Experimental climate warming alters aspen and birch phytochemistry and performance traits for an outbreak insect herbivore.

Climate change and insect outbreaks are key factors contributing to regional and global patterns of increased tree mortality. While links between these environmental stressors have been established, our understanding of the mechanisms by which elevated temperature may affect tree-insect interactions is limited. Using a forest warming mesocosm, we investigated the influence of elevated temperature on phytochemistry, tree resistance traits, and insect performance. Specifically, we examined warming effects on forest tent caterpillar (Malacosoma disstria) and host trees aspen (Populus tremuloides) and birch (Betula papyrifera). Trees were grown under one of three temperature treatments (ambient, +1.7 °C, +3.4 °C) in a multiyear open-air warming experiment. In the third and fourth years of warming (2011, 2012), we assessed foliar nutrients and defense chemistry. Elevated temperatures altered foliar nitrogen, carbohydrates, lignin, and condensed tannins, with differences in responses between species and years. In 2012, we performed bioassays using a common environment approach to evaluate plant-mediated indirect warming effects on larval performance. Warming resulted in decreased food conversion efficiency and increased consumption, ultimately with minimal effect on larval development and biomass. These changes suggest that insects exhibited compensatory feeding due to reduced host quality. Within the context of observed phytochemical variation, primary metabolites were stronger predictors of insect performance than secondary metabolites. Between-year differences in phytochemical shifts corresponded with substantially different weather conditions during these two years. By sampling across years within an ecologically realistic and environmentally open setting, our study demonstrates that plant and insect responses to warming can be temporally variable and context dependent. Results indicate that elevated temperatures can alter phytochemistry, tree resistance traits, and herbivore feeding, but that annual weather variability may modulate warming effects leading to uncertain consequences for plant-insect interactions with projected climate change.

Simulated climate warming alters phenological synchrony between an outbreak insect herbivore and host trees.

As the world's climate warms, the phenologies of interacting organisms in seasonally cold environments may advance at differing rates, leading to alterations in phenological synchrony that can have important ecological consequences. For temperate and boreal species, the timing of early spring development plays a key role in plant-herbivore interactions and can influence insect performance, outbreak dynamics, and plant damage. We used a field-based, meso-scale free-air forest warming experiment (B4WarmED) to examine the effects of elevated temperature on the phenology and performance of forest tent caterpillar (Malacosoma disstria) in relation to the phenology of two host trees, aspen (Populus tremuloides) and birch (Betula papyrifera). Results of our 2-year study demonstrated that spring phenology advanced for both insects and trees, with experimentally manipulated increases in temperature of 1.7 and 3.4 °C. However, tree phenology advanced more than insect phenology, resulting in altered phenological synchrony. Specifically, we observed a decrease in the time interval between herbivore egg hatch and budbreak of aspen in both years and birch in one year. Moreover, warming decreased larval development time from egg hatch to pupation, but did not affect pupal mass. Larvae developed more quickly on aspen than birch, but pupal mass was not affected by host species. Our study reveals that warming-induced phenological shifts can alter the timing of ecological interactions across trophic levels. These findings illustrate one mechanism by which climate warming could mediate insect herbivore outbreaks, and also highlights the importance of climate change effects on trophic interactions.

Pea aphids, Acyrthosiphon pisum, suppress induced plant volatiles in broad bean, Vicia faba.

Plants defend themselves against herbivory through several means, including the production of airborne volatile organic compounds (VOCs). These VOCs benefit plants by attracting natural enemies of their herbivores. The pea aphid, Acyrthosiphon pisum, is able to feed on its host plant, Vicia faba, without inducing detectable changes in plant VOC emission. Levels of VOCs emission are not significantly different between control plants and those fed upon by aphids for up to 5 days. Using a second herbivore, the beet armyworm caterpillar, Spodoptera exigua, we demonstrate that several expected caterpillar-induced VOCs are reduced when co-infested with pea aphids, thus demonstrating that pea aphids have the ability to inhibit the release of certain VOCs. This study shows, for the first time, that aphids not only avoid triggering plant volatile emission, but also can actively inhibit herbivore-induced volatiles.

