Mistletoe-induced carbon, water and nutrient imbalances are imprinted on tree rings

Mistletoes are xylem-tapping hemiparasites that rely on their hosts for water and nutrient uptake. Thus, they impair tree performance in the face of environmental stress via altering the carbon and water relations and nutritional status of trees. To improve our understanding of physiological responses to mistletoe and ongoing climate change, we investigated radial growth, stable carbon and oxygen isotopic signals, and elemental composition of tree rings in silver fir (Abies alba Mill.) and Scots pine (Pinus sylvestris L.) forests infested with Viscum album L. We compared temporal series (1990-2020) of basal area increment (BAI), intrinsic water-use efficiency (iWUE), oxygen isotope composition (δ18O), nutrient concentrations and stoichiometric ratios between non-infested (NI) and severely infested (SI) fir and pine trees from populations located close to the xeric distribution limit of the species in north-eastern Spain. The SI trees showed historically higher growth, but the BAI trend was negative for more than three decades before 2020 and their growth rates became significantly lower than those of NI trees by the mid-2010s. Mistletoe infestation was related to an enhanced sensitivity of radial growth to vapour pressure deficit (atmospheric drought). The SI trees showed less pronounced iWUE increases (fir) and lower iWUE values (pine) than NI trees. The lower tree-ring δ18O values of SI trees may be the result of several superimposed effects operating simultaneously, including leaf-level evaporative enrichment, source water isotopic signals, and anatomical and phenological differences. We observed a deterioration of potassium (K) nutrition in tree-ring wood of both species in SI trees, along with accumulation of manganese (Mn). We suggest that such nutritional patterns are driven by the indirect effect of mistletoe-induced drought stress, particularly in pine. The combined analyses of different physiological indicators imprinted on tree rings provided evidence of the progressive onset of carbon, water and nutrient imbalances in mistletoe-infested conifers inhabiting seasonally dry regions.