Marine Microzooplankton Research Articles

Linear scaling between microbial predator and prey densities in the global ocean.

It has been proposed that microbial predator and prey densities are related through sublinear power laws. We revisited previously published biomass and abundance data and fitted Power-law Biomass Scaling Relationships (PBSRs) between marine microzooplankton predators (Z) and phytoplankton prey (P), and marine viral predators (V) and bacterial prey (B). We analysed them assuming an error structure given by Type II regression models which, in contrast to the conventional Type I regression model, accounts for errors in both the independent and the dependent variables. We found that the data support linear relationships, in contrast to the sublinear relationships reported by previous authors. The scaling exponent yields an expected value of 1 with some spread in different datasets that was well-described with a Gaussian distribution. Our results suggest that the ratios Z/P, and V/B are on average invariant, in contrast to the hypothesis that they systematically decrease with increasing P and B, respectively, as previously thought.

Tintinnid ciliates (marine microzooplankton) of the Ross Sea

For the Ross Sea, the only Marine Protected Area in Antarctica, available data on the tintinnid ciliates of the marine microzooplankton are mostly limited to nearshore waters near Terra Nova Bay or the vicinity of the McMurdo Sound. Here, we report results from a geographically extensive sampling across the Ross Sea conducted in December 2020. Material from plankton net tows (20 µm mesh), made at 38 stations spanning over 30° of latitude, was examined. We found 11 tintinnid species of varying commonality or rarity, many showing considerable morphological variability that is here documented. We found four forms that had not been previously reported from the Ross Sea. Based on our findings and previous reports, we assembled a species accumulation curve showing the growth in the inventory of tintinnid species recorded from the Ross Sea as a function of sampling effort and time since 1983. Extrapolation of the species accumulation curve, derived from sampling over the last 37 years, indicates that continued sampling will likely provide new species records, suggesting that the Ross Sea is under-sampled at present. This complicates efforts to detect temporal changes in species compositions, at least with regard to tintinnid ciliates. Comparing species accumulation curves for the Ross Sea and the relatively well-studied Weddell Sea, it appears that the Ross Sea may be more species-rich.

Notes on the Occurrence of Tintinnid Ciliates, and the Nasselarian Radiolarian Amphimelissa setosa of the Marine Microzooplankton, in the Chukchi Sea (Arctic Ocean) Sampled each August from 2011 to 2020

Here we summarize the results from 10 cruises in the Chukchi Sea, in August, each year from 2011 to 2020. Samples for the qualitative analysis of the microzooplankton were obtained from stations located across the Chukchi Sea using a 20μm plankton net. Conditions encountered, in terms of sea ice coverage and chlorophyll concentrations, varied widely from year to year without any obvious relationship with the composition of the microzooplankton assemblage. Examining a total of 242 samples gathered, we found a total of 44 tintinnid species (morphologically distinct forms). Plotting cumulative number of tintinnid species encountered vs cumulative number of samplings gave a typical species accumulation curve showing no sign of saturation suggesting that continued sampling in the Chukchi Sea will likely yield increases in the tintinnid species catalogue. The tintinnid species found ranged widely in lorica opening diameters (LOD) from about 11 μm to 80 μm in diameter. However, the median size of the LOD of the tintinnid assemblages varied little from year to year ranging only from about 30 μm to 40 μm. Most of the forms encountered were found in samples from only 1 or 2 cruises. Very few forms were found every year throughout the 10 years of sampling. These were 5 species of tintinnids (Acanthostomella norvegica, Leprotintinnus pellucidus, Pytchocylis obtusa, Salpingella acuminata, Salpingella faurei) and the nasselarian radiolarian Amphimelissa setosa. Examples of the morphological variability observed among individuals of Acanthostomella norvegica and Pytchocylis obtusa within single samples are shown with some individuals easily confused with forms described as other species are shown. To our knowledge, our data are the most extensive data set on Chukchi Sea microplankton. We provide all of the data recorded, which may serve as a baseline from which to assess changes projected in Arctic Sea systems, in a supplementary data file.

