Wei-Ming Zhou

Stipules are specialized appendages borne at the base of a leaf petiole and may perform a variety of functions including sheltering delicate growing tissues from environmental exposure, facilitating vegetative propagation and dispersal, and providing climbing hooks or protective spines. While stipules are widespread in extant angiosperms and a few fern groups, their origins in geological history remain poorly understood. This study critically reconsiders the absence of stipules in the ancestry of Marattiales. Based on extraordinary collections from the early Permian Wuda Tuff Flora, we report, for the first time, aphlebia fossils organically attached to psaroniaceous petioles. The psaroniaceous aphlebiae are homologous to marattiaceous stipules, as evidenced by numerous shared characteristics. Functionally, psaroniaceous stipules appear to shelter juvenile fronds and the stem apex, with a continued role in mature fronds. Furthermore, their continued and potentially indeterminate growth, along with their fully laminated structure, suggests a possible role in vegetative propagation after detachment from the parent frond. However, no direct fossil evidence of stipules acting as vegetative propagules is currently available. Our discovery provides unprecedented view of stipules in psaroniaceous tree ferns. The discovery of psaroniaceous stipules is significant, as it represents the earliest known stipule in the plant kingdom and underscores their multifunctional roles in plant development.

Stipules are specialized appendages borne at the leaf base with roles as diverse as sheltering of delicate growing tissues from environmental exposure, vegetative propagation and dispersal, and modification into climbing hooks or protective spines. Stipules are widely present in extant vascular plants, but their origins in geological history remain obscure and must have involved convergent evolution more than once, perhaps as early as the late Paleozoic emergence of forested terrestrial ecosystems. Based on extraordinary collections from the early Permian Wuda Tuff Flora, the earliest known stipule structure in the plant kingdom has been identified in marattialean tree ferns Psaroniaceae, the dominant element of Permo-Carboniferous wetland forests. Psaroniaceous stipules are consistent with protection of juvenile fronds and the stem apex as well as retention of a functional role in mature and withered fronds. Furthermore, the continued and perhaps indeterminate growth and the fully laminated stipules invite speculation of a potential role in vegetative propagation following detachment from the parent frond. However, no direct fossil evidence of stipules acting as vegetative propagules is currently available.

Interactions between arthropods and plants have been documented extensively in late Paleozoic trees and ground cover plants, but they have rarely been recorded in late Paleozoic climbers. In this study, we present the second example of coprolites preserved within the plant tissue from the early Permian fossil Lagerstätte Wuda Tuff Flora. The host axis is identified as a phyllophore of the climbing fern Hansopteris uncinatus by the combined evidence of anatomy, morphology, and associated plants. Unlike the first coprolites, which were suggested to be produced by oribatid mites, the culprit of the studied coprolites was likely a myriapod or beetle, indicated by their slightly larger size and the boring behaviour. Furthermore, anomalous parenchymatous cells, sclerenchymatous cells, and metaxylem tracheids have been observed surrounding the tunnel, suggesting responses to traumatic stimulus caused by arthropod damage. This discovery provides an informative example of arthropod herbivory on late Paleozoic climbers and sheds light on how the host plant responded during the early stage of injury.

Plants and arthropods interact with each other and constitute an important part of the modern terrestrial ecosystem (Schoonhoven et al., 2005). Historically, fossil records of plant-arthropod interactions have been well documented in Paleozoic terrestrial ecosystems, which were evidenced by large coprolites containing various plant fragments (e.g., Salter et al., 2012), small larvae and coprolites remained in plant organs (e.g., Feng et al., 2017), and diverse functional feeding groups discovered on plant stems, rachises, roots, leaves and fertile organs (e.g., Liu et al., 2020).

Gigantopterid plants share common traits of megaphyllous leaves with multi-ordered venation and have a stratigraphic distribution restricted to the Permian Period. They display a large variety of leaf morphologies which may indicate affinities from more than one plant groups including ferns and pteridosperms such as the peltasperms. Here we describe a new genus of gigantopterid with two species from the upper Permian Nayixiong Formation in the Daha Coalfield, Qinghai Province, China. The new genus Filigigantopteris is markedly different from other gigantopterid genera in having fern-like leaf architecture with double-meshed venation. Filigigantopteris asymmetrica gen. et sp. nov. is characterised by its asymmetric pinnules with dissected lobes, while Filigigantopteris dahaia gen. et sp. nov. is characterised by its once-pinnate frond. A gigantopterid leaf figured from the Lopingian of southwest China that was previously incorrectly assigned to Gigantopteris nicotianaefolia may represent a third species of Filigigantopteris. The new genus further emphasises the morphological diversity and obscure systematic position of the Permian gigantopterids. In addition, three types of functional feeding groups, including hole feeding, margin feeding and probably skeletonisation, are present on laminae of Filigigantopteris, suggesting frequent and diverse plant-insect interactions between gigantopterid megaphylls and herbivorous insects in Cathaysia.