Great Tits Learn Odors and Colors Equally Well, and Show No Predisposition for Herbivore-Induced Plant Volatiles

Ability to efficiently localize productive foraging habitat is crucial for nesting success of insectivorous birds. Some bird species can use olfaction to identify caterpillar-infested trees by detection of herbivore induced plant volatiles (HIPVs), but these cues probably need to be learned. So far, we know very little about the process of olfactory learning in birds, whether insectivorous species have a predisposition for detecting and learning HIPVs, due to the high ecological significance of these odors, and how olfaction is integrated with vision in making foraging decisions. In a standardized setup, we tested whether 35 wild-caught great tits (Parus major) show any preference for widely abundant HIPVs compared to neutral (non-induced) plant odors, how fast they learn to associate olfactory, visual and multimodal foraging cues with food, and whether the olfactory preferences and learning speed were influenced by bird sex or habitat (urban or rural). We also tested how fast birds switch to a new cue of the same modality. Great tits showed no initial preference for HIPVs compared to neutral odors, and they learned all olfactory cues at a similar pace, except for methyl salicylate (MeSA), which they learned more slowly. We also found no differences in learning speeds between visual, olfactory and multimodal foraging cues, but birds learned the second cue they were offered faster than the first one. Bird sex or habitat had no effect on learning speed or olfactory preference, but urban birds tended to learn visual cues more slowly. We conclude that insectivorous birds utilize olfactory and visual cues with similar efficiency in foraging, and that they probably don‘t have any special predisposition toward the tested HIPVs. These results confirm that great tits are flexible foragers with good learning abilities.

Exogenous Application of Methyl Jasmonate Increases Emissions of Volatile Organic Compounds in Pyrenean Oak Trees, Quercus pyrenaica

The tri-trophic interactions between plants, insects, and insect predators and parasitoids are often mediated by chemical cues. The attraction to herbivore-induced Plant Volatiles (HIPVs) has been well documented for arthropod predators and parasitoids, and more recently for insectivorous birds. The attraction to plant volatiles induced by the exogenous application of methyl jasmonate (MeJA), a phytohormone typically produced in response to an attack of chewing herbivores, has provided controversial results both in arthropod and avian predators. In this study, we examined whether potential differences in the composition of bouquets of volatiles produced by herbivore-induced and MeJA-treated Pyrenean oak trees (Quercus pyrenaica) were related to differential avian attraction, as results from a previous study suggested. Results showed that the overall emission of volatiles produced by MeJA-treated and herbivore-induced trees did not differ, and were higher than emissions of Control trees, although MeJA treatment showed a more significant reaction and released several specific compounds in contrast to herbivore-induced trees. These slight yet significant differences in the volatile composition may explain why avian predators were not so attracted to MeJA-treated trees, as observed in a previous study in this plant-herbivore system. Unfortunately, the lack of avian visits to the experimental trees in the current study did not allow us to confirm this result and points out the need to perform more robust predator studies.

Eliciting Plant Defenses Through Herbivore-Induced Plant Volatiles’ Exposure in Sweet Peppers

Insect herbivory activates plant defense mechanisms and releases a blend of herbivore-induced plant volatiles (HIPVs). These volatile compounds may be involved in plant-plant communication and induce defense response in undamaged plants. In this work, we investigated whether the exposure of sweet pepper plants to HIPVs [(Z)-3-hexenol, (Z)-3-hexenyl acetate, (Z)-3-hexenyl propanoate, (Z)-3-hexenyl butanoate, hexyl butanoate, methyl salicylate and methyl jasmonate] activates the sweet pepper immune defense system. For this, healthy sweet pepper plants were individually exposed to the each of the above mentioned HIPVs over 48 h. The expression of jasmonic acid and salicylic acid related genes was quantified. Here, we show that all the tested volatiles induced plant defenses by upregulating the jasmonic acid and salicylic acid signaling pathway. Additionally, the response of Frankliniella occidentalis, a key sweet pepper pest, and Orius laevigatus, the main natural enemy of F. occidentalis, to HIPV-exposed sweet pepper plants were studied in a Y-tube olfactometer. Only plants exposed to (Z)-3-hexenyl propanoate and methyl salicylate repelled F. occidentalis whereas O. laevigatus showed a strong preference to plants exposed to (Z)-3-hexenol, (Z)-3-hexenyl propanoate, (Z)-3-hexenyl butanoate, methyl salicylate and methyl jasmonate. Our results show that HIPVs act as elicitors to sweet pepper plant defenses by enhancing defensive signaling pathways. We anticipate our results to be a starting point for integrating HIPVs-based approaches in sweet pepper pest management systems which may provide a sustainable strategy to manage insect pests in horticultural plants.

