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Draft:Calcidiscus leptoporus

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Microfossils of C. leptoporus

Calcidiscus leptoporus is a coccolithophore species found globally and is recognized for its extensive fossil record, which dates back to the Early Miocene[1]. C. leptoporus, like all coccolithophores, is a unicellular marine phytoplankton within the Haptophyta phylum and plays a vital role in the production of calcium carbonate in the oceans[1]. As one of the most productive marine calcifying species, its distribution and calcification patterns are impacted by environmental factors like temperature, seasonality, and ocean chemistry[1][2][3].

Classification

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The first recorded observation of C. leptoporus was made in 1989 by George Murray and Vernon H. Blackman in a sample of seawater collected by Murray from the Atlantic Ocean[4]. They called their observation a new species, given its comparably small size and circular coccoliths, and gave it the name Coccosphaera leptoporus.

Coccolithophore classification shifted in the 1950s as new genera were described. Two new species, C. medusoides and C. quadriforatus, were described by Erwin Kamptner in 1950 as members of a new genus, Calcidiscus[5][6]. In 1958, Kamptner reclassified C. medusoides as a member of the genus Tiarolithus. Later TEM analysis of coccoliths determined that T. medusoides and C. quadriforatus were of the same species as Coccosphaera leptoporus[7][8]. In 1954 Kamptner also re-classified Coccosphaera leptoporus as a member of the new genus Cyclococcolithus[9], along with other previously described species Umbilicosphaera mirabilis[10]. However, as U. mirabilis is the type species for genus Umbilicosphaera, this classification was in conflict with the International Code of Botanical Nomenclature (ICBN)[11], and was therefore rejected[6]. In years following several other genera of coccolithophore were proposed in lieu of the rejected name. C. foliosus was used as a type species for the newly propposed name Cycloplacolithella in 1968[12], though it was later determined that the C. foliosus images used for the classification were of the same species as Coccosphaera leptoporus. [13], making this name invalid[3][6]. Another genus, Cyclococcolithina, was proposed with a variant of C. leptoporus, C. leptoporus var. inversus[14], as its type species[15]. However, C. leptoporus var. inversus was promoted to species status within the genus Markalius[16], and was made the type species for that genus, therefore making Cyclococcolithina invalid[3][6]. By the late 1970s, several genera that contained Coccosphaera leptoporus, or coccolithophores later identified as Coccosphaera leptoporus, had been proposed, though they all had problems as listed above. As a solution, these genera were combined. Due to it being the oldest of the generic names, and the only one that was not previously rejected by the ICBN, Calcidiscus was the name given to this genus that now contained C. leptoporus and other members of the previously rejected genera[6].

Morphotypes and subspecies

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C. leptoporus, like many coccolithophorids[17][18], has great intra-species diversity and variability[19][20].This variability was noted from its first observation in 1898, which describes variability in both the number structure of coccoliths[4]. C. leptoporus has been consistently shown to vary distinctly with regards to size, and it often divided into morphotypes based on this. Commonly, three morphotypes are described generally as 'small', 'intermediate', and 'large'[21][22] (see 'Subspecies and Morphotypes' below). Though, there has been discussion as to whether these morphotypes are due to genetic differences or are phenotypic differences based on environment (see 'Morphotype Distribution and Environmental Preferences' below).

C. leptoporus leptoporus and C. leptoporus quadriperforatus

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There is evidence to suggest that intermediate and large morphotypes of C. leptoporus are distinct enough to be considered separate subspecies, or even different species. In 2002, differences in lifecycles was used as evidence to suggest that the intermediate morphotype be called C. leptoporus leptoporus, and the large morphotype be called C. leptoporus quadriperforatus, as subspecies of C. leptoporus[23]. In 2003, genetic differences in both the conserved 18S rDNA gene and the tufA gene was used to suggest that C. leptoporus quadriperforatus was different enough to be considered its own species, C. quadriperforatus[24]. However, this morphotype is still referred to both as C. leptoporus quadriperforatus[25][26] and C. quadriperforatus[27][28] in research since these publications. As of 2022, the International Nannoplankton Association refers to the intermediate and large morphotypes as C. leptoporus leptoporus and C. leptoporus quadriperforatus[29].

Life Cycle

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C. leptoporus, along with other Coccolithophores, exhibit a halo-diplontic life cycle, each classified based on the coccoliths produced. Life stages alternate between heterococcolith bearing (diploid) and holococcolith bearing (haploid) phases and are intended to facilitate their adaption to environmental variability, expanding their ecological niche[30].

Haplo-diplontic life cycle

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Life cycle strategies of phytoplankton
TEM of C. leptoporus in its haploid phase

Defined by the number of chromosomes an organism has during asexual reproduction (mitosis), life cycle is characterized as diplontic, as is the case for diatoms, or haplontic, as is the case for dinoflagellates with few organisms possessing the ability to exhibit both. Haplo-diplontic life cycles are classified by the ability of an organism to divide in both haploid and diploid phases[31]. Organisms exhibiting this life cycle divide by mitosis in both haploid and diploid phases to retain their ploidy levels. Organisms are able to switch from a diploid life phase to a haploid life phase by undergoing meiosis. Alternatively, haploid cells fuse with other haploid cells, presenting as cells in the diploid phase[31].