Wax structures of Scymnus louisianae attenuate aggression from aphid-tending ants.

The cuticular wax structures of Scymnus louisianae J. Chapin larvae were investigated as a defense against ant aggression by Lasius neoniger Emery. The presence of wax structures provided significant defense against ant aggression compared with denuded larvae in that these structures attenuated the aggressive behavior of foraging ants. Furthermore, reapplication of wax dissolved in hexane partially restored defenses associated with intact structures, showing an attenuation of aggression based in part on cuticular wax components rather than solely on physical obstruction to ant mouthparts.

The influence of Lasius neoniger (Hymenoptera: Formicidae) on population growth and biomass of Aphis glycines (Hemiptera: Aphididae) in soybeans.

In the United States, the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), are often tended by the aphid-tending ant, Lasius neoniger Emery (Hymenoptera: Formicidae). In this study, we examined the effects of tending by ants on the density and biomass of soybean aphids on soybeans in Kentucky. We performed cage studies that limited access by ants and/or natural enemies. We used a split-plot design with natural enemy access as the main plot and ant attendance as the sub plot. We found that natural enemy access negatively affected aphid population density in the presence of tending ants, seen as a three- to four-fold increase in aphid density when natural enemies were excluded. In addition, we found that ant tending positively affected aphid biomass, both when natural enemies were given access to aphids or when natural enemies were excluded, seen by a two-fold increase in aphid biomass when ants tended aphids, both in the presence or absence of natural enemies. Biomass accumulation is seen as an important measurement for assessing aphid performance, and we argue that aphid-tending by ants can have an influence on natural field populations of soybean aphids. Agronomic practices that affect ant abundance in soybeans may influence the performance and hence pest outbreaks for this economically important pest.

Juvenile hormone titres and winged offspring production do not correlate in the pea aphid, Acyrthosiphon pisum.

Pea aphids, Acyrthosiphon pisum, reproduce parthenogenetically and are wing-dimorphic such that offspring can develop into winged (alate) or unwinged (apterous) adults. Alate induction is maternal and offspring phenotype is entirely determined by changes in the physiology and environment of the mother. Juvenile hormones (JHs) have been implicated in playing a role in wing differentiation in aphids, however until recently, methods were not available to accurately quantify these insect hormones in small insects such as aphids. Using a novel LC-MS approach we were able to quantify JH III in pea aphids that were either producing a high proportion of winged morphs among their offspring or mainly unwinged offspring. We measured JH III titres by pooling the hemolymph of 12 or fewer individuals (1 microL hemolymph) treated identically. Levels of JH ranged from 30 to 163 pg/microL. While aphids in the two treatments strongly differed in the proportion of winged morphs among their offspring, their JH III titres did not differ significantly. There was also no correlation between JH III titre and the proportion of winged offspring in induced aphids. This supports earlier findings that wing dimorphism in aphids may be regulated by other physiological mechanisms.

Real-time analysis of alarm pheromone emission by the pea aphid (acyrthosiphon pisum) under predation.

Upon attack by predators or parasitoids, aphids emit volatile chemical alarm signals that warn other aphids of a potential risk of predation. Release rate of the major constituent of the alarm pheromone in pea aphids (Acyrthosiphon pisum), (E)-b-farnesene (EBF), was measured for all nymphal and the adult stage as aphids were attacked individually by lacewing (Chrysoperla carnae) larvae. Volatilization of EBF from aphids under attack was quantified continuously for 60 min at 2-min intervals with a rapid gas chromatography technique (zNose) to monitor headspace emissions. After an initial burst, EBF volatilization declined exponentially, and detectable amounts were still present after 30 min in most cases. Total emission of EBF averaged 16.33 +/- 1.54 ng and ranged from 1.18 to 48.85 ng. Emission was higher in nymphs as compared to adults. No differences between pea aphid life stages were detected for their speed of alarm signal emission in response to lacewing larvae attack. This is the first time that alarm pheromone emission from single aphids has been reported.