Plant‐derived environmental DNA complements diversity estimates from traditional arthropod monitoring methods but outperforms them detecting plant–arthropod interactions

Abstract

Our limited knowledge about the ecological drivers of global arthropod decline highlights the urgent need for more effective biodiversity monitoring approaches. Monitoring of arthropods is commonly performed using passive trapping devices, which reliably recover diverse communities, but provide little ecological information on the sampled taxa. Especially the manifold interactions of arthropods with plants are barely understood. A promising strategy to overcome this shortfall is environmental DNA (eDNA) metabarcoding from plant material on which arthropods leave DNA traces through direct or indirect interactions. However, the accuracy of this approach has not been sufficiently tested. In four experiments, we exhaustively test the comparative performance of plant‐derived eDNA from surface washes of plants and homogenized plant material against traditional monitoring approaches. We show that the recovered communities of plant‐derived eDNA and traditional approaches only partly overlap, with eDNA recovering various additional taxa. This suggests eDNA as a useful complementary tool to traditional monitoring. Despite the differences in recovered taxa, estimates of community α‐ and β‐diversity between both approaches are well correlated, highlighting the utility of eDNA as a broad scale tool for community monitoring. Last, eDNA outperforms traditional approaches in the recovery of plant‐specific arthropod communities. Unlike traditional monitoring, eDNA revealed fine‐scale community differentiation between individual plants and even within plant compartments. Especially specialized herbivores are better recovered with eDNA. Our results highlight the value of plant‐derived eDNA analysis for large‐scale biodiversity assessments that include information about community‐level interactions.

Environmental DNA metabarcoding reliably recovers arthropod interactions which are frequently observed by video recordings of flowers

“…As found by Weber et al. (2024), we confirmed that plant‐derived eDNA recovered a plant‐associated arthropod community. For example, the species with the first and third highest occupancy found in the present study, namely the great banded furrow bee ( Halictus scabiosae , Halictidae, Hymenoptera) and Lygus pratensis , are known to be associated with Asteraceae and sunflowers, respectively (Table S1).…”

“…Our data supports that terrestrial eDNA‐ based monitoring approaches could not only be used to identify arthropod species lists on plants but to simultaneously assess the plant‐arthropod interactome (Deiner et al., 2017; Ruppert et al., 2019; Weber et al., 2024). This underlines that plant‐derived eDNA can broadly describe whole plant‐arthropod interaction networks, possibly providing new insights into dynamic biodiversity changes (Derocles et al., 2018; Makiola et al., 2020).…”

“…A detailed analysis of the release and longevity of plant‐derived eDNA and its capabilities to recover a comprehensive image of a plant‐arthropod interactome is still pending. To evaluate eDNA results, previous studies have focused on verifying whether the recovered arthropod species are expected in the corresponding habitat (Thomsen & Sigsgaard, 2019; van der Heyde et al., 2020) or compared eDNA analysis with data about plant‐arthropod associations, but without a direct observation of interactions (Weber et al., 2024). To gather a more exhaustive picture of the plant‐arthropod interactome, a plant needs to be observed in real time, before eDNA sampling is performed.…”

“…To overcome this shortfall, researchers have begun to utilize environmental DNA (eDNA) analysis to monitor arthropods in terrestrial ecosystems (Valentin et al., 2020; van der Heyde et al., 2020), possibly providing a fast and simple method to characterize their interactions with plants (Banerjee et al., 2022). Environmental DNA analysis has already been demonstrated to be a useful assessment tool for arthropod biodiversity on plants (Allen et al., 2022; Krehenwinkel et al., 2022; Macher et al., 2023; Thomsen & Sigsgaard, 2019; Yoneya et al., 2023) and for the assessment of more detailed community wide plant‐arthropod interactions than by using traditional methods (Weber et al., 2024). Yet, little is known about the release, transport, and long‐term persistence of terrestrial arthropod eDNA (Valentin et al., 2021).…”

Environmental DNA from ethanol eluent of flowers reveals a widespread diversity in cowpea associated animal communities in Hainan Island

“…A recent study based on plant-derived environmental DNA showed that there are signi cant differences of species composition of arthropod communities in different parts (e.g. ower, stem or root) of the same plant (Weber et al, 2023). In view of this, we believe that there is still a wider diversity of cowpea associated animal communities, which need for more extensive long-term monitoring of such communities in the future.…”