The effect of sea water salinity on the morphology of Emiliania huxleyi in plankton and sediment samples

doi:10.1016/j.epsl.2009.05.003

Earth and Planetary Science Letters

Volume 284, Issues 3–4, 15 July 2009, Pages 320-328

https://doi.org/10.1016/j.epsl.2009.05.003 Get rights and content

Abstract

We analysed the morphology of Emiliania huxleyi from globally distributed plankton samples and demonstrate that the size of E. huxleyi placoliths is highly correlated to in-situ sea surface water salinity. We used multiple linear regression analysis to link morphological parameters of E. huxleyi to in-situ salinity and in-situ temperature. The best multiple regression model yielded an R² = 0.84 with a standard residual error of 0.65 for in-situ salinity over a gradient from 32.6 to 38.8. No significant correlation existed with temperature. Our results suggest that the morphology of E. huxleyi placoliths of recent and ancient sediments may provide a robust method to reconstruct sea surface salinities. One caveat is that the plankton-derived multiple regression model for in-situ salinities is different from that reported from previous work on Holocene sediments. This discrepancy is most likely caused by taphonomic processes or from the biogeographically biased data sets which were used (open ocean versus near shore). The cause of the tight relation between salinity and morphological response is not well understood but may be related to cell turgor regulation that affects the size of the cell and thus the size of a single coccolith.

Introduction

Variations in salinity and temperature result in density differences of ocean water which is the single most important parameter that defines water masses, ocean stratification and deep water thermohaline circulation. All of these parameters are major factors affecting the climate system and therefore, the precise knowledge of past ocean salinity and temperature is of utmost importance to identify mechanisms that drive the climate system. In contrast to temperature, salinity cannot be easily reconstructed from geological archives with the same accuracy and reliability as temperature because several assumptions need to be made that lead to a significant error of the salinity estimates (Rohling and Bigg, 1998, Rohling, 2000). This explains why no widely accepted paleo-salinity proxy is currently available (Henderson, 2002, Bollmann and Herrle, 2007).

Recent approaches to develop a reliable salinity proxy utilize single celled marine algae, coccolithophores. Culture experiments indicate a significant relationship between the hydrogen isotopic composition of long chain alkenones synthesized by the species Gephyrocapsa oceanica and Emiliania huxleyi and salinity (Schouten et al., 2006). Although the growth rate of G. oceanica and E. huxleyi also affects the fractionation factor, the hydrogen isotopic composition of alkenones appears to have great potential for the reconstruction of past salinities, especially if it is used in a multi proxy approach (van der Meer et al., 2007, van der Meer et al., 2008).

Also the morphological variation of the world's most abundant coccolithophore species, E. huxleyi, in core-top samples is related to sea surface salinity (Bollmann and Herrle, 2007). Bollmann and Herrle (2007) established a salinity transfer function based on the morphological variation of E. huxleyi and used it to reconstruct the ocean salinity during the LGM. Although the results are in good agreement with published values for the LGM, this promising technique needs to be further constrained by plankton analysis and controlled laboratory culture experiments. Towards this goal, we have analysed the morphology of E. huxleyi from globally distributed plankton samples.

Section snippets

Materials and methods

A total of 28 plankton samples were collected from the Atlantic, Pacific and Southern oceans (Fig. 1, Table 1) covering an in-situ salinity gradient from 32.6 to 38.8 and an in-situ temperature gradient from 1.93° to 28.31 °C.

Results

The morphology of around 1400 placoliths of the coccolithophore species E. huxleyi was analyzed from 28 globally distributed plankton samples that cover an in-situ salinity gradient from 32.6 to 38.8 and an in-situ temperature gradient from 1.93° to 28.31 °C. From the morphometric measurements several parameters such as the length and width of the distal shield (DL, DW) and the area of the central area (CAA) were calculated (Fig. 2, Fig. 3). Multiple linear regression analysis was applied to

