Characterization of species diversity of zooplankton is key to understanding, assessing, and predicting the function and future of pelagic ecosystems throughout the global ocean. The marine ...zooplankton assemblage, including only metazoans, is highly diverse and taxonomically complex, with an estimated ~28,000 species of 41 major taxonomic groups. This review provides a comprehensive summary of DNA sequences for the barcode region of mitochondrial cytochrome oxidase I (COI) for identified specimens. The foundation of this summary is the MetaZooGene Barcode Atlas and Database (MZGdb), a new open-access data and metadata portal that is linked to NCBI GenBank and BOLD data repositories. The MZGdb provides enhanced quality control and tools for assembling COI reference sequence databases that are specific to selected taxonomic groups and/or ocean regions, with associated metadata (e.g., collection georeferencing, verification of species identification, molecular protocols), and tools for statistical analysis, mapping, and visualization. To date, over 150,000 COI sequences for ~ 5600 described species of marine metazoan plankton (including holo- and meroplankton) are available via the MZGdb portal. This review uses the MZGdb as a resource for summaries of COI barcode data and metadata for important taxonomic groups of marine zooplankton and selected regions, including the North Atlantic, Arctic, North Pacific, and Southern Oceans. The MZGdb is designed to provide a foundation for analysis of species diversity of marine zooplankton based on DNA barcoding and metabarcoding for assessment of marine ecosystems and rapid detection of the impacts of climate change.
We analyzed the seasonal and interannual variability of the planktonic communities in a densely sampled region of the northeastern Chukchi Sea as part of a multidisciplinary ecosystem study from 2008 ...to 2010. Observations of chlorophyll-a, inorganic macronutrients, and zooplankton (using both 150-μm and 505-μm mesh nets) were made within two 900-NM 2 grids (Klondike and Burger) at high spatial resolution three times each in 2008 and 2009, with a third grid (Statoil) sampled twice in 2010. Sea-ice conditions prior to sampling varied notably during the study: seasonal sea ice retreat was earlier and sea-surface temperatures (SSTs) were warmer in 2009 than in 2008, whereas SSTs for 2010 were intermediate between the 2008 and 2009 values. Eighty taxonomic categories of zooplankton, including 11 meroplanktonic categories, were recorded, with the greatest diversity found within the copepods (25 species), followed by the cnidarians (11 species). All species are typical for the region and most are seeded from the Bering Sea. A seasonal progression of the community structure was apparent over each survey area and was likely influenced by temperature. Cold oceanographic conditions in 2008 likely slowed growth and development of the zooplankton, such that holozooplankton abundance averaged 2389 and 106 individualsm–3 and biomass averaged 10.5 and 8.3mgDWm–3 in the 150- and 505-μm nets, respectively. An early phytoplankton bloom in 2009 apparently supported a zooplankton community of greater abundance, but moderate biomass, averaging 6842 and 189 individualsm–3, and 16.3 and 7.0mgDWm–3 in the 150- and 505-μm nets, respectively. Highest zooplankton abundance and biomass values among the three years occurred in 2010: 7396 and 198 individualsm–3 and 102.9 and 33.5mgDWm–3 in the 150- and 505-μm nets, respectively. Holozooplankton biomass changes were driven by increases in large-bodied, lipid-rich copepods. The contribution of meroplankton was substantial in this shallow-water ecosystem: numerically, they contributed 28% in 2008, 8% in 2009 and 56% in 2010 to the total zooplankton community and 43%, 27%, and 11%, respectively, terms of biomass for the 150-μm nets. Interannual differences in ice-melt timing, water temperatures, northward transport of water masses, and nutrients and chlorophyll concentrations resulted in highly variable pelagic productivity.
► Eighty taxonomic categories of zooplankton were observed in the study area; most are of Pacific Ocean affinity. ► Contribution of meroplankton was substantial. ► The seasonal progression of the community structure appears to be moderated by sea–ice and temperature. ► The planktonic community shows large interannual variability.
