Abstract
Coccolithophores are unique primary producers in the ocean with the ability to calcify. They are known to produce calcareous scales, which form the significant part of calcite oozes or chalk deposits on the seafloor. Coccolithophores are very noteworthy and they are explored to a great extent as nannofossils to reconstruct the past climate. Calcite plates in coccolithophores make them a vital tool in global climate change studies specifically with ocean acidification. These microscopic plants are the major contributor of the carbonate rain that controls the inorganic carbon pump in the ocean, which in turn influences both carbon and carbonate cycles. The emergence of advanced techniques enables us to study the biological aspects of this pelagic calcifier with improved precision. But still, they are understudied world over compared to any other phytoplankton groups. The northern Indian Ocean, being landlocked in three sides and vulnerable to climate change and ocean acidification, severely lacks focused studies on coccolithophores, though the US JGOFS in the 1990s have outlined the ecological significance of coccolithophores in the Arabian Sea. This paper reviews and outlines our understanding of coccolithophores as well as the nix in the northern Indian Ocean.
Similar content being viewed by others
Introduction
Coccolithophores or coccolithophorids, commonly known as golden-brown algae, are members of the group Haptophyceae belonging to the class Prymnesiophyceae or Coccolithophyceae (Tyrrell and Young 2009). Coccolithophores are almost exclusively marine with only one freshwater species—Hymenomonas roseola. They generate extensive blooms (milky sea) identified with bright patches of water or turquoise coloured water masses in certain parts of the ocean (https://visibleearth.nasa.gov/images/71344/coccolithophore-bloom-off-brittany-france). These blooms may even extend over 2,000,000 km2 (Tyrrell and Merico 2004). This group of unicellular eukaryotic phytoplankton is characterised by the presence of calcite plates or scales known as coccoliths which cover their cells as an exoskeleton (Young and Henriksen 2003; Siesser and Winter 1994) This exoskeleton around the coccolithophores is called coccospheres. These calcite plates are very important nannofossils, and they are the major components of calcareous oozes, otherwise known as chalk deposits found on the sedimentary bed, which is a major source of mineral calcite in the ocean. Most of these chalk deposits dates back to the cretaceous period suggesting the presence of these organisms from the cretaceous period onwards (Bown et al. 2004).
Coccolithophores are responsible for the 1.5 million tons of calcite produced every year. They are the only known calcifying marine phytoplankton to date, and this character makes them part of the essential global biogeochemical cycles, which are always affected by the changing climate situation. Coccolithophores are part of the organic carbon pump as they are phytoplankton and their photosynthesis fixes CO2 from the atmosphere; also, they are a part of the carbonate counter pump as they can produce calcium carbonate scales (Baumann et al. 2005; Beaufort et al. 2008). Calcification is a process that generates CO2 as a byproduct. The calcification requires the uptake of dissolved inorganic carbon (HCO3-) and calcium ions (Ca2+) and gives out CaCO3, CO2 and water. As coccolithophores are phytoplankton, the carbon dioxide from calcium carbonate production can be used during their photosynthesis, except when there is a high concentration of CO2 within the cell. Even at risk from the change in global climate, they emerged to be successful enough not only from getting extinct but also to adapt to become extant organisms and the major producer of calcite in the open seas (Hay 2004).
Even though the primary role of coccolithophore is as a primary producer, they could also assimilate the organic carbon from the surroundings as well (de Vargas et al. 2007; Marsh 2003). In addition to these, coccolithophores produce calcareous liths which have an add-on effect on marine biogeochemistry in carbon as well as in the carbonate cycle, making themselves a part of more than one biogeochemical cycle. It is because of this reason that they have gained immense attention and resulted in many advanced studies using them as biogeochemical agents and palaeontological proxies (Baumann et al. 2005; Rost and Riebesell 2004). As the palaeontological and biostratigraphic studies progressed, the knowledge of fundamental biological aspects of coccolithophores was lacking. It became necessary to fill this void to provide answers as well as to advance in those studies. With the increase in concern about global climate change, there was substantial progress in the necessary biological studies.
Phytoplankton are usually found abundant around high latitudes, around the upwelling zones along the equator and ubiquitously near coasts (Geisen et al. 2004; Jordan and Chamberlain 1997). Studies show that coccolithophores are found to prefer placid, nutrient-poor waters with moderate temperatures (Young et al. 2009). This does not negate the fact that they are also found in cold nutrient carrying upwelled waters. Coccolithophores can thrive very successfully in those areas where other phytoplankton starves to survive (Young et al. 2009). As a result, it is considered as non-competitor to other phytoplankton. They make up even 90% of the phytoplankton biomass in those regions with phytoplankton non-friendly environment (Geisen et al. 2004). Calcification is a high-energy demanding process for marine organisms. Even though the presence of calcite plates may have some benefits such as reduce grazing pressure, avoid photodamage; the energy requirement for calcification is very high as for a marine nanophytoplankton (Westbroek et al. 1983). Other suggested benefit from coccoliths includes viral or bacterial resistance (Tyrrell and Young 2009; Anning et al. 1996; Taylor et al. 2017; Young 1994). These advantages that coccolithophores have over other phytoplankton may have caused their increased diversity and broad-spectrum ecology (Monteiro et al. 2016). The difference of shape, size, crystallography, number and the arrangement of coccoliths in each species points to highly diverse coccoliths which provide a robust and reliable means for classification and taxonomy identification of these minute organisms (Young et al. 2009). This is very important because the basic body plan of every coccolithophore is the same with the only difference during alternate phases of their life cycle or for some species, in the different organelles within.
