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Two-year seasonality (2017, 2018), export and long-term changes in coccolithophore communities in the subtropical ecosystem of the Gulf of Aqaba, Red Sea
Abstract
A two-year (2017, 2018) study of coccolithophores was undertaken in the Gulf of Aqaba in the northern Red Sea to 1) determine the local diversity and community succession patterns with high temporal and taxonomic resolution, 2) determine the contribution to exported inorganic carbon and 3) evaluate changes in communities relative to those in the mid-1970's reported in Winter et al. (1979). As typical, the oceanographic conditions in the Gulf alternated between stratified, oligotrophic through spring/summer, and mesotrophic during winter due to deep convective mixing. Noticeably, the second summer (2018) was warmer resulting in a more pronounced thermocline. Overall, the coccolithophore dynamics followed the seasonal changes in oceanographic conditions. During the mixing period, coccolithophores were denser (>25 coccospheres mL⁻¹) and were estimated to account on average for 3.46% of the total Chl-a. The communities were fairly homogeneous through depths and over time with a marked dominance of Emiliania huxleyi and Gephyrocapsa ericsonii. During the stratified season, coccolithophore densities were lower, particularly at the surface, such that coccolithophores were estimated to represent on average 0.72% of the total Chl-a. However, the diversity was higher and a clear vertical zonation developed with well-defined upper, intermediate and deep-dwelling communities. These included Umbellosphaera spp., Rhabdosphaera clavigera, a variety of Syracosphaera spp., holococcolithophores and Florisphaera profunda, respectively, as typical in oligotrophic systems. This further underscores the pelagic nature of the Gulf of Aqaba. Noticeably, however, coccolithophores declined in abundances and diversity during 2018, possibly due to the warmer conditions. The relative export of inorganic carbon by coccolithophores largely correlated with the density of living communities, representing <4% and <10% of total inorganic carbon exports during the stratified and mixing periods, respectively. A marked differentiation between different coccolithophore life phases was also detected. Broadly, holococcolithophores inhabited preferentially shallow, oligotrophic water layers in the stratified season, while heterococcolithophores prevailed in deeper water layers or in winter. Yet, species-specific deviations to this pattern were also detected. Finally, comparisons with the 1970's revealed marked changes compared to current communities. G. ericsonii appeared less prevalent and Umbellosphaera spp. displayed a wider temporal residence through spring/summer. Moreover, F. profunda and other deep dwelling species absent in the past are now common during the peak of summer. These observations are indicative of changes in local microbial communities, possibly linked to the ongoing rise in sea temperatures. This study provides a detailed baseline information on coccolithophores for future reassessments of community changes in the GoA.
... For example, coccolithophores may be able to persist during short-term heat waves via their slowly increasing maximum growth rates at their optimum temperatures and diversity of thermal niche widths, which may increase stored resources and resilience to temperature fluctuation (76,77). Because G. huxleyi tends to be comparatively resilient to warming temperatures and fluctuating nutrients among coccolithophores (56,78), the intraspecific diversity in thermal niche (e.g., generalist v. specialist) observed here may offer a still greater mechanistic advantage against temperature warming and variability. Measuring the phenotypic flexibility that confers diverse thermal traits and encoding it in models is hence essential to projecting future change in the balance of phytoplankton functional types with global climate. ...
Temperature has a primary influence on phytoplankton physiology and affects biodiversity and ecology. To examine how intraspecific diversity and temperature shape plankton populations, we grew 12 strains of the ecologically-important coccolithophore Gephyrocapsa huxleyi isolated from regions of different temperature for ∼45 generations (2 months), each at 6-8 temperatures, and characterized the acclimated thermal response curve of each strain. Even with virtually identical temperature optima and overlapping cell size, strain growth rates varied between 0.45 and 1 day ⁻¹ . While some thermal curves were effectively symmetrical, others had more slowly declining growth rates above the “thermal optimum,” and thermal niche widths varied between 16.7 and 24.8 °C. This suggests that different strains use distinct thermal response mechanisms. We investigated the ecological implications of such intraspecific diversity on thermal response using an ocean ecosystem simulation resolving distinct phytoplankton thermal phenotypes. Resolving model analogs of thermal “generalists” and “specialists” (similar to those observed in G. huxleyi) resulted in a distinctive global biogeography of preferred thermal niche widths with a nonlinear latitudinal pattern. We leveraged the model output to predict the ranges of the 12 strains we studied in the laboratory and demonstrated how this approach could refine predictions of phytoplankton thermal geographic range in situ . Our combination of observed thermal traits and modeled biogeography highlights the capacity of diverse groups to persist through temperature shifts.
Significance Statement
Intraspecific diversity in the phytoplankton may underpin their distribution. We show that within a single coccolithophore species, thermal response curves have diverse trait parameters. For example, many strains had a variable range of temperatures at which they could survive (thermal niche width). Adding this thermal niche width diversity to an ecosystem model simulation impacted phytoplankton coexistence and overall biomass. These observations show that thermal niche width is a gap in phytoplankton representation in ecosystem models that impacts modeled phytoplankton biogeography and concomitant carbon cycle dynamics. Including thermal tolerance is crucial to predictive modeling as ocean temperature dynamics change.
Phytoplankton bloom in the Gulf of Elat/Aqaba (the Gulf) was studied before, mainly using one‐dimensional models and observations from the northern Gulf. Thus, the spatial variability within the Gulf and the contribution of physical processes such as horizontal advection to the bloom have not yet been studied. Moreover, various factors such as the effect of light limitation on phytoplankton growth in the Gulf are still debated. Here, we used a three‐dimensional coupled physical‐ecological model for the Gulf to study the mechanisms for phytoplankton bloom throughout the Gulf. We found the southern surface bloom to be higher than the northern surface bloom. In contrast, southern integrated bloom is lower than the northern integrated bloom. These differences result from spatial variations in the mixed layer depth, which is much deeper in the northern Gulf compared with the south. Moreover, horizontal advection controls phytoplankton integrated biomass during the northern bloom, a process often neglected when dealing with phytoplankton blooms. Finally, we found that light limits growth in the northern integrated bloom. The results from the northern Gulf are compared to the North Atlantic bloom, while those from the southern Gulf are compared to the bloom in subtropical oceans due to similarities in mixing depth and consequently in nutrient versus light limitation on phytoplankton growth.
Coccolithophores are a diverse group of calcifying phytoplankton, which are responsible for a large part of the modern oceanic carbonate production. Here, we describe novel or poorly known coccolithophores and novel life cycle combination coccospheres detected in samples collected either in the Gulf of Aqaba in the northern Red Sea or in the Gulf of Naples in the western Mediterranean. These include Syracosphaera winteri, for which detached coccoliths have previously been recorded but both a formal description and taxonomic affiliation were lacking, and five undescribed sets of combination cells linking HET and HOL forms for S. pulchra, S. mediterranea, S. azureaplaneta, S. lamina and S. orbicula. We also propose the replacement name S. kareniae for the fossil species Deutschlandia gaarderae. We describe a new species of the genus Ophiaster, O. macrospinus, displaying a unique morphological and ecological distribution as well as putative combination cells of two variants of the deep-dwelling Florisphaera profunda, which provide new insights on the affiliation of this genus within the Calcihaptophycideae. Additionally, in the family Papposphaeraceae we detected a new species, Pappomonas vexillata, and combination cells of Picarola margalefi and of a species resembling Papposphaera arctica. Finally, we detected three novel, unpaired holococcolithophore forms (Calyptrosphaera lluisae, Calicasphaera bipora and one form designated as Holococcolithophore A). Overall, this set of novel observations and ensuing discussions provide further insights into the diversity, evolution and life cycle complexity of coccolithophores in the oceans.
Coccolithophores are globally important marine calcifying phytoplankton that utilize a haplo-diplontic life cycle.
The haplo-diplontic life cycle allows coccolithophores to divide in both life cycle phases and potentially expands coccolithophore niche volume. Research has, however, to date largely overlooked the life cycle of coccolithophores and has instead focused on the diploid life cycle phase of coccolithophores. Through the synthesis and analysis of global scanning electron microscopy (SEM) coccolithophore abundance data (n=2534), we find that calcified haploid coccolithophores generally constitute a minor component of the total coccolithophore abundance (≈ 2 %–15 % depending on season).
