Using eDNA to understand predator–prey interactions influenced by invasive species

Oecologia https://doi.org/10.1007/s00442-023-05434-6 ORIGINAL RESEARCH Using eDNA to understand predator–prey interactions influenced by invasive species Maria Riaz1,2,3 · Dan Warren4,5 · Claudia Wittwer1,2,3 · Berardino Cocchiararo1,2 · Inga Hundertmark6 · Tobias Erik Reiners1,6 · Sven Klimpel2,3,5 · Markus Pfenninger2,5,7 · Imran Khaliq8,9,10 · Carsten Nowak1,2 Received: 16 March 2022 / Accepted: 3 August 2023 © The Author(s) 2023 Abstract Invasive predatory species may alter population dynamic processes of their prey and impact biological communities and ecosystem processes. Revealing biotic interactions, however, including the relationship between predator and prey, is a difficult task, in particular for species that are hard to monitor. Here, we present a case study that documents the utility of environmental DNA analysis (eDNA) to assess predator–prey interactions between two invasive fishes (Lepomis gibbosus, Pseudorasbora parva) and two potential amphibian prey species, (Triturus cristatus, Pelobates fuscus). We used speciesspecific TaqMan assays for quantitative assessment of eDNA concentrations from water samples collected from 89 sites across 31 ponds during three consecutive months from a local amphibian hotspot in Germany. We found a negative relationship between eDNA concentrations of the predators (fishes) and prey (amphibians) using Monte-Carlo tests. Our study highlights the potential of eDNA application to reveal predator–prey interactions and confirms the hypothesis that the observed local declines of amphibian species may be at least partly caused by recently introduced invasive fishes. Our findings have important consequences for local conservation management and highlight the usefulness of eDNA approaches to assess ecological interactions and guide targeted conservation action. Keywords Amphibian decline · Biotic interactions · Environmental DNA · Invasive species · Predator–prey interactions Introduction Communicated by Leon A. Barmuta. * Maria Riaz 1 Conservation Genetics Section, Senckenberg Research Institute and Natural History Museum, 63571 Frankfurt, Gelnhausen, Germany 2 LOEWE Centre for Translational Biodiversity Genomics (LOEWE-TBG), Senckenberganlage 25, 60325 Frankfurt Am Main, Germany 3 Faculty of Biological Sciences, Institute for Ecology, Evolution and Diversity, Goethe University, Max‑Von‑Laue‑Straße 9, 60438 Frankfurt Am Main, Germany 4 Biodiversity and Biocomplexity Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan Revealing biotic interactions is a challenging but important task to understand the ecological integrity and functioning of biological communities (Beauchamp et al. 2007; Lee et al. 2019). The intrinsic complexity of biotic interactions poses 5 Senckenberg Biodiversity and Climate Research Centre (BiK-F), Senckenberganlage 25, 60325 Frankfurt Am Main, Germany 6 Hessische Gesellschaft Für Ornithologie Und Naturschutz (HGON E. V.), Lindenstrasse 5, 61209 Echzell, Germany 7 Institute for Molecular and Organismic Evolution, Johannes Gutenberg University, Johann‑Joachim‑Becher‑Weg 7, 55128 Mainz, Germany 8 Department of Education, Punjab, Pakistan 9 Department of Aquatic Ecology Eawag (Swiss Federal Institute of Aquatic Science and Technology) Überlandstrasse 133, 8600 Dübendorf, Switzerland 10 Snow and Landscape Research (WSL), Swiss Federal Institute for Forest, Flüelastr. 11, 7260 Davos Dorf, Switzerland 13 Vol.:(0123456789) Oecologia a particular difficulty when aiming to understand predator–prey interactions in aquatic habitats (Campanella et al. 2019). This challenge can be partly attributed to established methods for monitoring the presence and abundance of species, including direct catch (Haubrock et al. 2020), electrofishing (Allard et al. 2014), radio telemetry, hydroacoustics (Campanella et al. 2019), visual counting, and trawls (Rodgers et al. 2017; Stevenson 2018). These methods are highly dependent upon the probability of species being present at a specific time and place, the effects of water quality on the visual census, and the investigator’s expertise and level of sampling effort (Jerde et al. 2011; Hayward et al. 2015). In addition, some of the above-listed tools are somewhat invasive and therefore detrimental to the monitored species and may disturb the habitat to various degrees (Meyer et al. 2021). In recent times, DNA-based studies have demonstrated promising and novel insights for evaluating predator–prey interactions in terrestrial and aquatic habitats (Roslin and Majaneva 2016). For instance, gut contents have been used to reveal trophic interactions, population structure and feeding preferences in pioneer sites of glacier forelands (Sint et al. 2019), predatory vampire bats (Bohmann et al. 2018), fisheries discard in marine fauna (Lejeune et al. 2022), terrestrial arthropods (Paula et al. 2016), spiders (Saqib et al. 2021) and among coral reefs (Casey et al. 2019). However, the application and resolution of invasive genetic methods involving catching and sampling of organisms may be unsuitable for rare, endangered, or elusive species. A robust, sensitive, and widely applicable non-invasive monitoring method to assess species interactions would therefore be of considerable importance given the rapid spread of invasive species in the Anthropocene (Cucherousset and Olden 2011). Environmental DNA (eDNA) as a non-invasive and robust assessment method has undergone rapid improvement during the past decade, involving quantitative detection of single species as well as metabarcoding-based assessment of entire communities (Taberlet et al. 2012; Thomsen et al. 2012; Bálint et al. 2017). Interestingly, however, only a few studies to date have assessed the potential of eDNA beyond mere species detection (Yamanaka and Minamoto 2016; Pawlowski et al. 2018; Riaz et al. 2020), pathogen surveillance (Mosher et al. 2017), and diet analysis to reveal trophic network structures (Thomsen and Sigsgaard 2019; Djurhuus et al. 2020; Meyer et al. 2020; D’Alessandro and Mariani 2021; Banerjee et al. 2022). eDNA may give a boost to the fields of ecology and population dynamics, particularly because of its ability to detect rare, unseen individuals for nearly all taxon types (Ficetola et al. 2008; Herder et al. 2014; Keskin 2014; Hunter et al. 2015) and across different habitats (Bohmann et al. 2014; Thomsen and Willerslev 2015; Sasso et al. 2017). 13 Here, we explored the potential of eDNA for assessment of biotic interactions using an aquatic study system involving invasive predatory fishes and locally endangered amphibian species as potential prey. In aquatic ecosystems, biological invasions of predatory fish species may lead to increased competition and can result in the restructuring of trophic interactions (Bishop et al. 2012) which influence prey species abundances (Allentoft and O’Brien 2010). For instance, predation by invasive fish species is one c (...truncated)