Morphology
Coccolithophores have a spherical shape which includes the cell protoplasm covered with numerous coccoliths to form an exoskeleton known as coccospheres (Fig. 1). The size of typical coccolithophorids varies from 5 to 100 μm and coccoliths from 2 to 25 μm (Tyrrell and Young 2009; Moheimani et al. 2012). Coccoliths are essentially mineralised scales formed outside the cell wall of coccolithophores (de Vargas et al. 2007; Moheimani et al. 2012). Coccoliths are made up of calcium carbonate with calcite as the mineral. The number of liths is found to be at least 30 around a cell (Yang and Wei 2003). The presence of coccoliths is the unique characteristic of this organism, and it is indeed cryptic. Coccoliths are unique in each species; thus, they are used for essential taxonomic identification of the organism. One of the remarkable features is the presence of two types of plates during different phases of generation. They show alteration of generation between haploid and diploid phases. Coccolithophores in haploid phase usually have holococcoliths made up of thousands of minute rhombic calcite crystals; these crystals are found to form partially outside the cell, while those in diploid phase have heterococcoliths made up of few hundreds of calcite plates and they vary in shape (Young and Henriksen 2003). The shape and structure of the coccospheres vary with species. Some larger coccolithophorids have highly modified coccospheres made up of specialised coccoliths (Young et al. 2009). Another type of liths present is nannoliths found in fossils (Young et al. 2009; Geisen et al. 2003). The presence of alternation of generation solved a lot of questions such as the presence of two types of coccoliths in a single coccolithophore, occurrence of mixed coccospheres, etc., even though this bought up even more puzzles after that. At least, for now, the presence of alternation of generation, usually with two or more morphologically distinct phases, is identified only in cultures, but it is expected as a natural character of the group (Cros et al. 2000).
Haptophytes are characterised by the presence of haptonema, which helps them for phagotrophy when necessary (Inouye and Kawachi 1994). In coccolithophores, a single-coiled haptonema is found which coils and uncoils according to environmental cues (Inouye and Kawachi 1994; Billard and Inouye 2004; Paasche 1968). There are two types of scales covering the cell surface of coccolithophores: mineralised and unmineralised scales (Inouye and Kawachi 1994). Coccoliths form the mineralised scales having calcite as the mineral for biomineralisation and occur in several different shapes (Billard and Inouye 2004). Unmineralised scales are also found in different shapes. Scales also vary with the ploidy of the cell. Flagellum not less than two numbers is found in coccolithophores, which help them to drift. Even though there is flagellum in both haploid and diploid cells, only haploid cells are found to be motile (Inouye and Kawachi 1994; Billard and Inouye 2004). The cells in the diploid phase depend much on ocean currents and ocean circulation patterns (de Vargas et al. 2007). The columnar deposits hold the scales to the cell wall in some of the species.
Structure
The coccolithophores cell structure is still not entirely known, even with all the recent discoveries (Inouye and Kawachi 1994; Billard and Inouye 2004). The spherical cell of coccospherales is covered with coccoliths which make up the coccospheres (Fig. 1). Coccoliths are formed in coccolith-forming vesicles, which are derived from Golgi bodies (Young and Henriksen 2003). The formation of coccoliths within the cell of a coccolithophore by using dissolved inorganic carbon and calcium is called coccolithogenesis (Moheimani et al. 2012). The coccoliths produced within the coccolith-forming vesicles are then expelled through the cell wall to become the part of coccospheres. Coccospheres will have the older coccoliths towards the outer side (Young and Henriksen 2003). Coccolithogenesis mechanisms vary with the type of coccolith produced and with the coccolith-forming vesicle (Billard and Inouye 2004). They have two brown coloured chloroplasts on both sides of the cell covering the nucleus, mitochondria and all other organelles. Chloroplasts encapsulate the pyrenoids that differ in their shape and composition with different species (Billard and Inouye 2004; Thierstein and Young 2013). The two flagella arise from the basal bodies situated in the endoplasmic reticulum. Flagellum not only helps in the motility but also plays an essential role during mitosis. It also assists in the formation of the cytoskeleton (Billard and Inouye 2004).
Reproduction
Coccolithophores show every protistan method of reproduction. Apart from that coccolithophores also show alternation of generations, the reproductive mechanisms that they use to jump in between these alternate life cycles are of prior interests. The study on reproductive techniques in coccolithophores becomes complicated as they show complex heteromorphic life cycles (Hori and Green 1994; Houdan et al. 2006). Coccolithophores reproduce either sexually or asexually. Binary fission is one of the common asexual reproduction methods used among them. Here in binary fission, a cell will divide into two daughter cells (Hori and Green 1994). During this process, most of the coccoliths around parent shed off, and one of the daughter cells keeps the rest. The newly formed cells with little or no coccoliths around it will start the process of coccolithogenesis immediately, thus producing its coccoliths. Coccolithophores in the diploid phase alter to haploid life by meiosis and haploid to diploid phase’s syngamy (Young and Henriksen 2003; Hori and Green 1994).
Diversity and biogeography
Coccolithophores show high diversity, even though their abundance is usually low compared to other phytoplankton groups, such as diatom and dinoflagellates (Bown et al. 2004; Jordan and Chamberlain 1997; O’Brien et al. 2016; Young 2003; Edvardsen et al. 2016). There are over 200 reported species, though only a few are dominant across the world (Fig. 2). With the broad spectrum of ecological characters, they can inhabit in almost all kinds of hydrographical settings in the ocean. The highly productive eutrophic environment such as temperate and subpolar oceans shows a very diverse and rich presence of coccolithophorids (Geisen et al. 2004; Jordan and Chamberlain 1997; Charalampopoulou 2011). The permanently oligotrophic waters such as subtropic gyres also do support these minute calcifiers. It is this broad-spectrum ecology that coccolithophorids have made them ubiquitous.