However, using case studies in the Atlantic Ocean and Mediterranean Sea, we show that, depending on environmental conditions, calcifying haploid coccolithophores can be significant contributors to the coccolithophore standing stock (up to ≈30 %). Furthermore, using hypervolumes to quantify the niche of coccolithophores, we illustrate that the haploid and diploid life cycle phases inhabit contrasting niches and that on average this allows coccolithophores to expand their niche by ≈18.8 %, with a range of 3 %–76 % for individual species.
Our results highlight that future coccolithophore research should consider both life cycle stages, as omission of the haploid life cycle phase in current research limits our understanding of coccolithophore ecology. Our results furthermore suggest a different response to nutrient limitation and stratification, which may be of relevance for further climate scenarios.
Our compilation highlights the spatial and temporal sparsity of SEM measurements and the need for new molecular techniques to identify uncalcified haploid coccolithophores. Our work also emphasizes the need for further work on the carbonate chemistry niche of the coccolithophore life cycle.
Mesocosm experiments have been fundamental to investigate the effects of elevated CO2 and ocean acidification (OA) on planktic communities. However, few of these experiments have been conducted using naturally nutrient-limited waters and/or considering the combined effects of OA and ocean warming (OW). Coccolithophores are a group of calcifying phytoplankton that can reach high abundances in the Mediterranean Sea, and whose responses to OA are modulated by temperature and nutrients. We present the results of the first land-based mesocosm experiment testing the effects of combined OA and OW on an oligotrophic Eastern Mediterranean coccolithophore community. Coccolithophore cell abundance drastically decreased under OW and combined OA and OW (greenhouse, GH) conditions. Emiliania huxleyi calcite mass decreased consistently only in the GH treatment; moreover, anomalous calcifications (i.e. coccolith malformations) were particularly common in the perturbed treatments, especially under OA. Overall, these data suggest that the projected increase in sea surface temperatures, including marine heatwaves, will cause rapid changes in Eastern Mediterranean coccolithophore communities, and that these effects will be exacerbated by OA.
Southern Ocean waters are projected to undergo profound changes in their physical and chemical properties in the coming decades. Coccolithophore blooms in the Southern Ocean are thought to account for a major fraction of the global marine calcium carbonate (CaCO3) production and export to the deep sea. Therefore, changes in the composition and abundance of Southern Ocean coccolithophore populations are likely to alter the marine carbon cycle, with feedbacks to the rate of global climate change. However, the contribution of coccolithophores to CaCO3 export in the Southern Ocean is uncertain, particularly in the circumpolar subantarctic zone that represents about half of the areal extent of the Southern Ocean and where coccolithophores are most abundant. Here, we present measurements of annual CaCO3 flux and quantitatively partition them amongst coccolithophore species and heterotrophic calcifiers at two sites representative of a large portion of the subantarctic zone. We find that coccolithophores account for a major fraction of the annual CaCO3 export, with the highest contributions in waters with low algal biomass accumulations. Notably, our analysis reveals that although Emiliania huxleyi is an important vector for CaCO3 export to the deep sea, less abundant but larger species account for most of the annual coccolithophore CaCO3 flux. This observation contrasts with the generally accepted notion that high particulate inorganic carbon accumulations during the austral summer in the subantarctic Southern Ocean are mainly caused by E. huxleyi blooms. It appears likely that the climate-induced migration of oceanic fronts will initially result in the poleward expansion of large coccolithophore species increasing CaCO3 production. However, subantarctic coccolithophore populations will eventually diminish as acidification overwhelms those changes. Overall, our analysis emphasizes the need for species-centred studies to improve our ability to project future changes in phytoplankton communities and their influence on marine biogeochemical cycles.
Coccolithophore export fluxes were investigated via the analysis of sinking matter, obtained from Eastern Mediterranean time-series sediment traps moored in three open sites of the north-eastern Mediterranean Sea located in the Athos Basin of North Aegean (M2 site), Cretan Sea of South Aegean (M3 site) and at Ionian Sea (Nestor site). The aim of our study was to determine the spatial, temporal and seasonal variability in coccolithophore fluxes, as well as to estimate coccolith biogenic carbonate contribution to the sedimentation process. Data from an additional time-series sediment trap located in the southwestern Black Sea were also considered for the comparison of the oligotrophic Eastern Mediterranean setting with the eutrophic Black Sea. Coccolithophore fluxes revealed a highly seasonal pattern during February–March in the North Aegean (peak in late February 2015: 85.6 x 10⁵ coccospheres m⁻² day⁻¹; 27.9 x 10⁸ coccoliths m⁻² day⁻¹), during March–May in the Cretan Sea (peak in late March 2015: 33.7 x 10⁵ coccospheres m⁻² day⁻¹; 19.5 x 10⁸ coccoliths m⁻² day⁻¹) and during February–March and May–June in the Ionian Sea (peak in late May 2012: 14.3 x 10⁵ coccospheres m⁻² day⁻¹; 1.53 x 10⁸ coccoliths m⁻² day⁻¹). The recorded maxima coincide with low sea surface temperatures, increased precipitation and high PIC fluxes. Coccosphere fluxes were dominated by Emiliania huxleyi comprising ~70% of the total abundance, in the North Aegean and ~50% in the Cretan and Ionian Seas. Syracosphaera pulchra was also prominent in the study sites, where its abundance reached 14% in the North Aegean and ~10% in the Cretan and Ionian Seas respectively. Florisphaera profunda represented one of the major taxa in the coccolith fluxes of all three Eastern Mediterranean sites (~25% in North Aegean, ~20% in Cretan and Ionian Seas), while Algirosphaera robusta and Umbilicosphaera sibogae were the most abundant among the minor taxa. The North Aegean Sea exhibited a considerably higher coccolith flux when compared to other sediment traps due to the prominent seasonal peak of E. huxleyi during winter (February–March) (>95% of the total abundance). In contrast to the Eastern Mediterranean sediment traps, the time-series data from the Black Sea showed presence of monospecific E. huxleyi assemblage increasing its abundance during late September–November (max 320 x 10⁵ coccospheres m⁻² day⁻¹; at least 7.79 x 10⁸ coccoliths m⁻² day⁻¹, coccolith flux derived only from coccospheres converted to coccoliths). In the Eastern Mediterranean, biogenic carbonate fluxes followed the general pattern of the total mass flux in all investigated areas, with the Black Sea coccolithophore CaCO3 flux being the lowest due to low the E. huxleyi coccolith mass. Overall, in the North Aegean Sea, coccolithophore fluxes are strongly dependent on surface waters nutrients enrichment due to winter vertical water column mixing, riverine inputs and Black Sea water inflows, while the fertilization and/or formation of fast-sinking aggregates due to episodic dust input event are affecting the coccolithophore fluxes in the Cretan and Ionian Seas. The intercomparison of the coccolith export fluxes in the studied NE-SW mooring transects implies a north-south and east-west decreasing pattern, depending on the variable oceanographic regimes and the associated environmental factors controlling the investigated areas.
Ongoing climate change is shifting species distributions and increasing extinction risks globally. It is generally thought that large population sizes and short generation times of marine phytoplankton may allow them to adapt rapidly to global change, including warming, thus limiting losses of biodiversity and ecosystem function. Here, we show that a marine diatom survives high, previously lethal, temperatures after adapting to above‐optimal temperatures under nitrogen (N)‐replete conditions. N limitation, however, precludes thermal adaptation, leaving the diatom vulnerable to high temperatures. A trade‐off between high‐temperature tolerance and increased N requirements may explain why N limitation inhibited adaptation. Because oceanic N limitation is common and likely to intensify in the future, the assumption that phytoplankton will readily adapt to rising temperatures may need to be reevaluated.
