Leaf traits linked to structure and palatability drive plant-insect interactions within three forested ecosystems.

PREMISE: Plant traits and insect herbivory have been highly studied within the modern record but only to a limited extent within the paleontological. Preservation influences what can be measured within the fossil record, but modern methods are also not compatible with paleobotanical methods. To remedy this knowledge gap, a comparable framework was created here using modern and paleobotanical methods, allowing for future comparisons within the fossil record. METHODS: Insect feeding damage on selected tree species at Harvard Forest, the Smithsonian Environmental Research Center, and La Selva were characterized using the damage type system prevalent within paleobotanical studies and compared with leaf traits. Linear models and random forest analyses tested the influence of leaf traits on total, specialized, gall, and mine frequency and diversity. RESULTS: Structural traits like leaf dry mass per area and palatability traits, including lignin and phosphorus concentrations, are important variables affecting gall and mine damage. The significance and strength of trait-herbivory relationships varied across forest types, which is likely driven by differences in local insect populations. CONCLUSIONS: This work addresses the persistent gap between modern and paleoecological studies focusing on the influence of leaf traits on insect herbivory. This is important as modern climate change alters our understanding of plant-insect interactions, providing a need for contextualizing these relationships within evolutionary time. The fossil record provides information on terrestrial response to past climatic events and, thus, should be implemented when considering how to preserve biodiversity under current and future global change.

Landscape-level variability and insect herbivore outbreak captured within modern forests provides a framework for interpreting the fossil record.

Temporal patterns of plant-insect interactions are readily observed within fossil datasets but spatial variability is harder to disentangle without comparable modern methods due to limitations in preservation. This is problematic as spatial variability influences community structure and interactions. To address this we replicated paleobotanical methods within three modern forests, creating an analogous dataset that rigorously tested inter- and intra-forest plant-insect variability. Random mixed effects models, non-metric multidimensional scaling (NMDS) ordinations, and bipartite network- and node-level metrics were used. Total damage frequency and diversity did not differ across forests but differences in functional feeding groups (FFGs) were observed across forests, correlating with plant diversity, evenness, and latitude. Overall, we found higher generalized herbivory within the temperate forests than the wet-tropical, a finding also supported by co-occurrence and network analyses at multiple spatial scales. Intra-forest analyses captured consistent damage type communities, supporting paleobotanical efforts. Bipartite networks captured the feeding outbreak of Lymantria dispar caterpillars; an exciting result as insect outbreaks have long been unidentifiable within fossil datasets. These results support paleobotanical assumptions about fossil insect herbivore communities, provide a comparative framework between paleobotanical and modern communities, and suggest a new analytical framework for targeting modern and fossil outbreaks of insect feeding.

Sampling bias and the robustness of ecological metrics for plant-damage-type association networks.

Plants and their insect herbivores have been a dominant component of the terrestrial ecological landscape for the past 410 million years and feature intricate evolutionary patterns and co-dependencies. A complex systems perspective allows for both detailed resolution of these evolutionary relationships as well as comparison and synthesis across systems. Using proxy data of insect herbivore damage (denoted by the damage type or DT) preserved on fossil leaves, functional bipartite network representations provide insights into how plant-insect associations depend on geological time, paleogeographical space, and environmental variables such as temperature and precipitation. However, the metrics measured from such networks are prone to sampling bias. Such sensitivity is of special concern for plant-DT association networks in paleontological settings where sampling effort is often severely limited. Here, we explore the sensitivity of functional bipartite network metrics to sampling intensity and identify sampling thresholds above which metrics appear robust to sampling effort. Across a broad range of sampling efforts, we find network metrics to be less affected by sampling bias and/or sample size than richness metrics, which are routinely used in studies of fossil plant-DT interactions. These results provide reassurance that cross-comparisons of plant-DT networks offer insights into network structure and function and support their widespread use in paleoecology. Moreover, these findings suggest novel opportunities for using plant-DT networks in neontological terrestrial ecology to understand functional aspects of insect herbivory across geological time, environmental perturbations, and geographic space.

Insect herbivory within modern forests is greater than fossil localities.

Fossilized leaves provide the longest running record of hyperdiverse plant-insect herbivore associations. Reconstructions of these relationships over deep time indicate strong links between environmental conditions, herbivore diversity, and feeding damage on leaves. However, herbivory has not been compared between the past and the modern era, which is characterized by intense anthropogenic environmental change. Here, we present estimates for damage frequencies and diversities on fossil leaves from the Late Cretaceous (66.8 Ma) through the Pleistocene (2.06 Ma) and compare these estimates with Recent (post-1955) leaves collected via paleobotanical methods from modern ecosystems: Harvard Forest, United States; the Smithsonian Environmental Research Center, United States; and La Selva, Costa Rica. Total damage frequency, measured as the percentage of leaves with any herbivore damage, within modern ecosystems is greater than any fossil locality within this record. This pattern is driven by increased frequencies across nearly all functional feeding groups within the Recent. Diversities of total, specialized, and mining damage types are elevated within the Recent compared with fossil floras. Our results demonstrate that plants in the modern era are experiencing unprecedented levels of insect damage, despite widespread insect declines. Human influence, such as the rate of global climate warming, influencing insect feeding and timing of life cycle processes along with urbanization and the introduction of invasive plant and insect species may drive elevated herbivory. This research suggests that the strength of human influence on plant-insect interactions is not controlled by climate change alone but rather, the way in which humans interact with terrestrial landscape.

Plant and insect herbivore community variation across the Paleocene-Eocene boundary in the Hanna Basin, southeastern Wyoming.

Ecosystem function and stability are highly affected by internal and external stressors. Utilizing paleobotanical data gives insight into the evolutionary processes an ecosystem undergoes across long periods of time, allowing for a more complete understanding of how plant and insect herbivore communities are affected by ecosystem imbalance. To study how plant and insect herbivore communities change during times of disturbance, we quantified community turnover across the Paleocene--Eocene boundary in the Hanna Basin, southeastern Wyoming. This particular location is unlike other nearby Laramide basins because it has an abundance of late Paleocene and Eocene coal and carbonaceous shales and paucity of well-developed paleosols, suggesting perpetually high water availability. We sampled approximately 800 semi-intact dicot leaves from five stratigraphic levels, one of which occurs late in the Paleocene-Eocene thermal maximum (PETM). Field collections were supplemented with specimens at the Denver Museum of Nature & Science. Fossil leaves were classified into morphospecies and herbivore damage was documented for each leaf. We tested for changes in plant and insect herbivore damage diversity using rarefaction and community composition using non-metric multidimensional scaling ordinations. We also documented changes in depositional environment at each stratigraphic level to better contextualize the environment of the basin. Plant diversity was highest during the mid-late Paleocene and decreased into the Eocene, whereas damage diversity was highest at the sites with low plant diversity. Plant communities significantly changed during the late PETM and do not return to pre-PETM composition. Insect herbivore communities also changed during the PETM, but, unlike plant communities, rebound to their pre-PETM structure. These results suggest that insect herbivore communities responded more strongly to plant community composition than to the diversity of species present.