Abstract
Biodiversity of zooplankton is central to the functioning of ocean ecosystems, yet morphological taxonomic analysis requires teams of experts and detailed examination of many samples. ...Metabarcoding (DNA sequencing of short amplified regions of one or a few genes from environmental samples) is a powerful tool for analysis of the composition and diversity of natural communities. The 18S rRNA V9 hypervariable region was sequenced for 26 zooplankton samples collected from the Gulf of Maine, Georges Bank, and Mid-Atlantic Bight during ecosystem monitoring surveys by the U.S. Northeast Fisheries Science Center during 2002–2012. A total of 7 648 033 sequences and 22 072 operational taxonomic units (OTUs) were identified and classified into 28 taxonomic groups of plankton. Comparative analysis of molecular (V9 sequence numbers) and morphological (abundance counts) focused on seven taxonomic groups and revealed similar patterns of variation among years and regions. Sequence numbers and abundance counts showed positive correlation for all groups, with significant correlations (p < 0.05) for Calanoida, Gastropoda, and Chaetognatha. Shannon diversity index values calculated using sequence numbers and abundance counts showed highly significant correlation (r = 0.625; p < 0.001) across all regions during 2002–2012. This study demonstrates the potential of metabarcoding for time-series analysis of zooplankton biodiversity, ocean ecosystem assessment, and fisheries management.
The calanoid copepod Calanus finmarchicus is one of the most abundant and ecologically important species of the zooplankton assemblage of the North Atlantic Ocean and occupies a pivotal position in ...the pelagic food web. This study used metabarcoding analysis (high throughput DNA sequencing of target gene regions) to examine the diversity of the copepod gut content, including both eukaryotic and prokaryotic components of the diet and microbiome. Zooplankton samples were collected during the 2013 EuroBASIN cruise of the R/V G.O. Sars, which crossed the North Atlantic to survey in the Norwegian, Icelandic, Irminger, and Labrador Seas. Zooplankton samples were examined microscopically for C. finmarchicus; species identification was confirmed by genetic markers based on insertion-deletion sequence variation. DNA was extracted from the dissected gut contents of adult female copepods and sequenced for eukaryotic 18S V4 and prokaryotic 16S V3–V4 rRNA hypervariable regions. Prokaryotes identified in the gut contents of all copepods analyzed included Cyanobacteria, Proteobacteria, Bacteroidetes, Planctomycetes, Actinobacteria, and Acidobacteria. The eukaryotic gut content assemblage was diverse, dominated by Ocrophyta (diatoms), Dinophyta (dinoflagellates), Ciliophora (ciliates), as well as Cnidaria and Ctenophora. The diverse assemblage revealed by metabarcoding analysis of copepod gut contents likely represents prey, microbiome, parasites, symbionts, and pathogens. Significant differences in prokaryotic and eukaryotic diversity of the gut contents of copepods collected from four regional seas of the North Atlantic Ocean reflect and contribute to basin-scale differences in the pelagic food web of these ecosystems. This study provides evidence that diversity and variation of the copepod gut contents may both reflect and impact the functioning of pelagic food webs and regional variation in ocean ecosystems.