SEM image of C. leptoporus in its diploid phase

Haplo-diplontic coccoliths

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Coccolith structure varies in coccolithophore diploid and haploid life phases. The haploid phase is characterized as lightly-calcified in which holococcoliths are comprised of simple rhombic crystals. Whereas in the diploid phase, hetercoccoliths are heavily calcified and comprised of elaborately shaped crystals[30].

Haplo-diplontic ecological niches

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Heterococcolithophores and holococcolithophores switch between ploidy levels based on environmental stressors. Stresses mainly include nutrient depletion and light availability. Holococcolithophores are more tolerant to high light, able to survive in both dark and light conditions, whereas hetercoccolithophores are only able to divide in low light conditions. Holococcoliths are also more tolerant of nitrate (N) and phosphate (P) depleted environments, whereas heterococcolithophores exhibit defects in coccolith formation under these conditions[30]. Differences in tolerances suggest that each life cycle occupies its own ecological niche with heterococcolithophores occupying light depleted and high nutrient environments and holococcolithophores occupying light abundant and low nutrient environments, made possible by a haplo-diplontic life cycle[30].

Morphology

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An important component of all coccolithophores is the coccolith, which consists of interlocking calcite (CaCO3) platelets that surround the cell, creating the coccosphere. However, despite being a shared, characteristic structural component, coccoliths have unique, species-specific morphology due to their intricate biosynthesis[32]. Coccospheres range in rigidity, spines, and other shape modifications to suit the species’ needs[33]. However, unfavourable environmental conditions can lead to coccolith malformation and reduced calcite production[34]. Artificial, laboratory conditions have also been shown to negatively impact the morphology of C. leptoporus[19]. Naturally-occurring C. leptoporus has coccoliths generally ranging from <5µm to 8µm or greater[19]. Its sutures are angular and serrated, though some variability exists between its subspecies.

Carbonate coccolith calcite contributes greatly to deep-sea carbonate sediments as it causes the sinking of other organic matter, while its precipitation serves as a carbonate counter pump by sequestering atmospheric CO2 and increasing aqueous CO2[25][35]. C. leptoporus has been shown to dominate the production of calcite in the South Atlantic, and therefore plays a crucial biogeochemical role in the Subantarctic Zone[25].

Changes in morphology over the life cycle

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Coccolithophores, including C. leptoporus, undergo calcified haploid or diploid life stages depending on the environment. The diploid stage is usually dominant under normal circumstances. Meanwhile, the haploid stage is dominant when environmental cues are received. During the diploid life stage, a protococcolith ring is first formed within a tightly associated coccolith vesicle (CV). This protococcolith ring consists of repeating sub-vertical and sub-radial calcite crystal units. The ring is then formed into various species-specific morphologies and becomes embedded within the mature coccolith[32][33]. The diploid stage is characterized by round calcite heterococcoliths, which join at the proximal and distal shields to form the coccosphere. However, during the haploid life stage, holococcoliths are formed intracellularly, which are smaller and composed of different crystal units than heterococcoliths. In addition, a relatively large vacuole space exists between the cell and the holococcosphere, which contrasts the tight association between heterococcoliths and CVs in the diploid stage. Unmineralized body scales are secreted to cover the cell, including smaller “lacey” body scales and larger, more densely structured baseplate scales[32]. However, despite these differences, C. leptoporus utilizes the same Ca2+ transport mechanisms for coccolith production, no matter the life stage.

Different coccolithophore species (a-e), C. leptoporus (c)

Subspecies and morphotypes

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C. leptoporus is divided into three subspecies, depending on the size and fine structure of the coccolith. The small morphotype includes those with a coccolith diameter of <5µm and has irregular, angular, and serrated suture lines, which can be used to differentiate from the intermediate morphotype[22]. The intermediate subspecies has a coccolith diameter of 5-8µm and a clear central area. The large (coccolith diameter >8µm) morphotype was raised to species level and now recognized as C. quadriperforatus[27]. In addition to the larger cocolith diameter, C. quadriperforatus also has more numerous and more curved distal shield suture lines, as well as an infilled central area in the coccolith.

Ecology

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Abundance patterns and seasonal dynamics

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C. leptoporus is found across a wide range of oceanic regions, from tropical to subpolar waters, and exhibits different abundance patterns shaped by seasonal oceanographic conditions[1].

