Biogeographic distribution of extant Coccolithophores in the Indian sector of the Southern Ocean

Accepted Manuscript Biogeographic distribution of extant Coccolithophores in the Indian sector of the Southern Ocean

Shramik M. Patil, Rahul Mohan, Suhas S. Shetye, Sahina Gazi, Karl-Heinz Baumann, Syed Jafar PII: DOI: Reference:

S0377-8398(17)30126-3 doi: 10.1016/j.marmicro.2017.08.002 MARMIC 1655

To appear in:

Marine Micropaleontology

Received date: Revised date: Accepted date:

28 March 2016 20 July 2017 22 August 2017

Please cite this article as: Shramik M. Patil, Rahul Mohan, Suhas S. Shetye, Sahina Gazi, Karl-Heinz Baumann, Syed Jafar , Biogeographic distribution of extant Coccolithophores in the Indian sector of the Southern Ocean, Marine Micropaleontology (2017), doi: 10.1016/j.marmicro.2017.08.002

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ACCEPTED MANUSCRIPT Biogeographic distribution of extant Coccolithophores in the Indian Sector of the Southern Ocean Shramik M. Patil1, Rahul Mohan1*, Suhas S. Shetye2, Sahina Gazi1, Karl-Heinz Baumann3, Syed Jafar4 National Centre for Antarctic and Ocean Research, Vasco-da-Gama, Goa, India-403804

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*[email protected], +91-(832) 2525531, fax- +91-(832) 2520877

of Geosciences, Universität Bremen, PO Box 330440, 28334 Bremen, Germany 5-B, Whispering Meadows, Haralur Road, Bangalore- 560 102, India.

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4Flat

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3Department

Institute of Oceanography, Dona Paula, Goa, India-403004

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2National

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Abstract:

Water samples from nine vertical profiles down to 110 m water depth and 19 samples from

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the sea-surface were studied for coccolithophore abundance and distribution across oceanic frontal regions of the Indian sector of the Southern Ocean. Sampling was performed along a north-south transect (between 39°S and 65.49°S, ~57.3°E) during the 4th Indian Southern

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Ocean Expedition (between 31st January and 18th February, 2010). Coccospheres and

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coccoliths were counted separately using a Scanning Electron Microscope (SEM). A total of 39 taxa (including morphotypes, types and subspecies) were recorded as intact coccospheres with abundances reaching up to 750x103 coccospheres/l. In addition, 85 taxa (including varieties, morphotypes) were counted as coccoliths reaching up to 900×105 coccoliths/l. Emiliania huxleyi was recognized as the most abundant species, accounting for more than 86% of the total coccolithophore assemblage at each station.

Elevated coccolithophore

diversity was observed in the subtropical zone whereas high coccolithophore abundance was 1

ACCEPTED MANUSCRIPT observed in the Subantarctic zone. A monospecific Emiliania huxleyi assemblage was recorded within and south of the Polar frontal zone. Three assemblages were recognized based on coccolithophore abundance and diversity. The assemblage of the Agulhas Retroflection frontal zone and Subtropical zone is highly diverse (39 taxa) and can be linked to relatively warm, high saline and oligotrophic waters. The Subantarctic zone assemblage is

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characterized by a reduced number (thirteen) of coccolithophore taxa, whereas the Polar

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Frontal zone comprises a monospecific E. huxleyi assemblage (preferentially morphotypes C

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and B/C). Multivariate statistics indicated that regions with elevated temperature and low nutrient concentration show high coccolithophore diversity whereas regions with high

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nutrient concentrations and low temperature show a strongly reduced coccolithophore

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diversity with abundant monospecific E. huxleyi (morphotypes B/C and C) assemblages. Keywords: Extant Coccolithophores, Southern Indian Ocean, Nutrients, Oceanic Fronts,

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Austral Summer.

