The four phases of plant-arthropod associations in deep time

Vascular-plant hosts, their arthropod herbivores, and associated functional feeding groups are distributed spatiotemporally into four major herbivore expansions during the past 420 m.y. They are: (1) a Late Silurian to Late Devonian (60 m.y.) phase of myriapod and apterygote, hexapod (perhaps pterygote) herbivores on several clades of primitive vascular-plant hosts and a prototaxalean fungus; (2) a Late Mississippian to end-Permian (85 m.y.) phase of mites and apterygote and basal pterygote herbivores on pteridophyte and basal gymnospermous plant hosts; (3) a Middle Triassic to Recent (245 m.y.) phase of mites, orthopteroids (in the broadest sense) and hemipteroid and basal holometabolan herbivores on pteridophyte and gymnospermous plant hosts; and (4) a mid Early Cretaceous to Recent (115 m.y.) phase of modern-aspect orthopteroids and derived hemipteroid and holometabolous herbivores on angiospermous plant hosts. These host-plant and herbivore associations are mediated by seven functional feeding groups: a) external foliage feeding, b) piercing-and-sucking, c) boring (Phase 1 origins); d) galling, e) seed predation, f) nonfeeding oviposition (Phase 2 origins); and leaf mining (early Phase 3 origin). Within about 20 m.y. of each herbivore expansion, there is a biota that expresses the nearly full spectrum of later plant-arthropod associations. These four associational phases may be linked to the paleoclimatologic variables of greenhouse/icehouse cycles and atmospheric O2 and CO2 levels by uncertain causes, although some relationship probably is present. The 7 functional feeding groups persist through most of the sampled interval but harbor host-plants and arthropod herbivores that are spatiotemporally ephemeral. Poor understanding of associations in Phases 1 to 3 is attributed to disproportionate focus on the angiosperm and holometabolan insect associations of Phase 4.