DNA-based analyses have become powerful tools for characterizing the metazoan biodiversity of diverse marine ecosystems. Metabarcoding (i.e., large-scale taxonomic identification of complex samples ...via high-throughput sequencing of a DNA barcode region) frequently uses hypervariable regions of the nuclear eukaryotic 18S ribosomal RNA (rRNA) gene. However, species-level taxonomic identification is hampered by the conservative nature of the 18S gene in comparison to the mitochondrial cytochrome oxidase I (COI) barcode gene. Additionally, metabarcoding relies on reference DNA sequence databases for classification of millions of unknown sequence reads and molecular operational taxonomic units (OTUs); databases that are at present depauperate for marine zooplankton taxa. Here, we characterized the mesozooplankton community for the Chukchi Borderland (CBL) region, western Arctic Ocean, through metabarcoding analysis of the V4 and V9 hypervariable regions of 18S rRNA and a portion of COI. Characterization of zooplankton diversity for the epipelagic and upper mesopelagic layers (0–500 m) was based upon 17 metazoan taxonomic categories encompassing 24 orders in 14 classes. Taxonomic classification using the V4 and V9 markers was most reliable for orders, with copepods dominating OTU counts. To increase taxonomic resolution and allow detection of species, V4, V9, and COI OTUs were classified against DNA sequence databases for the Arctic Ocean for the subclass Copepoda. The geographic region-specific databases for 18S rRNA and COI resulted in the detection and identification of 6 genera and 49 species of copepods representing 23 families, a marked increase in the taxonomic classification of the 18S rRNA markers. The greatest copepod species diversity was captured with V4 (34 species) followed by COI (28 species) with the least copepod diversity detected by V9 (5 species). Our results demonstrate the power of using multiple gene markers, with DNA reference databases that are specific to the geographic region of interest, providing more accurate metabarcoding biodiversity measures for the copepod assemblages compared to universal metazoan sequence reference databases. Results from this study highlight the need for continued DNA barcode sequencing to increase species representation in the reference sequence databases that are crucial for accurate characterization of mesozooplankton communities.
Abstract
The euphausiid genus Stylocheiron includes species with biogeographical distributions spanning multiple ocean basins. Despite their circumglobal distributions, the species show low levels of ...genetic diversity and little or no evidence of population structure based on the mitochondrial cytochrome oxidase I (COI) barcode region, with the exception of a possible cryptic species within Stylocheiron affine. Stylocheiron elongatum showed < 1% variation of the COI barcode region among populations in different ocean basins, but analysis of samples collected from the Florida Current (February, 1993) and Gulf Stream Meander Region (April, 1993) in the Northwest Atlantic Ocean revealed small-but-significant genetic differentiation between samples based on a different section of COI and mitochondrial cytochrome b (CYB). Both COI and CYB showed large haplotype and small nucleotide diversities, departures from neutral expectations, and haplotype networks consistent with persistent genetic structuring of the species population. These patterns of diversity indicate the presence of selection driving population divergence. We hypothesize that position-keeping by this deep-living, non-migrating euphausiid species may prevent genetic homogenization (panmixia) in the dynamic Gulf Stream System. This study demonstrates the importance of analyzing patterns of genetic diversity and structure at regional and global scales to understand the ecological and evolutionary processes impacting marine zooplankton.
Observations of the marine carbonate system were made in 2010 in the northeastern Chukchi Sea to constrain the seasonal progression of carbonate mineral saturation states (Ω) throughout the water ...column and determine the air–sea flux of carbon dioxide (CO2). As sea ice retreats from the Chukchi Shelf, primary production consumes dissolved inorganic carbon (DIC) in the euphotic zone causing pH and carbonate mineral saturation states to increase. Throughout the summer and early autumn months of 2010, saturation states for calcite and aragonite ranged from 2.5 to 4.0 and 1.5 to 2.5, respectively, well about the saturation horizon of 1.0. Much of the organic matter produced during the bloom was vertically exported from the relatively small study area leading to an uptake of CO2 from the atmosphere of at least 340,000kg-C. The exported organic matter settled near the bottom and was remineralized back into DIC, causing concentrations to increase sharply, particularly in autumn months, driving down pH to as low as 7.75 and suppressing the concentrations of important carbonate minerals to the point that aragonite became undersaturated. The data showed a definitive seasonal progression of this process with aragonite becoming partially undersaturated along the bottom in September, and broadly undersaturated in October. While carbonate saturation states would naturally be suppressed by the high rates of export production and the accumulation of DIC near the bottom, the penetration of anthropogenic CO2 into the water column (ocean acidification) has caused these observed undersaturations, which will likely expand as CO2 levels in the atmosphere continue to rise in the coming decades.