Discussion

Our results indicate that the morphological variability of E. huxleyi placoliths is significantly related to salinity variability and support the results of Bollmann and Herrle (2007). Their regression model showed a significant relationship between morphology of E. huxleyi placoliths and sea surface salinity based on Holocene sediment core-top samples. However, their stepwise regression analysis of the sediment data set revealed that width and not length (as was found in this study) of the

Conclusions

We have demonstrated that the morphology of E. huxleyi, the world's most abundant coccolithophore species, varies systematically in plankton samples over a large salinity gradient. Our analysis confirms that the morphology of E. huxleyi responds in plankton samples in a similar way to that reported from culture experiments (Green et al., 1998) and surface sediments (Bollmann and Herrle, 2007). However, the derived multiple linear regression model for in-situ salinities is different from that

Acknowledgements

We thank Claire Findlay, Patrick Holligan, Ralf Schiebel, Toby Tyrrell and Cornelius Veltkamp. The manuscript benefited from the comments of five anonymous reviewers. Financial support came from JOH and JB's Natural Sciences and Engineering Research Council Canada Discovery Grant and JOH's support from Canada Research Chairs.

References (22)

BollmannJ.
Morphology and biogeography of Gephyrocapsa coccoliths in Holocene sediments
Mar. Micropaleont.
(1997)
BollmannJ. et al.
Morphological variation of Emiliania huxleyi and sea surface salinity
Earth Planet. Sci. Lett.
(2007)
BollmannJ.
Techniques for quantitative analyses of calcareous marine phytoplankton
Mar. Micropaleont.
(2002)
HendersonG.
New oceanic proxies for paleoclimate
Earth Planet. Sci. Lett.
(2002)
RohlingE.J.
Paleosalinity: confidence limits and future applications
Mar. Geol.
(2000)
van der MeerM.
Hydrogen isotopic compositions of long-chain alkenones record freshwater flooding of the Eastern Mediterranean at the onset of sapropel deposition
Earth Planet. Sci. Lett.
(2007)
van der MeerM.
Molecular isotopic and dinoflagellate evidence for Late Holocene freshening of the Black Sea
Earth Planet. Sci. Lett.
(2008)
YoungJ.R. et al.
Genotypic variation in the coccolithophorid species Emiliania huxleyi
Mar. Micropaleontol.
(1991)
BrandL.E.
Genetic variability and spatial patterns of genetic differentiation in the reproductive rates of the marine coccolithophores Emiliania huxleyi and Gephyrocapsa oceanica
Limnol. Oceanogr.
(1982)
GreenJ.C. et al.
Changes in calcification and the dimensions of coccoliths of Emiliania huxleyi (Haptophyta) grown at reduced salinities
Phycologia
(1998)

HasegawaD. et al.

How islands stir and fertilize the upper ocean

Geophys. Res. Lett.

(2003)

Cited by (39)

