was consumed on quaking aspen, Populus tremuloides Michx., versus red oak, Quercus spp. L., foliage. Laboratory assays in which various doses of Gypchek and salicin (a phenolic glycoside present in aspen foliage) were tested in combination demonstrated that salicin significantly increased total larval mortality and lowered the LD50 estimates (dose of Gypchek that resulted in 50% population mortality) for the virus, although not significantly. While salicin did not impact larval survival in the absence of Gypcek, it did act to significantly deter feeding when it was present in high concentrations (up to 5.0%) within the treatment formulations. The enhanced activity of Gypchek in the presence of salicin is similar to prior reports of enhanced activity of the bacterial pathogen Bacillus thuringiensis when consumed concurrently with phenolic glycosides commonly present in aspen foliage. The enhancement of viral activity is in contrast to the inhibitory effects on the virus reported for another common group of phenolic compounds, tannins.     

Metabolism of poplar salicinoids by the generalist herbivore Lymantria dispar (Lepidoptera)

The survival of insect herbivores on chemically defended plants may often depend on their ability to metabolize these defense compounds. However, only little knowledge is available on how insects actually process most plant defense compounds. We investigated the metabolism of salicinoids, a major group of phenolic glycosides in poplar and willow species, by a generalist herbivore, the gypsy moth (Lymantria dispar). Seven salicinoid metabolites identified in gypsy moth caterpillar feces were mostly conjugates with glucose, cysteine or glycine. Two of the glucosides were phosphorylated, a feature not previously reported for insect metabolites of plant defense compounds. The origins of these metabolites were traced to specific moieties of three major poplar salicinoids ingested, salicin, salicortin and tremulacin. Based on the observed metabolite patterns we were able to deduce the initial steps of salicinoid breakdown in L. dispar guts, which involves cleavage of ester bonds. The conjugated molecules were effectively eliminated within 24 h after ingestion. Some of the initial breakdown products (salicin and catechol) demonstrated negative effects on insect growth and survival in bioassays on artificial diets. Gypsy moth caterpillars with prior feeding experience on salicinoid-containing poplar foliage converted salicinoids to the identified metabolites more efficiently than caterpillars pre-fed an artificial diet. The majority of the metabolites we identified were also produced by other common poplar-feeding insects. The conversion of plant defenses like salicinoids to a variety of water-soluble sugar, phosphate and amino acid conjugates and their subsequent excretion fits the general detoxification strategy found in insect herbivores and other animals.     

Compound effects of induced plant responses on insect herbivores and parasitoids: implications for tritrophic interactions

1. Induced plant responses can affect herbivores either directly, by reducing herbivore development, or indirectly, by affecting the performance of natural enemies. Both the direct and indirect impacts of induction on herbivore and parasitoid success were evaluated in a common experimental system, using clonal poplar trees Populus nigra (Salicales: Salicaceae), the gypsy moth Lymantria dispar (L.) (Lepidoptera: Lymantriidae), and the gregarious parasitoid Glyptapanteles flavicoxis (Marsh) (Hymenoptera: Braconidae). 2. Female parasitoids were attracted to leaf odours from both damaged and undamaged trees, however herbivore‐damaged leaves were three times more attractive to wasps than undamaged leaves. Parasitoids were also attracted to herbivore larvae reared on foliage and to larval frass, but they were not attracted to larvae reared on artificial diet. 3. Prior gypsy moth feeding elicited a systemic plant response that retarded the growth rate, feeding, and survival of gypsy moth larvae, however induction also reduced the developmental success of the parasitoid. 4. The mean number of parasitoid progeny emerging from hosts fed foliage from induced trees was 40% less than from uninduced trees. In addition, the proportion of parasitised larvae that survived long enough to issue any parasitoids was lower on foliage from induced trees. 5. A conceptual and analytical model is provided to describe the net impacts of induced plant responses on parasitoids, and implications for tritrophic interactions and biological control of insect pests are discussed.     