•The northeastern Chukchi Sea is a strong seasonal sink for atmospheric CO2.•Removal of CO2 from surface layer increases carbonate mineral saturation states.•Mineralization of organic matter suppresses carbonate mineral saturation states.•Aragonite can become undersaturated near the bottom in late summer and fall.
The first record of the parasite Alebion carchariae in the waters of Ascension Island collected from Galapagos sharks, Carcharhinus galapagensis (Carcharhinidae), is described. No previous record of ...this parasite exists for Ascension Island, nor have Galapagos sharks previously been listed as a host. Specimens of A. carchariae were identified using morphological techniques and DNA barcoding of the cytochrome c oxidase I subunit (COI) gene. This study provides the first COI barcodes for this species and a brief review of known hosts. We recommend further research to understand the life cycle of this parasite, its plasticity in terms of host/habitat selection, and to determine the implications of its presence on the hosts it inhabits.
The dramatic warming of the Arctic Ocean will impact pelagic ecosystems in complex ways, including shifting patterns of species distribution and abundance, and altering migration pathways and ...population connectivity. The Phylum Chaetognatha (arrow worms) are abundant in the zooplankton assemblage and are highly effective predators, with key roles in pelagic food webs. They are useful indicator species for impacts of climate change on marine ecosystems. This study examined the population genetic diversity, structure and connectivity of the chaetognath, Eukrohnia hamata, based on sampling from six regions defined by geography, bathymetry, and major currents flowing through the Arctic Ocean. A 650-bp region of mitochondrial cytochrome oxidase I (mtCOI) sequenced for 130 specimens resulted in 78 haplotypes and very high haplotype diversity. Analysis of mtCOI haplotype frequencies provided no evidence of population genetic structure. Genomic Single Nucleotide Polymorphisms (SNPs) detected from the same specimens by double-digest Restriction-Associated Digestion (ddRAD) confirmed high levels of gene flow among the regions, but supported the genetic distinctiveness of two population clusters: Atlantic-Arctic versus Pacific-Arctic. Removal of SNPs subject to selection resulted in slightly higher probability of three clusters, and suggested the possibility of local adaptation of regional populations of E. hamata. Comparative analysis revealed evidence that random selection of subsets of SNPs, perhaps impacted by different ecological and (micro) evolutionary drivers, can result in marked differences in numbers and distributional patterns of clusters and associated variation in F-statistics. Analysis of population connectivity using SNPs supported the primary migration pathway via flow from the Atlantic to the Pacific Arctic regions.
Euphausiids are an ecologically significant and abundant group of marine zooplankton that form key links between primary producers and consumers in pelagic food webs throughout the world ocean. The ...euphausiid species,
Thysanoessa inermis
and
T. raschii
, have boreal-Arctic distributions, occurring in the North Atlantic, North Pacific, and Arctic Oceans. The species differ in depth ranges and habitat preferences:
T. raschii
is found in coastal waters on continental shelf habitats, while
T. inermis
is abundant in slope and deep water regions. Population genetic analysis based on DNA sequence variation of the mitochondrial cytochrome oxidase I (COI) barcode region was carried out for identified specimens of
T. inermis
and
T. raschii
collected in the Arctic (Beaufort/Chukchi and Norwegian Seas, Svalbard Area) and North Atlantic (Gulf of St. Lawrence, Labrador Sea, Iqaluit, Hudson Bay). Populations of
T. inermis
in the N. Atlantic showed high connectivity, but were genetically isolated from the Beaufort/Chukchi Sea population. Population genetic diversity of
T. inermis
showed high haplotype and nucleotide diversity and no departures from neutral expectations. In contrast,
T. raschii
showed lower haplotype and nucleotide diversity, with highly significant departures from neutral expectations. A possible hypothesis is that
T. raschii
experienced a significant historical demographic event (e.g., population bottleneck), while
T. inermis
maintained a stable population over recent evolutionary history. The results provide new insights into population dynamics and implications for responses to climate change of these key euphausiid species for the Arctic Ocean.
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