Exceptional plant penetration and feeding upon cortical parenchyma cells by the woolly poplar aphid

Forty percent of aphids live wholly or partly on trees, most species being associated with leaves or petioles. Species able to exploit woody parts have either specific adaptations, such as extra long stylets that allow them to reach the phloem, or the ability to induce galls. The woolly poplar aphid, Phloeomyzus passerinii (Signoret) (Hemiptera: Aphididae), colonizes the trunks and base of the lower branches of mature poplars and causes cortical necrosis leading to the death of trees where infestation is heavy. Very little is known about the mode of feeding of P. passerinii. This study looked at the feeding behavior of P. passerinii on stem-cuttings of Populus x canadensis Moench using: (i) histological analyses of the feeding site and stylet pathway and (ii) electrical penetration graphs (EPG, DC) based on parthenogenetic apterous females on woody tissues. The histological and EPG results showed that stylets of P. passerinii penetrated into the plant tissues following a straight unbranched extracellular and intracellular pathway to reach the cortical parenchyma. Compared to EPGs for phloem sap feeding aphids, there were differences in the waveforms A and C whereas a new waveform Icp was described. Based on histological analyses and previous descriptions of EPG waveforms, correlations with the stylet tip position and aphid activities within bark tissues are discussed. A pathway and a sustained intracellular phase were distinguished, both occurring in the cortical parenchyma cells. The bark aphid feeding mode is discussed in relation to the damage caused and in terms of changes in the aphid's diet.