Effects of genotype and nutrient availability on phytochemistry of trembling aspen (Populus tremuloides Michx.) during leaf senescence

We documented temporal patterns in phytochemical composition of Populus tremuloides Michx. during leaf senescence, and the influence of genotype and soil nutrient availability on such patterns. Levels of foliar nitrogen, carbohydrates, phenolic glycosides and condensed tannins were quantified for four aspen genotypes grown in a common garden, with low and high levels of soil nutrients. Levels of all compounds tended to decline over time, although the magnitude of change was influenced by plant genotype and nutrient availability. Genetic variation in concentrations of phytochemicals was much greater for phenolic glycosides and tannins than for nitrogen and carbohydrates, and these phenolic signatures generally persisted through leaf abscission. Our results suggest that genotypic and nutrient effects on patterns of chemical change during senescence will likely influence the performance of late-season herbivores on aspen. Moreover, nutrient and especially genotypic variation in phytochemistry of abscised leaves is likely to affect litter decomposition rates.     

Biochemical ecology of the forest tent caterpillar: responses to dietary protein and phenolic glycosides

Summary Interactions between quaking aspen (Populus tremuloides) and the forest tent caterpillar (Malacosoma disstria) are likely to be influenced by leaf protein and phenolic glycoside levels, and insect detoxication activity. We investigated the direct and interactive effects of dietary protein and phenolic glycosides on larval performance and midgut enzyme activity of forest tent caterpillars. We conducted bioassays with six artificial diets, using both first and fourth stadium larvae. Four of the diets comprised a 2×2 factorial design-two levels of protein, each with and without phenolic glycosides. Additionally, we assayed high protein diets containing S,S,S-tributylphosphorotrithioate (DEF, an esterase inhibitor) and DEF plus phenolic glycosides. Enzyme solutions were prepared from midguts of sixth instars and assayed for -glucosidase, esterase and glutathione transferase activities. First instar mortality and development times were higher for larvae on diets low in protein or containing phenolic glycosides. Effects of phenolic glycosides were especially pronounced at low protein levels and when administered with DEF. Fourth instar development times were prolonged, and growth rates reduced, in response to consumption of low protein diets. Effects of phenolic glycosides on growth were less pronounced, although the effect for larvae on the low protein diet was nearly significant. Activity of each of the enzyme systems was reduced in larvae reared on low protein diets, and esterase activity was induced in larvae fed phenolic glycosides. Our results suggest that larval performance may be strongly affected by levels of protein and phenolic glycosides commonly occurring in aspen foliage, and that these factors may play a role in differential defoliation of aspen by forest tent caterpillars.     

Effect of nitrogen fertilization upon the secondary chemistry and nutritional value of quaking aspen (Populus tremuloides Michx.) leaves for the large aspen tortrix (Choristoneura conflictana (Walker))

Summary We investigated the effects of nitrogen fertilization upon the concentrations of nitrogen, condensed tannin and phenolic glycosides of young quaking aspen (Populus tremuloides) leaves and the quality of these leaves as food for larvae of the large aspen tortrix (Choristoneura conflictana), a Lepidopteran that periodically defoliates quaking aspen growing in North America. Nitrogen fertilization resulted in decreased concentrations of condensed tannin and phenolic glycosides in aspen leaves and an increase in their nitrogen concentration and value as food for the large aspen tortrix. These results indicate that plant carbon/nutrient balance influences the quality of aspen leaves as food for the large aspen tortrix in two ways, by increasing the concentrations of positive factors (e.g. nitrogen) and decreasing the concentrations of negative factors (eg. carbon-based secondary metabolites) in leaves. Addition of purified aspen leaf condensed tannin and a methanol extract of young aspen leaves that contained condensed tannin and phenolic glycosides to artificial diets at high and low levels of dietary nitrogen supported this hypothesis. Increasing dietary nitrogen increased larval growth whereas increasing the concentrations of condensed tannin and phenolic glycosides decreased growth. Additionally, the methanol extract prevented pupation. These results indicate that future studies of woody plant/insect defoliator interactions must consider plant carbon/nutrient balance as a potentially important control over the nutritional value of foliage for insect herbivores.     