Cell counts of C. leptoporus performed in 1991 in the Sargasso Sea at Hydrostation S provide an in-depth analysis of abundance patterns[1]. Between January and February, cells were distributed throughout the water column, with the highest concentrations (up to 109 cells/litre) observed at depths of 100 to 150 m[1]. With the onset of thermal stratification in March/April, C. leptoporus populations migrated to deeper layers, reaching peak concentrations near the nutricline while overall abundance declined (maximum of 28 cells/litre at 150 m)[1]. During this time, abundance in the upper 100 m remained low (approximately 10 cells/litre)[1]. As late spring/summer approached, cell concentrations increased sharply, peaking at over 500 cells/litre in the upper 50 m of the water column before dropping toward the end of summer[1]. The upper 100 m of the water column experienced a second increase in abundance in the fall, but remained lower in concentrations than in the spring and summer periods (maximum of 69 cells/litre)[1]. Thus, two seasonal peaks of abundance occur throughout the year: a major peak in the spring/summer (May/July) and a smaller, secondary peak in the fall/winter (November to March)[1].

Time series sediment trap studies showed seasonal variations in the abundance of C. leptoporus at several geographical sites. In the North East Atlantic, C. leptoporus populations peaked during spring at the beginning of summer stratification[35]. Peak abundances occurred in late spring-start of summer in the North West Atlantic, followed by a minor peak in the winter[35]. Seasonal, reversing wind patterns in the Arabian Sea lead to a rise in C. leptoporus abundance during monsoon periods[35]. However, the magnitude of this increase was smaller than that observed in the other sites[35]. While C. leptoporus populations in the North Atlantic reach their maximum abundance during spring and summer, the Arabian Sea experiences its highest concentrations in the fall[35].

Morphotype distribution and environmental preferences

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The interplay between C. leptoporus morphotypes and environmental parameters is complex and can vary depending on the geographic location. Multiple studies infer that the three C. leptoporus morphotypes have different environmental preferences[2][35][36][37].

It has been proposed that the intermediate morphotype of C. leptoporus prefers colder temperatures and lower nutrient availability based on relative abundance data from the North Atlantic and Arabian Sea[35]. However, the intermediate morphotype has been found to have an affinity for cooler waters and higher nutrient availability in the South Atlantic[2][37]. The large morphotype seems to favour productive environments with higher temperatures and nutrient levels[35][36][37]. While data on the small morphotype of C. leptoporus is limited, observations suggest a preference for nutrient-enriched waters[2][35][37].

Effects of ocean acidification

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An experimental study showed that coccolith formation in C. leptoporus is impaired under conditions of elevated CO2 concentrations and low pH[3]. Further research examined various manipulations of the seawater carbonate system on C. leptoporus coccolith morphology and revealed that increased numbers of malformed coccoliths were driven by the increase in CO2 concentration, rather than changes in pH, total alkalinity, dissolved inorganic carbon, bicarbonate, or carbonate ion concentrations[38]. Moreover, pCO2 levels over 1500 μatm were found to promote cell aggregation[38].

Ecological Importance of Calcidiscus leptoporus

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Paleo-Proxy for Growth Rate

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C. leptoporus Coccolith size (mass and area) exhibits a statistically significant positive correlation with growth rate. Supported consistent patterns by sediment trap studies in the Subantarctic Southern Ocean and North Atlantic Ocean show a consistent, statistically significant positive correlation between coccolith flux and both mass and area, suggesting a biological mechanism instead of a site-specific[25][35]. Furthermore, controlled experiments have demonstrated that slower growth rates lead to smaller coccoliths, while faster growth rates yield larger, well-formed ones[3][30]. However, further studies are required to validate this relationship under varying environmental conditions.

Measuring the size of coccoliths and calibrating with δ¹³C have the potential to strengthen interpretation and provide valuable insight into past ocean productivity and environmental shifts, particularly in areas where C. leptoporus is a significant contributor to carbonate export. If the current positive correlation is validated, this approach holds promise as a useful tool in paleoceanographic research, although this is still a developing field.

Important Contributor to Carbonate Export

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In the studies within the Southern Ocean's Subantarctic Zone, C. leptoporus is considered to be disproportionately significant in calcium carbonate export in the ocean. Despite being much less abundant than smaller coccolithophores such as Emiliania huxleyi, C. leptoporus produces larger and denser calcited coccoliths that facilitate sinking, strengthening contribution to long-term carbon export, even in circumstances where it is less numerically dominant. These contribute more mass per cell to carbonate sedimentation[39].

This ecological significance is magnified in the Great Calcite Belt (GCB), where calcite production is particularly high between 40–60°S. Sediment trap studies indicate C. leptoporus, account for 30–70% annual carbonate export in this region[39]. Furthermore, The GCB spans roughly 16% of the global ocean surface, highlighting C. leptoporus significance in oceanic carbon cycles[40].

Impact on the Biological Pump

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The dense and heavy coccoliths of C. leptoporus facilitate the process of ballast organic material and enhance the efficiency of the biological pump. These coccoliths increase the sinking velocity of both organic and inorganic material. As a result, there is an increased likelihood of carbon being exported to the deep ocean for long-term carbon sequestration, rather than being recycled in surface waters [41].

References

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