Changes in the Sea-Ice Brine Community During the Spring-Summer Transition, McMurdo Sound, Antarctica .2. Phagotrophic Protists

The land-fast sea-ice brine contains a diverse phagotrophic protist assemblage consisting of \u3c 5 mum heterotrophic flagellates, Cryothecomonas spp., heterotrophic dinoflagellates, and heterotrophic and mixotrophic ciliates. Fine-scale horizontal spatial variability is a feature of this assemblage; samples taken within 1 m of each other can be dominated by different heterotrophic protists. Many of the larger heterotrophic protists found in the brine are also found in the water column. The photosynthetic ciliate Mesodinium rubrum is also common. In mid to late austral spring, the heterotrophic assemblage accounts for ca 10% of the total protist biomass in the brine and is dominated by Cryothecomonas spp. This flagellate can reach densities of over 106 cells l-1 of brine. In the early austral summer, ciliates (primarily Strombidium spp., Mesodinium rubrum and Didinium spp.) and heterotrophic dinoflagellates (primarily a small Gymnodinium sp. and Polykrikos sp.) increase in abundance in the brine. Ciliate densities of ≥ 3 x 103 l-1 and heterotrophic dinoflagellate densities of 104 cells l-1 are common in the brine during early summer. By the end of January (just prior to ice decay and break-out), heterotrophic flagellates and ciliates can account for 50 % of the protist biomass

Ecophysiological traits of mixotrophic Strombidium spp

This is a pre-copyedited, author-produced version of an article accepted for publication in Journal of Plankton Research following peer review. The version of record Maselli, M., Altenburger, A., Stoecker, D. K. & Hansen, P. J. (2020). Ecophysiological traits of mixotrophic Strombidium spp. Journal of Plankton Research, 42(5), 485-496 is available online at: https://doi.org/10.1093/plankt/fbaa041.Ciliates represent an important trophic link between nanoplankton and mesoplankton. Many species acquire functional chloroplasts from photosynthetic prey, being thus mixotrophs. Little is known about which algae they exploit, and of the relevance of inorganic carbon assimilation to their metabolism. To get insights into these aspects, laboratory cultures of three mixotrophic Strombidium spp. were established and 35 photosynthetic algal species were tested as prey. The relative contributions of ingestion and photosynthesis to total carbon uptake were determined, and responses to prey starvation were studied. Ciliate growth was supported by algal species in the 2–12 μm size range, with cryptophytes and chlorophytes being the best prey types. Inorganic carbon incorporation was only quantitatively important when prey concentration was low (3–100 μgCL−1), when it led to increased gross growth efficiencies. Chla specific inorganic carbon uptake rates were reduced by 60–90% compared to that of the photosynthetic prey. Inorganic carbon uptake alone could not sustain survival of cultures and ciliate populations declined by 25–30% during 5 days of starvation. The results suggest that mixotrophy in Strombidium spp. may substantially bolster the efficiency of trophic transfer when biomass of small primary producers is low

The Effect of Dissolved Polyunsaturated Aldehydes on Microzooplankton Growth Rates in the Chesapeake Bay and Atlantic Coastal Waters

Allelopathy is wide spread among marine phytoplankton, including diatoms, which can produce cytotoxic secondary metabolites such as polyunsaturated aldehydes (PUA). Most studies on diatom-produced PUA have been dedicated to their inhibitory effects on reproduction and development of marine invertebrates. However, little information exists on their impact on key herbivores in the ocean, microzooplankton. This study examined the effects of dissolved 2E,4E-octadienal and 2E,4E-heptadienal on the growth rates of natural ciliate and dinoflagellate populations in the Chesapeake Bay and the coastal Atlantic waters. The overall effect of PUA on microzooplankton growth was negative, especially at the higher concentrations, but there were pronounced differences in response among common planktonic species. For example, the growth of Codonella sp., Leegaardiella sol, Prorodon sp., and Gyrodinium spirale was impaired at 2 nM, whereas Strombidium conicum, Cyclotrichium gigas, and Gymnodinium sp. were not affected even at 20 nM. These results indicate that PUA can induce changes in microzooplankton dynamics and species composition

