Yellow, red, dead: the nutritional consequences for Cardiaspina densitexta (Hemiptera: Aphalaridae) nymphs of inducing senescence in old Eucalyptus fasciculosa leaves

Many psyllids are manipulative herbivores that alter their hosts to provide shelter and ameliorate nutritional quality. Among eucalypt-feeding psyllids, Cardiaspina have specialised to manipulate natural processes of foliar senescence and thereby host nutritional quality but not foliar morphology. Using a natural outbreak, we assessed the effects of feeding by nymphs of Cardiaspina densitexta Taylor, ultraviolet exposure and temperature on changes in nutritional quality and leaf abscission. Over 6 months, we followed the responses of tagged Eucalyptus fasciculosa F.Muell. leaves that, at the beginning of the study, were at one of three different stages of utilisation by psyllids (no psyllids, only eggs present, or leaves with late instar nymphs and red lesions). We measured foliar pigments, free amino acids and polyphenols every second month to characterise foliar nutritional quality. Psyllid feeding was briefly associated with chlorosis but lesions rapidly turned red (anthocyanic) and died after nymphs had matured. Red leaves had shortened longevities and their risk of abscission was positively correlated with the UV-index rating of the preceding fortnight but not with psyllid abundance or area necrotic. Hence, psyllids altered the balance of chlorophylls and anthocyanin-equivalents of green leaves and presumably therefore their ability to fully utilise incoming light energy. Green leaves had distinct free amino acids and polyphenol compositions compared to red leaves. In green leaves, changes in anthocyanin-equivalents were negatively correlated with methionine while in red leaves psyllids were positively correlated with threonine and negatively correlated with leucine. Feeding by Cardiaspina densitexta nymphs is associated with the visible symptoms of photodamage which are associated with pronounced changes in nutritional quality. These changes are not analogous to foliar hypersensitive responses because they are expressed by old leaves, necrotic tissues are not abscised, they occur late in the development of nymphs and do not directly affect their survival. Specialisation of Cardiaspina on old eucalypt leaves may appear maladaptive if these modules are considered to be low in amino nitrogen and high in polyphenols. This perspective needs refining given the influence of photodamage on nutrient availability and because condensed tannins (weak pro-oxidants) are more abundant than hydrolysable tannins in old leaves.