Globally enhanced calcification across the coccolithophore Gephyrocapsa complex during the mid-Brunhes interval
2023, Quaternary Science Reviews
Evolutionary or adaptative changes in Noelaerhabdaceae coccolithophores occurred in parallel with major changes in carbonate export and burial during scenarios of low orbital eccentricity, with a ∼400 kyr recurrence, during the Pleistocene. Coeval with these conditions of enhanced proliferation, here we report that the calcification of specimens was enhanced at a global scale and across multiple species or morphotypes within the Gephyrocapsa complex during the Mid-Brunhes (MB) interval. This acme of increased production of organic and inorganic carbon by Gephyrocapsa, suggests that such global changes may originate from a common driver. Increased seawater alkalinity, with an appropriately long residence time, is proposed as environmental trigger on the selection of a wide variety of highly calcified and prolific Gephyrocapsa taxa. This new perspective highlights the role of orbital forcing in phytoplankton evolution or adaptation, via a global environmental driver in the form of seawater carbon chemistry. Our results fit with earlier proposals appealing for an intensified biological pump and respiration dissolution during this interval. We hypothesize that the Gephyrocapsa acme may play a double-edged role, by increasing shallow respiration dissolution rates, limiting the removal of alkalinity by burial, which may help to recycle alkalinity and maintain constant levels at the ∼400 kyr scale. This idea suggests the potential capacity of the Noelaerhabdaceae coccolithophore acmes to modify the typical behaviour of carbonate compensation in the ocean and that the changes in coccolithophore calcification may be indicative of changes in ocean carbonate chemistry and the operation of the global carbon cycle in the past.
New insights into the Barremian–lower Aptian calcareous nannofossils of the Mediterranean Tethys: Chronostratigraphic and paleobiogeographic implications
2022, Marine Micropaleontology
Citation Excerpt :
Although the driving factors for size changes of calcareous nannofossils have been discussed in the last decades, both for living assemblages and for fossil species, these still remain unclear. In living assemblages, some link was found between coccolith morphology and environmental factors such as sea-water temperature and salinity (e.g., Bollmann and Klaas, 2008; Bollmann et al., 2009; Triantaphyllou et al., 2010). In deeper time, studies are more problematic due to difficulties in the reconstruction of the paleoenvironmental conditions and the effects of preservation in the fossil assemblages.
A detailed study of calcareous nannofossil assemblages from twelve uppermost lower Barremian–lower Aptian sections in the Subbetic Domain of the Betic Cordillera was performed. Seven new nannofossil species (Crucibiscutum bastetanum, Crucibiscutum gracile, Chiastozygus lamprostauros, Cyclagelosphaera platyaspis, Lithraphidites aichmoides, Lithraphidites pugio, and Rhagodiscus sicutclipeus) are described, one species is emended (Lithraphidites magnus) and the taxonomic concept of the marker species Hayesites irregularis is discussed and clarified. The detailed stratigraphic ranges of the new species, together with those of other relevant taxa, are determined and correlated to standard ammonite biostratigraphy. Age estimates of biostratigraphically relevant calcareous nannofossil biohorizons are calculated using astrochronologically tuned cyclostratigraphic data. Five new calcareous nannofossil subzones are proposed which enhance upper Barremian biostratigraphic resolution at a regional scale and are directly correlated with respect to the standard Tethyan ammonite zonation. Two of the new species described here are used as biostratigraphic markers for the newly proposed subzones. The duration of each subzone is provided through astrochronological calibration. This study allows the refinement of the calcareous nannofossil zonation for the Mediterranean–Atlantic province of the Tethyan Realm. The implications of these new results are discussed regarding the extant definition and use of the Barremian/Aptian boundary. The morpho-evolutionary trends of selected nannofossil groups are reviewed in relation to the latest Barremian–Aptian paleogeographic changes, showing these were a prominent factor controlling calcareous nannoplankton evolution and biogeographical distribution in the west European-Atlantic region.
Coccolith size rules – What controls the size of coccoliths during coccolithogenesis?
2022, Marine Micropaleontology
Heterococcoliths are calcite platelets produced inside diploid coccolithophore cells and extruded to form a covering on the cell surface called a coccosphere. The size of coccoliths is an important parameter sometimes used to identify species, and it is observed to be influenced in extant species by abiotic parameters (e.g., CO₂, light). However, the variable distribution of coccolith sizes occurring within a single coccosphere questions the mechanisms controlling coccolith size. A relationship between cell/coccosphere size and mean coccolith size was previously identified, called the “coccolithophore size rules”. In this study, we query the mechanisms controlling the size of a coccolith during coccolithogenesis. A culture experiment on Gephyrocapsa huxleyi strain RCC1216 shows that coccolithogenesis occurs during the cell growth G1 interphase and newly produced coccoliths get bigger as the cell grows. These observations provide parameters for the development of two numerical models used to simulate the coccolith size distribution within a coccolithophore population. Neither model can accurately reproduce an empirical monoclonal coccolith size distribution, indicating that additional factors influence coccolith size. According to our results, coccolith size is only clearly related to cell size at the time of its formation. We confirm that application of the coccolithophore size rules model should be limited to inferring average cell dimensions from (fossil) coccolith biometry, and that comparisons are valid only in multipopulational studies. The coccolith size rule model – the constraining effect of coccolith production during G1 interphase cell growth on coccolith size – proposed here is applicable only for some placolith-forming species.