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ACCEPTED MANUSCRIPT Introduction Coccolithophores are calcified, unicellular, photosynthetic marine microalgae found in coastal and open ocean regions. They are the most important marine carbonate producers dwelling in the upper photic layer of the world oceans (Westbroek et al., 1993) and play a

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significant role in the marine food web and carbon cycling (Rost and Riebesell, 2004). Coccolithophore abundance and species fluctuations in the oceans are linked to changes in

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environmental parameters such as Sea Surface Temperature (SST), Sea Surface Salinity

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(SSS), solar radiation, and nutrient content (Winter et al., 1994). In recent years, increase in

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SST and decrease in oceanic pH generated appreciable interest in the coccolithophore ecology and biogeography (Orr et al., 2005; Iglesias-Rodriguez et al., 2008; Beaufort et al.,

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2011). A latitudinal expansion of coccolithophore species such as Emiliania huxleyi in the Southern Ocean, south of 60°S latitude was recorded by several authors (Winter et al., 1999;

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Findlay and Giraudeau, 2000; Cubillos et al., 2007; Gravalosa et al., 2008; Patil et al., 2014;

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Winter et al., 2014), but the actual cause of this southward expanse is still debated. Thus, detailed knowledge about coccolithophore species diversity, spatial and vertical distribution

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and their production in this region is needed. In the past decade, studies of plankton and sediment samples on coccolithophore biogeography, taxonomy, ecological preferences were

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carried out in various regions of the Southern Ocean (SO) (Winter et al., 1999; Findlay and Giraudeau, 2000; Mohan et al. 2008; Gravalosa et al., 2008; Saavedra-Pellitero et al., 2014; Malinverno et al., 2015; Malinverno et al., 2016). However, studies on coccolithophores of the Indian sector of the SO still remain relatively scarce. In this study, vertical and latitudinal distribution and community composition of coccolithophores were examined quantitatively along a N-S transect in the Indian sector of the Southern Ocean (Fig. 1, Table 1). Coccolithophore species diversity and its relationship 3

ACCEPTED MANUSCRIPT with the present environmental conditions were studied across the major oceanic frontal regions of the study area. The relationship between species and environmental conditions was assessed by Canonical Correspondence Analysis (CCA) and the obtained results are compared with those published from other sectors of the Southern Ocean. The investigation of coccolithophores in extreme southern latitudes was carried out to verify whether

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coccolithophores showed any southward expansion, as was previously suggested (e.g.,

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Winter et al., 2014). The probable forcing mechanisms involved and the general response of

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coccolithophores to the physico-chemical characteristics of the southern latitudes and oceanic frontal regions of the Indian Sector of the Southern Ocean are also investigated.

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Hydrographical settings of the study region

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The Antarctic Circumpolar Current (ACC) is a massive eastwardly flowing current that surrounds the Antarctic continent and comprises various water masses and fronts

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(Nowlin and Klinck, 1986). The ACC flows eastward due to the intense Southern hemisphere

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westerly winds and connects all the major oceans (Orsi et al., 1995). Distinct fronts and surface water mass regimes observed in the Southern Ocean in a poleward direction are the

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Agulhas Retroflection Front (ARF), Subtropical Front (STF), Subtropical zone (STZ), Subantarctic Zone (SAZ), Subantarctic Front (SAF), Polar Frontal Zone (PFZ), Polar Front

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(PF) and the Antarctic Zone (AZ) (Orsi et al., 1995) (Fig. 1). The Subtropical Front (STF) defines the northern boundary of the ACC (Clifford, 1983; Orsi et al., 1995) which is usually documented between 35°S and 45°S in the study area. The STF shows two different entities, the Northern Subtropical Front (NSTF) and the Southern Subtropical Front (SSTF). Average Sea Surface Temperature (SST) at NSTF changes from about 22°C to 21°C while Sea Surface Salinity (SSS) is consistent at ~35.5 (Belkin and Gordon, 1996; Holliday and Read, 1998). At the SSTF, SST changes from 17°C to 11°C (and 12°C to 10°C at 100m) and SSS 4

ACCEPTED MANUSCRIPT decreases from 35.35 to 35.05 (35.0 to 34.6 at 100m). The ARF occurs between NSTF and SSTF with SST and SSS ranging from 19°C to 17°C and 35.54 to 35.39 (Belkin and Gordon, 1996; Holliday and Read, 1998). At the SAF the temperature ranges between 11oC to 6oC at surface and 8oC to 4oC at 200m water depth whereas salinity ranges between 34.0 to ~33.85 at surface and 34.40 to 34.11 at 200m water depth (Belkin and Gordon 1996; Orsi et al.,

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1995). The PF lies between the Agulhas Basin to the north and the Enderby Basin to the

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south. The PF is defined by the subsurface temperature minimum of 2°C at the depth above

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200m (Orsi et al., 1995) (Table 2).

