Abstract
Bark beetles and associated fungi are among the greatest natural threats to conifers worldwide. Conifers have potent defenses, but resistance to beetles and fungal pathogens may be reduced if tree stored resources are consumed by fungi rather than used for tree defense. Here, we assessed the relationship between tree stored resources and resistance to Ceratocystis polonica, a phytopathogenic fungus vectored by the spruce bark beetle Ips typographus. We measured phloem and sapwood nitrogen, non-structural carbohydrates (NSC), and lipids before and after trees were attacked by I. typographus (vectoring C. polonica) or artificially inoculated with C. polonica alone. Tree resistance was assessed by measuring phloem lesions and the proportion of necrotic phloem around the tree's circumference following attack or inoculation. While initial resource concentrations were unrelated to tree resistance to C. polonica, over time, phloem NSC and sapwood lipids declined in the trees inoculated with C. polonica. Greater resource declines correlated with less resistant trees (trees with larger lesions or more necrotic phloem), suggesting that resource depletion may be caused by fungal consumption rather than tree resistance. Ips typographus may then benefit indirectly from reduced tree defenses caused by fungal resource uptake. Our research on tree stored resources represents a novel way of understanding bark beetle-fungal-conifer interactions.
Highlights
Symbiotic relationships between blue-stain fungi and bark beetles have fascinated researchers since they were first described more than 100 years ago [1]–[5], and conifer resistance to beetles and fungi has been the subject of much research [6]–[12]
To determine the relationship between tree stored resources and tree resistance or fungal consumption of resources, we developed the following predictions: (1) If stored resources benefit tree resistance more than they benefit C. polonica as a food source, trees with more initial resources and larger resource depletion over time will be more resistant to fungal colonization (Figure 1A). (2) If stored resources do not have a net influence on tree resistance, resistance will be independent of initial resource concentrations and resource depletion may benefit trees or fungi (Figure 1B). (3) If stored resources benefit C. polonica more than the tree, trees with higher initial resource concentrations and larger resource depletion over time will be less resistant to fungal colonization (Figure 1C)
Only three of nine trees attacked by I. typographus had more than 50% necrotic phloem, and only two of those trees appeared dead by the following year (Table 1)
Summary
Symbiotic relationships between blue-stain fungi and bark beetles have fascinated researchers since they were first described more than 100 years ago [1]–[5], and conifer resistance to beetles and fungi has been the subject of much research [6]–[12]. One basis for bark beetle-fungal mutualisms may be that fungal phytopathogenicity helps beetles to overcome conifer defenses [13], [14], while alternatively, some mutualistic fungi provide important nutritional benefits to their beetle partner and do not seem to engage tree defenses [5], [15]–[19]. These different perspectives on the nature of beetle-fungal mutualisms may be complementary because bark beetles and their different fungal associates must all overcome tree resistance and obtain nutrients from the tree in order to thrive. A better appreciation of how tree resources may benefit the fungi is necessary to understand bark beetle-fungal interactions and their consequences for conifer resistance
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