Using low volume eDNA methods to sample pelagic marine animal assemblages.

Environmental DNA (eDNA) is an increasingly useful method for detecting pelagic animals in the ocean but typically requires large water volumes to sample diverse assemblages. Ship-based pelagic sampling programs that could implement eDNA methods generally have restrictive water budgets. Studies that quantify how eDNA methods perform on low water volumes in the ocean are limited, especially in deep-sea habitats with low animal biomass and poorly described species assemblages. Using 12S rRNA and COI gene primers, we quantified assemblages comprised of micronekton, coastal forage fishes, and zooplankton from low volume eDNA seawater samples (n = 436, 380-1800 mL) collected at depths of 0-2200 m in the southern California Current. We compared diversity in eDNA samples to concurrently collected pelagic trawl samples (n = 27), detecting a higher diversity of vertebrate and invertebrate groups in the eDNA samples. Differences in assemblage composition could be explained by variability in size-selectivity among methods and DNA primer suitability across taxonomic groups. The number of reads and amplicon sequences variants (ASVs) did not vary substantially among shallow (<200 m) and deep samples (>600 m), but the proportion of invertebrate ASVs that could be assigned a species-level identification decreased with sampling depth. Using hierarchical clustering, we resolved horizontal and vertical variability in marine animal assemblages from samples characterized by a relatively low diversity of ecologically important species. Low volume eDNA samples will quantify greater taxonomic diversity as reference libraries, especially for deep-dwelling invertebrate species, continue to expand.

The Pelagic Species Trait Database, an open data resource to support trait-based ocean research.

Trait-based frameworks are increasingly used for predicting how ecological communities respond to ongoing global change. As species range shifts result in novel encounters between predators and prey, identifying prey 'guilds', based on a suite of shared traits, can distill complex species interactions, and aid in predicting food web dynamics. To support advances in trait-based research in open-ocean systems, we present the Pelagic Species Trait Database, an extensive resource documenting functional traits of 529 pelagic fish and invertebrate species in a single, open-source repository. We synthesized literature sources and online resources, conducted morphometric analysis of species images, as well as laboratory analyses of trawl-captured specimens to collate traits describing 1) habitat use and behavior, 2) morphology, 3) nutritional quality, and 4) population status information. Species in the dataset primarily inhabit the California Current system and broader NE Pacific Ocean, but also includes pelagic species known to be consumed by top ocean predators from other ocean basins. The aim of this dataset is to enhance the use of trait-based approaches in marine ecosystems and for predator populations worldwide.

Harnessing a mesopelagic predator as a biological sampler reveals taxonomic and vertical resource partitioning among three poorly known deep-sea fishes.

Pelagic predators are effective biological samplers of midtrophic taxa and are especially useful in deep-sea habitats where relatively mobile taxa frequently avoid observation with conventional methods. We examined specimens sampled from the stomachs of longnose lancetfish, Alepisaurus ferox, to describe the diets and foraging behaviors of three common, but poorly known deep-sea fishes: the hammerjaw (Omosudis lowii, n = 79, 0.3-92 g), juvenile common fangtooth (Anoplogaster cornuta, n = 91, 0.6-22 g), and juvenile Al. ferox (n = 138, 0.3-744 g). Diet overlap among the three species was high, with five shared prey families accounting for 63 ± 11% of the total prey mass per species. However, distinct differences in foraging strategies and prey sizes were evident. Resource partitioning was greatest between An. cornuta that specialized on small (mean = 0.13 ± 0.11 g), shallow-living hyperiid amphipods and O. lowii that specialized on large (mean = 0.97 ± 0.45 g), deep-dwelling hatchetfishes. Juvenile Al. ferox foraged on a high diversity of prey from both shallow and deep habitats. We describe the foraging ecologies of three midtrophic fish competitors and demonstrate the potential for biological samplers to improve our understanding of deep-sea food webs.

Pacific bluefin tuna, Thunnus orientalis, exhibits a flexible feeding ecology in the Southern California Bight.