Oviposition Preferences of Oriental Fruit Moth Grapholita Molesta (Lepidoptera: Tortricidae) To Pear HIPVs

Herbivore-induced plant volatiles (HIPVs) are regarded as an indirect plant defense against herbivores, since they attract natural enemies to the infested plant. On the other hand, HIPVs also affect behavioral responses of herbivores. In a previous study, Lytopylus rufipes, a parasitoid of the oriental fruit moth (Grapholita molesta), showed positive responses to pear HIPVs, but the influence of pear HIPVs on G. molesta is still unclear. To better understand these responses, we first tested oviposition preferences of G. molesta to uninfested and infested pear shoots (US and IS, respectively) and uninfested mature leaves (ML) in dual-choice bioassays with a cylindrical tube. Then, preferences to volatile components were also assessed. Results show that G. molesta females preferred US-, IS-, and ML-treated areas compared to the control area (no leaves), respectively. Subsequently, G. molesta females preferred IS over US, and US more than ML when comparing pear tissues. Furthermore, G. molesta females didn’t show any significant preference to individual volatile components, but more eggs were laid in the area treated with a synthetic pear HIPV blend, compared to the hexane-treated area (control). These results indicate that G. molesta females do not avoid infested pear shoots nor HIPVs. Moreover, HIPVs may recruit not only natural enemies, but herbivores to the release point of HIPVs. Thus, it is important to examine the responses of G. molesta females to HIPVs in the field before employing them for pest management.

Volatiles Emission by Crotalaria nitens after Insect Attack

Plants are known to increase the emission of volatile organic compounds upon the damage of phytophagous insects. However, very little is known about the composition and temporal dynamics of volatiles released by wild plants of the genus Crotalaria (Fabaceae) attacked with the specialist lepidopteran caterpillar Utetheisa ornatrix (Linnaeus) (Erebidae). In this work, the herbivore-induced plant volatiles (HIPV) emitted by Crotalaria nitens Kunth plants were isolated with solid phase micro-extraction and the conventional purge and trap technique, and their identification was carried out by GC/MS. The poly-dimethylsiloxane/divinylbenzene fiber showed higher affinity for the extraction of apolar compounds (e.g., trans-β-caryophyllene) compared to the Porapak™-Q adsorbent from the purge & trap method that extracted more polar compounds (e.g., trans-nerolidol and indole). The compounds emitted by C. nitens were mainly green leaf volatile substances, terpenoids, aromatics, and aldoximes (isobutyraldoxime and 2-methylbutyraldoxime), whose maximum emission was six hours after the attack. The attack by caterpillars significantly increased the volatile compounds emission in the C. nitens leaves compared to those subjected to mechanical damage. This result indicated that the U. ornatrix caterpillar is responsible for generating a specific response in C. nitens plants. It was demonstrated that HIPVs repelled conspecific moths from attacked plants and favored oviposition in those without damage. The results showed the importance of volatiles in plant–insect interactions, as well as the choice of appropriate extraction and analytical methods for their study.

The Effect of Mirid Density on Volatile-Mediated Foraging Behaviour of Apolygus lucorum and Peristenus spretus

Plants would release herbivore-induced plant volatiles (HIPVs) to repel herbivores and attract natural enemies after being damaged by herbivores. In this study, after cotton plants were damaged by different densities of Apolygus lucorum, the behavioral responses of A. lucorum and Peristenus spretus to cotton plants volatiles were evaluated, and the quality and quantity of volatiles from cotton plants were analyzed. Only when cotton plants were damaged by four bugs did both A. lucorum and P. spretus show an obvious response to damaged cotton plants, which indicates that cotton defense is correlated with pest density. The collection and analysis of volatiles reveals that the increase in pest density results in the emission of new compounds and an increase in the total number of volatiles with an alteration in proportions among the compounds in the blend. These changes in volatile profiles might provide wasps and mirids with specific information on host habitat quality and thus could explain the behavioral responses of parasitoids and pests.

A larval aggregation pheromone as foraging cue for insectivorous birds

Although birds have traditionally been considered anosmic, increasing evidence indicates that olfaction plays an important role in the foraging behaviours of insectivorous birds. Recent studies have shown that birds can exploit herbivore-induced plant volatiles and sexual pheromones of adult insects to locate their prey. Many insectivorous birds prey on immature insects, providing relevant ecosystem services as pest regulators in natural and agricultural ecosystems. We asked whether birds could rely on chemical cues emitted by the immature stages of insects to prey on them. To address this question, we performed field experiments to evaluate if insectivorous birds can detect the aggregation pheromone produced by the larvae of the carpenter worm, Chilecomadia valdiviana . Groups of five artificial larvae were placed in branches of 72 adult trees in a remnant fragment of a sclerophyllous forest in central Chile. Each grouping of larvae contained a rubber septum loaded with either larval pheromone as treatment or solvent alone as control. We found that the number of larvae damaged by bird pecks was significantly higher in groups with dispensers containing the larval extract than in control groups. Our results show that birds can rely on immature insect-derived chemical cues used for larvae aggregation to prey on them.