Microzooplankton Grazing in the Eastern Bering Sea in Summer

Dilution experiments to estimate microzooplankton grazing on phytoplankton were conducted during the summers of 2008, 2009, and 2010 in the Eastern Bering Sea as part of the BEST-BSIERP integrated ecosystem project. All three summers followed cold springs in the Bering Sea. Average microzooplankton grazing coefficients were relatively similar among regions, ranging from 0.16 to 0.34 d−1 in simulated in situ incubations with mixed-layer water collected from the depth of the 55% Io isolume. In Off Shelf and Outer Shelf domains, microzooplankton consumed 67–78% of phytoplankton daily growth but in the Middle and Inner Shelf domains, microzooplankton grazing exceeded phytoplankton daily growth. Regional estimates of microzooplankton ingestion of phytoplankton carbon ranged from 4.4 to 11.0 µg C d−1, with highest ingestion in the Off Shelf, Outer Shelf, and Alaska Peninsula regions and, lower ingestion in the Middle Shelf and Inner Shelf regions. On the northern Middle Shelf, a deep chlorophyll maximum (DCM) occurred at most stations. Grazing coefficients in the DCM were similar in magnitude to coefficients in the corresponding mixed layer. However, because of the higher phytoplankton biomass in the DCM, estimated microzooplankton ingestion and secondary production per liter were higher in the DCM than in the mixed layer. Measurements of photosynthetic quantum yields (Fv/Fm) in whole seawater and diluted treatments indicated that with some plankton assemblages, dilution had a negative effect on phytoplankton physiology and could have compromised their growth rates. This could have also resulted in an underestimation of microzooplankton grazing. Nevertheless, it is clear that microzooplankton grazing consumed most of the phytoplankton production in summer, and that microzooplankton were an important link in food webs supporting larger zooplankton and in carbon flow in the Eastern Bering Sea

Trait trade-offs in phagotrophic microalgae: the mixoplankton conundrum

Analysis of trait trade-offs, through which physiological traits requiring common resources are ‘traded’ to optimize competitive advantage, provides a route to simplify and more readily understand the complexities of ecology. The concept of trait trade-offs has found favour in plankton research, especially directed at phytoplankton, defined here as phototrophs incapable of phagotrophy. Mixoplankton, defined as protists that combine phototrophy and phagotrophy, are now recognized as being widespread and significant members of the protist plankton community; many photoflagellate ‘phytoplankton’ are actually mixoplankton, as are many ‘(microbial) zooplankton’. Mixoplankton might be expected to be dominant, being able to exploit different trophic strategies while simultaneously eliminating competitors. That mixoplankton are not dominant suggests that physiological trait trade-offs erode their apparent competitive edge. We present a systematic analysis of potential trait trade-offs in phototrophic protists focused on mixoplankton. We find no clear evidence to support trait trade-off arguments in plankton research, except perhaps for acquired phototrophy in mixoplanktonic ciliates versus zooplanktonic ciliates. Our findings suggest that the presence of various mixoplankton throughout the surface ocean waters is most likely explained by factors other than trait trade-offs. Diversities in mixoplankton form and function thus reflect that evolution of these organisms from very different lineages, provide them with advantages to function competitively in mature ecosystems with complex trophic interplay. Indeed, the complexity of those lineages is inconsistent with core trait trade-off definitions; there is no single ancestral mixoplankton nor a common environment supporting trait-trade-off-directed evolution

High Grazing Rates on Cryptophyte Algae in Chesapeake Bay

Cryptophyte algae are globally distributed photosynthetic flagellates found in freshwater, estuarine, and neritic ecosystems. While cryptophytes can be highly abundant and are consumed by a wide variety of protistan predators, few studies have sought to quantify in situ grazing rates on their populations. Here we show that autumnal grazing rates on in situ communities of cryptophyte algae in Chesapeake Bay are high throughout the system, while growth rates, particularly in the lower bay, were low. Analysis of the genetic diversity of cryptophyte populations within dilution experiments suggests that microzooplankton may be selectively grazing the fastest-growing members of the population, which were generally Teleaulax spp. We also demonstrate that potential grazing rates of ciliates and dinoflagellates on fluorescently labeled (FL) Rhodomonas salina, Storeatula major, and Teleaulax amphioxeia can be high (up to 149 prey predator−1 d−1), and that a Gyrodinium sp. and Mesodinium rubrum could be selective grazers. Potential grazing was highest for heterotrophic dinoflagellates, but due to its abundance, M. rubrum also had a high overall impact. This study reveals that cryptophyte algae in Chesapeake Bay can experience extremely high grazing pressure from phagotrophic protists, and that this grazing likely shapes their community diversity

Ocean acidification with (de)eutrophication will alter future phytoplankton growth and succession

Human activity causes ocean acidification (OA) though the dissolution of anthropogenically generated CO2 into seawater, and eutrophication through the addition of inorganic nutrients. Eutrophication increases the phytoplankton biomass that can be supported during a bloom, and the resultant uptake of dissolved inorganic carbon during photosynthesis increases water-column pH (bloom-induced basification). This increased pH can adversely affect plankton growth. With OA, basification commences at a lower pH. Using experimental analyses of the growth of three contrasting phytoplankton under different pH scenarios, coupled with mathematical models describing growth and death as functions of pH and nutrient status, we show how different conditions of pH modify the scope for competitive interactions between phytoplankton species. We then use the models previously configured against experimental data to explore how the commencement of bloom-induced basification at lower pH with OA, and operating against a background of changing patterns in nutrient loads, may modify phytoplankton growth and competition. We conclude that OA and changed nutrient supply into shelf seas with eutrophication or de-eutrophication (the latter owing to pollution control) has clear scope to alter phytoplankton succession, thus affecting future trophic dynamics and impacting both biogeochemical cycling and fisheries