Quantitative coccolithophore analyses were performed on data of 2011–2015 dataset derived from the examination of plankton samples (until 100 m water depth), the sinking particulate matter (collected by a time series sediment trap) and surface and core sediments of the North Aegean Sea sampling site M2 (Athos Basin, NE Mediterranean). The aim was to achieve a better understanding of the potential modifications of the coccolithophore assemblage between the surface waters (plankton), the water column (sidocoenosis) and the underlying sediment (thanatocoenosis). Sediment trap calcareous nannoplankton multiannual mean fluxes (20 × 10 ⁸ coccoliths m ² day ⁻¹ ) documented similar values to the accumulation rates recorded in the surface sediment (23.6 × 10 ⁸ coccoliths m ⁻² day ⁻¹ ), whereas within the last 500 years the rates have ranged from 2.19 × 10 ⁸ to 5.4 × 10 ⁸ coccoliths m ⁻² day ⁻¹ . The dominant species in all sampling types was Emiliania huxleyi, reaching in some cases striking relative abundances of 85–90%. Morphometric analyses on E. huxleyi coccoliths documented the presence of a lightly calcified morphotype in the water column and sediment trap samples in addition to the seasonal occurrence of heavier calcified E. huxleyi coccoliths, indicating enhanced Black Sea water inflows during May 2011, February 2015 and October 2015. However, such a signal was not preserved in the surface sediment assemblage mostly due to processes of diagenetic calcite overgrowth. Notably, Florisphaera profunda was not included in the upper water column plankton assemblage but in the sediment traps and surface sediments. Thus, it is presumed to flourish in nutrient-enriched layers below the sampled 100 m water column depth. Several fragile Syracosphaeraceae and holococcolithophore species and the delicate Algirosphaera robusta were not present in the sinking assemblage or on the seafloor; however, the main features of the living assemblages were generally preserved. The recorded high relative abundances of E. huxleyi (~60%) in the sediment were in accordance with positive North Atlantic Oscillation (NAO) shifts during recent production of dense water masses in the North Aegean.
Abstract Anthropogenic CO2 emissions are inundating the upper ocean, acidifying the water, and altering the habitat for marine phytoplankton. These changes are thought to be particularly influential for calcifying phytoplankton, namely, coccolithophores. Coccolithophores are widespread and account for a substantial portion of open ocean calcification; changes in their abundance, distribution, or level of calcification could have far‐reaching ecological and biogeochemical impacts. Here, we isolate the effects of increasing CO2 on coccolithophores using an explicit coccolithophore phytoplankton functional type parameterization in the Community Earth System Model. Coccolithophore growth and calcification are sensitive to changing aqueous CO2. While holding circulation constant, we demonstrate that increasing CO2 concentrations cause coccolithophores in most areas to decrease calcium carbonate production relative to growth. However, several oceanic regions show large increases in calcification, such the North Atlantic, Western Pacific, and parts of the Southern Ocean, due to an alleviation of carbon limitation for coccolithophore growth. Global annual calcification is 6% higher under present‐day CO2 levels relative to preindustrial CO2 (1.5 compared to 1.4 Pg C/year). However, under 900 μatm CO2, global annual calcification is 11% lower than under preindustrial CO2 levels (1.2 Pg C/year). Large portions of the ocean show greatly decreased coccolithophore calcification relative to growth, resulting in significant regional carbon export and air‐sea CO2 exchange feedbacks. Our study implies that coccolithophores become more abundant but less calcified as CO2 increases with a tipping point in global calcification (changing from increasing to decreasing calcification relative to preindustrial) at approximately ∼600 μatm CO2.
Coccolithophores are key components of phytoplankton communities, exerting a critical impact on the global carbon cycle and the Earth’s climate through the production of coccoliths made of calcium carbonate (calcite) and bioactive gases. Microzooplankton grazing is an important mortality factor in coccolithophore blooms, however little is currently known regarding the mortality (or growth) rates within non-bloom populations. Measurements of coccolithophore calcite production (CP) and dilution experiments to determine microzooplankton (≤63 µm) grazing rates were made during a spring cruise (April 2015) at the Central Celtic Sea (CCS), shelf edge (CS2), and within an adjacent April bloom of the coccolithophore Emiliania huxleyi at station J2.
CP at CCS ranged from 10.4 to 40.4 µmol C m⁻³ d⁻¹ and peaked at the height of the spring phytoplankton bloom (peak chlorophyll-a concentrations ∼6 mg m⁻³). Cell normalised calcification rates declined from ∼1.7 to ∼0.2 pmol C cell⁻¹ d⁻¹, accompanied by a shift from a mixed coccolithophore species community to one dominated by the more lightly calcified species E. huxleyi and Calciopappus caudatus. At the CCS, coccolithophore abundance increased from 6 to 94 cells mL⁻¹, with net growth rates ranging from 0.06 to 0.21 d⁻¹ from the 4th to the 28th April. Estimates of intrinsic growth and grazing rates from dilution experiments, at the CCS ranged from 0.01 to 0.86 d⁻¹ and from 0.01 to 1.32 d⁻¹, respectively, which resulted in variable net growth rates during April. Microzooplankton grazers consumed 59 to >100% of daily calcite production at the CCS. Within the E. huxleyi bloom a maximum density of 1986 cells mL⁻¹ was recorded, along with CP rates of 6000 µmol C m⁻³ d⁻¹ and an intrinsic growth rate of 0.29 d⁻¹, with ∼80% of daily calcite production being consumed.
Our results show that microzooplankton can exert strong top-down control on both bloom and non-bloom coccolithophore populations, grazing over 60% of daily growth (and calcite production). The fate of consumed calcite is unclear, but may be lost either through dissolution in acidic food vacuoles, and subsequent release as CO2, or export to the seabed after incorporation into small faecal pellets. With such high microzooplankton-mediated mortality losses, the fate of grazed calcite is clearly a high priority research direction.
Coccolithophores are calcifying phytoplankton and major contributors
to both the organic and inorganic oceanic carbon pumps. Their export
fluxes, species composition, and seasonal patterns were determined in
two sediment trap moorings (M4 at 12° N, 49° W and
M2 at 14° N, 37° W) collecting settling particles
synchronously from October 2012 to November 2013 at 1200 m
of water depth in the open equatorial North Atlantic.
The two trap locations showed a similar seasonal pattern in total
coccolith export fluxes and a predominantly tropical coccolithophore
settling assemblage. Species fluxes were dominated throughout the
year by lower photic zone (LPZ) taxa (Florisphaera
profunda, Gladiolithus flabellatus) but also included
upper photic zone (UPZ) taxa (Umbellosphaera spp.,
Rhabdosphaera spp., Umbilicosphaera spp.,
Helicosphaera spp.). The LPZ flora was most abundant during
fall 2012, whereas the UPZ flora was more important during
summer. In spite of these similarities, the western part of the
study area produced persistently higher fluxes, averaging 241×107 ± 76×107 coccoliths m−2 d−1 at station M4 compared to
only 66×107 ± 31×107 coccoliths m−2 d−1 at station M2. Higher fluxes
at M4 were mainly produced by the LPZ species, favoured by the
westward deepening of the thermocline and nutricline. Still, most
UPZ species also contributed to higher fluxes, reflecting enhanced
productivity in the western equatorial North Atlantic. Such was the
case of two marked flux peaks of the more opportunistic species
Gephyrocapsa muellerae and Emiliania huxleyi in
January and April 2013 at M4, indicating a fast response to
the nutrient enrichment of the UPZ, probably by wind-forced
mixing. Later, increased fluxes of G. oceanica and
E. huxleyi in October–November 2013 coincided with the
occurrence of Amazon-River-affected surface waters. Since the spring
and fall events of 2013 were also accompanied by two dust flux peaks,
we propose a scenario in which atmospheric dust also provided
fertilizing nutrients to this area. Enhanced surface buoyancy
associated with the river plume indicates that the Amazon acted not
only as a nutrient source, but also as a surface density retainer
for nutrients supplied from the atmosphere. Nevertheless, lower
total coccolith fluxes during these events compared to the maxima
recorded in November 2012 and July 2013 indicate that transient
productivity by opportunistic species was less important than
background tropical productivity in the equatorial North
Atlantic. This study illustrates how two apparently similar sites in
the tropical open ocean actually differ greatly in ecological and
oceanographic terms. The results presented here provide valuable
insights into the processes governing the ecological dynamics and
the downward export of coccolithophores in the tropical North
Atlantic.
Ocean warming is a major consequence of climate change, with the surface of the ocean having warmed by 0.11 °C decade⁻¹ over the last 50 years and is estimated to continue to warm by an additional 0.6 – 2.0 °C before the end of the century¹. However, there is considerable variability in the rates experienced by different ocean regions, so understanding regional trends is important to inform on possible stresses for marine organisms, particularly in warm seas where organisms may be already operating in the high end of their thermal tolerance. Although the Red Sea is one of the warmest ecosystems on earth, its historical warming trends and thermal evolution remain largely understudied. We characterized the Red Sea’s thermal regimes at the basin scale, with a focus on the spatial distribution and changes over time of sea surface temperature maxima, using remotely sensed sea surface temperature data from 1982 – 2015. The overall rate of warming for the Red Sea is 0.17 ± 0.07 °C decade⁻¹, while the northern Red Sea is warming between 0.40 and 0.45 °C decade⁻¹, all exceeding the global rate. Our findings show that the Red Sea is fast warming, which may in the future challenge its organisms and communities.
