Interactions among Norway spruce, the bark beetle Ips typographus and its fungal symbionts in times of drought

Abstract

Resilience and functionality of European Norway spruce forests are increasingly threatened by mass outbreaks of the bark beetle Ips typographus promoted by heat, wind throw and drought. Here, we review current knowledge on Norway spruce and I. typographus interactions from the perspective of drought-stressed trees, host selection, colonisation behaviour of beetles, with multi-level effects of symbiotic ophiostomatoid fungi. By including chemo-ecological, molecular and behavioural perspectives, we provide a comprehensive picture on this complex, multitrophic system in the light of climate change. Trees invest carbon into specialised metabolism to produce defence compounds against biotic invaders; processes that are strongly affected by physiological stress such as drought. Spruce bark contains numerous terpenoid and phenolic substances, which are important for bark beetle aggregation and attack success. Abiotic stressors such as increased temperatures and drought affect composition, amounts and emission rates of volatile compounds. Thus, drought events may influence olfactory responses of I. typographus, and further the pheromone communication enabling mass attack. In addition, I. typographus is associated with numerous ophiostomatoid fungal symbionts with multiple effects on beetle life history. Symbiotic fungi degrade spruce toxins, help to exhaust tree defences, produce beetle semiochemicals, and possibly provide nutrition. As the various fungal associates have different temperature optima, they can influence the performance of I. typographus differently under changing environmental conditions. Finally, we discuss why effects of drought on tree-killing by bark beetles are still poorly understood and provide an outlook on future research on this eruptive species using both, field and laboratory experiments.

Keywords: Drought; Ophiostomatoid fungi; Picea abies; Specialised metabolites; Spruce bark beetle; Tree defence.

Fig. 1

Conceptual scheme of interactions among Norway spruce, Ips typographus and symbiotic ophiostomatoid fungi under drought conditions. Stressors such as heat and drought activate stress hormones and stress proteins and trigger the closure of stomata via activation of abscisic acid. Stomatal closure and reduced photosynthetic activity cause a cascade of biochemical reactions in the tree involving pathways for the biosynthesis of antioxidants and specialised metabolites from non-structural carbohydrates. Activation of hormones and proteins as well as biochemical reactions are indicated by brown arrows. Defence compounds in the bark and volatile organic compounds (VOC) such as monoterpene hydrocarbons and oxygenated monoterpenes as well as pheromone components (fair blue clouds) are important gustatory and olfactory signals for host searching and attacking bark beetles. Associated fungi play a crucial role in detoxification of compounds and attraction of beetles to the tree

Fig. 2

Chemical structures of some selected compounds that mediate interactions among Norway spruce trees, bark beetles and fungi. The compounds are divided into four major groups based on their origin: Host tree (Picea abies)—monoterpene hydrocarbons, oxygenated monoterpenes and non-volatile phenolics; bark beetle (Ips typographus) pheromones; nonhost tree volatiles; symbiotic fungal volatiles that function as insect semiochemicals. See Table 2 for more details on the ecology of individual compounds. Several bark beetle semiochemicals have multiple origins, and other known sources are denoted as H: host tree or B: beetle or F: fungus in suffixes next to compound names

Fig. 3

Behavioural sequence for Ips typographus in a landscape (dispersal), b habitat and c tree (both host selection), and d tissue (host acceptance) by positive (fair blue arrows and boxes) and negative cues (red arrows and boxes). Focus is set on the pioneering male beetles, whose rapidly produced pheromone signals guide the vast majority of both males and females to aggregate. The individual beetle follows a sequence of steps, guided by visual, chemo-sensory and thigmotactic cues