DNA metabarcoding unveils multiscale trophic variation in a widespread coastal opportunist

Abstract

A thorough understanding of ecological networks relies on comprehensive information on trophic relationships among species. Since unpicking the diet of many organisms is unattainable using traditional morphology‐based approaches, the application of high‐throughput sequencing methods represents a rapid and powerful way forward. Here, we assessed the application of DNA metabarcoding with nearly universal primers for the mitochondrial marker cytochrome c oxidase I in defining the trophic ecology of adult brown shrimp, Crangon crangon, in six European estuaries. The exact trophic role of this abundant and widespread coastal benthic species is somewhat controversial, while information on geographical variation remains scant. Results revealed a highly opportunistic behaviour. Shrimp stomach contents contained hundreds of taxa (>1,000 molecular operational taxonomic units), of which 291 were identified as distinct species, belonging to 35 phyla. Only twenty ascertained species had a mean relative abundance of more than 0.5%. Predominant species included other abundant coastal and estuarine taxa, including the shore crab Carcinus maenas and the amphipod Corophium volutator. Jacobs’ selectivity index estimates based on DNA extracted from both shrimp stomachs and sediment samples were used to assess the shrimp's trophic niche indicating a generalist diet, dominated by crustaceans, polychaetes and fish. Spatial variation in diet composition, at regional and local scales, confirmed the highly flexible nature of this trophic opportunist. Furthermore, the detection of a prevalent, possibly endoparasitic fungus (Purpureocillium lilacinum) in the shrimp's stomach demonstrates the wide range of questions that can be addressed using metabarcoding, towards a more robust reconstruction of ecological networks.

From metabarcoding to metaphylogeography: separating the wheat from the chaff

“…This parameter was set for the COI fragment used here after comparing the number of MOTUs obtained at different values and checking that this number remained constant for values of d in the range of 9-13. The value of d = 13 has been previously used in other studies involving the same COI fragment (Mac ıas-Hern andez et al 2018, Kemp et al 2019, Siegenthaler et al 2019). The taxonomic assignment of the MOTU was performed using ecotag (Boyer et al 2016), which uses a local reference database and a phylogenetic tree-based approach (using the NCBI taxonomy) for assigning sequences without a perfect match.…”

Cobble community DNA as a tool to monitor patterns of biodiversity within kelp forest ecosystems

“…Metabarcoding has been successfully applied in a number of studies as a powerful and repeatable method for characterizing biodiversity (Hänfling et al, ; Leray & Knowlton, ). The flexibility of metabarcoding protocols allows the analyses of a wide range of sample types (sediment: Guardiola et al, , substrate: Wangensteen et al, , seawater: Bakker et al, , bulk invertebrate samples: Elbrecht & Leese, , stomach contents: Siegenthaler, Wangensteen, Benvenuto, Campos, & Mariani, and scat: Berry et al, ), to more recent approaches that utilize natural environmental samplers as a tool to survey marine biodiversity such as utilizing the diet profiles of benthic scavengers to assess fish diversity or harnessing water‐filtering sponges to sample environmental DNA (natural sampler DNA—nsDNA; Mariani, Baillie, Colosimo, & Riesgo, ; Siegenthaler, Wangensteen, Soto, et al, ). While metabarcoding of environmental samples has many limitations associated with primer performance, bioinformatic workflows and study design (Elbrecht, Hebert, & Steinke, ), it overcomes many morphology‐based challenges in identifying species at different levels (e.g.…”

Introduction: Special issue on species interactions, ecological networks and community dynamics – Untangling the entangled bank using molecular techniques

“…In a similar vein, molecular diet analysis sheds new light on the trophic position of individual species within larger communities and interaction networks. Siegenthaler et al () use metabarcoding of gut contents to establish the diet of the brown shrimp, Crangon crangon , in six European estuaries. The species turns out to be an extreme generalist, feeding on hundreds of taxa, with its overall diet dominated by crustaceans, polychaetes and fish.…”

“…The species turns out to be an extreme generalist, feeding on hundreds of taxa, with its overall diet dominated by crustaceans, polychaetes and fish. Substantial variation in diet at both regional and local scales adds to the impression of extreme flexibility in this common species (Siegenthaler et al, ), but also reveals the potential for bottom‐dwelling marine generalists to harvest the “environmental DNA” (Bohmann et al, ; Creer et al, ; Deiner et al, ) signal of broader fish communities for biomonitoring purposes.…”

“…Where Siegenthaler et al () use molecular techniques to identify what the shrimp feeds on, Tiusanen et al, () apply them to the opposite task of identifying which arthropods visit the flowers of several arctic Dryas species (all known as mountain avens). Targeting multiple sites around the Arctic, they too find an astonishing taxonomic range and richness, in this case of literally thousands of arthropod species sharing this common floral resource.…”