Adaptation of an outbreaking insect defoliator to chronic nutritional stress.

During insect outbreaks, the high number of individuals feeding on its host plant causes a depletion of the food source. Reduced availability and decreased quality of nutrients negatively influence life-history traits of insects driving them to develop adaptive strategies to persist in the environment. In a laboratory experiment with three repetitions, we tested the effect of chronic nutritional stress on spruce budworm performance during three generations to determine the adaptive strategies employed by the insect to deal with a selection pressure produced by low-quality diet. Our results show that all tested life-history traits (mortality, developmental time, pupal mass, growth rate and female fecundity) but female fertility were negatively influenced by the low-quality diet simulating food depletion during outbreak conditions. However, especially females in the third generation under chronic nutritional stress show an adaptive response in life-history traits when compared to those reared only one generation on low-quality diet. Larval developmental time significantly decreased and pupal mass, growth rate and fecundity significantly increased. The study demonstrates the capacity of spruce budworm to react to chronic nutritional stress with adaptations that may be caused by epigenetic parental effects. This information can help to understand the course of an outbreak especially at peak densities and during the collapse.

Carry-over effect of host nutritional quality on performance of spruce budworm progeny.

The effect of host nutritional quality on spruce budworm (Choristoneura fumiferana (Clemens)) parental and offspring performance was studied using field and laboratory rearing experiments, and foliar chemical analyses. Foliage of balsam fir (Abies balsamea (L.) Mill.), white spruce (Picea glauca (Moench) Voss) and black spruce (P. mariana (Mill.) BSP) was used to rear the parental generation in the field, whereas an artificial diet was used to rear the progeny under laboratory conditions. Important differences in the food quality were provided by the three hosts. Black spruce foliage had higher concentrations of certain monoterpene deterrents and total phenolics, together with stronger seasonal declines in nutrients such as N, P and Mg, compared with the other hosts. We hypothesise that this trend may be related to poor performance and survival of the progeny. Laboratory rearing showed that progeny of parents that fed on black spruce exhibited longer developmental times and greater mortality, and had lower pupal mass than progeny of parents fed on the other hosts. Further, artificial food-fed progeny of insects reared on black spruce reached sixth-instar later, with lower mass, and exhibited higher relative growth rate (RGR) than progeny of parents fed on the other hosts. These results suggest nutritionally-based parental effects. These results also confirmed that the quality of food consumed by the parents can influence the fitness of the next generation.

Impact of host tree on forest tent caterpillar performance and offspring overwintering mortality.

One of the most damaging insect pests in deciduous forests of North America is the forest tent caterpillar, Malacosoma disstria Hübner. It can feed on a variety of plants, but trembling aspen (Populus tremuloides Michaux) is its preferred host and sugar maple (Acer saccharum Marshall) serves as a secondary one in the northern part of its distribution. Because host plant characteristics influence insect performance and survival, we evaluated the impact of trembling aspen and sugar maple foliage on M. disstria performance. Host effects on insect cold hardiness and overwintering survival of offspring were also studied. Forest tent caterpillar reared on aspen leaves had a shorter development time, higher pupal weights and fecundity, and superior egg parameters (length and weight) compared with those reared on sugar maple leaves. Larvae from the two food treatments had low glucose levels during diapause, whereas glycerol content of insects reared on maple was significantly higher during diapause than larvae fed on aspen. Lower glycerol content may explain the higher overwinter mortality of pharate larvae from aspen-reared parents even though their supercooling points were as low as -36 degrees C. This study shows the influence of host plant on insect life history and the need to consider overwintering success and offspring performance in studies to understand and predict population growth and cycling.

Host tree age as a selective pressure leading to local adaptation of a population of a polyphagous Lepidoptera in virgin boreal forest.