A note on the differences found between examining whole water vs. phytoplankton net (52 μm mesh) samples to characterize abundance and community composition of tintinnid ciliates (marine microzooplankton)

AbstractMost tintinnid species have a shortest linear dimension < 50 μm. Hence, a priori, nets of mesh sizes ≥ 50 μm will likely under‐sample most tintinnid species. However, studies often appear (23 since 2015) using sampling with nets of meshes sizes ≥ 50 μm, reporting both tintinnid concentrations, and community composition. How biased are results from using coarse mesh nets? We provide a comparison of whole water vs. net sampling based on fortuitous, that is, unplanned, parallel sampling. Pairs of samples from a standard monitoring station in the Bay of Villefranche (N.W. Mediterranean Sea) taken on 44 dates from 2013 to 2018 were compared. Tintinnids were enumerated in settled material from a water column sample, an integration of six discrete depth samples between 5 and 70 m, prepared for analysis of phytoplankton composition and in material from a plankton net (52 μm mesh) tow from 70 to 0 m, taken the same day. Despite the large confidence limits due to low raw cell counts from whole water samples, cell concentration estimates were about an order of magnitude higher than those from plankton net samples and frequently biomass estimates as well. Community composition also differed. The most common species in whole water samples were small (diameter ≤ 20 μm), and some common forms were absent, or nearly, from the net samples. We show that, while valuable for collecting larger and rarer species, coarse net samples do not yield robust estimations of overall concentrations, nor allow identification of the dominant tintinnid species.

Novel insights into the genetic diversity of Parafavella based on mitochondrial CO1 sequences

AbstractWe used both nuclear ribosomal genes (28S rDNA, 18S rDNA, 5.8S rDNA, internal transcribed spacer regions: ITS1, ITS2) and mitochondrial CO1 sequences to group or distinguish morphotypes of Parafavella, a problematic genus of tintinnid ciliates of the marine microzooplankton. We sequenced 30 single cells of Parafavella from the Bering Sea, the Greenland Sea, and the East/Japan Sea. Sequences were obtained from 4 morphotypes, typically ascribed to P. gigantea, P. greenlandica, P. jorgenseni, and P. subrotundata and from GenBank, the nuclear ribosomal genes of P. parumdentata were retrieved. Cells of the five morphotypes had identical 18S and 5.8S gene sequences. ITS1, ITS2 and 28S sequences produced two clusters: one grouping P. greenlandica and P. parumdentata and the other grouping P. jorgenseni, P. gigantea, and P. subrotundata. In contrast, CO1 nucleotide data yielded eight haplotypes clustered into five groups: one composed of P. greenlandica morphotypes, two distinct haplotypes of P. jorgenseni, and two distinct haplotypes of P. gigantea with one including P. subrotundata morphotypes. We investigated the co‐occurrence of different morphotypes in samples from sites across a large gradient of latitude and concentrations of Parafavella cells. Natural communities contained 2–6 different morphotypes. We conclude that both crypticity and polymorphism characterize Parafavella, as known for other tintinnid genera.

Effects of small-scale turbulence on growth and grazing of marine microzooplankton

We report the effects of small-scale turbulence at realistic intensity (e = 1.1 × 10−2 cm2 s−3) on the growth and grazing rates of three marine heterotrophic dinoflagellates (Peridiniella danica, Gyrodinium dominans and Oxyrrhis marina) and one ciliate (Mesodinium pulex). All the dinoflagellates showed a reduction of volume-based growth rates, whereas M. pulex did not. P. danica was the most affected by small-scale turbulence, followed by G. dominans, and O. marina. Turbulence slightly increased O. marina ingestion rates, but this increase was not statistically significant. G. dominans and M. pulex ingestion rates were modestly lower under turbulence, and P. danica completely ceased feeding in turbulent treatments. Gross growth efficiencies of G. dominans and O. marina were negatively affected by turbulence, whereas they remained unaltered for M. pulex. P. danica feeding and growth rates in the presence of turbulence were close to zero. Overall, there was a negative relationship between the effects of turbulence on ingestion rates and the time needed to process a prey item. Neglecting the effects of turbulence in microzooplankton grazing estimates in the field could produce biased approximations of their impacts on primary producers.

Diel feeding rhythms in marine microzooplankton: effects of prey concentration, prey condition, and grazer nutritional history

In this study, we aim at disentangling the causes and consequences of diel feeding rhythms in marine microzooplankton. We focused on the diel feeding activity of two heterotrophic dinoflagellate species, Gyrodinium dominans (one laboratory strain) and Oxyrrhis marina (laboratory cultivated and wild strains). We observed higher ingestion during the day in both dinoflagellate species. Feeding rhythms appeared to be independent of circadian changes in prey biochemical composition. Grazers fed with prey under stationary phase, with equivalent stoichiometric composition between day and night, showed 5 (G. dominans) and 10 (O. marina) times higher ingestion rates during the day. Previous grazer feeding history (starved vs well-fed) did not affect the feeding rhythm. However, prey concentration altered the rhythm; food limiting conditions reduced the amplitude of the rhythms. Our results establish a resource dependence of diel periodicity in microzooplankton grazing, which can have unanticipated consequences for standard field dilution grazing experiments.