Coccolithophore species composition was determined in 199 samples collected from the upper 300 m of the Atlantic Ocean, spanning temperate, tropical and subtropical waters in both hemispheres during four Atlantic Meridional Transect (AMT) cruises over the period 2003 to 2005. Of the 171 taxa observed, 140 consistently represented less than 5% of total cell numbers, and were classed as rare. Multivariate statistical techniques were used on the common taxa to assess variability in community composition vertically in the water column, horizontally across hydrographic provinces (subtropical gyres, equatorial waters, temperate waters), and temporally between cruises. Sharper gradients of statistical dissimilarity in species composition occurred vertically over a few tens of metres than horizontally over hundreds of kilometres. Three floral groups were identified from analysis of the depth of normalised abundance maxima in the subtropical gyres and equatorial waters: the upper euphotic zone (UEZ, >10% surface irradiance); the lower euphotic zone (LEZ, 10-1% surface irradiance); and the sub-euphotic zone (SEZ, <1% surface irradiance). The LEZ includes the deep chlorophyll maximum (DCM) and nutricline, and was characterised by species such as Emiliania huxleyi and Gephyrocapsa ericsonii which were also abundant at higher latitudes. It is suggested that this pattern reflects similarities in the light (and inorganic nutrient) conditions between the LEZ and temperate waters. The SEZ is below the depth where light is thought to be sufficient to support photosynthesis, suggesting that deep-dwelling species such as Florisphaera profunda and Gladiolithus spp. may be mixotrophic or phagotrophic, although conclusive proof will need to be gained experimentally. Mixotrophy could also be an important nutritional strategy for species abundant (Umbellosphaera spp., holococcolithophores) in the UEZ where inorganic nutrient concentrations are depleted and limiting to growth, although other nutritional strategies, such as the use of organic nutrients, are also possible. Statistical differences were also found in the species composition between the different cruises, with high levels of similarity for similar timed cruises (May or September-October). Few individual taxa showed significant variability in abundance over the time-span of sampling, except species such as E. huxleyi and G. ericsonii at higher latitudes. In subtropical and equatorial waters, high levels of species richness and low levels of species dominance remained throughout the sampling period indicating that seasonal fluctuations reflected differences in the whole coccolithophore community rather than in just one or a few species. Multivariate analyses of the taxa classified as rare also indicated some level of temporal, as well as vertical, zonation. Such insights into coccolithophore ecology and community composition provide important new perspectives that require innovative research to fully understand their impact on ocean biogeochemistry.
Coccolithophores are a key functional group in terms of the pelagic
production of calcium carbonate (calcite), although their contribution to
shelf sea biogeochemistry, and how this relates to environmental conditions,
is poorly constrained. Measurements of calcite production (CP) and
coccolithophore abundance were made on the north-west European shelf to
examine trends in coccolithophore calcification along natural gradients of
carbonate chemistry, macronutrient availability and plankton composition.
Similar measurements were also made in three bioassay experiments where
nutrient (nitrate, phosphate) and pCO2 levels were manipulated.
Nanoflagellates (< 10 μm) dominated chlorophyll biomass and
primary production (PP) at all but one sampling site, with CP ranging from
0.6 to 9.6 mmol C m−2 d−1. High CP and coccolithophore abundance
occurred in a diatom bloom in fully mixed waters off Heligoland, but not in two distinct coccolithophore blooms in the central North Sea and Western
English Channel. Coccolithophore abundance and CP showed no correlation with
nutrient concentrations or ratios, while significant (p < 0.01)
correlations between CP, cell-specific calcification (cell-CF) and irradiance
in the water column highlighted how light availability exerts a strong
control on pelagic CP. In the experimental bioassays, Emiliania-huxleyi-dominated coccolithophore communities in shelf waters (northern
North Sea, Norwegian Trench) showed a strong response in terms of CP to
combined nitrate and phosphate addition, mediated by changes in cell-CF and
growth rates. In contrast, an offshore diverse coccolithophore community (Bay
of Biscay) showed no response to nutrient addition, while light availability or mortality may have been more important in controlling this
community. Sharp decreases in pH and a rough halving of calcite saturation
states in the bioassay experiments led to decreased CP in the Bay of Biscay
and northern North Sea, but not the Norwegian Trench. These decreases in CP
were related to slowed growth rates in the bioassays at elevated pCO2
(750 μatm) relative to those in the ambient treatments. The
combined results from our study highlight the variable coccolithophore
responses to irradiance, nutrients and carbonate chemistry in north-west
European shelf waters, which are mediated by changes in growth rates, cell-CF
and species composition.
Calcifying marine phytoplankton—coccolithophores— are some of the most successful yet enigmatic organisms in the ocean and are at risk from global change. To better understand how they will be affected, we need to know “why” coccolithophores calcify. We review coccolithophorid evolutionary history and cell biology as well as insights from recent experiments to provide a critical assessment of the costs and benefits of calcification. We conclude that calcification has high energy demands and that coccolithophores might have calcified initially to reduce grazing pressure but that additional benefits such as protection from photodamage and viral/bacterial attack further explain their high diversity and broad spectrum ecology. The cost-benefit aspect of these traits is illustrated by novel ecosystem modeling, although conclusive observations remain limited. In the future ocean, the trade-off between changing ecological and physiological costs of calcification and their benefits will ultimately decide how this important group is affected by ocean acidification and global warming.
This study presents the species composition of living coccolithophore communities in the Aegean Sea (northeastern Mediterranean), investigating their spatial and temporal variations in various environmental conditions from mesotrophic to ultra-oligotrophic regions. Coccolithophores of the photic zone in theAegean Sea are relatively diverse (65 heterococcolithophores and 34 holococcolithophores) and dominated mostly by Emiliania huxleyi, Syracosphaera spp.,Rhabdosphaeraceae and holococcolithophores. Hierarchical classification using R-mode cluster analysis distinguished five coccolithophore groups: Group Ia (Emiliania huxleyi, Syracosphaera molischii and Syracosphaera ossa) prevails in the high cell density and low diversity assemblages during the winter and early spring, when low temperatures and high nutrient concentrations are prevailing. Particularly in the northAegean, E. huxleyi is dominating the upper photic zone being affected by the Black SeaWater inflow and the associated control on the water column stratification. Group Ib (Florisphaera profunda, Algirosphaera robusta, Syracosphaera anthos and Syracosphaera lamina) becomes important in the lower photic zone, making up the typical deep assemblages, whereas Group Ic (mainly Helicosphaera carteri and Gephyrocapsa oceanica) implies an opportunistic behavior in distinctly polluted neritic regions. Group IIa (Rhabdosphaera clavigera, Syracosphaera protrudens, Syracosphaera halldalii and numerous holococcolithophores) dominates the late spring-early autumn low cell density and high diversity assemblages, mainly in the thermally-stratified south Aegean and/or shallow, coastal environments with normal/ oligotrophic conditions, while Group IIb (Umbellosphaera tenuis and Syracosphaera pulchra) dominates the coccolithophore assemblages mainly during the early autumn in the north Aegean, thus reflecting the influence of Levantine IntermediateWater masses in the middle-lower photic zone.Our results suggest that abundance and variability in Aegean Sea coccolithophore assemblages are primarily controlled by surfacewater circulation and the associatedwater column stratification,with the sea temperature gradient affecting species composition.
Significance
Phytoplankton play essential roles in marine food webs and global biogeochemical cycles, yet the responses of individual species and entire phytoplankton communities to anthropogenic climate change in the coming century remain uncertain. Here we map the biogeographies of commonly observed North Atlantic phytoplankton and compare their historical (1951–2000) and projected future ranges (2051–2100). We find that individual species and entire communities move in space, or shift, and that communities internally reassemble, or shuffle. Over the coming century, most but not all studied species shift northeastward in the basin, moving at a rate faster than previously estimated. These pronounced ecological changes are driven by dynamic changes in ocean circulation and surface conditions, rather than just warming temperatures alone.