The Southern Ocean is also known as a region of intense eddy activity which

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influences global thermohaline circulation and, thus, affects global climate (Hughes and Ash,

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2001). The oceanic fronts in the Southern Indian Ocean split, merge, fluctuate seasonally and vary spatially over regional topographic features. The average SST north of the SAF is

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generally more than 4°C whereas south of the PF it is less than 2°C (Orsi et al., 1995; Klinck

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and Nowlin, 2001).

Materials and methods

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Samples

At the 9 vertical profile stations, samples were collected at 6 different depths (0, 20,

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40, 60, 80 and 110m) using 5 litre (capacity) Niskin bottles attached to a CTD rosette (12 bottles) (Sea-Bird Electronics). Additionally, 19 surface water samples were collected using the ship’s pumping system at one degree intervals during the 4th Indian Southern Ocean Expedition onboard Ocean Research Vessel Sagar Nidhi (between 31st January and 18th February, 2010) within the area 39°S to 65.49°S and 57.3°E to 51.09°E (Table 1). The vertical profile observations were made in the oceanic frontal zones identified by using insitu sea surface temperature and Expendable Bathythermograph (XBD) measurements. 5

ACCEPTED MANUSCRIPT Defining oceanic frontal locations and zones The locations of fronts were defined by using a temperature sensor installed on the ship which monitors the in-situ sea surface temperature and by using frequent XBT measurements (every half degree interval). Concerning the criteria used for defining the

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fronts, we followed Belkin and Gordon (1996), Kostianoy et al. (2004), Anilkumar et al. (2006), and Luis and Sudhakar (2009). Conductivity Temperature Depth (CTD)

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measurements provided vertical water column temperature and salinity profiles. The

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temperature and salinity data displayed in Fig. 3 are based on in-situ measurements performed using a Seabird CTD system. In this study, temperature varied between 18.4°C to -

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1.4°C and salinity between 35.48 and 33.56. Stations S1 to S4 were located in the Agulhas

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Retroflection Frontal zone and Subtropical zone; stations S5 and S6 in the Subantarctic zone whereas, stations S7 and S8 were positioned in the polar frontal zone. The southernmost

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station S9 was located near the Antarctic coastal region.

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Sample preparation and identification of coccolithophore taxa For the coccolithophore study, one litre of water was collected in a prewashed plastic

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bottle and filtered through 0.2µm pore size Whatman Nuclepore Track-Etched membrane filters of 47mm diameter using Pall (TM) manifold unit. Without washing, rinsing or any

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chemical conservation, filters were dried in the oven at 45°C for 48 hours and kept in the Millipore sterile petridish until analysis. In the laboratory at the National Centre for Antarctic and Ocean Research, a small piece of filter paper (~5mm2) was cut and placed on a double sided carbon tape attached to a 1cm diameter aluminum stub and sputter coated with platinum. The sample was inspected under a JEOL-JSM 6360LV Scanning Electron Microscope (SEM) at 2,000× magnification using 5-15 KV accelerating voltage. To identify coccolithophores up to the species level, a 6

ACCEPTED MANUSCRIPT higher magnification up to 20,000× was used. For quantification, up to 1000 fields of views were observed. A total of 36-367 coccospheres and up to 800 coccoliths were counted for each sample. The identification of coccolithophore species followed the taxonomic descriptions

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given by Young et al. (2003) and on the Nannotax 3 website (ina.tmsoc.org/Nannotax3). Differentiation of Emiliania huxleyi morphotypes was carried out following Young et al.

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(2003). The E. huxleyi morphotype A consists of medium sized (3-4 μm) coccoliths, robust

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distal shield elements and curved central area elements. Emiliania huxleyi morphotype B contains large coccoliths (3-5 μm), delicate distal shield elements and the central area either

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open or covered by a thin plate. Emiliania huxleyi morphotype C contains small coccoliths (2.5-3.5 μm), delicate distal shield elements and a central area which is open or covered by a

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with delicate distal shield elements.

