Expression of foliar secondary compounds and extrafloral nectaries (EFNs) within the same leaves may be incompatible if secondary compounds repel beneficial insects that might otherwise be attracted to EFNs. This study examined the within-plant distributions of phenolic glycosides and EFNs in trembling aspen, Populus tremuloides, and their relationships to herbivore damage. Populus tremuloides expresses extrafloral nectaries (EFNs) on a subset of its leaves. We studied short and tall naturally occurring aspen ramets across multiple sites in interior Alaska. Contrary to our expectations, foliar phenolic glycoside concentrations were approximately 30% greater on leaves bearing EFNs than on leaves without EFNs. The mean concentration of foliar phenolic glycosides in short ramets was nine times that in tall ramets. Phenolic glycoside concentration was negatively related to leaf mining damage by Phyllocnistis populiella (Lepidoptera; Gracilliadae) at concentrations greater than 27 mg/g, whereas the presence of EFNs was unrelated to mining damage. The positive association of chemical defensive compounds and EFNs in leaves suggests that, for species with variation in EFN expression, negative correlations between herbivory and EFN expression may arise indirectly from associated effects of other, correlated types of defense.
We studied the effect of epidermal leaf mining on the leaf chemistry of quaking aspen, Populus tremuloides, during an outbreak of the aspen leaf miner, Phyllocnistis populiella, in the boreal forest of interior Alaska. Phyllocnistis populiella feeds on the epidermal cells of P. tremuloides leaves. Eleven days after the onset of leaf mining, concentrations of the phenolic glycosides tremulacin and salicortin were significantly higher in aspen leaves that had received natural levels of leaf mining than in leaves sprayed with insecticide to reduce mining damage. In a second experiment, we examined the time course of induction in more detail. The levels of foliar phenolic glycosides in naturally mined ramets increased relative to the levels in insecticide-treated ramets on the ninth day following the onset of leaf mining. Induction occurred while some leaf miner larvae were still feeding and when leaves had sustained mining over 5% of the leaf surface. Leaves with extrafloral nectaries (EFNs) had significantly higher constitutive and induced levels of phenolic glycosides than leaves lacking EFNs, but there was no difference in the ability of leaves with and without EFNs to induce phenolic glycosides in response to mining. Previous work showed that the extent of leaf mining damage was negatively related to the total foliar phenolic glycoside concentration, suggesting that phenolic glycosides deter or reduce mining damage. The results presented here demonstrate that induction of phenolic glycosides can be triggered by relatively small amounts of mining damage confined to the epidermal tissue, and that these changes in leaf chemistry occur while a subset of leaf miners are still feeding within the leaf.
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