Emiliania huxleyi biometry and calcification response to the Indian sector of the Southern Ocean environmental gradients
2022, Palaeogeography, Palaeoclimatology, Palaeoecology
An increase in the atmospheric pCO₂ and temperature is expected to reduce ocean CO₃²⁻ concentration, make oceans warmer and alter ocean circulation patterns. This will also affect the production and biogeographic distribution of marine calcifying organisms including coccolithophores. The lowering of oceanic CO₃²⁻ is expected to interfere with the coccolithophore calcification process and cause malformation of coccoliths, whereas changes in the oceanic temperature and circulation patterns may shift their biogeographic boundaries. In this study, we have investigated Emiliania huxleyi coccolith and coccosphere size response to the wide-ranging physico-chemical conditions of the Indian sector of the Southern Ocean between latitudes 38^oS and 58^oS during the austral summer of 2010 (January–February). This study helps to understand the response of E. huxleyi coccolith/coccosphere morphometry and mass changes to the fluctuating temperature, salinity, CO₃²⁻, pCO₂, and nutrient values. Our results show that in the Indian sector of the Southern Ocean, E. huxleyi coccoliths are larger and coccospheres are smaller in the Subtropical Zone (STZ). In contrast, coccoliths size is smaller and coccospheres size is larger in the Subantarctic Zone (SAZ), which is due to the decrease in Sea Surface Temperature, Sea Surface Salinity and increase in nutrient concentrations. In the Indian sector of the Southern Ocean, E. huxleyi shows a north-to-south morphotype shift from the heavily calcified ‘Group A’ (E. huxleyi morphotype A) to the weakly calcified ‘Group B’ (E. huxleyi morphotypes B/C, C) forms. We demonstrate that although weakly calcified E. huxleyi morphotypes (morphotypes B/C and C) comprise less mass than that of the E. huxleyi morphotype A, due to the large-sized coccospheres and numerous coccoliths per coccosphere, ‘Group B’ coccospheres precipitate large amount of CaCO₃ in the SAZ compared to ‘Group A’ coccospheres located in the STZ. We have documented the presence of large E. huxleyi overcalcified coccospheres with large-sized coccoliths in the southernmost cold, high pCO₂, and nutrient-rich waters which show extracellular calcite precipitation. The energy dispersive spectrometry analysis indicates the presence of a large amount of Mg in the overcalcified E. huxleyi specimens. We suspect that E. huxleyi in the colder nutrient-rich waters, with future projected changes in the carbonate chemistry, may adapt to low pH, high pCO₂ conditions through extracellular Ca and Mg mineralization.
Interannual changes of austral summer coccolithophore assemblages and southward expanse in the Southern Indian Ocean
2020, Deep-Sea Research Part II: Topical Studies in Oceanography
Coccolithophore ecology and biogeography in the Southern Indian Ocean was studied during the austral summer of 2009 (SOE09; late austral summer), 2010 (SOE10; mid-austral summer), and 2012 (ISEA12; early austral summer). During the SOE09 and SOE10, surface water samples (55 and 54 water samples, respectively) were collected from two different transects between Mauritius and Antarctica (~48°E; ~57.3°E); whereas during the ISEA12, 22 sea surface water samples were collected between Cape-Town and Prydz Bay. Highest coccolithophore diversity was during SOE10 (36 taxa), followed by SOE09 and ISEA12 (12 and 7 taxa, respectively) whereas, highest coccolithophore abundance was reported during the ISEA12 (up to 2203 × 10³ coccospheres/l) followed by SOE10 (up to 742 × 10³ coccospheres/l) and SOE09 (up to 217 × 10³ coccospheres/l). During each expedition, elevated coccolithophore diversity was documented at the Subtropical zone whereas the highest abundance was recorded at the Subantarctic zone, which was dominated by Emiliania huxleyi. Differences in the occurrence and southward expanse of coccolithophores were documented during each expedition, i.e. maximum southward expanse during the SOE10 and lowest during the ISEA12. We show that, biogeographic boundaries of coccolithophores are highly variable in the Southern Indian Ocean which is controlled by environmental factors in the early and mid-austral summer, and grazing pressure in the late austral summer. In addition, the physical forcing also may play a key role in transport of coccoliths and coccospheres in the high latitudes. We indicate that, southward expanse of coccolithophores is significant and may occur for short periods during austral summer.
Late Quaternary coccolith weight variations in the northern South China Sea and their environmental controls
2020, Marine Micropaleontology
Coccolithophores are one of the most abundant and widespread groups of calcifying plankton and have attracted extensive study in terms of their likely response to ocean acidification. Conflicting results concerning coccolithophore calcification have been reported from both experimental and field studies. Due to their minute size, it is difficult to estimate the amount of calcite in coccoliths. Here we apply the SYRACO system to analyzing the weights and lengths of coccoliths produced by the dominant coccolithophore family Noëlaerhabdaceae. We obtain high-resolution coccolith weight and length records of GEO (Gephyrocapsa oceanica) and SPC (Emiliania huxleyi and small Gephyrocapsa spp.) groups from sediment core MD05-2904 in the northern South China Sea (SCS) over the past 200 kyr. A calcification index (CI) based on the coccolith weight and length is applied to evaluate the changes in coccolithophore calcification. The two groups of coccolith weights / CIs show different patterns on long term variations and during the last two terminations. We compare the coccolith weight and CI records with the environmental variables and carbonate chemistry parameters calculated in the same core. Our data reveals that sea surface temperature and insolation have weak correlations to coccolith weight and CI on long-term variations. The SPC weight / CI are correlated with the seawater pH and pCO₂ variations while the GEO weight/ CI are more related to the nutrient variations. This implies a more significant role of ocean carbonate chemistry in the calcification of less calcified coccolithophores and nutrient concentration in the heavier calcifying coccolithophores.