Pacific bluefin tuna, Thunnus orientalis, migrates from spawning grounds in the western Pacific Ocean to foraging grounds in the California Current System (CCS), where they are thought to specialize on high energy, surface schooling prey. However, there has been substantial variability in estimates of forage availability in the CCS over the past two decades. To examine the foraging ecology of juvenile T. orientalis in the face this variability, we quantified the diet and prey energetics of 963 individuals collected in the Southern California Bight (SCB) from 2008 to 2016. Using classification and regression tree analysis, we observed three sampling periods characterized by distinct prey. In 2008, T. orientalis diet was dominated by midwater lanternfishes and enoploteuthid squids. During 2009-2014, T. orientalis consumed diverse fishes, cephalopods, and crustaceans. Only in 2015-2016 did T. orientalis specialize on relatively high energy, surface schooling prey (e.g. anchovy, pelagic red crab). Despite containing the smallest prey, stomachs collected in 2009-2014 had the highest number of prey and similar total energetic contents to stomachs collected in 2015-2016. We demonstrate that T. orientalis is an opportunistic predator that can exhibit distinct foraging behaviors to exploit diverse forage. Expanding our understanding of T. orientalis foraging ecology will improve our ability to predict its responses to changes in resource availability as well as potential impacts on the fisheries it supports.

Temporal Stability of Genetic Structure in a Mesopelagic Copepod.

Although stochasticity in oceanographic conditions is known to be an important driver of temporal genetic change in many marine species, little is known about whether genetically distinct plankton populations can persist in open ocean habitats. A prior study demonstrated significant population genetic structure among oceanic gyres in the mesopelagic copepod Haloptilus longicornis in both the Atlantic and Pacific Oceans, and we hypothesized that populations within each gyre represent distinct gene pools that persist over time. We tested this expectation through basin-scale sampling across the Atlantic Ocean in 2010 and 2012. Using both mitochondrial (mtCOII) and microsatellite markers (7 loci), we show that the genetic composition of populations was stable across two years in both the northern and southern subtropical gyres. Genetic variation in this species was partitioned among ocean gyres (FCT = 0.285, P < 0.0001 for mtCOII, FCT = 0.013, P < 0.0001 for microsatellites), suggesting strong spatial population structure, but no significant partitioning was found among sampling years. This temporal persistence of population structure across a large geographic scale was coupled with chaotic genetic patchiness at smaller spatial scales, but the magnitude of genetic differentiation was an order of magnitude lower at these smaller scales. Our results demonstrate that genetically distinct plankton populations persist over time in highly-dispersive open ocean habitats, and this is the first study to rigorously test for temporal stability of large scale population structure in the plankton.

Multilocus evidence for globally distributed cryptic species and distinct populations across ocean gyres in a mesopelagic copepod.

Zooplanktonic taxa have a greater number of distinct populations and species than might be predicted based on their large population sizes and open-ocean habitat, which lacks obvious physical barriers to dispersal and gene flow. To gain insight into the evolutionary mechanisms driving genetic diversification in zooplankton, we developed eight microsatellite markers to examine the population structure of an abundant, globally distributed mesopelagic copepod, Haloptilus longicornis, at 18 sample sites across the Atlantic and Pacific Oceans (n = 761). When comparing our microsatellite results with those of a prior study that used a mtDNA marker (mtCOII, n = 1059, 43 sample sites), we unexpectedly found evidence for the presence of a cryptic species pair. These species were globally distributed and apparently sympatric, and were separated by relatively weak genetic divergence (reciprocally monophyletic mtCOII lineages 1.6% divergent; microsatellite FST ranging from 0.28 to 0.88 across loci, P < 0.00001). Using both mtDNA and microsatellite data for the most common of the two species (n = 669 for microsatellites, n = 572 for mtDNA), we also found evidence for allopatric barriers to gene flow within species, with distinct populations separated by continental landmasses and equatorial waters in both the Atlantic and Pacific Ocean basins. Our study shows that oceanic barriers to gene flow can act as a mechanism promoting allopatric diversification in holoplanktonic taxa, despite the high potential dispersal abilities and pelagic habitat for these species.