Carbon starvation by light deprivation does not constrain the ability of young pines to produce induced chemical defences in response to a bark-chewing herbivore

Abstract

Pine tree chemical defence is based on constitutive and inducible carbon-rich substances (mainly oleoresin and phenolic compounds) present in pine tissues in conspicuously high concentrations. Resistance at early stages is essential for future fitness, and allocation of carbon resources to chemical defences may signify a relevant carbon sink for juvenile pines. However there is still poor knowledge about the extent to which allocation priorities of recently assimilated and stored C pools to chemical defences are plastic in response to biotic stress. We aimed to determine the extent to which the production of induced chemical defences in pine trees in response to herbivory depends on the availability of current photosynthates or if they can be built upon stored C pools. Two years-old trees of three pine species (P. pinaster, P. sylvestris and P. radiata) were exposed to real herbivory by the pine weevil Hylobius abietis, a bark-chewing insect, during one week under conditions of either natural sunlight or complete light deprivation. Weevil damage and the concentration of chemical defences in the whole stem were measured in a time-course design with destructive sampling. We analysed, using an ANCOVA approach, whether the ability to increase the concentration of chemical defences in response to weevil damage was altered by light deprivation. We hypothesised that if induced defences are built mainly upon current photoassimilates, then carbon starvation by light deprivation should strongly hamper the production of new defences. For all pine species, concentration of non-volatile resin significantly increased in response to weevil damage, which was more intense under dark conditions. ANCOVA analysis showed that light deprivation did not constrain the ability of young 3 pines to respond to weevil damage by increasing non-volatile resin content in the stems. No significant covariation was found for total polyphenolics. By evaluating chemical defences in the whole stem, and restricting C assimilation by complete light deprivation, we can infer that young pines were able to use other carbon sources than current photosynthates, likely stored carbon pools, for de novo synthesis of induced chemical defences in response to insect herbivory. Disentangling the plasticity in the use of C sources for the synthesis of induced defences is crucial for understanding the ability of pine trees to respond to multiple stressors in a changing environment. Please refer to the video summary (Appendix F) for a quick overview.

Effect of Light Availability on the Interaction between Maritime Pine and the Pine Weevil: Light Drives Insect Feeding Behavior But Also the Defensive Capabilities of the Host

“…The experiment was done with Maritime pine ( Pinus pinaster Ait. ), the species for which larger effects of the light treatments, and stronger inducibility of defenses were observed in our previous work ( López-Goldar et al, 2016 ). In order to enhance the scope of the study, three Maritime pine provenances originating from contrasting environmental conditions were included in the experimental design.…”

“…These results agree with previous findings that reveal maximum mobility and feeding activities of the pine weevils during the night ( Merivee et al, 1998 ; Pszczolkowski and Dobrowolski, 1999 ; Fedderwitz et al, 2014 ). Although weevils, as many other insects, are known to follow circadian rhythms ( Pszczolkowski and Dobrowolski, 1999 ), artificial light/cycles are known to be sufficient to trigger consistent feeding behavior patterns in relation to the availability of light ( Fedderwitz et al, 2014 ; López-Goldar et al, 2016 ). Pine weevils seem, thus, to be more confident under dark conditions, spending more time on each feeding aperture, which results in bigger feeding scars, and thus in greater total debarked area.…”

“…Based on all these premises we can speculate that potential constrains in the inducibility of defenses in absence of light may be critical for effective resistance against the weevil. Previous results by López-Goldar et al (2016) showed that concentration of chemical defenses strongly covariated with the intensity of weevil damage, and suggested no detectable effects of prolonged light deprivation on inducibility of chemical defenses. Nevertheless, in that work, light/dark treatments were simultaneously applied to both the plant and the insect, being impossible to disentangle whether the observed responses to the light treatments were mediated by direct effects on the insect behavior or by indirect changes in the plant physiology or both.…”

“…On the other hand, changes in plant primary metabolism and physiology during light/dark cycles directly alter the availability of current photosynthates, potentially affecting the ability of plants for synthesizing induced chemical defenses in absence of light ( Guérard et al, 2007 ; Kangasjarvi et al, 2012 ; López-Goldar et al, 2016 ). For instance, the synthesis of terpenes in conifers is known to be constrained in absence of light ( Gleizes et al, 1980 ).…”

“…Particularly, in the interaction between pine trees and the pine weevil Hylobius abietis L. (a major insect pest that causes severe economic losses), previous results have shown that the damage was notably more intense under light deprivation conditions than under natural sunlight ( López-Goldar et al, 2016 ). Other studies also denoted higher activity of the pine weevil during the dark phase of the daily cycle ( Fedderwitz et al, 2014 ).…”