As mentioned before, coccolithophores are found everywhere in the world ocean although their distribution varies with the nature of the ecosystems. Spatial distribution varies with different temporal zones and is identified based on the blooms detected year after year from all over the florid world zones. According to that, there are four coccolithophorid floral zones: subarctic and temperate, subtropical, tropical and sub-Antarctic (McIntyre and Bé 1967; Geitzenauer et al. 1977; Winter and Siesser 1994). This is in contrary to the fact that the distribution pattern of coccolithophores is entirely not known primarily in the Indian Ocean and some regions of Pacific and Atlantic (Kinkel et al. 2000). This is mainly due to the lack of studies from these regions. The vertical diversity varies with the presence of stratified layers. This haptophyte with a relatively large diversity is said to have only a few dominant species all over the world. This information may be biased because major tropical ocean systems are not at all explored to the least minimum required. Even when tried to explore, the practical difficulties faced during the primary step of sample collection as well as the collection practises may impede at least some of attempts from being addressed.
Extant coccolithophores prefer stratified oligotrophic waters. The temporal zones in subtropics with temperate climate have high diversity than other zones (Jordan and Chamberlain 1997). The biogeography of all organisms shows the presence of a similar but opposing counterpart in the opposite hemispheres (Baumann et al. 2005). This can be the case of coccolithophore assemblages too. Emiliania huxleyi, which is said to be the most abundant coccolithophorid in most of the studies, should be subjected to validation with data from tropical ocean studies. It is the most studied coccolithophore species and also the type species of the group (Bown et al. 2004). Emiliania huxleyi dominates in the high-nutrient, high-latitude, low-temperature regions (Charalampopoulou 2011; McIntyre and Bé 1967; Okada and Honjo 1975; Boeckel and Baumann 2008). And these regions being the most explored for coccolithophores, it is not unusual that Emiliania is considered a type species and also the dominant, abundant species among coccolithophores than other much older species.
The information of coccolithophores on cell physiology, microbial interactions, metabolism, biomineralisation, genetics and ecology are mainly from studies on Emiliania, to be specific, from the culture studies of Emiliania. It is also known that coccolithophores are a group of organisms with relatively high diversity than their abundance (Bown et al. 2004; Thierstein and Young 2013; O’Brien et al. 2016; Young et al. 2003). This high diversity does not only come with the morphology of the coccoliths but also with every aspect concerning to this organism physiological diversity and genetic diversity on top of ecological diversity (Thierstein and Young 2013; Young et al. 2003; Iglesias-Rodriguez et al. 2006). Thus, it is essential to expand the study subject primarily when we come to the northern Indian Ocean so that we can understand more of valid reasons behind the questions we pose, because coccolithophore diversity is found to be highest when it comes to low-nutrient, low-latitude, optimum-temperature ecosystems (Charalampopoulou 2011; McIntyre and Bé 1967; Boeckel and Baumann 2008; Okada and Honjo 1973a, 1973b) which matches with the conditions in many areas of the northern Indian Ocean.
Environmental relevance
Coccolithophores are considered as the third most crucial primary producer globally (Rost and Riebesell 2004). Their ecological role and its influence on flora and fauna are important aspects to be studied in the context of the ecosystem functioning. Subtropics and temperate oceans show a great abundance of coccolithophores along with diatoms and dinoflagellates (Geisen et al. 2004; Jordan and Chamberlain 1997; Young et al. 2009; Kinkel et al. 2000; Okada and Honjo 1975). Fast turnover rates, along with high abundance, are a crucial factor for the productivity of any primary producer. This organism is said to contribute 1–10% of the total primary production in subpolar, temperate and subtropical oceans. This account may even rise to 40% during bloom conditions (Brown and Yoder 1994; Fernandez et al. 1993; Hopkins et al. 2015). All these facts suggest that coccolithophores are the most productive marine pelagic calcifiers but with no exact records of their contribution. Even then, their contribution to the primary productivity of tropical as well as most of the subtropical ocean is yet to be recorded (Rost and Riebesell 2004). When compared to any mineralising plankton or even among the calcifying planktons, the turnover rate in coccolithophores is very high. This is because they have a high reproduction rate with a short life span. During this small life span, they will help to sink a massive amount of CO2 which will be stored in sediments, thus removing considerable part of CO2 from the atmosphere (de Vargas et al. 2007; Marsh 2003).
Coccolithophores are found to play a unique role in the global carbon cycle (Fig. 3). They are known for their influence on organic carbon cycle as well as on carbonate pump. And it is the combined effect of these processes that make them preferred the most to study the global carbon cycle (Baumann et al. 2005). Albeit coccolithophores account for most of the calcite production on earth, the mechanism/s involving in their cellular calcification demands are very poorly understood so far (Beaufort et al. 2008; Müller 2019). Only when we have this prior knowledge, we can estimate the response of calcification to the increasing carbon dioxide levels in the future atmosphere. Even then, the data related to the contribution of this calcifying plankton is the least among all other calcifying organisms (Milliman 1993).
