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. 2022 Oct 18;119(42):e2202852119.
doi: 10.1073/pnas.2202852119. Epub 2022 Oct 10.

Insect herbivory within modern forests is greater than fossil localities

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Insect herbivory within modern forests is greater than fossil localities

Lauren Azevedo-Schmidt et al. Proc Natl Acad Sci U S A. .

Abstract

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.

Keywords: conservation paleobiology; herbivory; human influence; paleoecology; plant–insect interactions.

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Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.
Leaf collection from fossil (A) and modern quarries (B). Leaf layers are identified, and overburden (fossil) or sediment (modern) is removed using a paleopick or trowel and sieve. A leaf compression fossil, Platanites raynoldsii, of Paleocene age (C; University of Wyoming Geologic Museum [UWGM] specimen no. PB968) and Recent Acer rubrum (D) are examples of excavated leaves. Insect damage (E; Gall functional feeding group [FFG], MD1903.2 no. 161; F, unknown Mine FFG, LS1901.2 no. 116) is abundant on Recent leaves across all depositional environments and forest types. Fossil insect damage on P. raynoldsii (G; DT38, Mining FFG, UWGM specimen no. PB922) was previously hypothesized to be made by the insect family [Incurvariidae; Lepidoptera (28)]. Arrows are used to clarify insect damage (EG). Modern specimens are deposited in the Rocky Mountain Herbarium. (Scale bars: 0.5 cm.).
Fig. 2.
Fig. 2.
(A) Frequency of herbivory damage and (B) diversity of DTs (total, specialized, mining, or galling) or plant species in fossil and Recent assemblages. Total damage frequencies for fossil and Recent assemblages were compared with published leaf-litter studies (A) (26, 27). Diversity is reported as the number of DTs or plant species observed and was standardized to 300 leaves to account for variance in sampling size. Rain cloud plots show density distribution (normalized), and box and whisker plots show quantile 1, mean, and quantile 3 along with raw data points. Colors correspond to fossil (blue), leaf-litter (mauve), or leaf-pack (orange) samples.
Fig. 3.
Fig. 3.
(A) Mean damage frequency (percentage of leaves with herbivory damage) on bulk assemblages through time. All identifiable leaves at a site were scored for herbivory, and damage frequency was calculated for each assemblage. Sites were binned by geologic epoch, and the mean was calculated. Total (TD) and specialized (SP) damage frequencies are plotted, as are frequencies of each functional feeding group: piercing and sucking (PS), surface feeding (SF), skeletonization (SK), margin feeding (MF), hole feeding (HF), galling (G), and mining (M). (B) Diversity of DTs (total, specialized, mine, or gall) or plant species (PL) is plotted, with each point representing the mean value for each epoch. Frequency and diversity at individual sites were calculated as in Fig. 2. Colors of points and lines correspond with the legend (upper left corner) and are shared between panels; the size of the points represents the sample size, and SDs are shown as whiskers extending from each point.
Fig. 4.
Fig. 4.
General linear models of MAT and total damage frequency (A), diversity of total (B), and specialized (C) damage types (calculated as in Fig. 2) show positive correlations between herbivory and MAT when considering fossil sites only. Herbivory at Recent (post-1955) sites exceeds that observed at fossil sites of similar MAT, highlighting the oddity of modern ecosystems. Recent data points (purple) include three leaf-pack samples each from Harvard Forest, SERC, and La Selva as well as published total damage frequency data for 17 leaf-litter samples collected using similar methods (26, 27). The legend is in geologic order (oldest to youngest), with colored points assigned to different epochs and shapes corresponding to climatic events (triangles, PETM; squares, EECO). The gray lines show the linear relationships, with CIs represented by the shaded gray areas. P values are given at the bottom right corners of the CIs.

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