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thin plate; whereas, E. huxleyi morphotype B/C contains medium sized coccoliths (3-4 μm)

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Hagino et al. (2011) differentiated E. huxleyi morphotype ‘O’ with an open central area from other existing E. huxleyi morphotypes based on molecular genetic studies. In this

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study, we have not separated E. huxleyi morphotype ‘O’ from other E. huxleyi morphotypes; specimens of this morphotype have been incorporated in E. huxleyi morphotypes B, B/C and

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C for better comparison of these morphotype assemblages with previous studies carried out in the Southern Ocean. The dissolved E. huxleyi type D with irregular ‘T’ elements (Findlay and Giraudeau, 2000; Mohan et al., 2008) was also observed and was counted separately. Intact coccospheres and detached coccoliths were documented and counted separately. For the study of the ecology of coccolithophores, only intact coccospheres were used, as they represent the living component of the assemblage. The total number of complete

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ACCEPTED MANUSCRIPT coccospheres, coccolith abundance and the number of species recorded as coccosphere and coccoliths are the main parameters which are considered in this study (Fig. 2, Appendix). The quantification of coccospheres/or coccoliths was carried out using the formula, Coccosphere or coccoliths concentration/l = (F×C)/(V×A) Where,

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F is the effective filtration area (mm2),

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C is the number of specimens counted, V is the filtration volume (l) and

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A is the investigated filter area (mm2)

Chemical analysis

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For nutrients [nitrate (NO3), nitrite (NO2), phosphate (PO4), and silicate (SiO4)], water samples from each sampled depth were collected in clean prewashed plastic bottles and for

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pH analysis in glass cuvettes. The water samples for nutrients were analyzed immediately

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onboard following standard protocols described by Grasshoff (1983), whereas, pH (pH in free ion scale) was measured at 25°C by cresol red spectrometry following Byrne and Breland

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(1989) using a Shimadzu UV-1800 spectrophotometer. The pH values on free ion scale were first converted to the pH in situ and then to pH on the recommended Total Scale (pHT).

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Analytical precision was ~0.002 for pH and accuracy was ±0.005.

Data analysis In order to investigate the relationship between coccolithophore species abundance and environmental data a Canonical Correspondence Analysis (CCA) was carried out using Multivariate Statistical Package Program (MVSP) (Kovach, 1998) for all vertical profile 8

ACCEPTED MANUSCRIPT stations where coccolithophores were documented. In the CCA plots, physico-chemical parameters are plotted as arrows that point in the direction of increasing values of the environmental variables. The length of the arrows is directly proportional to their importance; the angle between arrows and ordination axis shows the extent of correlation between them (the smaller the angle, the stronger the correlation). A perpendicular line drawn from an

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arrow through coccolithophore species indicates the relative location of species along the

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environmental gradient (Palmer 1993). In order to better understand the assemblage composition, coccolithophore data were also analyzed for the Shannon-Wiener diversity

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index (H’), Margalef’s Species richness (d) and Pielou’s evenness (J’) using PRIMER-

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version 5 (developed by PRIMER-E Limited, UK); statistically significant differences were determined by two-way ANOVA (Table 3). Two-way ANOVA was also performed on

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coccolithophore abundance to evaluate their spatial and temporal variation.

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Results

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Coccolithophore and coccolith density and diversity The analysis of vertical profiles and surface water samples exhibited significant

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changes in species abundance and diversity across the oceanic frontal zones of the Indian

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sector of the Southern Ocean. Consistent increase in the coccosphere and coccolith abundance was observed from the ARF zone (ARFZ) to the SAZ. A diversity decrease was observed south of the SAZ (Fig. 2). High abundances of coccolithophores and coccoliths were observed at the SAZ (up to ~750x103 coccospheres/l and ~900x105 coccoliths/l, at 20m depth) and at the PFZ (~350x103 coccospheres/l and ~550x105 coccoliths/l, at the surface). At the southernmost station S9 only detached coccoliths of Emiliania huxleyi were observed.