Most of the CO2 produced from anthropogenic activities will enter the marine system as dissolved CO2 due to mixing air-sea exchange. Carbon dioxide in the system drives the biological pump. The dissolution of CO2 in water results in the formation of carbonic acid (H2CO3), which, in turn, increases the concentration of bicarbonate (HCO3-) as well as carbonate ions (CO32-). Increase in CO2 can change the ocean pH, thus altering plankton composition, which will, in turn, affect the food web. Fundamentally, the increase in CO2 level influences the calcification process in coccolithophorids. There is no concrete answer to this problem on how the rise in CO2 will affect this calcifying phytoplankton. Ocean acidification studies have contradictory results showing a negative as well as a positive impact on coccolithophores. A decrease in calcification can create a high impact on carbonate counter pump as the CaCO3 flux that removes excess carbon from the system get reduced (Rost and Riebesell 2004). The increase in CO2 is also found to affect the species diversity, distribution and abundance as a result of acidification.
Coccolithophores are used to study and understand the effects due to global climate change (Rost and Riebesell 2004; Beaufort et al. 2011; Irie et al. 2010). They are inevitably affected by climate change, and different studies have helped us to know the magnitude of the impact. Gitau 2015 has recently shown that the rise in carbon dioxide has increased coccolithophore population, considering that most of the living beings been negatively affected. This can be overcome only with the understanding of cellular calcification mechanism that each coccolithophore species use. Therefore, the most effective way to understand this subject would be to use molecular techniques to investigate on different species of coccolithophores at diverse ecosystems around the world rather than focusing on the single species of Emiliania.
The change in global climate will unquestionably cause impacts on coccolithophores in the same way it would affect any other organisms on this planet. The rise in surface temperature due to global warming and the decrease in pH due to ocean acidification are not the only climate change-induced factors. The amount of available light, ocean currents, etc. are some other prime factors that control the distribution of these organisms (Luan et al. 2013; Baumann and Boeckel 2013). With significant climate change, the amount of light entering the atmosphere will fluctuate. This will certainly affect coccolithophores who prefer optimum light for survival. Another interesting fact is that the liths from coccospheres can backscatter light, thus increasing the albedo effect (Tyrrell and Young 2009; Charlson et al. 1987; Gordon 2006; Gordon et al. 2009; Balch et al. 2001; Balch and Utgoff 2009), but rise in temperature, as a result, is not confirmed (Marsh 2003; Balch 2018). Coccolithophores are found to produce more dimethyl sulphide (Andreae and Raemdonck 1983; Franklin et al. 2009; Franklin et al. 2010; Malin and Krist 1997; Malin and Steinke 2004), which act as the nuclei for cloud condensation, thus increasing the solar radiation reflecting capacity of earth’s atmosphere.
Use of tracers or indicators is done in all the fields of science as it is the easiest way to keep track of several processes that may otherwise remain abstruse. Coccolithophores are such an indicator widely used to track ocean water masses, surface water temperature, palaeoproductivity, palaeosalinity and such past environmental changes (Baumann et al. 2005; Baumann et al. 1999; Silva et al. 2013; Mertens et al. 2009). Earlier coccolithophores were the least used planktonic components for palaeoecological reconstruction. But the discovery of certain key variations among some of the extant species/groups of coccolithophores made them an efficient tool for palaeoceanographic studies (Baumann et al. 2005; Geisen et al. 2004). Gephyrocapsa oceanica is one of the widely used coccolithophorids as a tracer. The reconstruction of the past productivity for the last 140,000 years in the equatorial Atlantic Ocean used G. oceanica along with the deep-dwelling species Florispheara profunda (Baumann et al. 2005). Some of the coccolithophores show an intense calcification, in turn, getting preserved so well in sediments (Calcidiscus leptoporous). This preservation potential makes them even more desirable in palaeoecology reconstruction processes.
Records from the Indian Ocean
The ecology of coccolithophorids from the Indian Ocean is mostly unknown due to the lack of studies (Table 1, Figs. 4 and 5). And the presence of this haptophyte is confirmed only in specific locations of the Arabian Sea and the Bay of Bengal having contrasting hydrography governed by diverse ocean processes. Krey 1973 identified 8 plankton-geographical regions in the Indian Ocean, of which 5 of them show either primary or secondary dominance of coccolithophores (Table 2). Central Arabian Sea and Bay of Bengal are some of the plankton-geographical regions that have secondary dominance of coccolithophores (Krey 1973). Northern Arabian Sea has records on coccolithophores from sediment trap studies as well as on ecological tolerances of coccolith and carbonate fluxes of extant coccolithophores. The northeastern Arabian Sea covered under several studies was maximum of Pakistan coast (Andruleit et al. 2000; Andruleit et al. 2003; Andruleit et al. 2005; Mergulhao et al. 2006). The studies from the northern Indian Ocean have reported the presence of over 25 species of coccolithophores from their collection periods either as coccospheres or detached coccoliths (Andruleit et al. 2003; Mergulhao et al. 2006, 2013; Stoll et al. 2007; Balch et al. 2000). The ecological aspects such as their contribution to the overall productivity of the region, the importance of calcite rain in maintaining the carbon chemistry of the oceans, coccolithophore as a primary producer and its contribution to the productivity as a primary trophic organism and influence on particulate inorganic carbon are not fully known (Rost and Riebesell 2004).
Frequently attempted studies using coccolithophores are climatological ones where they are either used as tracers or studied to see the effect of ocean acidification. There are no related studies from the Indian Ocean even on these most addressed topics. Samples taken using sediment traps collect the marine snow that is settling to the bottom of the ocean. As a result, these studies will confirm the presence of coccolithophores but does not account the organisms during the collection period. Rogolla and Andruleit et al. (2005) have established the existence of coccolithophore assemblages during the last 200,000 years and also attempted to map the effects of monsoon on these organisms. Southwest and northeast monsoons being the prime signature of Arabian Sea, there are attempts to map the distribution of coccolithophores during monsoon (Balch et al. 2000; Schiebel et al. 2004), with the presence of living coccolithophores confirmed at various locations over northern Indian Ocean (Andruleit et al. 2003; Schiebel et al. 2004; Guptha et al. 1995; Guptha et al. 2005; Liu et al. 2018).
