Age-dependent resistance and tolerance of an invasive tree to above- and belowground herbivore interactions: Implications for invasiveness and biological control

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Resistance (reducing herbivore attack) and tolerance (buffering the negative impacts of herbivory) of invasive plants to pressure imposed by aboveground (AG) or belowground (BG) herbivore interactions have been largely overlooked. Experimental manipulations of native and invasive populations consisting of plants of various ages can help elucidate the long-term adaptations of invasive plant genotypes. Here, we subjected first-year and second-year tallow trees (Triadica sebifera) from the native and the invasive range to AG herbivory by the specialist caterpillar Gadirtha fusca and/or BG herbivory by the root-knot nematode Meloidogyne incognita, and tested their interactive effects on levels of resistance or tolerance. The results showed that in comparison to native genotypes, the invasive tallow plants showed lower resistance (higher percent leaf damage) but higher tolerance (regrew faster) to AG damage from G. fusca herbivory alone, but showed similar resistance to nematode herbivory alone, regardless of plant age. Dissimilarly, only the younger (first-year) invasive plants showed higher tolerance to BG herbivory alone. For plants under combined attack by G. fusca and M. incognita, younger invasive plants showed a mixed defense strategy that had both higher resistance (fewer root-knots) and higher tolerance to the BG nematode, while the older (second-year) invasive tallow plants showed similar levels of resistance but greater AG tolerance to both AG and BG herbivores. Our results suggest that the efficacy of a biological agent might be affected by native resident generalist herbivores. Resistance and tolerance of invasive plants to AG-BG herbivory are likely to change as plants age. Higher tolerance of invasive plants like tallow to AG-BG herbivory in the area of introduction compared to the original range may explain the invasion success of the plants as well as the reduced efficacy of biocontrol agents.