This study examined recent coccolith surface sediment assemblages across the Pacific sector of the SouthernOcean (from Punta Arenas, Chile toWellington, New Zealand). Twenty five stations located within 44.4°S to 65.4°S and 80.1°W to 174.5°E were selected in order to assess if and how the surface sediment assemblages reflect the present-day coccolithophore community and surface-water oceanographic conditions. The highest numbers of coccoliths in the surface sediments are reached near the East Pacific Rise and close to the Subtropical Front, at the New Zealand Margin (>6x109 coccoliths/g of sediment). The dominant taxa are Emiliania huxleyi (including types A, B, B/C and C), Calcidiscus leptoporus, Gephyrocapsa spp. (including G. muellerae, G. oceanica and G. ericsonii), Umbellosphaera tenuis and Coccolithus braarudii. Despite the recognition of species morphotypes being hampered by carbonate dissolution at some locations, we observed that numbers generally decrease southward until almost a monospecific and sporadic record of E. huxleyi (types B/C and C) and C. leptoporus south of the Polar Front occurs. The recent coccolithophore distribution was compared to already published living coccolithophore distributions (i.e., water column samples collected at the same specific locations) showing a fairly similar pattern. Combining the numbers of cells/l and coccoliths/g of sediment, different coccolithophore assemblages were established coincidentwith areas bounded by the major surface oceanographic fronts, i.e.The Subantarctic Zone and the Polar Front Zone.
Concerning their sensitivity to ocean acidification, coccolithophores, a
group of calcifying single-celled phytoplankton, are one of the best-studied
groups of marine organisms. However, in spite of the large number of studies
investigating coccolithophore physiological responses to ocean
acidification, uncertainties still remain due to variable and partly
contradictory results. In the present study we have used all existing data
in a meta-analysis to estimate the effect size of future pCO2 changes
on the rates of calcification and photosynthesis and the ratio of
particulate inorganic to organic carbon (PIC / POC) in different
coccolithophore species. Our results indicate that ocean acidification has a
negative effect on calcification and the cellular PIC / POC ratio in the two most
abundant coccolithophore species: Emiliania huxleyi and Gephyrocapsa oceanica. In contrast, the more heavily
calcified species Coccolithus braarudii did not show a distinct response when exposed to elevated
pCO2/reduced pH. Photosynthesis in Gephyrocapsa oceanica was positively affected by high
CO2, while no effect was observed for the other coccolithophore
species. There was no indication that the method of carbonate chemistry
manipulation was responsible for the inconsistent results regarding observed
responses in calcification and the PIC / POC ratio. The perturbation method,
however, appears to affect photosynthesis, as responses varied significantly
between total alkalinity (TA) and dissolved inorganic carbon (DIC)
manipulations. These results emphasize that coccolithophore species respond
differently to ocean acidification, both in terms of calcification and
photosynthesis. Where negative effects occur, they become evident at
CO2 levels in the range projected for this century in the case of unabated
CO2 emissions. As the data sets used in this meta-analysis do not
account for adaptive responses, ecological fitness and ecosystem
interactions, the question remains as to how these physiological responses play
out in the natural environment.
Many coccolithophores have complex life cycles with haploid and diploid stages bearing structurally different coccolith types (holococcoliths and heterococcoliths, respectively). Laboratory studies suggest that holo- and heterococcolithophores may occupy distinct ecological niches, but the potential ecological implications of the existence of haploid and diploid stages are poorly known. We present here a study of holo-and heterococcolithophore distributions in the Catalano-Balearic Sea, during 2 cruises (MESO-96, from 18 June to 3 July, and FRONTS-96, from 16 to 21 September) that covered 2 intervals of the stratification period of 1996. We define a holococcolithophore prevalence index (HOLP index), calculated for each coccolithophore-containing sample, as the percent ratio between the number of holococcolithophores and the total number of holo-and heterococcolithophores belonging to families with alternation of holo- and heterococcolithophore life stages (coccolithophores having HOL-HET life cycles; Total_HHLC). In both cruises, the distribution of holo-and heterococcolithophores and the HOLP index indicated a preference of the holococcolithophores for shallower waters and of the heteroccolithophores for deeper layers. This segregation may be linked to a differentiation of ecological niches, with the haploid holococcolithophores occupying the more oligotrophic upper layers and the diploid heterococcolithophores inhabiting relatively rich deeper waters.
The Mediterranean Sea is considered a "hot spot" for climate change, being
characterized by oligotrophic to ultra-oligotrophic waters and rapidly increasing seasurface temperature and
changing carbonate chemistry. Coccolithophores are considered a dominant
phytoplankton group in these waters. As marine calcifying organisms they are
expected to respond to the ongoing changes in seawater carbonate chemistry.
We provide here a description of the
springtime coccolithophore distribution in the Mediterranean Sea and relate
this to a broad set of in situ-measured environmental variables. Samples were taken
during the R/V Meteor (M84/3) oceanographic cruise in April 2011, between 0 and 100 m water
depth from 28 stations. Total diatom and silicoflagellate cell
concentrations are also presented. Our results highlight the importance of
seawater carbonate chemistry, especially [CO32−] but also
[PO43−] in unraveling the distribution of heterococcolithophores,
the most abundant coccolithophore life phase. Holo- and
heterococcolithophores respond differently to environmental factors. For
instance, changes in heterococcolithophore assemblages were best linked to
the combination of [CO32−], pH, and salinity (ρ = 0.57),
although salinity might be not functionally related to coccolithophore
assemblage distribution. Holococcolithophores, on the other hand, showed
higher abundances and species diversity in oligotrophic areas (best fit,
ρ = 0.32 for nutrients), thriving in nutrient-depleted waters.
Clustering of heterococcolithophores revealed three groups of species
sharing more than 65% similarities. These clusters could be assigned to
the eastern and western basins and deeper layers (below 50 m),
respectively. In addition, the species Gephyrocapsa oceanica, G. muellerae,
and Emiliania huxleyi morphotype B/C are spatially
distributed together and trace the influx of Atlantic waters into the
Mediterranean Sea. The results of the present work emphasize the importance
of considering holo- and heterococcolithophores separately when analyzing
changes in species assemblages and diversity. Our findings suggest that
coccolithophores are a main phytoplankton group in the entire Mediterranean
Sea and can dominate over siliceous phytoplankton. They have life stages
that are expected to respond differently to the variability in seawater
carbonate chemistry and nutrient concentrations.
Coccolithophores, a diverse group of phytoplankton, make important contributions to pelagic calcite production and export, yet the comparative biogeochemical role of species other than the ubiquitous Emiliania huxleyi is poorly understood. The contribution of different coccolithophore species to total calcite production is controlled by inter-species differences in cellular calcite, growth rate and relative abundance within a mixed community. In this study we examined the relative importance of E. huxleyi and two Coccolithus species in terms of daily calcite production. Culture experiments compared growth rates and cellular calcite content of E. huxleyi (Arctic and temperate strains), Coccolithus pelagicus (novel Arctic strain) and Coccolithus braarudii (temperate strain). Despite assumptions that E. huxleyi is a fast-growing species, growth rates between the three species were broadly comparable (0.16–0.85 d-1) under identical
temperature and light conditions. Emiliania huxleyi grew only 12% faster on average than C. pelagicus, and 28% faster than C. braarudii. As the cellular calcite content of C. pelagicus and C. braarudii is typically 30–80 times greater than E. huxleyi, comparable growth rates suggest that Coccolithus species have the potential to be major calcite producers in mixed populations. To further explore these results we devised a simplistic model comparing daily calcite production from Coccolithus and E. huxleyi across a realistic range of relative abundances and a wide range of relative growth rates. Using the relative differences in growth rates from our culture studies, we found that C. pelagicus would be a larger source of calcite if abundances of E. huxleyi to C. pelagicus were below 34:1. Relative abundance data collected from North Atlantic field samples (spring and summer 2010) suggest that, with a relative growth rate of 88 %, C. pelagicus dominated calcite production at 69% of the sites sampled. With a more extreme difference in growth rates, where C. pelagicus grows at 1 / 10th of the rate of E. huxleyi, C. pelagicus still dominated calcite production in 14% of the field samples. These results demonstrate the necessity of considering interactions between inter-species differences in growth rates, cellular calcite and relative abundances when evaluating the contribution of different coccolithophores to pelagic calcite production. In the case of C. pelagicus, we find that there is strong potential for this species to make major contributions to calcite production in the North Atlantic, although estimates of relative growth rates from the field are needed to
confirm our conclusions.