Recent observations
Coccolithophore study methods pose numerous difficulties even from the sampling stage, forcing researchers to omit this only calcifying marine phytoplankton. The sampling of live coccolithophores is just one of those difficulties but also the most important for any kind of biological studies. Our recent studies have helped us to confirm their presence in the Indian waters in the Arabian Sea (Fig. 6).
Why so crucial to the Indian Ocean
The northern Indian Ocean, including the regional seas of Arabian Sea and Bay of Bengal, is hydrographically very unique. The northern Indian Ocean as a whole is landlocked in the northeast and west and very much vulnerable to ocean warming and associated ecosystem change. The poor ventilation of the ocean mid-depth waters makes it to host the world’s largest Oxygen Minimum Zone (Naqvi 2020). The Arabian Sea and the Bay of Bengal are a part of the monsoon gyre of the Asian monsoon system (Wyrtki 1973). Both these seas have many differences like the Bay of Bengal getting a lot of fluvial inputs (Milliman and Meade 1983), whereas Arabian Sea has few major river outlets that drain into it. There are several critical hydrographic features and seasonal changes, which will, in turn, be coupled with the oceanographic processes and create two extremely different ecosystems. Even with all these unique features, interestingly, this calcifying marine phytoplankton is not accounted when it comes to the northern Indian Ocean. This need to be perceived with the need to map climate change and in such scenario coccolithophores can be used as indicators and tracers for past as well as the ongoing climate change (Malin and Krist 1997).
Summary
There are a lot of developments in the studies that provide us with more and more knowledge on coccolithophores which in turn have improved our understanding of this organism as well as the ecological role it plays. Much of this understanding is not benefitted when it comes to some areas of the world ocean to be particular the major part of the Indian Ocean. The Bay of Bengal and the Arabian Sea are two large ocean basins which are explored to the minimum to this particular organism. Global climate change and its associated impacts being the prime focus of most of the research work going on today, coccolithophores have gained immense recognition as they can be used as tracers for these changes. Coccolithophores have these calcite plates around them, which makes them vulnerable to increasing pH in the ocean. The increase in carbon in the system will also influence them as they have a significant role in the carbon sink. The northern Indian Ocean is also vulnerable to this changing climate scenario, and coccolithophores are the vital organisms that can help us map these changes. Coccolithophores are considered to have crucial ecological roles across the world, whereas, in the Indian Ocean, their environmental importance is still unmapped.
References
Andreae, M. O., & Raemdonck, H. (1983). Dimethyl sulfide in the surface ocean and the marine atmosphere: a global view. Science, 221(4612), 744–747.
Andruleit, H. A., & Rogalla, U. (2002). Coccolithophores in surface sediments of the Arabian Sea in relation to environmental gradients in surface waters. Marine Geology, 186, 505–526.
Andruleit, H., Rad, U. V., Bruns, A., & Ittekkot, V. (2000). Coccolithophore fluxes from sediment traps in the northeastern Arabian Sea off Pakistan. Marine Micropaleontology, 38, 285–308.
Andruleit, H., Stäger, S., Rogalla, U., & Cepek, P. (2003). Living coccolithophores in the northern Arabian Sea: ecological tolerances and environmental control. Marine Micropaleontology, 49, 157–181.
Andruleit, H., Rogalla, U., & Staeger, S. (2005). Living coccolithophores recorded during the onset of upwelling conditions off Oman in the western Arabian Sea. Journal of Nannoplankton Research, 27(1), 1–14.
Anning, T., Nimer, N., Merrett, M. J., & Brownlee, C. (1996). Costs and benefits of calcification in coccolithophorids. Journal of Marine Systems, 9, 45–56.
Balch, W. M. (2018). The ecology, biogeochemistry, and optical properties of coccolithophores. Annual Review of Marine Science, 10, 71–98.
Balch, W. M., & Utgoff, W. M. (2009). Potential interactions among ocean acidification, coccolithophores, and the optical properties of seawater. Oceanography., 22(4), 146–159.
Balch, W. M., Drapeau, D. T., & Fritz, J. J. (2000). Monsoonal forcing of calcification in the Arabian Sea. Deep Sea Res. Part II Top. Stud. Oceanogr., 47(7-8), 1301–1337.
Balch, W. M., Drapeau, D. T., Fritz, J. J., Bowler, B. C., & Nolan, J. (2001). Optical backscattering in the Arabian Sea--continuous underway measurements of particulate inorganic and organic carbon. Deep Sea Res. Part I Oceanogr Res. Pap., 48(11), 2423–2452.
Baumann, K. H., & Boeckel, B. (2013). Spatial distribution of living coccolithophores in the southwestern Gulf of Mexico. Journal of Micropalaeontology, 32(2), 123–133.
Baumann, K. -H., Cepek, M. and Kinkel, H., (1999) Coccolithophores as indicators of ocean water masses, surface water temperature, and paleoproductivity, In Proxies in paleoceanography, (eds Fischer, G. and Wefer, G.), 117-144.
Baumann, K. H., Andruleit, H., Böckel, B., Geisen, M., & Kinkel, H. (2005). The significance of extant coccolithophores as indicators of ocean water masses, surface water temperature, and paleoproductivity: a review. Palaeontologische Zeitschrift, 79(1), 93–112.
