Contrasting effects of two exotic invasive hemipterans on whole-plant resource allocation in a declining conifer

Invasive herbivores can cause widespread dieback of naïve native hosts in the invaded range. Some consume leaves, some bore through wood, whereas others, such as piercing-sucking insects, alter plant resource allocation through changes to source-sink dynamics and depletion of long-term stores. Invasive sap-sucking herbivores that target cells critical to resource transport and storage may have particularly large effects. Herbivory by two exotic hemipterans, hemlock woolly adelgid (HWA), Adelges tsugae Annand (Adelgidae), and elongate hemlock scale (EHS), Fiorinia externa Ferris (Diaspididae), have very different effects on eastern hemlock, Tsuga canadensis (L.) Carrière (Pinaceae). Although these insects differ in both timing and feeding site on their hemlock host, the reasons for their differential effects are poorly understood. Here, using potted seedlings in a common garden, we examined the effects of these two herbivores on resource uptake and allocation immediately after an initial attack. We labeled the plants with a single pulse of ¹³CO₂ and a supply of ¹⁵NH₄¹⁵NO₃ every third day to obtain a whole-plant perspective on resource uptake and allocation. After 10 weeks of controlled infestation, plants were measured and divided into tissue types (needles, branches, main stem, and roots). In each tissue we quantified biomass, ¹³C, ¹⁵N, total carbon (C), nitrogen (N), protein, and starch pools. Hemlock woolly adelgid feeding decreased new needle biomass by 34%, increased ¹³C allocation to roots and main stems by 130%, and increased ¹⁵N allocation to old foliage by 18%. Hemlock woolly adelgid infestation also resulted in increased starch storage in old branches over new needles, and marginally increased protein content plant-wide. Elongate hemlock scale infestation resulted in a different growth pattern, with a 27% increase in biomass allocation to the main stem. Elongate hemlock scale also caused a 23% increase in N allocation to roots and main stem. Increases in resource allocation to main stem and belowground may indicate herbivore-induced changes to storage patterns, or compensatory increased fine root growth to facilitate nutrient and water uptake. These resource allocation effects likely underlie the rapid and dramatic decline of hemlock in response to HWA feeding, and the considerably milder effects of EHS feeding.