A comprehensive, but simple-to-use software package for executing a range of standard numerical analysis and operations used in quantitative paleontology has been developed. The program, called PAST (PAleontological STatistics), runs on standard Windows computers and is available free of charge. PAST integrates spreadsheettype data entry with univariate and multivariate statistics, curve fitting, time-series analysis, data plotting, and simple phylogenetic analysis. Many of the functions are specific to paleontology and ecology, and these functions are not found in standard, more extensive, statistical packages. PAST also includes fourteen case studies (data files and exercises) illustrating use of the program for paleontological problems, making it a complete educational package for courses in quantitative methods.
The Gulf of Aqaba (Gulf of Eilat) is a terminal elongated basin that
exchanges water with the northern Red Sea via the Straits of Tiran. The
gulf's hydrography exhibits strong seasonal variability, with deep
mixing during February-March and stable stratification afterward. We use
an oceanic model to investigate the annual cycle of the general
circulation and hydrographic conditions in the gulf. We demonstrate that
on a subannual time scale, the general circulation deviates from the
standard depiction of inverse estuarine circulation. During the
restratification season (April-August), the exchange flux with the
northern Red Sea is maximal and is driven by density differences between
the basins, while atmospheric fluxes actually counteract this exchange
flow. The observed warming of the surface layer is mainly due to
advection of warm water from the northern Red Sea, with a smaller
contribution from surface heating. During the mixing season
(September-March), the exchange flux and the advection of heat are
minimal and atmospheric fluxes drive convection rather than the exchange
flow. We estimate the seasonality of the exchange flow through the
Straits of Tiran. The seasonal variability in the exchange flow is large
and ranges from 0.04 Sv during early spring to 0.005 Sv during early
winter.
Past meta-analyses of the response of marine organisms to climate change
have examined a limited range of locations, taxonomic groups and/or
biological responses. This has precluded a robust overview of the effect
of climate change in the global ocean. Here, we synthesized all
available studies of the consistency of marine ecological observations
with expectations under climate change. This yielded a meta-database of
1,735 marine biological responses for which either regional or global
climate change was considered as a driver. Included were instances of
marine taxa responding as expected, in a manner inconsistent with
expectations, and taxa demonstrating no response. From this database,
81-83% of all observations for distribution, phenology, community
composition, abundance, demography and calcification across taxa and
ocean basins were consistent with the expected impacts of climate
change. Of the species responding to climate change, rates of
distribution shifts were, on average, consistent with those required to
track ocean surface temperature changes. Conversely, we did not find a
relationship between regional shifts in spring phenology and the
seasonality of temperature. Rates of observed shifts in species'
distributions and phenology are comparable to, or greater, than those
for terrestrial systems.
Coccolithophore seasonality was examined in the southeastern Mediterranean Sea, both at the edge of the coastal shelf and in the open sea offshore Israel during 2018–2019. Oceanographic conditions varied seasonally between markedly stratified and ultraoligotrophic from April to September and water column-mixing with relatively higher nitrate levels from October to February. Coccolithophores were quantified during the early (April), mid (July) and late (October) stratification period and in the mixing period (January). During stratification, cell densities progressively declined to <1.5 × 10⁴ cells L⁻¹, while both diversity and vertical differentiation of communities markedly increased. Emiliania huxleyi, Umbellosphaera spp., Syracosphaeraceae and Rhabdosphaeraceae as well as holococcolithophores were prevalent in the upper and mid-water layers. Florisphaera profunda characterized deeper sub-euphotic layers. During winter, mixing eroded the vertical zonation of species and coccolithophore density increased up to ~3.5 × 10⁴ cells L⁻¹. Communities became largely dominated by E. huxleyi, coincident with higher nutrient availability. The observed composition of coccolithophore assemblages and succession patterns support previous descriptions that the eastern Mediterranean largely resembles oceanic gyre systems. At the shelf station, the presence of higher fractions of r-selected species, and the rarity of oligotrophic coccolithophores (namely Umbellosphaera irregularis and holococcolithophores), suggest a somewhat greater influence of nutrients towards the shore. Finally, cells from different life phases were identified for a variety of species, highlighting the clear ecological divergence between coccolithophore life-phases. These data represent important baseline values for this area of the global ocean which is affected by major climate and environmental changes.
The Eastern Mediterranean Sea (EMS) is a poorly studied ultra-oligotrophic marine environment, dominated by small-size phyto- and bacterioplankton. Here, we describe the dynamics of a single annual cycle (2018–19) of phyto- and bacterioplankton (abundances, pigments and productivity) in relation to the physical and chemical conditions in the photic water column at an offshore EMS site (Station THEMO-2, ∼1,500m depth, 50km offshore). We show that phytoplankton biomass (as chlorophyll a), primary and bacterial productivity differed between the mixed winter (January–April) and the thermally stratified (May–December) periods. Prochlorococcus and Synechococcus numerically dominated the picophytoplankton populations, with each clade revealing different temporal and depth changes indicative to them, while pico-eukaryotes (primarily haptophytes) were less abundant, yet likely contributed significant biomass. Estimated primary productivity (∼32 gC m⁻² y⁻¹) was lower compared with other well-studied oligotrophic locations, including the north Atlantic and Pacific (BATS and HOT observatories), the western Mediterranean (DYFAMED observatory) and the Red Sea, and was on-par with the ultra-oligotrophic South Pacific Gyre. In contrast, integrated bacterial production (∼11 gC m⁻² y⁻¹) was similar to other oligotrophic locations. Phytoplankton seasonal dynamics were similar to those at BATS and the Red Sea, suggesting an observable effect of winter mixing in this ultra-oligotrophic location. These results highlight the ultra-oligotrophic conditions in the EMS and provide, for the first time in this region, a full-year baseline and context to ocean observatories in the region.
Rising ocean temperatures will alter the diversity of marine phytoplankton communities, likely leading to modifications in food-web and biogeochemical dynamics. Here we focus on the coccolithophores, a prominent group of calcifying phytoplankton the play a central role in the global carbon cycle. We found using both new (2017-2020) and historical (1975-1976) data from the northern Red Sea that during ‘mild summers’, the most common coccolithophores, Emiliania huxleyi and Gephyrocapsa ericsonii, co-exist at similar densities. Both species then particularly flourish during subsequent winter periods where nutrient availability is higher due to convective mixing. However, during ‘hot summers’, which are progressively the norm over the last decades with average surface temperatures surpassing 27 °C for long time-periods, G. ericsonii density markedly declines. Moreover, it specifically remains at low background levels even during winter mixing periods, while E. huxleyi succession and development during winter appears unchanged. Further incubation assays using native assemblages validate that G. ericsonii’s growth over 27 °C is significantly reduced relative to E. huxleyi. Likely additional factors contribute to impair G. ericsonii populations at sea. Yet temperature is a key determinant. Our results illustrate the divergent impact of ongoing ocean warming in tropical phytoplankton species.
Marine particulate fluxes were studied between 2014 – 2017 in the oligotrophic Gulf of Aqaba (GOA), northern Red Sea. A bottom tethered mooring mounted with 5 sediment trap stations (KC Denmark Inc.) at approximately equal depth intervals between 120 and 570 meters (water depth ~610 m) was rotated monthly. The bulk particulate fluxes were determined for the entire period, with organic C and N, CaCO3 and lithogenic fluxes determined for the first two and half years of the deployment. The results are evaluated in the context of monthly resolved records of seawater temperature, chlorophyll-a concentrations, and macro-nutrient concentrations, and primary productivity rates, as well as hourly to weekly dust load records, and rare fluvial events. The results are further compared to core-tops collected from varying water depths, and are combined to produce a basin source-to-sink mass balance of particulate fluxes. The GOA undergoes strong seasonal changes expressed by surface water temperatures and water column stratification and mixing, which control the vertical and temporal distribution of nutrients and primary and export production. Accordingly, the seasonal variability in particulate fluxes varies over a wide range, typically displaying peak bulk fluxes in bottom waters during the winter (~5-7 g m-2 d-1) and minimum values in shallow waters during summer (<0.5 g m-2 d-1). Organic C and N fluxes are highest in shallow waters and display strong vertical attenuation that varies seasonally, reflecting enhanced remineralization in the warm shallow waters during summer. By contrast, particulate organic carbon and nitrogen fluxes are enhanced in bottom waters during winter, due to the combined effect of increased presence of mineral ballasts and vertical water column mixing. The quantification of particulate fluxes in the GOA suggests that while most of the bulk particulates are introduced into the basin via episodic fluvial events, with direct dust inputs contributing approximately an order of magnitude less material, the internal cycling of terrigenous material is complex, with a lag between initial deposition of influxing material along shallow margins and seasonal reworking and transport of sediments to the deep seafloor. Nevertheless, the fluxes of terrigenous and organic particulates are largely independent of each other, with export production fluxes driven by water column mixing and nutrient availability in the photic zone. In addition to being the first quantitative report of bulk and export production fluxes in the region, our results provide an improved understanding of the interplay between export production and terrigenous fluxes, as well as an interpretation of the paleo-record in the GOA and in comparable environments. On a wider scale, the findings reported here relate to global processes such as the role of dust deposition and hemipelagic sedimentation in the oceans and their impact on export production, and particle cycling in coastal regions. Combined, these findings illuminate the factors impacting marine habitats and ecosystems, the cycling and sequestration of trace elements and anthropogenic components in the oceans, and facilitate reconstructing past oceanographic and climatic conditions from marine sediment cores.