Tintinnid ciliates of the marine microzooplankton in Arctic Seas: a compilation and analysis of species records

We set out to examine a postulated latitudinal trend in species richness within the Arctic Ocean. We compiled species records of tintinnid ciliates in the Arctic from the literature and added our own unpublished Chukchi Sea data to produce a database (available as an Online Resource data file) consisting of 1427 records of 89 species from 414 locations above 65°N sampled from 1885 to 2015. While there was no trend of species richness throughout the Arctic, there was a significant positive relationship between species richness and the number of sites sampled in a 2° band, suggesting a sampling effect. Plotting cumulative numbers of species and cumulative number of sites sampled by year, we found a linear relationship in log cumulative numbers of species and log sites sampled, and a lack of a plateau in the species accumulation trend. Species records are highly dominated by four species, accounting for 45% of the records: Acanthostomella norvegica, Parafavella denticulata, Ptychocylis obtusa and Salpingella acuminata, all of which, except S. acuminata, have long been suspected to be morphologically variable, with different morphotypes given undue species status. Pooling all reported species of Acanthostomella, Parafavella and Ptychocylis yielded little qualitative differences but considerable quantitative differences. We found large discrepancies in geographic coverage. We conclude that many zones projected to experience large changes in sea ice coverage are under-sampled. Based on the historical trend, the list of Arctic tintinnid ciliate species will likely continue to grow with new sampling, regardless of changes in the Arctic Seas.

Toxic effects of chemical dispersant Corexit 9500 on water flea Daphnia magna.

In 2010, approximately 2.1 million gallons of chemical dispersants, mainly Corexit 9500, were applied in the Gulf of Mexico to prevent the oil slick from reaching shorelines and to accelerate biodegradation of oil during the Deepwater Horizon oil spill. Recent studies have revealed toxic effects of Corexit 9500 on marine microzooplankton that play important roles in food chains in marine ecosystems. However, there is still little known about the toxic effects of Corexit 9500 on freshwater zooplankton, even though oil spills do occur in freshwater and chemical dispersants may be used in response to these spills. The cladoceran crustacean, water flea Daphnia magna, is a well-established model species for various toxicological tests, including detection of juvenile hormone-like activity in test compounds. In this study, we conducted laboratory experiments to investigate the acute and chronic toxicity of Corexit 9500 using D. magna. The acute toxicity test was conducted according to OECD TG202 and the 48 h EC50 was 1.31 ppm (CIs 0.99-1.64 ppm). The reproductive chronic toxicity test was performed following OECD TG211 ANNEX 7 and 21 days LOEC and NOEC values were 4.0 and 2.0 ppm, respectively. These results indicate that Corexit 9500 has toxic effects on daphnids, particularly during the neonatal developmental stage, which is consistent with marine zooplankton results, whereas juvenile hormone-like activity was not identified. Therefore, our findings of the adverse effects of Corexit 9500 on daphnids suggest that application of this type of chemical dispersant may have catastrophic impacts on freshwater ecosystems by disrupting the key food chain network. Copyright © 2016 John Wiley & Sons, Ltd.

Two distinct lineages in the radiolarian Order Spumellaria having different ecological preferences

The radiolarian group Spumellaria compose a diverse assemblage of marine microzooplankton with widespread geographic and vertical distributions. Spumellarians are useful paleoceanographic indicators, because their siliceous shells are preserved in the sediment at water depths deeper than the carbonate compensation depth. However, lack of detailed biologic knowledge has slowed the establishment of definitive taxonomic criteria, particularly for higher-level taxa. Recent studies on molecular phylogeny based on small subunit ribosomal DNA (SSU rDNA) confirmed spumellarian taxonomic position within radiolarians. However, these sequences were obtained from spumellarian specimens taken from subtropical to tropical surface waters. In order to clarify the taxonomy of widely distributed spumellarians, we obtained seven novel SSU rDNA sequences of specimens collected from the subarctic region. Our phylogenetic analyses revealed two distinct spumellarian groups (Spumellaria I and II) and six subgroups, which mostly correspond with family level taxonomy inferred from the inner shell structures. The Family Spongodiscidae is however separated into two lineages associated with Pyloniidae (Spumellaria I) and Coccodiscidae (Spumellaria II) in our phylogeny. Notably, two groups (Spumellaria I and II) are composed of ecologically different species: Spumellaria I consists of temperate to cold water species and one group of Spumellaria II consists of warm water species. These two distinct groups have probably evolved in cold and warm environments, respectively.

