Arthropod and Pathogen Damage on Fossil and Modern Plants: Exploring the Origins and Evolution of Herbivory on Land

Abstract

The use of the functional feeding group–damage type system for analyzing arthropod and pathogen interactions with plants has transformed our understanding of herbivory in fossil plant assemblages by providing data, analyses, and interpretation of the local, regional, and global patterns of a 420-Myr history. The early fossil record can be used to answer major questions about the oldest evidence for herbivory, the early emergence of herbivore associations on land plants, and later expansion on seed plants. The subsequent effects of the Permian–Triassic ecological crisis on herbivore diversity, the resulting formation of biologically diverse herbivore communities on gymnosperms, and major shifts in herbivory ensuing from initial angiosperm diversification are additional issues that need to be addressed. Studies ofherbivory resulting from more recent transient spikes and longer-term climate trends provide important data that are applied to current global change and include herbivore community responses to latitude, altitude, and habitat. Ongoing paleoecological themes remaining to be addressed include the antiquity of modern interactions, differential herbivory between ferns and angiosperms, and origins of modern tropical forests. The expansion of databases that include a multitude of specimens; improvements in sampling strategies; development of new analytical methods; and, importantly, the ability to address conceptually stimulating ecological and evolutionary questions have provided new impetus in this rapidly advancing field.

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

“…Some unique ichnotaxa can be assigned to a specific tracemaker with a relatively high level of confidence. Such assignments are particularly so in the case of mines that display morphologies that are sufficiently characteristic of the biological tracemaker that they can be used to assign an order, or family, or even genus to a first approximation (Maccracken et al ., 2021; Labandeira & Wappler, 2023). However, given that this endophytic structure is of late Paleozoic origin, many of the distinguishing characteristics used to determine the ordinal level Mesozoic and Cenozoic miners may not be accurate since these criteria are derived from what we know of leaf mine morphologies within the four extant holometabolous orders known to exhibit leaf‐mining behavior (Diptera, Hymenoptera, Lepidoptera and Coleoptera).…”

“…Evidence from trace fossils has established that land plants and arthropods have dominated macroscopic diversity and biomass (Bar‐On et al ., 2018) and have been a cornerstone of terrestrial ecosystems for > 400 M (Wilf, 2008). Associations between extant plants and insects number in the tens to hundreds of millions (Labandeira & Wappler, 2023). These interactions across time and space have resulted in co‐associations, often leading to reciprocal coevolution, and correlated diversification of both plants and insects, with phytophagy being the dominant interaction observed through the geological record.…”

“…Phytophagous insects engage in ectophagy that consists of feeding on external foliage such as leaf margins, perforations of leaf interiors, various plant surfaces, and occasionally skeletonization that produce delicate lattice patterns (see Kristensen, 1999; Labandeira & Wappler, 2023). Insect phytophagy also involves endophagy, prominently consisting of mining, galling, borings in plant tissues, and a variety of feeding modes resulting in seed predation (Tooker & Giron, 2020; Labandeira & Wappler, 2023). Endophagy has evolved numerous times across various insect lineages and includes taxa that are endophagous at any stage of their development (Tooker & Giron, 2020).…”

Recent origin and diversification accompanied by repeated host shifts of thallus-mining flies (Diptera: Agromyzidae) on liverworts and hornworts

“…While fossils can provide profound insight into the plant–herbivore interactions in geologic time [62], bryophyte–arthropod interactions are poorly documented in the fossil record. The oldest evidence of external feeding on liverworts was found in Middle Devonian body fossils, making it one of the few records of herbivory in bryophyte fossils [63].…”

Sampling bias and the robustness of ecological metrics for plant–damage‐type association networks

“…The node classes in functional bipartite networks that can be used for such studies are plant hosts (often determined using compression leaf fossils in palaeoecological cases), and insect/arthropod or pathogen damage (often termed as damage types). Insect feeding damage or DTs are morphologically distinct, stereotyped, feeding patterns preserved on plant tissue, which have remained almost unchanged in structure over large periods of geological time and geographical space (Labandeira & Wappler, 2022), making them a good functional representative of insect herbivory and other damages on plants. DTs are the most abundant available data on ancient herbivorous insects and their ecological associations, whereas insect body fossils are sporadic through the geologic record (Labandeira & Eble, 2000) and do not often preserve information regarding their ecological associations (i.e., plant–insect interactions).…”