Clonal variation in foliar chemistry of aspen: effects on gypsy moths and forest tent caterpillars

Quaking aspen (Populus tremuloides) exhibits striking intraspecific variation in concentrations of phenolic glycosides, compounds that play important roles in mediating interactions with herbivorous insects. This research was conducted to assess the contribution of genetic variation to overall phenotypic variation in aspen chemistry and interactions with gypsy moths (Lymantria dispar) and forest tent caterpillars (Malacosoma disstria). Thirteen aspen clones were propagated from field-collected root material. Insect performance assays, measuring survival, development, growth, and food utilization indices, were conducted with second and/or fourth instars. Leaf samples were assayed for water, nitrogen, total nonstructural carbohydrates, condensed tannins, and phenolic glycosides. Results showed substantial among-clone variation in the performance of both insect species. Chemical analyses revealed significant among-clone variation in all foliar constituents and that variation in allelochemical contents differed more than variation in primary metabolites. Regression analyses indicated that phenolic glycosides were the dominant factor responsible for among-clone variation in insect performance. We also found significant genetic trade-offs between growth and defense among aspen clones. Our results suggest that genetic factors are likely responsible for much of the tremendous phenotypic variation in secondary chemistry exhibited by aspen, and that the genetic structure of aspen populations may play important roles in the evolution of interactions with phytophagous insects. Received: 14 May 1996 / Accepted: 29 January 1997     

Long-term effects of defoliation on quaking aspen in relation to genotype and nutrient availability: plant growth,phytochemistry and insect performance

This research tested the long-term effects of defoliation on aspen chemistry and growth in relation to genotype and nutrient availability. We grew saplings of four aspen genotypes in a common garden under two conditions of nutrient availability, and subsequently subjected them to two levels of artificial defoliation. Artificial defoliation suppressed plant growth, and saplings of the four genotypes did not show evidence of genetic variation in tolerance to defoliation. Phenolic glycoside concentrations did not respond to defoliation, but were influenced by genotype and nutrient availability. Condensed tannins responded to defoliation and varied among genotypes. Although defoliation affected condensed tannins, plant quality was not altered in a manner important for gypsy moth performance. Regression analyses suggested that phenolic glycoside concentrations accounted for most of the variation in insect performance. The lack of a strong response important for herbivores was surprising given the severity of the defoliation treatment (nearly 100% of leaf area was removed). In this study, plant genotype was of primary importance, nutrient availability was of secondary importance and long-term induced responses were unimportant as determinants of insect performance.     

Potential interactions between invasive woody shrubs and the gypsy moth (Lymantria dispar), an invasive insect herbivore

As the range of the invasive and highly polyphagous gypsy moth (Lymantria dispar) expands, it increasingly overlaps with forest areas that have been subject to invasion by non-native shrubs. We explored the potential for interactions between these co-occurring invasions through a gypsy moth feeding trial using the following three highly invasive, exotic shrubs: honeysuckle (Lonicera maackii), privet (Ligustrum sinense) and burning bush (Euonymus alatus). We compared these with two native shrubs: spicebush (Lindera benzoin) and pawpaw (Asimina triloba). We fed gypsy moth caterpillars foliage exclusively from one of the five shrubs and measured their relative consumptive rate (RCR), relative growth rate (RGR), and development time (DT). The RCR of gypsy moth was strongly influenced by the species of foliage (F = 31.9; P < 0.0001) with little or no consumption of honeysuckle and privet. Caterpillar RGR was influenced by the shrub species (F = 66.2; P < 0.0001), and those caterpillars fed spicebush, honeysuckle or privet lost weight over the course of the assay. Caterpillar DT was also significantly (F = 11.79, P < 0.0001) influenced by the shrub species and those fed honeysuckle, privet and spicebush died prior to molting. Overall, our data suggest that honeysuckle, privet, and spicebush could benefit (indirectly) from the invasion of gypsy moth, while burning bush and pawpaw could be negatively impacted due to direct effects (herbivory). Similarly, invading gypsy moth populations could be sustained on a shrub layer of burning bush and pawpaw in the event of canopy defoliation. Further field and laboratory analysis is needed to clarify herbivore resistance of invasive shrubs, and to investigate the potential interactions among co-occurring insect and plant invasions.     