Beaufort, L., Couapel, M., Buchet, N., Claustre, H., & Goyet, C. (2008). Calcite production by coccolithophores in the south east Pacific Ocean. Biogeosciences, 5(4), 1101–1117.
Beaufort, L., Probert, I., de Garidel-Thoron, T., Bendif, E. M., Ruiz-Pino, D., Metzl, N., & Rost, B. (2011). Sensitivity of coccolithophores to carbonate chemistry and ocean acidification. Nature, 476(7358), 80–83.
Billard, C. and Inouye, I., (2004) What’s new in coccolithophore biology? In Coccolithophores - From molecular processes to global impact. Springer, (eds Thierstein, H. R. and Young, J. R.) , 1-30.
Boeckel, B., & Baumann, K. H. (2008). Vertical and lateral variations in coccolithophore community structure across the subtropical frontal zone in the South Atlantic Ocean. Marine Micropaleontology, 67(3-4), 255–273.
Bown, P. R., Lees, J. A. and Young, J. R., (2004) Calcareous nannoplankton evolution and diversity through time. In Coccolithophores - From molecular processes to global impact. Springer (eds Thierstein, H. R. and Young, J. R.), 481-508.
Broerse, A. T. C., Brummer, G. J. A., & van Hinte, J. E. (2000). Coccolithophore export production in response to monsoonal upwelling of Somalia (northwestern Indian Ocean). Deep Sea Research Part II: Topical Studies in Oceanography, 47, 2179–2205.
Brown, C. W., & Yoder, J. A. (1994). Coccolithophorid Blooms in the Global Ocean. Journal of Geophysical Research, Oceans, 99(C4), 7467–7482.
Charalampopoulou, A., (2011) Coccolithophores in high latitude and Polar Regions: Relationships between community composition, calcification and environmental factors. PhD thesis, Southampton University, 1-300.
Charlson, R. J., Lovelock, J. E., Andreae, M. O., & Warren, S. G. (1987). Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature, 326, 655–661.
Cros, L., Kleijne, A., Zeltner, A., Billard, C., & Young, J. R. (2000). New examples of holococcolith-heterococcolith combination coccospheres and their implications for coccolithophorid biology. Marine Micropaleontology, 39(1-4), 1–34.
de Vargas, C., Aubry, M. -P., Probert, I. and Young, J. R., (2007) Origin and evolution of coccolithophores: from coastal hunters to oceanic farmers. In Evolution of Primary Producers in the Sea. Elsevier, (eds Falkowski, P. G. and Knoll, A. H.), 251-285.
Edvardsen, B., Egge, E. S., & Vaulot, D. (2016). Diversity and distribution of haptophytes revealed by environmental sequencing and metabarcoding–a review. Perspectives in Phycology, 3, 77–91.
Fernandez, E., Boyd, P., Holligan, P. M., & Harbour, D. S. (1993). Production of organic and inorganic carbon within a mesoscale coccolithophore bloom in the north-east Atlantic. Marine Ecology Progress Series, 97, 271–285.
Franklin, D. J., Poulton, A. J., Steinke, M., Young, J. R., Peeken, I., & Malin, G. (2009). Dimethylsulphide, DMSP-lyase activity and microplankton community structure inside and outside of the Mauritanian upwelling. Progress in Oceanography, 83(1-4), 134–142.
Franklin, D. J., Steinke, M., Young, J. R., Probert, I., & Malin, G. (2010). Dimethylsulphoniopropionate (DMSP), DMSP-lyase activities (DLAs) and dimethylsulphide (DMS) in 10 species of coccolithophore. Marine Ecology Progress Series, 410(1), 13–23.
Geisen, M., Hamm, C., & Young, J. R. (2003). Material properties and functional morphology of coccoliths - Testing old hypotheses. Gaia, 11, 56.
Geisen, M., Young, J. R., Probert, I., Sáez, A. G., Baumann, K. H., Sprengel, C. and Medlin, L. K., (2004) Species level variation in coccolithophores. In Coccolithophores, Springer (eds Rost, B. and U. Riebesell), 327-366.
Geitzenauer, K. R., Roche, M. B. and McIntyre, A., (1977) Coccolith biogeography from North Atlantic and Pacific surface sediments. In Oceanic Micropaleontology (ed Ramsay, A. T. S.), 973-1008.
Gitau, B. (2015). What’s fueling the rise of coccolithophores in the oceans?. An article in www.csmonitor.com (The Christian Science Monitor ). Accessed 28 Nov 2015.
Gordon, H. R. (2006). Backscattering of light from disklike particles: is fine-scale structure or gross morphology more important? Applied Optics, 45(27), 1–8.
Gordon, H. R., Smyth, T. J., Balch, W. M., Boynton, G. C., & Tarran, G. A. (2009). Light scattering by coccoliths detached from Emiliania huxleyi. Applied Optics, 48(31), 6059–6073.
Guptha, M. V. S., Mohan, R., & Muralinath, A. S. (1995). Living coccolithophorids from the Arabian Sea. Rivista Italiana di Paleontologia e Stratigrafia, 100(4), 551–574.
Guptha, M. V. S., Mergulhao, L. P., Murty, V. S. N., & Shenoy, D. M. (2005). Living coccolithophores during the northeast monsoon from the Equatorial Indian Ocean: Implications on hydrography. Deep Sea Research Part II: Topical Studies in Oceanography, 52, 2048–2062.
Hay, W. W., (2004) Carbonate fluxes and calcareous nannoplankton. In Coccolithophores - From molecular processes to global impact. Springer, (eds Thierstein, H. R. and Young, J. R.), 509-528.
