Changes in invertebrate food web structure between high- and low-productivity environments are driven by intermediate but not top-predator diet shifts

Authors: MILLER-TER KUILE, ANA - UNIVERSITY OF CALIFORNIA; APIGO, AUSTEN - UNIVERSITY OF CALIFORNIA; BUI, AN - UNIVERSITY OF CALIFORNIA; BUTNER, KIRSTEN - UNIVERSITY OF CALIFORNIA; CHILDRESS, JASMINE - UNIVERSITY OF CALIFORNIA; COPELAND, STEPHANIE - UNIVERSITY OF CALIFORNIA; DIFIORE, BARTHOLOMEW - UNIVERSITY OF CALIFORNIA; FORBES, ELIZABETH - UNIVERSITY OF CALIFORNIA; KLOPE, MAGGIE - UNIVERSITY OF CALIFORNIA; MOTTA, CARINA - UNIVERSITY OF CALIFORNIA; ORR, DEVYN; PLUMMER, KATHERINE - STANFORD UNIVERSITY; PRESTON, DANIEL - COLORADO STATE UNIVERSITY; YOUNG, HILLARY - UNIVERSITY OF CALIFORNIA

Submitted to: Biology Letters
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/6/2022
Publication Date: 10/26/2022
Citation: Miller-ter Kuile, A., Apigo, A., Bui, A., Butner, K., Childress, J.N., Copeland, S., DiFiore, B.P., Forbes, E.S., Klope, M., Motta, C.I., Orr, D.A., Plummer, K.A., Preston, D.L., Young, H.S. 2022. Changes in invertebrate food web structure between high- and low-productivity environments are driven by intermediate but not top-predator diet shifts. Biology Letters. 18(10). Article 20220364. https://doi.org/10.1098/rsbl.2022.0364.
DOI: https://doi.org/10.1098/rsbl.2022.0364

Interpretive Summary: Predator-prey interactions can change across different habitats due to changes in resources (e.g. food, shelter), which in turn changes the types of species present and their relative abundances. As a result, environmental disturbances, such as plant species invasions, can alter interactions among predators and their prey. Such effects can reverberate throughout entire food webs, and ultimately impact how resilient food webs are to further perturbations. However, predicting when and how changes in predator-prey interactions can occur as a result of species invasions and other disturbances remains a challenge. Given that human influences now shape a majority of the earth's ecosystems, understanding what makes complex communities resilient (or not) to change is imperative. In this study, we address this challenge by combining two diet-tracing methods: diet DNA (using predator gut contents to determine the species identity of the organism they last ate) and stable isotope analyses (which yields more general information about the relative importance of food sources to each predator over time), for two groups of spiders (top predators and secondary predators). Combining these methods elucidates where in the food chain trophic structure shifts in response to change in plant community composition, which is linked to underlying changes in nutrient availability in the environment. We demonstrate that neither the isotopic niche nor diet DNA composition changes for top predators across invaded and uninvaded habitats. Conversely, secondary predators show clear turnover in diet DNA composition between the two environmental contexts. These findings highlight how the same shift in environmental context leads to differing dietary responses across spider predator groups. Taking this multi-trophic approach highlights how predator identity and predator diet preference can shape responses in predator-prey interactions across environments, improving predictive power for understanding the outcomes of ongoing anthropogenic change.

Technical Abstract: Predator–prey interactions shape ecosystem stability and are influenced by changes in ecosystem productivity. However, because multiple biotic and abiotic drivers shape the trophic responses of predators to productivity, we often observe patterns, but not mechanisms, by which productivity drives food web structure. One way to capture mechanisms shaping trophic responses is to quantify trophic interactions among multiple trophic groups and by using complementary metrics of trophic ecology. In this study, we combine two diet-tracing methods: diet DNA and stable isotopes, for two trophic groups (top predators and intermediate predators) in both low- and high-productivity habitats to elucidate where in the food chain trophic structure shifts in response to changes in underlying ecosystem productivity. We demonstrate that while top predators show increases in isotopic trophic position (d15N) with productivity, neither their isotopic niche size nor their DNA diet composition changes. Conversely, intermediate predators show clear turnover in DNA diet composition towards a more predatory prey base in high-productivity habitats. Taking this multi-trophic approach highlights how predator identity shapes responses in predator–prey interactions across environments with different underlying productivity, building predictive power for understanding the outcomes of ongoing anthropogenic change.