We tested the hypothesis that host tree age may act as a selective factor and lead to local adaptation of the hemlock looper (Lambdina fiscellaria), a geometrid Lepidoptera that has a wide geographical distribution and has evolved in different eco-zones characterized by different levels of floristic composition, age structure and fragmentation level. Considering that hemlock looper outbreaks mainly occurred in old forests, we compared the biological performances of two populations. The first population was collected in the northern virgin boreal forest, which is dominated by mature and overmature coniferous stands that have not suffered from human disturbance. The other population was collected in the southern mixed-wood forest, which is more diversified and has been modified by forest harvesting. Larvae were reared under controlled conditions on foliage from three age classes of balsam fir trees: juvenile, mature and overmature. Although we measured significant variations of biological performances between the two populations, no significant effect of the age of the balsam fir trees could be detected for males from both populations or for females from the southern population. However, northern females were strongly affected by the age of balsam fir trees on which they fed, as their pupal weight was 12% higher and their fecundity increased by 27% on overmature trees compared with juvenile ones. These results indicate that under the same selective pressure, females adapt their strategy to maximize their fitness, and thus they appear as the driving force of evolution through the local adaptation concept. Furthermore, the two populations evolved in distinct habitats and their adaptation reflects selective pressures occurring inside their original environment. This is the first report on local adaptation of an herbivore that is mediated by host tree age. Changes in forest age structure may have a considerable impact on insect local adaptation and presumably on their population dynamics.

White pine weevil (Pissodes strobi) biological performance is unaffected by the jasmonic acid or wound-induced defense response in Norway spruce (Picea abies).

In eastern Canada, the white pine weevil (Pissodes strobi Peck) is a pest of several native pine and spruce species and of the introduced species, Norway spruce (Picea abies Karst). We evaluated the feeding activities, oviposition and rate of adult emergence of white pine weevil on field-grown Norway spruce subjected to jasmonic acid or wounding pretreatments. We also monitored the host-plant reaction to white pine weevil attack, jasmonic acid and wounding treatments by quantifying several mono- and sesquiterpenes in bark and characterizing some molecular aspects of the terpenoid response. Two cDNA sequences were identified that had a high percentage of identity with genes encoding monoterpene or sesquiterpene synthases. Both putative terpene synthase genes showed distinctive profiles in Norway spruce bark and needles following all treatments. Although the Norway spruce trees showed different physiological responses to mechanical wounding and white pine weevil attack, transcript activity of the gene encoding terpenoid synthase and consequent accumulation of terpenoid resin did not significantly affect the weevils' feeding activities, oviposition or rate of adult emergence.

Interactions among white spruce tannins, Bacillus thuringiensis subsp. kurstaki, and spruce budworm (Lepidoptera: Tortricidae), on larval survival, growth, and development.

The interactions among white spruce, Picea glauca (Moench) Voss, purified acetone tannin extracts (hydrolyzable and condensed tannin), Bacillus thuringiensis subsp. kurstaki Cry1A(c) delta-endotoxin strain HD-73 (Btk), and spruce budworm, Choristoneura fumiferana (Clemens) (Lepidoptera: Tortricidae) on larval survival, growth, and development were investigated over the whole larval feeding period by using artificial diet supplemented with three concentrations of Btk toxins per milliliter of diet (0, 0.021, and 1.72 microg/ml) and three concentrations of foliar tannin extract (0, 8, and 15% dry mass basis). At high Btk concentration, tannin antagonized Btk potency against spruce budworm by lowering Btk-related larval mortality from 83 to 43%. At moderate Btk concentration tannin did not affect Btk potency. Host tree tannins antagonized not only the lethal effects of Btk toxin but also sublethal Btk-related impacts in terms of larval development, pupal weight, relative consumption rate, and growth rate. When alone in the diet, tannin negatively affected larval survival, growth, and development. Maximum potency of tannins against spruce budworm larvae (60% mortality) was reached at dietary concentrations corresponding to what is found in the plant (8% dry mass). The addition of Btk toxin in food containing tannin reduced percentage of larval mortality by one-third, indicating that Btk toxin can antagonize tannin potency against the insect. Development of Btk transgenic spruce trees should consider the antagonistic effect the toxin may have on the resistance conferred by tannins that have evolved naturally in spruce trees.

