Characterizing the secret diets of siphonophores (Cnidaria: Hydrozoa) using DNA metabarcoding

Abstract

Siphonophores (Cnidaria: Hydrozoa) are abundant and diverse gelatinous predators in open-ocean ecosystems. Due to limited access to the midwater, little is known about the diets of most deep-dwelling gelatinous species, which constrains our understanding of food-web structure and nutrient flow in these vast ecosystems. Visual gut-content methods can rarely identify soft-bodied rapidly-digested prey, while observations from submersibles often overlook small prey items. These methods have been differentially applied to shallow and deep siphonophore taxa, confounding habitat and methodological biases. DNA metabarcoding can be used to assess both shallow and deep species’ diets under a common methodological framework, since it can detect both small and gelatinous prey. We (1) further characterized the diets of open-ocean siphonophores using DNA metabarcoding, (2) compared the prey detected by visual and molecular methods to evaluate their technical biases, and (3) evaluated tentacle-based predictions of diet. To do this, we performed DNA metabarcoding analyses on the gut contents of 39 siphonophore species across depths to describe their diets, using six barcode regions along the 18S gene. Taxonomic identifications were assigned using public databases combined with local zooplankton sequences. We identified 55 unique prey items, including crustaceans, gelatinous animals, and fish across 47 siphonophore specimens in 24 species. We reported 29 novel predator-prey interactions, among them the first insights into the diets of nine siphonophore species, many of which were congruent with the dietary predictions based on tentilla morphology. Our analyses detected both small and gelatinous prey taxa underrepresented by visual methods in species from both shallow and deep habitats, indicating that siphonophores play similar trophic roles across depth habitats. We also reveal hidden links between siphonophores and filter-feeders near the base of the food web. This study expands our understanding of the ecological roles of siphonophores in the open ocean, their trophic roles within the ‘jelly-web’, and the importance of their diversity for nutrient flow and ecosystem functioning. Understanding these inconspicuous yet ubiquitous predator-prey interactions is critical to predict the impacts of climate change, overfishing, and conservation policies on oceanic ecosystems.

Vertical trophic structure and niche partitioning of gelatinous predators in a pelagic food web: Insights from stable isotopes of siphonophores

“…Isotope values generally suggest that cluster 3 species are feeding on lower trophic level taxa, likely small crustaceans. This supports previous diet studies (Purcell 1981a;Damian-Serrano et al 2022), which identified copepods, ostracods, and other small crustaceans as prey items. The fourth cluster (Agalma, Sphaeronectes, Frillagalma, Forskalia, Chuniphyes, Rosacea, and Praya) also includes both calycophorans and physonects.…”

“…Relative to other CSIA‐AA literature, the span of ~1.5 trophic positions is ecologically reasonable for siphonophores. Calycophorans, for example, primarily consume smaller crustaceans (e.g., copepods, ostracods) (Purcell 1981 a ; Damian‐Serrano et al 2022). Décima et al (2013) used CSIA‐AA on the copepod Calanus pacificus in the California Current Ecosystem and estimated their Trophic Position Glu‐Phe as 1.8 to 2.5.…”

“…The cluster column was determined by a Ward's hierarchical cluster analysis of bulk isotope values. Hypothesized diets were based on a limited number of previous studies that characterized siphonophore diets from remotely operated vehicle observations (Choy et al 2017), gut contents analysis (Purcell 1981a,b), or metabarcoding of gut contents (Damian-Serrano et al 2022).…”

“…Stable isotope analysis is particularly advantageous for siphonophores because it requires a tissue sample and not the collection of a fully intact colony. Stable isotope values can provide trophic position estimates and diet integrated over time (determined by tissue turnover rate), unlike dietary snapshots inferred from gut contents analysis (Purcell 1981 a ), gut content DNA metabarcoding (Damian‐Serrano et al 2022), or in situ feeding observations (Choy et al 2017).…”

Distributed propulsion enables fast and efficient swimming modes in physonect siphonophores

“…Nanomia bijuga is a widely distributed physonect siphonophore ( 6 ). Inhabiting depths from the sea surface to at least 800 m, N. bijuga performs twice daily migrations of hundreds of meters ( 6 , 7 ) and is an important predator on crustaceans in some regions ( 8 ); in Monterey Bay, it is the dominant gelatinous organism at midwater depths ( 9 , 10 ). Siphonophores are an order of colonial marine cnidarians; physonect siphonophores have the most complex modular architecture of any colonial organism with highly specialized individuals called zooids ( 11 – 13 ).…”