Abstract
The fossil record demonstrates that past climate changes and extinctions significantly affected the diversity of insect leaf-feeding damage, implying that the richness of damage types reflects that of the unsampled damage makers, and that the two are correlated through time. However, this relationship has not been quantified for living leaf-chewing insects, whose richness and mouthpart convergence have obscured their value for understanding past and present herbivore diversity. We hypothesized that the correlation of leaf-chewing damage types (DTs) and damage maker richness is directly observable in living forests. Using canopy access cranes at two lowland tropical rainforest sites in Panamá to survey 24 host-plant species, we found significant correlations between the numbers of leaf chewing insect species collected and the numbers of DTs observed to be made by the same species in feeding experiments, strongly supporting our hypothesis. Damage type richness was largely driven by insect species that make multiple DTs. Also, the rank-order abundances of DTs recorded at the Panamá sites and across a set of latest Cretaceous to middle Eocene fossil floras were highly correlated, indicating remarkable consistency of feeding-mode distributions through time. Most fossil and modern host-plant pairs displayed high similarity indices for their leaf-chewing DTs, but informative differences and trends in fossil damage composition became apparent when endophytic damage was included. Our results greatly expand the potential of insect-mediated leaf damage for interpreting insect herbivore richness and compositional heterogeneity from fossil floras and, equally promisingly, in living forests.
Highlights
The plant-insect system’s response to climate change and extinction in deep time has been studied using tens of thousands of fossil leaves with insect-feeding damage as primary data [1,2,3,4,5,6,7,8,9,10,11]
Insect-mediated damage types (DTs) in the leaf-fossil record consistently show that DT richness (DTR) positively tracks paleotemperatures [1], [5], [9], and severe and sustained drops in DTR in the western USA remain the only spatially and temporally well-constrained data that show the fate of insects across the end-Cretaceous extinction [1,2,3,4], [12]
The number of leaf-chewing insect species collected from each host-plant species showed a robust, positive correlation with the number of DTs recorded for the same host-plant species (Fig. 2A). This correlation was significant at the insect-family level (Spearman’s rs = 0.79, P,0.001; Table S3); when considering coleopteran and noncoleopteran species separately (Figs. 2B,C); and after removing all DTs that had low fossilization potential (Fig. 2D; see Materials and Methods)
Summary
The plant-insect system’s response to climate change and extinction in deep time has been studied using tens of thousands of fossil leaves with insect-feeding damage as primary data [1,2,3,4,5,6,7,8,9,10,11]. Insect-mediated damage types (DTs) in the leaf-fossil record consistently show that DT richness (DTR) positively tracks paleotemperatures [1], [5], [9], and severe and sustained drops in DTR in the western USA remain the only spatially and temporally well-constrained data that show the fate of insects across the end-Cretaceous extinction [1,2,3,4], [12] These paleontological results are consistent among many basins and time periods, making them highly relevant as context for current climatic and other anthropogenic change [13]; they are observed both for host-specific endophytic DTs (leaf mines and galls) and for total damage, including piercing and external leaf-chewing damage. Due to widespread mouthpart and behavioral convergence, only in few cases do external feeding DTs found in fossils appear to be assignable to specific taxonomic groups [20], [21], whereas most DTs that are confidently associated to a particular culprit correspond to endophagous feeding such as leaf mining [22]
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