Insect Fluid-Feeding on Upper Pennsylvanian Tree Ferns (Palaeodictyoptera, Marattiales) and the Early History of the Piercing-and-Sucking Functional Feeding Group

We document the presence of the piercing-and-sucking functional feeding group and the dietary targeting of vascular tissue (phloem and xylem) in marattialean tree-fern rhachises from a Late Pennsylvanian (302 Ma) coal-swamp forest in the Illinois Basin. Our evidence originates from permineralized peat that exhibits cellular-level preservation of tissues from whole Psaronius tree-fern rhachises; it includes 3 stylet probes, each of which traverses epidermal tissues and parenchyma, and terminates in a distinctive feeding cavity within phloem and xylem of a vascular strand. The stylet probes are lined with an opaque, sheathlike material, and are principally intracellular, although large gum sac cells are avoided. One of their most diagnostic features is 1 or 2 ridges occurring on the inner surface of each stylet probe, paralleling most of the probe length. These ridges, documented by light and scanning electron microscopy, are interpreted as host tissue casts of interstyletal sulci. From these and other features of stylet-trace morphology, we conclude that the herbivore was an insect of the order Palaeodictyoptera rather than an hemipteroid insect. Well developed reaction tissue surrounding the stylet trace developed while the plant host was alive, demonstrating herbivory. Previous studies have documented piercing-and-sucking in several examples of plant damage from the Early Devonian to Late Pennsylvanian (395–290 Ma). The oldest credible examples are plant lesions indicating piercing-and-sucking arthropods from 2 Lower Devonian deposits. We hypothesize that in later Middle Pennsylvanian, equatorial, coal-swamp forests of Euramerica, the dominant arborescent plants possessed vascular tissues largely unavailable to insects, because they were either deeply embedded in thick cortical tissues or protected by outer indurated, peridermal tissues. Subsequent tree-fern forests of the Late Pennsylvanian provided accessible vascular and other tissues to surface-dwelling insects with stylate mouthparts–a condition which continued into the Permian and propelled the hemipteroid radiation.