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ACCEPTED MANUSCRIPT Though detached coccoliths were much higher in numbers when compared to coccospheres, they displayed a rather similar distribution pattern in the study. Distribution of major coccolithophore species We identified 39 taxa as coccospheres and 85 taxa as coccoliths (Appendix table 1).

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The maximum coccolithophore species diversity was recorded in the ARFZ and STZ whereas maximum abundance was observed in the SAZ. Poleward of the SAZ, occurrence of intact

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spheres of E. huxleyi morphotypes C, B/C and detached coccoliths of other species were

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observed as far as 59°S. The presence of detached coccoliths of E. huxleyi morphotypes C

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and B/C was documented as far south as station S9, located at the Antarctic coastal region. Emiliania huxleyi was recognized as the most abundant coccolithophore species in the

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study area (Fig. 3) and was found with four morphotypes (E. huxleyi morphotypes A, B, C and B/C) showing significant changes in their abundance and distribution in response to the

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varying environmental settings. Emiliania huxleyi morphotypes A and B were most abundant

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at the ARFZ and STZ, showing preference for an elevated temperature, salinity and low nutrient conditions. The abundance of E. huxleyi morphotypes A and B decreased south of

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the STZ, whereas the abundance of E. huxleyi morphotypes B/C and C increased with decreasing temperature, salinity and increasing nutrient concentrations. The other most

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common coccolithophore species observed were Calcidiscus leptoporus (subsp. small and leptoporus), Gephyrocapsa muellerae, Oolithotus fragilis, Polycrater galapagensis, Poricalyptra aurisinae, Syracosphaera histrica HOL (“Calyptrolithophora papillifera”), Helicosphaera carteri HOL solid ("Syracolithus catilliferus"). Their presence, however, was restricted to the area north of the SAZ. All other recorded species only showed discrete/uneven distribution patterns. Six species of the genus Syracosphaera were recorded, which were restricted to the ARFZ and STZ. 10

ACCEPTED MANUSCRIPT Distribution of Emiliania huxleyi morphotypes Emiliania huxleyi (average relative abundance 97.2%) was present at all the stations between 39°S and 59°S (between ARFZ and PFZ), whereas further south only detached coccoliths were documented. The maximum abundance of E. huxleyi recorded in the study

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was 740x103 coccospheres/l, at 20m water depth of station S6 located in the SAZ. Among the recorded four E. huxleyi morphotypes, morphotype C was most abundant (average relative

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abundance 75.7%), followed by morphotypes B/C (average relative abundance 21.2%), A

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(2.54%) and B (0.4%). E. huxleyi morphotype C was recorded at all stations between 39°S and 59°S (between ARFZ and PFZ), with a maximum of 660x103 coccospheres/l at the

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surface at station S5 (located in the SAZ). A strong decrease in the abundance of E. huxleyi

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type C was observed south of the SAZ (320x103 to 1.5x103 coccospheres/l) and this morphotype was absent south of the PFZ. Emiliania huxleyi morphotype B/C varied between 0 and 290x103 coccospheres/l, and showed a comparable distribution pattern to that of E.

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huxleyi morphotype C. The highest abundance of E. huxleyi morphotype B/C was recorded in the surface sample of station S6 (located in the SAZ). Emiliania huxleyi morphotypes A and B dominated in the stations located in the ARFZ and STZ. Emiliania huxleyi morphotype A

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showed a maximum abundance of 18x103 coccospheres/l at 20m depth at the ARFZ. This

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morphotype occurred as far south as the PFZ in low abundance (>3x103 coccospheres/l). Emiliania huxleyi morphotype B occurred only at the ARFZ and reached a maximum abundance of 15x103 coccospheres/l at at 20m depth. Distribution of coccolithophores other than Emiliania huxleyi According to their lateral and vertical distribution patterns, all other coccolithophores showed preference to different oceanographic areas. 28 taxa (including subspecies and types) were recorded in the ARFZ, comprising a total abundance up to 570×103 coccospheres/l (at 11

ACCEPTED MANUSCRIPT surface and between surface and 100m water depth) and 32.3% of the total coccolithophore assemblage. Common coccolithophore species recorded in this zone were Gephyrocapsa muellerae (2.6%), Syracosphaera rotula (1.5%), Umbellosphaera sibogae (1%), Calcidiscus leptoporus

subsp.

small

Holococcolithophores,

(3.5%),

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as

and

C.

leptoporus

Syracosphaera

histrica

subsp.

leptoporus

(2.5%).