Hopkins, J., Henson, S. A., Painter, S. C., Tyrrell, T., & Poulton, A. J. (2015). Phenological characteristics of global coccolithophore blooms. Global Biogeochemical Cycles, 29(2), 239–253.
Hori, T. and Green, J. C., (1994) Mitosis and cell division. In The Haptophyte Algae. Systematics Association Special Volume, (eds Green, J. C. and Leadbeater, B. S. C.), 51(51), 47-71.
Houdan, A., Probert, I., Zatylny, C., Véron, B., & Billard, C. (2006). Ecology of oceanic coccolithophores. I. Nutritional preferences of the two stages in the life cycle of Coccolithus braarudii and Calcidiscus leptoporus. Aquatic Microbial Ecology, 44(3), 291–301.
Iglesias-Rodriguez, M. D., Schofield, O. M., Batley, J., Medlin, L. K., & Hayes, P. K. (2006). Intraspecific genetic diversity in the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae): the use of microsatellite analysis in marine phytoplankton population studies. Journal of Phycology, 42(3), 526–536.
Inouye, I. and Kawachi, M., (1994) The haptonema, In The Haptophyte Algae. Systematics Association Special Volume, (eds Green, J. C. and Leadbeater, B. S. C.), 73-89.
Irie, T., Bessho, K., Findlay, H. S., & Calosi, P. (2010). Increasing costs due to ocean acidification drives phytoplankton to be more heavily calcified: optimal growth strategy of coccolithophores. PLoS One, 5(10), e13436.
Jordan, R. W., & Chamberlain, A. H. L. (1997). Biodiversity among haptophyte algae. Biodiversity and Conservation, 6, 131–152.
Kinkel, H., Baumann, K. H., & Cepek, M. (2000). Coccolithophores in the equatorial Atlantic Ocean: response to seasonal and Late Quaternary surface water variability. Marine Micropaleontology, 39(1-4), 87–112.
Krey, J. (1973). Primary production in the Indian Ocean I. In The biology of the Indian Ocean (pp. 115-126). Springer, Berlin, Heidelberg.
Liu, H., Sun, J., Wang, D., Zhang, X., Zhang, C., Song, S., & Thangaraj, S. (2018). Distribution of living coccolithophores in eastern Indian Ocean during spring intermonsoon. Scientific Reports, 8(1), 1–12.
Luan, Q., Sun, J., Niu, M., & Wang, J. (2013). Warm currents affecting the spring and winter distributions of living coccolithophores in the Yellow Sea, China, Oceanol. Hydrobiol. Stud., 42(4), 431–441.
Malin, G., & Krist, G. O. (1997). Algal production of dimethyl sulfide and its atmospheric role. Journal of Phycology, 33(6), 889–896.
Malin, G. and Steinke, M., (2004) Dimethyl sulphide production: what is the contribution of the coccolithophores? In Coccolithophores - From molecular processes to global impact, Springer, (eds Thierstein, H. R. and Young, J. R.), 127-164.
Marsh, M. E. (2003). Regulation of CaCO3 formation in coccolithophores. Comparative Biochemistry and Physiology. B, 136(4), 743–754.
McIntyre, A., & Bé, A. W. (1967). Modern coccolithophoridae of the Atlantic Ocean—I. Placoliths and cyrtoliths. In Deep Sea Research and Oceanographic Abstracts, 14(5), 561–597.
Mergulhao, L. P., Mohan, R., Murty, V. S. N., Guptha, M. V. S., & Sinha, D. K. (2006). Coccolithophores from the central Arabian Sea: sediment trap results. Journal of Earth System Science, 115(4), 415–428.
Mergulhao, L. P., Guptha, M. V. S., Unger, D., & Murty, V. S. N. (2013). Seasonality and variability of coccolithophore fluxes in response to diverse oceanographic regimes in the Bay of Bengal: sediment trap results. Palaeogeography Palaeoclimatology Palaeoecology, 371, 119–135.
Mertens, K. N., Lynn, M., Aycard, M., Lin, H. L., & Louwye, S. (2009). Coccolithophores as palaeoecological indicators for shifts of the ITCZ in the Cariaco Basin during the late Quaternary. Journal of Quaternary Science, 24(2), 159–174.
Milliman, J. D. (1993). Production and accumulation of calcium carbonate in the ocean: budget of a nonsteady state. Global Biogeochem Cycles, 7(4), 927–957.
Milliman, J. D., & Meade, R. H. (1983). World-wide delivery of river sediment to the oceans. Journal of Geology, 91(1), 1–21.
Moheimani, N. R., Webb, J. P., & Borowitzka, M. A. (2012). Bioremediation and other potential applications of coccolithophorid algae: a review. Algal Research, 1(2), 120–133.
Monteiro, F. M., Bach, L. T., Brownlee, C., Bown, P., Rickaby, R. E. M., Poulton, A. J., Tyrrell, T., Beaufort, L., Dutkiewicz, S., Gibbs, S., & Gutowska, M. A. (2016). Why marine phytoplankton calcify. Science Advances, 2(7), e1501822.
Müller, M. N. (2019). On the genesis and function of coccolithophore calcification. Frontiers in Marine Science, 6, 49.
Naqvi, S. W. A. (2020). Ocean deoxygenation. Journal of the Geological Society of India, 96(5), 427–432.
O’Brien, C. J., Vogt, M., & Gruber, N. (2016). Global coccolithophore diversity: Drivers and future change. Progress in Oceanography, 140, 27–42.