Global diversity of aloricate Oligotrichea (Protista, Ciliophora, Spirotricha) in marine and brackish sea water.

Oligotrichids and choreotrichids are ciliate taxa contributing to the multi-step microbial food web and episodically dominating the marine microzooplankton. The global diversity and distribution of aloricate Oligotrichea are unknown. Here, the geographic ranges of the 141 accepted species and their synonyms in marine and brackish sea water are analyzed, using hundreds of taxonomical and ecological studies; the quality of the records is simultaneously evaluated. The aloricate Oligotrichea match the moderate endemicity model, i.e., the majority (94) of morphospecies has a wide, occasionally cosmopolitan distribution, while 47 morphospecies show biogeographic patterns: they are restricted to single geographic regions and probably include 12 endemic morphospecies. These endemics are found in the Antarctic, North Pacific, and Black Sea, whereas the “flagship” species Strombidinopsis cercionis is confined to the Caribbean Sea. Concerning genera, again several geographic patterns are recognizable. The species richness is distinctly lower in the southern hemisphere than in the northern, ranging from nine morphospecies in the South Pacific to 95 in the North Atlantic; however, this pattern is probably caused by undersampling. Since the loss of species might affect higher trophical levels substantially, the aloricate Oligotrichea should not any longer be ignored in conservation issues. The ecophysiological diversity is considerably larger than the morphological, and even tops the richness of SSrRNA and ITS haplotypes, indicating that probably more than 83–89% of the diversity in aloricate Oligotrichea are unknown. The huge challenge to discover all these species can only be managed by combining the expertises of morphological taxonomists, molecular biologists, ecologists, and physiologists.

Another Really, Really Big Virus

Viruses with genomes larger than 300 kb and up to 1.2 Mb, which encode hundreds of proteins, are being discovered and characterized with increasing frequency. Most, but not all, of these large viruses (often referred to as giruses) infect protists that live in aqueous environments. Bioinformatic analyses of metagenomes of aqueous samples indicate that large DNA viruses are quite common in nature and await discovery. One issue that is perhaps not appreciated by the virology community is that large viruses, even those classified in the same family, can differ significantly in morphology, lifestyle, and gene complement. This brief commentary, which will mention some of these unique properties, was stimulated by the characterization of the newest member of this club, virus CroV (Fischer, M.G.; Allen, M.J.; Wilson, W.H.; Suttle, C.A. Giant virus with a remarkable complement of genes infects marine zooplankton. Proc. Natl. Acad. Sci. USA 2010, 107, 19508–19513 [1]). CroV has a 730 kb genome (with ∼544 protein-encoding genes) and infects the marine microzooplankton Cafeteria roenbergensis producing a lytic infection.

Enhanced Production of Oceanic Dimethylsulfide Resulting from CO2-Induced Grazing Activity in a High CO2 World

Oceanic dimethylsulfide (DMS) released to the atmosphere affects the Earth's radiation budget through the production and growth of cloud condensation nuclei over the oceans. However, it is not yet known whether this negative climate feedback mechanism will intensify or weaken in oceans characterized by high CO(2) levels and warm temperatures. To investigate the effects of two emerging environmental threats (ocean acidification and warming) on marine DMS production, we performed a perturbation experiment in a coastal environment. Two sets of CO(2) and temperature conditions (a pCO(2) of ∼900 ppmv at ambient temperature conditions, and a pCO(2) of ∼900 ppmv at a temperature ∼3 °C warmer than ambient) significantly stimulated the grazing rate and the growth rate of heterotrophic dinoflagellates (ubiquitous marine microzooplankton). The increased grazing rate resulted in considerable DMS production. Our results indicate that increased grazing-induced DMS production may occur in high CO(2) oceans in the future.