Coccolithophorids are key player in the marine biological pump and marine carbon cycle, as their production and community-structure are crucial for export and sequestration of carbon from the atmosphere to the deep sea with important implications to climatic trends. Variations in the species composition of coccolithophore communities largely reflect environmental changes and are therefore fundamental for palaeoceanographic reconstructions. The South China Sea (SCS) is an ideal area to study the response of coccolithophores to environmental change because of the remarkable seasonal and interannual variations of the monsoonal climate and the hydrography. However, to date only limited studies on the temporal changes of coccolithophores in the modern SCS have been reported. In the present work, coccolithophores in the northern SCS were investigated using time-series sediment traps during 2009–2010 and 2011–2012. Extinct coccoliths which had their last occurrence in the Miocene (e.g. Triquetrorhabdulus longus, Reticulofenestra floridanus), Pliocene (e.g. Reticulofenestra pseudoumbilica, Discoaster tamilis), and Pleistocene (e.g. Pseudoemiliania locunosa, Discoaster variabilis) were a frequent component of the coccoliths throughout all the seasons and provided, for the first time, a strong micropaleontological evidence for lateral advective transport in the deep SCS. The source of the fossil coccoliths most likely were the reworked Pleistocene sands which cover the outer shelf and upper slope to the west and south of the Dongsha Islands between 20 m and 600 m water depth. These sediments contain limestone fragments with foraminiferal assemblages of Miocene to Pliocene age, and, to the north and south of the islands, Miocene strata are exposed on the sea floor. Mesoscale eddies, both cyclonic and anticyclonic, were probably the main agent for resuspending and transporting the coccoliths as they propagated westwards along-slope from the Dongsha area to the mooring site. Extant coccolithophore were composed of 31 taxa with Florisphaera profunda, Gephyrocapsa oceanica, and Emiliania huxleyi contributing 91.4% and 83.8% of the annual coccolithophore export flux in 2009–2010 and 2011–2012, respectively; F. profunda was the predominant species. Enhanced fluxes of extant coccoliths occurred in the summer of 2009/2010, spring 2010, autumn 2011 and winter 2011/2012, but varied in phase with the extinct species. Therefore, lateral advection of extant taxa may have also taken place but the extent to which this may have masked primary signals from in-situ coccolithophore production remains open. The low fluxes of coccoliths in the winter of 2009/2010 in association with relatively reduced wind strength, higher SST and a shallower mixed layer might compared to those of 2011/2012 have been driven by the weak El Niño event, which affected the northern SCS during that season.
The production and ultimate fate of calcium carbonate in the global ocean has implications for the efficiency of the biological carbon and alkalinity pumps. Historically, sediment trap flux data and/or mass balance equations have been used to estimate the rate of particulate inorganic carbon production in the ocean. More recently satellite data has been used to provide a more comprehensive global overview of this important biogeochemical process based on relationships determined from multi‐linear regression of measured calcification rates against a number of measurable variables. Here we describe a simple model to estimate calcification rate based around elements of coccolithophore physiology that can be easily parametrized with satellite ocean color data. The model output conforms to our understanding of the spatial and temporal distribution of coccolithophores and performs relatively well at reproducing global rates that are of the correct order of magnitude, whilst capturing the variability in such a complex, natural process when compared to field calcification rate measurements (slope = 0.98; R2 = 0.28; p<0.05; RMSE = 0.53 mg C m‐3 d‐1). Average, global, euphotic zone depth integrated calcification rate is estimated to be 1.42 ± 1.69 Pg PIC yr‐1 with the oceanic gyres contributing the greatest influence. Estimates of global calcification rate are essential for understanding the efficiency of both the alkalinity and biological carbon pumps. A simple model parameterized with remotely sensed data can be used to estimate global calcification rates. Average, global, coccolithophore calcification rate is estimated to be 1.42 GT C yr‐1
Coccolithophores are unicellular pelagic algae, capable of calcification. In the Mediterranean Sea, several species have a well-known haplo-diploid life cycle, alternating the production of different types of calcite plates, the holo- and hetero-coccoliths. We analyzed the distribution of both phases along a W-E Mediterranean transect during April 2011 and May 2013 (spring season), following strong environmental gradients in salinity, oxygen and nutrient concentration, temperature, carbonate chemistry and fluorescence. The proportion of holococcolithophores:heterococcolithophores of selected species varies not only vertically through the water column, but also longitudinally, following the main environmental gradients. Based on the environmental affinities of the coccolithophore life phases, we conclude that a dimorphic life cycle might provide the ability to adapt to the south-eastern (SE) Mediterranean environment, in conditions characterized by surface water with relatively high calcite saturation state, high temperature, stratification and nutrient limitation, and support the survival of species whose diploid phases are in contrast adapted to Atlantic or south-western (SW) Mediterranean conditions. Thus, a haplo-diploid life cycle could provide a way to adapt to environmental changes.
The spring phytoplankton bloom is a major, extensively studied phenomenon in temperate oceans. Much less is known about blooms in subtropical seas. Yet, even in temperate seas the processes determining the initiation of the bloom and the phytoplankton dynamics during the preceding mixed-layer deepening are still debated. Here we assess the validity of two bloom-initiation mechanisms, previously proposed for temperate oceans, for the case of the subtropical oligotrophic Gulf of Aqaba (northern Red Sea): the Critical Depth Hypothesis and the Dilution-Recoupling Hypothesis. The Gulf is a unique water body, where convective mixing during winter reaches hundreds of meters in depth, entraining nutrients that support conspicuous spring blooms. Our study is based on a long time series of oceanographic and meteorological parameters complemented with experimental measurements of grazing rates. We show that neither the Critical Depth nor the Dilution-Recoupling hypotheses explain the phytoplankton dynamics during the winter and spring in the Gulf. Instead, we suggest that the phytoplankton dynamics is governed by a “Dispersion-Confinement Mechanism”. During winter, phytoplankton cells that photosynthesize and grow in the upper (illuminated) layer are homogeneously dispersed by vertical mixing. Thereby the deepening of the mixed layer leads to the dilution of the cells with plankton-free water from below, which together with grazing, maintain their relatively low concentration. Once mixing stops, the cells are no longer vertically dispersed, allowing their accumulation in the upper layer and, in turn, the development of the spring bloom. High specific growth rates, necessary to maintain the increase of the entire (integrated) phytoplankton biomass during the deepening of the mixed layer (the “Dispersion Phase”) as well as supporting their rapid growth during the bloom (the “Confinement Phase”) are possible due to the entrainment of nutrients by deep vertical mixing. Although this mechanism is proposed here for the case of a nutrient-limited oligotrophic sea, its relevance for temperate oceans deserves further consideration.
Coccolithophores—single-celled calcifying phytoplankton—are an important group of marine primary producers and the dominant builders of calcium carbonate globally. Coccolithophores form extensive blooms and increase the density and sinking speed of organic matter via calcium carbonate ballasting. Thereby, they play a key role in the marine carbon cycle. Coccolithophore physiological responses to experimental ocean acidification have ranged from moderate stimulation to substantial decline in growth and calcification rates, combined with enhanced malformation of their calcite platelets. Here we report on a mesocosm experiment conducted in a Norwegian fjord in which we exposed a natural plankton community to a wide range of CO2-induced ocean acidification, to test whether these physiological responses affect the ecological success of coccolithophore populations. Under high-CO2 treatments, Emiliania huxleyi, the most abundant and productive coccolithophore species, declined in population size during the pre-bloom period and lost the ability to form blooms. As a result, particle sinking velocities declined by up to 30% and sedimented organic matter was reduced by up to 25% relative to controls. There were also strong reductions in seawater concentrations of the climate-active compound dimethylsulfide in CO2-enriched mesocosms. We conclude that ocean acidification can lower calcifying phytoplankton productivity, potentially creating a positive feedback to the climate system.