Geographic biotype and host-associated local adaptation in a polyphagous species, Lambdina fiscellaria (Lepidoptera: Geometridae) feeding on balsam fir on Anticosti Island, Canada.

The debate about mechanisms underlying the evolution of host specialization by herbivorous insects remains open. Natural selection may act locally and lead to different patterns of geographic variation in life history traits of polyphagous herbivores. The hypothesis of genetically-based trade-offs in offspring performance on different hosts has been proposed but this has rarely been demonstrated. Under laboratory conditions, the biological performance of two populations of the hemlock looper Lambdina fiscellaria (Guenée), a highly polyphagous lepidopteran, was compared when reared on three different tree host species: balsam fir, eastern hemlock and sugar maple. One population originated from Anticosti Island, Québec, Canada, where the insect has evolved without having access to two of the three tree species tested, the other being from the mainland where all tree species are present. When reared on balsam fir foliage, which was naturally available to each population, larvae from Anticosti Island underwent four instars compared with five for the mainland population, indicating the existence of geographic biotypes in L. fiscellaria. When reared on the foliage of non-naturally available host trees, larvae from Anticosti Island had a higher incidence of supernumerary instars. This is a unique example where local adaptation to environmental conditions of an insect herbivore is expressed through a differential number of larval instars. Moreover, the Anticosti Island population showed a higher growth related index on the host available to both populations indicating that a fitness trade-off was the evolutionary process underlying the local adaptation of this population on balsam fir.

Does nutrition-related stress carry over to spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae) progeny?

Three different patterns of feeding of sixth-instar spruce budworm, Choristoneura fumiferana Clemens were simulated in the laboratory. Larvae were fed artificial diets whose nitrogen and total soluble sugar contents varied according to levels similar to those found in three types of balsam fir, Abies balsamea (L.) Miller foliage (current-year foliage from middle and lower crown sections and one-year-old foliage). The biological performance of offspring was studied according to the nutrition of their parents. Although food quality had no impact on pupal weight of female parents and individual mean egg weight, progeny fitness was influenced by parental nutrition. Old foliage simulated diet, poor in nitrogen, clearly affected the early larval development of progeny, especially the percent of egg hatch and first-instar survival. Lower crown current-year foliage simulated diet, with low total soluble sugar content, reduced the first-instar survival of the progeny. However, the selective pressure exerted by low food qualities on the parental generation and on the early stages of their progenies resulted in C. fumiferana populations having higher tolerance to starvation and higher survival after the diapause period. These results highlighted the potentially direct and indirect effects of C. fumiferana parental nutrition on the next generation. The patterns of feeding of parental generations would appear to affect the quality and size of subsequent populations through several selections on the different life-history stages of both generations.

Testing the ecophysiological basis for the control of monoterpene concentrations in thinned and unthinned balsam fir stands across different drainage classes.

Stand thinning across different soil drainage types was used to test the ecophysiological basis for the control of foliar monoterpenes in current-year foliage of balsam trees [Abies balsamea (L.) P. Mill.] the year following treatment. Photosynthetic capacity (A max) was greater on mesic sites than on sub-hygric and hydric sites (1.81, 1.33 and 0.88 µmol m-2 s-1, respectively) and greater in mid-July than at the end of June (1.86 vs 0.77 µmol m-2 s-1). Foliar N was greater on thinned plots than control plots (2.6 vs 2.2 g m-2); starch was greater on mesic control plots than mesic thinned plots (16.3 vs 10.9 g m-2); and total soluble sugars (TSS) were higher in mid-July than at the end of June (16.5 vs 12.8 g m-2). Total monoterpenes, as well as five individual monoterpenes, showed a complex interaction between site drainage class, thinning treatment and time of sampling (P<0.05). For all sites and dates combined, total monoterpenes were negatively correlated with specific leaf area (r 2=0.46), and positively but weakly correlated with A max (r 2=0.35), foliar N (r 2=0.29) and TSS (r 2=0.24). Total monoterpenes were not correlated with the different measures of carbon to nitrogen ratio as predicted by the carbon-nutrient balance hypothesis. Our results offer partial support to the different hypotheses proposing that foliage having greater resource availability, enzymatic machinery and potential for building storage structures will have greater monoterpene content. However, the strength of the relationships with monoterpenes often varied with sampling date, suggesting that phenological development may play a strong role in determining which factors control monoterpenes at a given time.