Seasonality of microzooplankton grazing in the northern Wadden Sea

A sequence of nine dilution experiments was conducted according to Landry and Hassett [Landry, M.R., Hassett, R.P., 1982. Estimating the grazing impact of marine microzooplankton. Mar. Biol. 67, 283–288] in the northern Wadden Sea from March until October 2004 to investigate the seasonality of microzooplankton grazing. From March until April, no grazing was observed. Microzooplankton grazing started in May (0.66 d − 1 ) and increased until August (1.22 d − 1 ). In October microzooplankton grazing was low again (0.17 d − 1 ). Phytoplankton growth rates varied between 0 and 1.1 d − 1 . Since the reliability of dilution experiments is still frequently discussed in literature, we tested if our data obtained by dilution experiments reflected short-term in situ phytoplankton dynamics of the study site. We scaled experimental growth rates to water column irradiance, calculated short-term chlorophyll- a dynamics and compared the results to in situ measured chlorophyll- a concentrations. Calculated chlorophyll- a concentrations correlated significantly with in situ measured chlorophyll- a concentrations but slightly overestimated the in situ measured chlorophyll- a. This overestimation was in the range of phytoplankton assimilation reported for the Wadden Sea benthos. We will show that microzooplankton grazing had a large impact during the Phaeocystis bloom and during summer suggesting that a large proportion of phytoplankton biomass remained the pelagic food web. Microzooplankton grazing did not impact the diatom spring bloom and its demise.

The influence of changes in predation rates on marine microbial predator/prey interactions: a modelling study

A mathematical model was developed to represent the dynamics of predation and assimilation of ingested material by heterotrophic marine micro-zooplankton. Predation rate was made a rectangular hyperbolic function of prey carbon (C) concentration modified to simulate the prey selectivity that these organisms have been observed experimentally to exhibit in response to prey nutritional quality. We chose prey N:C ratio as an index of selectivity and related both the maximum predation rate (PM) and the assimilation efficiency (AE) to changes in prey nitrogen:carbon (N:C). Changes in PM simulated the phenomena of “surge feeding” and “prey rejection”. Changes in AE simulated sub-optimal assimilation of material from ingested prey, which in turn, served to decrease the ingestion rate on this material. The model was parameterised using laboratory data sets that followed ingestion of non-growing phytoplankton prey of different N:C ratio by a micro-flagellate predator. Investigative simulations in transient conditions, incorporating growing prey and hence with changing N:C ratio, indicated both PM and AE influenced the quantitative and temporal dynamics of C transfer to the higher trophic level. In particular, we noted that although various model formulations predicted similar trophic transfer of C, this was achieved on very different time scales. The inclusion of heterotrophic micro-zooplankton within food web models is a necessary step in accurate prediction of pelagic nutrient flux but requires physiological models carefully parameterised and tested in both steady state and transient conditions to ensure accurate simulation.

Zooplankton feeding ecology: bacterivory by metazoan microzooplankton

Bacterivory by the rotifer Brachionus plicatilis Müller, nauplii and copepodites of the copepods Centropages Krøyer sp. and Acartia tonsa Dana, and the tintinnid Favella panamensis Kofoid & Campbell was examined using fluorescently labelled bacteria (FLB) and epifluorescence microscopy. FLB were < 1 μm in diameter, and were offered at environmental concentrations (1.47−9.08 × 10 6 cells·ml −1). FLB were visible within rotifers, nauplii, copepodites, and tintinnids, confirming ingestion. Rotifer clearance rates (32–418 μl·animal −1·h −1) exhibited no relation with FLB concentration. In some cases rates of clearance of FLB by rotifers were different with alternative phytoplankton food ( Nanochloris Naumann sp.) than in replicates with FLB alone, whereas in other cases presence of alternative food exhibited no clear effects on rates of ingestion of FLB. Clearance rates for all six naupliar stages of A. tonsa nauplii (0–320 μl·animal −1·h −1) were stage-related, with higher rates by NIII-VI nauplii than NI-II nauplii. Nauplii had higher rates of clearance of FLB in the absence of alternative phytoplankton food ( Isochrysis Parke sp.). Clearance rates of FLB by a single stage of Centropages sp. nauplii, A. tonsa CI copepodites and F. panamensis (each obtained at only a single food concentration of either 1.5 or 5.0 × 10 6 cells·ml −1) were within the range of 85–142 μl·animal −1·h −1. These ranges were similar to those of rotifers and A. tonsa nauplii. This is the first report of FLB ingestion by metazoan marine microzooplankton. Although rotifers and ciliates might be expected to ingest small particles such as FLB using ciliary induced feeding currents, the means by which nauplii and copepodites eat FLB is less clear. We propose that they may “eat” bacteria as they “drink” to osmoregulate.