It is generally accepted that most of the oceanic CaCO3 production is biogenic, whereas homogeneous, inorganic CaCO3 nucleation and precipitation from seawater is inhibited by the presence of other seawater constituents, including dissolved organic carbon. Notwithstanding, heterogeneous CaCO3 precipitation (HCP) from supersaturated seawater onto solid surfaces is well documented, evidence for HCP in the open-ocean settings has not been convincingly demonstrated. In this study, we provide evidence for inorganic CaCO3 precipitation in the water column of the Red Sea and in the neighboring Gulf of Aqaba. The evidence includes a decrease in alkalinity and dissolved inorganic carbon (DIC) at a 1.7:1 ratio along the southward route of Red Sea deep-water, and an alkalinity deficiency in the Gulf of Aqaba deep-water. These observations are made after correcting alkalinity and DIC for changes in nutrient content and salinity and are therefore not the result of mixing, respiration or photosynthesis. We suggest that the interaction between seawater and suspended solids, providing precipitation nuclei, resulted in HCP and accounted for the above-mentioned observations. We base this suggestion on: 1. time-series measurements in the Gulf of Aqaba, showing abrupt alkalinity decrease following the entrainment of large amounts of solids; 2. incubation experiments confirming that suspension of Gulf of Aqaba sediments in seawater induces a decrease in alkalinity; 3. precipitation of inorganic aragonite needles within the pores of the skeleton of a local coral. Based on the data presented here, we postulate that HCP may occur in parts of the ocean that receive a substantial influx of solid particles, and areas subject to frequent dust storms. Hence, HCP may be an overlooked pathway in the oceanic CaCO3 cycle.
Coccolithophores (calcifying haptophyte algae) commonly exhibit a heteromorphic life cycle, alternating between morphologically distinct heterococcolith (diploid) and holococcolith (haploid) phases. The prevalence of each life phase in a coccolithophore community defines its overall ecological and biogeochemical performance due to differences in physiology, biomass and calcification. The main drivers of life-cycle dynamics and ecological preferences of the two life-phases are still unclear and field data of high taxonomic resolution are needed. We investigated the distribution and abundance patterns of the life-phases of 14 coccolithophore species. The study was conducted along the strong environmental gradients of the Krka River estuary (Eastern Adriatic Sea) during winter (February) and summer (July) 2013. The results reveal characteristic life-phase seasonality with an overall dominance of the heterococcolith phase during winter and a holococcolith phase during summer. However, we also detected exceptions to the strictly seasonal patterns as well as species-specific ecological preferences. Our findings provide new insights into coccolithophore life-phase dynamics in the Mediterranean Sea that will further advance the understanding of ecology and evolution of the group.
The effects of elevated partial pressure of CO2 (pCO2) on plankton communities in oligotrophic ecosys- tems were studied during two mesocosm experiments: one during summer 2012 in the Bay of Calvi, France, and another during winter 2013 in the Bay of Villefranche, France. Here we report on the relative abundances of coccolithophores versus siliceous phytoplankton, coccolithophore community structure, Emiliania huxleyi coccolith morphology and calcification degree. A pCO2 mediated succession of phyto- plankton groups did not occur. During both experiments, coccolithophore abundance and community structure varied with time independently of pCO2 levels. Changes in the community structure were partly explained by the concentration of phosphate during the winter experiment. During the summer experiment, it was not clearly related to any of the parameters measured but possibly to changes in temperature. Phenological changes in the community and an attenuated response due to the low biomass building during the winter experiment could have masked the response to pCO2. E. huxleyi dominated the coccolithophore community in winter; it was not affected by elevated pCO2 at any time. In contrast, the abundance of Rabdosphaera clavigera, the dominant species in summer, increased with time and this increase was affected at elevated pCO2. Thus, a different coccolithophore community response based on species-specific sensitivities to pCO2 is still likely. Finally, elevated pCO2 had no traceable effect on E. huxleyi (type A) coccolith morphology or on the degree of coccolith calcification. Our results highlight the possibility that, in oligotrophic regions, nutrient availability, temperature or intrinsic phenological changes might exert larger constrains on the coccolithophore community structure than high pCO2 does solely.
A. Introduction.- A.1 Background and History of Research.- A.2 List of Participants and Their Contributions.- A. 3 Purpose of the Book.- B. Synopsis.- C. The Gulf of Aqaba - a Rift-Shaped Depression.- D. A Desert-Enclosed Sea.- D.1 Climate.- D.2 Hydrography.- D.3 Circulation Pattern.- D.4 Seasonality.- D.5 Nutrients.- D.6 Primary Production.- D.7 Composition of Plankton.- D.8 Light.- D.9 Characteristics of Water Masses.- E. Shell Producers in the Water Column.- E.1 Calcareous Plankton.- E.2 Coccolithophorida.- E.3 Foraminiferida.- E.4 Pteropoda.- E.5 Aqaba Calcareous Plankton: Significance and Problems.- F. The Sea Bottom - a Mosaic of Substrates.- F.1 Methods of Investigation.- F.2 Selected Areas.- F.2.1 The "Shelf" in Front of the H. Steinitz Marine Biology Laboratory.- F.2.2 Geziret Fara'oun ("Coral Island").- F.2.3 Ras Burka.- F.2.4 Dahab.- F.2.5 Mangroves.- F.2.6 Marset el At.- F.2.7 Ras Muhammed.- F.2.8 Grafton Passage, Tiran.- F.3 Significance of the Depth Gradient.- F.4 Significance of Substrates.- F.5 Seasonality.- G. Benthic Foraminifera: Response to Environment.- G.1 Larger Foraminiferans.- G.1.1 Soritines.- G.1.2 Alveolinids.- G.1.3 Amphisteginids.- G.1.4 Nummulitids.- G.2 "Smaller" Benthic Foraminifera.- G.3 Significance of Shell Morphogenesis.- G.4 Significance of Symbiosis.- G.5 Stable Isotopes and Related Problems.- G.6 Thanatocoenoses.- H. 150,000 Years Gulf of Aqaba.- H.1 Deep Sea Cores.- H.2 Microfossil Assemblages from Cores.- H.3 Stratigraphy.- H.4 Paleoenvironments.- H.5 Paleoceanographic History.- References.- Taxonomic Index.
Present-day production of CaCO3 in tne world ocean is calculated to be about 5 billion tons (bt) per year, of which about 3 bt accumulate in sediments; the other 40% is dissolved. Nearly half of the carbonate sediment accumulates on reefs, banks, and tropical shelves, and consists largely of metastable aragonite and magnesian calcite. Deep-sea carbonates, predominantly calcitic coccoliths and planktonic foraminifera, have orders of magnitude lower productivity and accumulation rates than shallow-water carbonates, but they cover orders of magnitude larger basin area. Twice as much calcium is removed from the oceans by present-day carbonate accumulation as is estimated to be brought in by rivers and hydrothermal activity (1.6 bt), suggesting that outputs have been overestimated or inputs underestimated, that one or more other inputs have not been identified, and/or that the oceans are not presently in steady state. One “missing” calcium source might be groundwater, although its present-day input is probably much smaller than that of rivers. If, as seems likely, CaCO3 accumulation presently exceeds terrestial and hydrothermal input, this imbalance presumably is offset by decreased accumulation and increased input during lowered sea level: shallow-water accumulation decreases by an order of magnitude with a 100 m drop in sea level, while groundwater influx increases because of heightened piezometric head and the diagenesis of metastable aragonite and magnesian calcite from subaerially exposed shallow-water carbonates.
The stability and persistence of coral reefs in the decades to come is uncertain due to global warming and repeated bleaching events that will lead to reduced resilience of these ecological and socio-economically important ecosystems. Identifying key refugia is potentially important for future conservation actions. We suggest that the Gulf of Aqaba (Red Sea) may serve as a reef refugium due to a unique suite of environmental conditions. Our hypothesis is based on experimental detection of an exceptionally high bleaching threshold of northern Red Sea corals and on the potential dispersal of coral planulae larvae through a selective thermal barrier estimated using an ocean model. We propose that millennia of natural selection in the form of a thermal barrier at the southernmost end of the Red Sea have selected coral genotypes that are less susceptible to thermal stress in the northern Red Sea, delaying bleaching events in the Gulf of Aqaba by at least a century. This article is protected by copyright. All rights reserved.