Testing the ecophysiological basis for the control of monoterpene concentrations along canopy profiles in thinned and unthinned balsam fir stands.

To determine which ecophysiological factors appear to control monoterpene concentrations in balsam fir foliage [Abies balsamea (L.) P. Mill.], the percentage of photosynthetically active radiation (%PAR), specific leaf area (SLA), light-saturated photosynthesis (A max), and concentrations per unit leaf area of foliar nitrogen (N), total soluble sugars (TSS), starch and monoterpenes were measured on current-year needles from three canopy levels (upper, middle and lower) the year following a pre-commercial thinning. The thinning only modestly changed the light profile within the canopy. %PAR was negatively correlated with SLA (r 2=0.62 in June, r 2=0.53 in July and August) and positively correlated with foliar nitrogen concentrations (r 2=0.51) within the crown profile. The positive relationship between N and A max was quite weak (r 2=0.15), suggesting significant variations in non-photosynthetic N within the canopies. Total monoterpenes were positively correlated with both %PAR (r 2=0.29) and A max (r 2=0.27), and negatively correlated with SLA (r 2=0.30). Contrary to that predicted by the carbon-nutrient balance hypothesis, total monoterpenes were negatively and only very weakly correlated with the starch/N ratio (r 2=0.06) and were not significantly correlated with either the TSS/N or the [TSS+starch]/N ratios. Monoterpenes were positively correlated with both N and TSS, although the relationship varied with the phenological state of the foliage, i.e., monoterpenes were more highly correlated with TSS (r 2=0.67) (immature foliage) in June, and in July and August with N (r 2=0.63) (mature foliage). Thus, it appears that monoterpene concentrations may be controlled primarily by carbohydrate supply in the early growing season and later by enzymatic capacity. Data expressed on a dry weight basis showed a similar pattern.

Spruce budworm growth, development and food utilization on young and old balsam fir trees.

Laboratory rearing of spruce budworm, Choristoneura fumiferana, in conjunction with field rearing, gravimetric analyses, a transfer experiment, and foliage chemical analyses at six dates during the period of budworm feeding activity indicated that the age of balsam fir, Abies balsamea, trees (70-year-old mature trees or 30-year-old juvenile trees) affected tree suitability for the spruce budworm via the chemical profile of the foliage. Insects reared on old trees had greater survival and pupal weight, shorter development times, and caused more defoliation than those reared on young trees. Young trees were more suitable for the development of young larvae (instars 2-5), while old trees were more suitable for the development of older, sixth-instar larvae. These results were confirmed by the laboratory transfer experiment. Young larvae fed foliage from young trees had higher relative growth rates (RGR), digestibility (AD), and efficiency of conversion of ingested foliage (ECI) than those fed foliage from old trees. These differences appeared to be related to the high N:tannins ratio, and the high contents of P present in young trees during the development of the young larvae. Old larvae fed foliage from old trees had higher relative growth rates, relative consumption rates (RCR), and digestibility of the foliage than those fed foliage from young trees. The high digestibility of the foliage of old trees was compensated for by a lower efficiency of conversion of digested food (ECD), which in turn resulted in no significant effect of tree age on the efficiency of conversion of ingested foliage by old larvae. The low relative consumption rate of old larvae fed foliage from young trees appeared to be related to the low N:tannins ratio, and the high contents of bornyl acetate, terpinolene, and °-3-carene present in young trees during the budworm sixth instar. Variations in these compounds in relation to tree age may serve as mechanisms of balsam fir resistance to spruce budworm by reducing the feeding rate of sixth instar larvae.