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.

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.

Infestation of the gall midge Dasineura oleae provides first evidence of induced plant volatiles in olive leaves

In this study, we present the first characterization of herbivore-induced plant volatiles (HIPVs) released from infested olive leaves. The gall midge Dasineura oleae is a specific pest of Olea europaea and endemic of the Mediterranean Basin, an area in which severe outbreaks currently occurred. Little is known about the damage caused by the pest and the relationship with its host. Since gall formation and larval feeding activity may lead to the release of specific plant volatile compounds, we investigated the volatile profiles emitted from infested plants compared with healthy plants under both laboratory and field conditions. Additionally, the volatiles emitted from mechanically damaged plants were considered. A blend of 12 volatiles was emitted from olive trees infested by D. oleae. Of these, β-copaene, β-ocimene, cosmene, unknown 1 and unknown 3 were found to be exclusively emitted in infested plants. The emission of germacrene-D, (E,E)-α-farnesene, and (Z,E)-α-farnesene, α-copaene, (E)-4,8-dimethylnona-1,3,7-triene, (E)-β-guaiene and heptadecane significantly increased in infested trees. Linalool, β-copaen-4-α-ol, β-bourbonene, β-cubebene, β-elemene, β-copaene and δ-amorphene were found only in the field trial and showed differences depending on the level of infestation and the plant stage. (Z)-3-Hexenol, (E)-4-oxohen-2-enal, and 2-(2-butoxyethoxy)-ethanol, were exclusively emitted from the leaves after mechanical damage. In a field trial in Italy, we also demonstrated spring synchronization between adults of D. oleae and O. europaea trees. Analyses of morphoanatomical malformations of gall leaves showed that tissue alterations occur at the spongy parenchyma causing an increase of the leaf blade thickness. We speculate that tissue alterations may lead to HIPV release, in turn potentially attracting D. oleae natural enemies.

Attraction of Trichogramma Wasps to Butterfly Oviposition-Induced Plant Volatiles Depends on Brassica Species, Wasp Strain and Leaf Necrosis

Within the Brassicaceae, wild as well as crop species are challenged by specialist herbivores including cabbage white butterflies (Pieris spp.). The wild crucifer Brassica nigra responds to oviposition by Pieris butterflies by the synergistic expression of two egg-killing traits. Genotypes that express a hypersensitive response (HR)-like necrosis (direct egg-killing) also emit oviposition-induced plant volatiles (OIPVs) attracting Trichogramma egg parasitoids (indirect egg-killing). This so-called double defense line can result in high butterfly egg mortalities. It remains unknown whether this strategy is unique to B. nigra or more common in Brassica species. To test this, we examined the response of different Trichogramma evanescens lines to OIPVs emitted by B. nigra and three close relatives (Brassica napus, Brassica rapa, and Brassica oleracea). Furthermore, we evaluated whether HR-like necrosis played a role in the attraction toward plant volatiles. Our results show a specificity in wasp attraction to different plant species. Three out of four plant species attracted a specific T. evanescens strain, including the crops B. rapa and B. napus. Parasitoid attraction was positively affected by presence of HR-like necrosis in one plant species. Our findings imply that, despite being a true generalist in terms of host range, T. evanescens shows intraspecific variation during host searching, which should be taken into account when selecting parasitoid lines for biocontrol of certain crops. Finally, we conclude that also crop plants within the Brassicaceae family possess egg-killing traits and can exert the double-defense line which may enable effective selection of egg-killing defense traits by cabbage breeders.