Okada, H., & Honjo, S. (1973a). Distribution of coccolithophorids in the North and Equatorial Pacific Ocean: quantitative data on samples collected during Leg 30, Oshoro Maru, 1968 and Leg HK69-4, Hakuho Maru, 1969. Woods Hole Oceanographic Institute Technical Report, 73(81), 1–59.
Okada, H., & Honjo, S. (1973b). The distribution of oceanic coccolithophorids in the Pacific. Deep Sea Research, 20, 355–374.
Okada, H., & Honjo, S. (1975). Distribution of coccolithophores in marginal seas along the western Pacific Ocean and in the Red Sea. Marine Biology, 31, 271–285.
Paasche, E. (1968). Biology and physiology of coccolithophorids. Annual Review of Microbiology, 22(1), 71–86.
Rogalla, U., & Andruleit, H. (2005). Precessional forcing of coccolithophore assemblages in the northern Arabian Sea: Implications for monsoonal dynamics during the last 200,000 years. Marine Geology, 217(1-2), 31–48.
Rost, B. and Riebesell, U, (2004) Coccolithophores and the biological pump: responses to environmental changes. Coccolithophores, Springer, 99-125.
Schiebel, R., Zeltner, A., Treppke, U. F., Waniek, J. J., Bollmann, J., Rixen, T., & Hemleben, C. (2004). Distribution of diatoms, coccolithophores and planktic foraminifers along a trophic gradient during SW monsoon in the Arabian Sea. Marine Micropaleontology, 51(3-4), 345–371.
Siesser, W. G. and Winter, A., (1994) Composition and morphology of coccolithophore skeletons, In Coccolithophores (eds Winter, A. and Siesser, W. G.),51-62.
Silva, A., Brotas, V., Valente, A., Sá, C., Diniz, T., Patarra, R. F., & Neto, A. I. (2013). Coccolithophore species as indicators of surface oceanographic conditions in the vicinity of Azores islands. Estuarine, Coastal and Shelf Science, 118, 50–59.
Stoll, H. M., Ziveri, P., Shimizu, N., Conte, M., & Theroux, S. (2007). Relationship between coccolith Sr/Ca ratios and coccolithophore production and export in the Arabian Sea and Sargasso Sea. Deep Sea Research Part II: Topical Studies in Oceanography, 54(5-7), 581–600.
Taylor, A. R., Brownlee, C., & Wheeler, G. (2017). Coccolithophore cell biology: chalking up progress. Annual Review of Marine Science, 9(1), 283–310.
Thierstein, H. R. and Young, J. R., (2013) Coccolithophores - From molecular processes to global impact. Springer, 1-570.
Tyrrell, T. and Merico, A, (2004) Emiliania huxleyi: bloom observations and the conditions that induce them. Coccolithophores, Springer, 75-97.
Tyrrell, T. and Young, J. R., (2009) Coccolithophores. In Encyclopedia of Ocean Sciences, 2nd edn , (eds Steel, J. H., Turekian, K. K. & Thorpe, S. A.), 3568-3576.
Westbroek, P., De Jong, E. W., Van der Wal, P., Borman, T., De Vrind, J. P. M., Van Emburg, P. E., & Bosch, L. (1983). Calcification in coccolithophoridae: Wasteful or Functional? Ecological Bulletins, 291-299, 9.
Winter, A. and Siesser W.G., (1994) Coccolithophores, Cambridge University Press, 242.
Wyrtki, K., (1973) Physical oceanography of the Indian Ocean, The biology of the Indian Ocean, 18-36.
Yang, T., & Wei, K. (2003). How many coccoliths are there in a coccosphere of the extant coccolithophorids? A compilation. Journal of Nannoplankton Research, 25(1), 7–15.
Young, J. R., (1994) Functions of coccoliths. In Coccolithophores, (eds Winter, A. and Siesser, W. G.), 63-82.
Young, J. R. (2003). How many species? Analysis of extant nannoplankton biodiversity. Gaia, 11, 87–87.
Young, J. R., & Henriksen, K. (2003). Biomineralization within vesicles: the calcite of coccoliths. Reviews in Mineralogy and Geochemistry, 54, 189–215.
Young, J. R., Geisen, M., Cros, L., Kleijne, A., Probert, I., & Ostergaard, J. B. (2003). A guide to extant coccolithophore taxonomy. Journal of Nannoplankton Research, 1, 1–132.
Young, J. R., Andruleit, H., & Probert, I. (2009). Coccolith function and morphogenesis, insights from appendage-bearing coccolithophores of the family Syracosphaeraceae (Haptophyta). Journal of Phycology, 2009(45), 213–226.
Young, J. R., Pratiwi, S. and Su, X. (2017) Expedition 359 Scientists, Data report: surface seawater plankton sampling for coccolithophores undertaken during IODP Expedition 359. C. Betzler, GP Eberli, CA Alvarez-Zarikian, & Expedition, 359, 1-7.
Acknowledgements
The authors thank the Director of CSIR-National Institute of Oceanography, India, and the Scientist-in-Charge (CSIR-NIO, Kochi) for facilities and encouragement. We record our sincere thanks to Directors of NCCR (MoES), Chennai, and Director of CMLRE (MoES), Kochi, India, for the funding to CSIR-NIO, Regional Center, Kochi, under SWQM-MEDAS programme to which this paper is associated with. This is CSIR-NIO contribution.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Arundhathy, M., Jyothibabu, R., Santhikrishnan, S. et al. Coccolithophores: an environmentally significant and understudied phytoplankton group in the Indian Ocean. Environ Monit Assess 193, 144 (2021). https://doi.org/10.1007/s10661-020-08794-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10661-020-08794-1