Tracing the history of plant traits under domestication in cranberries: potential consequences on anti-herbivore defences

The process of selecting certain desirable traits for plant breeding may compromise other potentially important traits, such as defences against pests; however, specific phenotypic changes occurring over the course of domestication are unknown for most domesticated plants. Cranberry (Vaccinium macrocarpon) offers a unique opportunity to study such changes: its domestication occurred recently, and we have access to the wild ancestors and intermediate varieties used in past crosses. In order to investigate whether breeding for increased yield and fruit quality traits may indirectly affect anti-herbivore defences, the chemical defences have been examined of five related cranberry varieties that span the history of domestication against a common folivore, the gypsy moth (Lymantria dispar). Direct defences were assessed by measuring the performance of gypsy moth caterpillars and levels of phenolic compounds in leaves, and indirect defences by assaying induced leaf volatile emissions. Our results suggest that breeding in cranberry has compromised plant defences: caterpillars performed best on the derived NJS98-23 (the highest-yielding variety) and its parent Ben Lear. Moreover, NJS98-23 showed reduced induction of volatile sesquiterpenes, and had lower concentrations of the defence-related hormone cis-jasmonic acid (JA) than ancestral varieties. However, induced direct defences were not obviously affected by breeding, as exogenous JA applications reduced caterpillar growth and increased the amounts of phenolics independent of variety. Our results suggest that compromised chemical defences in high-yielding cranberry varieties may lead to greater herbivore damage which, in turn, may require more intensive pesticide control measures. This finding should inform the direction of future breeding programmes.     

Herbivory meets fungivory: insect herbivores feed on plant pathogenic fungi for their own benefit

Plants are regularly colonised by fungi and bacteria, but plant‐inhabiting microbes are rarely considered in studies on plant–herbivore interactions. Here we show that young gypsy moth (Lymantria dispar) caterpillars prefer to feed on black poplar (Populus nigra) foliage infected by the rust fungus Melampsora larici‐populina instead of uninfected control foliage, and selectively consume fungal spores. This consumption, also observed in a related lepidopteran species, is stimulated by the sugar alcohol mannitol, found in much higher concentration in fungal tissue and infected leaves than uninfected plant foliage. Gypsy moth larvae developed more rapidly on rust‐infected leaves, which cannot be attributed to mannitol but rather to greater levels of total nitrogen, essential amino acids and B vitamins in fungal tissue and fungus‐infected leaves. Herbivore consumption of fungi and other microbes may be much more widespread than commonly believed with important consequences for the ecology and evolution of plant–herbivore interactions.     

Elevated atmospheric CO2: effects on phytochemistry, insect performance and insect-parasitoid interactions

This study was conducted to examine the effects of CO₂-mediated changes in tree chemistry on the performance of the gypsy moth ((Lymantria dispar L.) and the parasitold Cotesia melanoscela (Ratz.). We used carbon-nutrient balance theory to develop hypotheses regarding changes in tree chemistry and the performance of both insects under elevated CO₂. As predicted, levels of foliar nitrogen declined and concentrations of carbon-based compounds (e.g. starch and phenolics) increased under elevated CO₂. Gypsy moth performance (e.g. growth, development) was altered by CO₂-mediated changes in foliar chemistry, but the magnitude was small and varied across tree species. Larvae feeding on high CO₂ aspen exhibited the largest reduction in performance, relative to larvae feeding on birch, oak, or maple. Parasitism by C. melanoscela significantly prolonged gypsy moth development and reduced growth rates. Overall, the effect of parasitism on gypsy moth performance did not differ between CO₂ treatments. Altered gypsy moth performance on high CO₂ foliage in turn affected parasitoid performance, but the response was variable: parasitoid mortality increased and adult female size declined slightly under high CO₂, while development time and adult male size were unaffected. Our results suggest that CO₂-induced changes in plant chemistry were buffered to the extent that effects on third trophic level interactions were weak to non-existent for the system examined in this study.     