Fluorescence, pigment and microscopic characterization of Bering Sea phytoplankton community structure and photosynthetic competency in the presence of a Cold Pool during summer

Spectral fluorescence measurements of phytoplankton chlorophyll a (Chl a), phytoplankton phycobilipigments and variable fluorescence (Fv/Fm), are utilized with High Performance Liquid Chromatography (HPLC) estimates of phytoplankton pigments and microscopic cells counts to construct a comprehensive picture of summer-time phytoplankton communities and their photosynthetic competency in the eastern Bering Sea shelf. Although the Bering Sea was ice-free during our study, the exceptionally cold winter that preceded the summer of 2008 when our cruise took place, facilitated the formation of a “Cold Pool” (<2 °C) and its entrapment at depth in the northern middle shelf. The presence of a strong pycnocline over the entire middle and outer shelves restricted inorganic nutrient fluxes into the surface waters resulting in phytoplankton populations that were photo-physiologically stressed due to nutrient limitation. Elevated Chl a concentrations recorded in the Green Belt along the shelf edge of the Bering Sea, were due to Phaeocystis pouchetii and nano-sized cryptophytes. Although inorganic nutrients were not limiting in the Green Belt, Fv/Fm values were low in all probability due to iron limitation. Phytoplankton communities in the low biomass surface waters of the middle shelf were comprised of prasinophytes, haptophytes, cryptophytes and diatoms. In the northern part of the middle shelf, a sinking bloom made up of the centric diatoms Chaeotoceros socialis, Thalassiosira nordenskioeldii and Porosira glacialis was located above the Cold Pool. The high biomass associated with this senescent bloom and its accretion above the pycnocline, suggests that the Cold Pool acts as a barrier, preventing sinking phytoplankton from reaching the bottom where they can become available to benthic organisms. We further posit that if summer-time storms are not energetic enough and the Cold Pool is not eroded, its presence facilitates the transfer of the large spring phytoplankton bloom to the pelagic ecosystem

The role of mixotrophic protists in the biological carbon pump

The traditional view of the planktonic food web describes consumption of inorganic nutrients by photoautotrophic phytoplankton, which in turn supports zooplankton and ultimately higher trophic levels. Pathways centred on bacteria provide mechanisms for nutrient recycling. This structure lies at the foundation of most models used to explore biogeochemical cycling, functioning of the biological pump, and the impact of climate change on these processes. We suggest an alternative new paradigm, which sees the bulk of the base of this food web supported by protist plankton communities that are mixotrophic – combining phototrophy and phagotrophy within a single cell. The photoautotrophic eukaryotic plankton and their heterotrophic microzooplankton grazers dominate only during the developmental phases of ecosystems (e.g. spring bloom in temperate systems). With their flexible nutrition, mixotrophic protists dominate in more-mature systems (e.g. temperate summer, established eutrophic systems and oligotrophic systems); the more-stable water columns suggested under climate change may also be expected to favour these mixotrophs. We explore how such a predominantly mixotrophic structure affects microbial trophic dynamics and the biological pump. The mixotroph-dominated structure differs fundamentally in its flow of energy and nutrients, with a shortened and potentially more efficient chain from nutrient regeneration to primary production. Furthermore, mixotrophy enables a direct conduit for the support of primary production from bacterial production. We show how the exclusion of an explicit mixotrophic component in studies of the pelagic microbial communities leads to a failure to capture the true dynamics of the carbon flow. In order to prevent a misinterpretation of the full implications of climate change upon biogeochemical cycling and the functioning of the biological pump, we recommend inclusion of multi-nutrient mixotroph models within ecosystem studies

Defining Planktonic Protist Functional Groups on Mechanisms for Energy and Nutrient Acquisition: Incorporation of Diverse Mixotrophic Strategies

Arranging organisms into functional groups aids ecological research by grouping organisms (irrespective of phylogenetic origin) that interact with environmental factors in similar ways. Planktonic protists traditionally have been split between photoautotrophic “phytoplankton” and phagotrophic “microzoo-plankton”. However, there is a growing recognition of the importance of mixotrophy in euphotic aquatic systems, where many protists often combine photoautotrophic and phagotrophic modes of nutrition. Such organisms do not align with the traditional dichotomy of phytoplankton and microzooplankton. To reflect this understanding,we propose a new functional grouping of planktonic protists in an eco- physiological context: (i) phagoheterotrophs lacking phototrophic capacity, (ii) photoautotrophs lacking phagotrophic capacity,(iii) constitutive mixotrophs (CMs) as phagotrophs with an inherent capacity for phototrophy, and (iv) non-constitutive mixotrophs (NCMs) that acquire their phototrophic capacity by ingesting specific (SNCM) or general non-specific (GNCM) prey. For the first time, we incorporate these functional groups within a foodweb structure and show, using model outputs, that there is scope for significant changes in trophic dynamics depending on the protist functional type description. Accord- ingly, to better reflect the role of mixotrophy, we recommend that as important tools for explanatory and predictive research, aquatic food-web and biogeochemical models need to redefine the protist groups within their frameworks