View all citing articles on Scopus

View full text

Article preview

Earth and Planetary Science Letters

Abstract

Introduction

Section snippets

Materials and methods

Results

Discussion

Conclusions

Acknowledgements

References (22)

Morphology and biogeography of Gephyrocapsa coccoliths in Holocene sediments

Mar. Micropaleont.

Morphological variation of Emiliania huxleyi and sea surface salinity

Earth Planet. Sci. Lett.

Techniques for quantitative analyses of calcareous marine phytoplankton

Mar. Micropaleont.

New oceanic proxies for paleoclimate

Earth Planet. Sci. Lett.

Paleosalinity: confidence limits and future applications

Mar. Geol.

Hydrogen isotopic compositions of long-chain alkenones record freshwater flooding of the Eastern Mediterranean at the onset of sapropel deposition

Earth Planet. Sci. Lett.

Molecular isotopic and dinoflagellate evidence for Late Holocene freshening of the Black Sea

Earth Planet. Sci. Lett.

Genotypic variation in the coccolithophorid species Emiliania huxleyi

Mar. Micropaleontol.

Genetic variability and spatial patterns of genetic differentiation in the reproductive rates of the marine coccolithophores Emiliania huxleyi and Gephyrocapsa oceanica

Limnol. Oceanogr.

Changes in calcification and the dimensions of coccoliths of Emiliania huxleyi (Haptophyta) grown at reduced salinities

Phycologia

How islands stir and fertilize the upper ocean

Geophys. Res. Lett.

Cited by (39)

Globally enhanced calcification across the coccolithophore Gephyrocapsa complex during the mid-Brunhes interval

New insights into the Barremian–lower Aptian calcareous nannofossils of the Mediterranean Tethys: Chronostratigraphic and paleobiogeographic implications

Coccolith size rules – What controls the size of coccoliths during coccolithogenesis?

Emiliania huxleyi biometry and calcification response to the Indian sector of the Southern Ocean environmental gradients

Interannual changes of austral summer coccolithophore assemblages and southward expanse in the Southern Indian Ocean

Late Quaternary coccolith weight variations in the northern South China Sea and their environmental controls