Oldest leaf mine trace fossil from East Asia provides insight into ancient nutritional flow in a plant–herbivore interaction

Abstract

The Late Triassic saw a flourish of plant–arthropod interactions. By the Late Triassic, insects had developed all distinct strategies of herbivory, notably including some of the earliest occurrences of leaf-mining. Herein we describe exceptionally well-preserved leaf-mine trace fossils on a Cladophlebis Brongniart fern pinnule from the Momonoki Formation, Mine Group, Japan (Middle Carnian), representing the oldest unequivocal leaf-mines from East Asia. The mines all display a distinctive frass trail—a continuous meandering line, which later becomes a broad band containing spheroidal particles—demonstrating larval development. Although the shapes of the frass trails are generally comparable to those of Lepidoptera or Coleoptera, they cannot be unequivocally assigned to a specific extant leaf-mining taxon. Furthermore, elemental analyses by X-ray fluorescence (XRF) reveals that the frass trail comprises phosphate coprolites. The quantitative variations in P, S, and Si between coprolites and leaf veins may reflect physiological processes (e.g., consumption, absorption, and excretion) mediated by plant chemicals. Our findings reinforce the idea that leaf-mining had become a pervasive feeding strategy of herbivorous insects by the Late Triassic.

Early land plants: Plentiful but neglected nutritional resources for herbivores?

“…Records of leaf damage on fern fossils seem to be more common. For clubmosses and ferns, Paleozoic indications of herbivory can be seen from the Late Silurian to Early Devonian (417 to 403 Ma ago; Labandeira, 2007) or from Triassic (252 to 201 Ma ago;Imada et al, 2022) and the Late Miocene (10.29 to 5.27 Ma ago), which has firmly been attributed to insects (Robledo et al, 2015).…”

“…Records of leaf damage on fern fossils seem to be more common. For clubmosses and ferns, Paleozoic indications of herbivory can be seen from the Late Silurian to Early Devonian (417 to 403 Ma ago; Labandeira, 2007 ) or from Triassic (252 to 201 Ma ago; Imada et al, 2022 ) and the Late Miocene (10.29 to 5.27 Ma ago), which has firmly been attributed to insects (Robledo et al, 2015 ). Nowadays, few insects are specialized in ferns, but some sawfly species (Hymenoptera: Tenthredinidae) are known to lay their eggs in new fern fronds, where their larvae can feed on fresh tissues right after hatching (Schreiner et al, 1984 ).…”

Endophytic ancestors of modern leaf miners may have evolved in the Late Carboniferous

“…Endophytic feeding behaviors such as galling, borings, and certain forms of seed predation have been recorded since the Early Devonian, Middle Devonian, and Early Pennsylvanian, respectively (Labandeira, 1997; Labandeira & Currano, 2013; Labandeira et al ., 2016; Imada et al ., 2022), but involved consuming tissues exclusively found on axes and reproductive structures, partly because during the Devonian, plant leaves were diminutive and needle‐like, lacking expanded foliar morphologies. Although galls occurred predominantly on plant axes during the Pennsylvanian (Labandeira & Phillips, 1996; Correia et al ., 2020), it was not until the Permian that insect‐induced galls first exploited foliar tissues, ushering in a successful transition to exploiting the dominant tissues upon which the majority of fossil and extant galls are found (Labandeira, 2021).…”

“…247–237 million years ago (Ma); Labandeira et al ., 2016), and an extensive diversification event of mining occurring during the Late Triassic ( c . 237–227 Ma) in Gondwana (Labandeira et al ., 2018; Imada et al ., 2022). Trace fossils showing mining activity are considerably less common in the Jurassic, but dramatically increases during the Early Cretaceous, with the world‐wide ecological expansion of angiosperms (Xiao et al ., 2022a,b).…”

Diversity underfoot of agromyzids (Agromyzidae, Diptera) mining thalli of liverworts and hornworts

“…Some insects consume specific layers of foliage while dwelling inside the internal plant tissues; such a means of herbivory is known as leaf mining ( Hering 1951 ). The earliest known credible trace fossils of leaf mining are known from the Middle-Late Triassic ( Labandeira 2006 ; Imada et al 2022 ), but the culprits are unknown. Many leaf-mining insect clades in the megadiverse insect orders, Coleoptera , Lepidoptera , Hymenoptera and Diptera , have become diverse in the Cenozoic.…”