Endogenous and induced monooxygenase activity in gypsy moth larvae feeding on natural and artificial diets

NADPH oxidase activity was measured in third to sixth instar gypsy moth larvae fed oak or pine foliage. Activity levels ranged from 400 to 1,900 pmol NADPH oxidized/min/mg microsomal protein, but enzyme activity was not correlated with host plant ingested. Similarly, activity levels in larvae fed diets containing inducers, such as the terpenoid α-pinene or pentamethylbenzene, ranged from 700 to 1,500 pmol NADPH oxidized/min/mg protein, levels that were comparable to those measured for larvae fed control diets. O-demethylase activity in older instar gypsy moth larvae fed pine averaged 109 pmol p-nitrophenol/min/mg protein, and activity levels in those fed diet containing α-pinene ranged from 22 to 55 pmol/min/mg protein. Although statistically significant, these induced O-demethylase levels are well below those observed for Heliothis zea larvae. Our findings indicate that monooxygenases play a minor, if any, role in the ability of later instar gypsy moth larvae to develop successfully on pine foliage.     

Foliage‐age mixing within balsam fir increases the fitness of a generalist caterpillar

1. Manipulative field studies were carried out to evaluate the foliage age preference–performance relationship for an extreme generalist herbivore, the whitemarked tussock moth (Orygia leucostigma Smith) (Lepidoptera: Lymantriidae), within balsam fir [Abies balsamea (L.) Mill]. 2. Field surveys indicated that early instar caterpillars fed almost exclusively on young (i.e. current‐year) foliage, whereas late instars caterpillars fed on both young and mature (i.e. 1‐ and 2‐year‐old) foliage. 3. Survival of early instar caterpillars was highest in treatments where current‐year and/or 1‐year old foliage were available, but decreased significantly on older foliage. In contrast, late instar caterpillars had the highest survival when allowed to feed on all age classes of foliage, whereas potential fecundity was highest for late instars that fed on young foliage. 4. Overall, caterpillars had 32–65% higher fitness when able to feed on all rather than just one age class of foliage. 5. These results support both the ‘complementary diet' hypothesis, which states that dietary mixing of different‐aged foliage can increase nutrient uptake and/or dilute harmful secondary plant chemicals, and the ‘ontogeny’ hypothesis, which attributes changes in diet to changes in the nutritional needs and/or tolerance to plant defences of juvenile insects as they develop.     

Facilitation between invasive herbivores: hemlock woolly adelgid increases gypsy moth preference for and performance on eastern hemlock

1. Interactions between invertebrate herbivores with different feeding modes are common on long-lived woody plants. In cases where one herbivore facilitates the success of another, the consequences for their shared host plant may be severe. Eastern hemlock (Tsuga canadensis), a canopy-dominant conifer native to the eastern U.S., is currently threatened with extirpation by the invasive stylet-feeding hemlock woolly adelgid (Adelges tsugae). The effect of adelgid on invasive hemlock-feeding folivores remains unknown. 2. This study evaluated the impact of feeding by hemlock woolly adelgid on gypsy moth (Lymantria dispar) larval preference for, and performance on, eastern hemlock. To assess preference, 245 field-grown hemlocks were surveyed for gypsy moth herbivory damage and laboratory paired-choice bioassays were conducted. To assess performance, gypsy moth larvae were reared to pupation on adelgid-infested or uninfested hemlock foliage, and pupal weight, proportional weight gain, and larval period were analysed. 3. Adelgid-infested hemlocks experienced more gypsy moth herbivory than did uninfested control trees, and laboratory tests confirmed that gypsy moth larvae preferentially feed on adelgid-infested hemlock foliage. Gypsy moth larvae reared to pupation on adelgid-infested foliage gained more weight than larvae reared on uninfested control foliage. 4. These results suggest that the synergistic effect of adelgid and gypsy moth poses an additional threat to eastern hemlock that may increase extirpation risk and ecological impact throughout most of its range.