HOL

(“Calyptrolithophora

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papillifera”), Coronosphaera mediterranea HOL gracillima type, Homozygosphaera spinosa,

aurisinae,

Poricalyptra

gaarderiae,

Syracosphaera

anthos

HOL

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Poricalyptra

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Helicosphaera carteri HOL solid ("Syracolithus catilliferus"), Homozygosphaera vercellii,

(Periphyllophora mirablis) and Zygosphaera marsilli, reached a maximum abundance up to

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18x103 coccospheres/l in the ARFZ.

In the STZ, 25 coccolithophore taxa were recorded comprising a total abundance up

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to 1650x103 coccospheres/l (from the surface down to 110m water depth), representing 16.7% of the total assemblage (including E. huxleyi). The most common coccolithophore

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species observed in this zone were C. leptoporus subsp. small (2.2%), Polycrater galapagensis (1.1%), Umbellosphaera tenuis IIIb (1%), Oolithotus fragilis (1%), C. leptoporus subsp. leptoporus (0.8%), and G. muellerae (0-5%). Holococcolithophore species

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reached a maximum abundance of 2.6% (21.8×103 coccospheres/l). Holococcolithophores

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observed in this zone were Syracosphaera histrica HOL (“Calyptrolithophora papillifera”), Corisphaera gracilis, Corisphaera tyrrheniensis, H. carteri HOL solid ("Syracolithus catilliferus"), H. vercellii, P. gaarderiae, Poritectolithus maximus, P. aurisinae and Syracosphaera anthos HOL (Periphyllophora mirablis). In the SAZ 13 coccolithophore taxa were recorded. Besides Emiliania huxleyi, species recorded were Oolithotus fragilis, Calcidiscus leptoporus subsp. small, Calcidiscus leptoporus subsp. leptoporus, Cyrtosphaera aculeata, Anacanthoica acanthos, Acanthoica 12

ACCEPTED MANUSCRIPT biscayensis and Polycrater galapagensis (together reaching up to <2×103 coccospheres/l). Holococcolithophore species such as Syracosphaera histrica HOL (“Calyptrolithophora papillifera”), Corisphaera gracilis, and S. anthos HOL (Periphyllophora mirablis) were only sporadically recorded in the SAZ.

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In the PFZ no coccolithophore taxa were recorded other than E. huxleyi (morphotypes A, B/C and C).

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Diversity indices

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The highest diversity of coccolithophores occurred in the ARFZ and STFZ in the

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upper 40m of the water column. Diversity decreased southward as well as with depth in the water column (down to 110m). The highest abundance of coccolithophores observed at the

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SAZ and PFZ in the upper 20m water column was mainly comprised of E. huxleyi morphotypes C and B/C. The stations located south of the PFZ contained detached E. huxleyi

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coccoliths and showed a high abundance of diatoms.

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The calculated values of Shannon-Wiener diversity index (H’), Margalef’s species richness (d) and Pielou’s evenness (J’) were nearly constant for the stations located in the

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ARFZ and STZ. These distribution patterns were similar for coccoliths as well as for coccospheres. The two-way ANOVA showed significant statistical differences between the

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stations, as also significant differences between the patterns of these indices (H’, d, J’) (Table 3) [(for depths, α=0.05; df=5; p<0.01) and (for stations α=0.05; df=8; p<0.01)].

Canonical correspondence analysis In the CCA biplots (Fig. 4) two axes, explaining 88% of the relationship between coccolithophore species and environmental variables, were extracted. The details of percentage relationship between coccolithophore species and environmental variables are 13

ACCEPTED MANUSCRIPT given in Table 3. Temperature, salinity, nitrate, phosphate concentrations and pH were the most important environmental variables influencing the coccolithophore community. Acanthoica biscayensis, C. tyrrheniensis, S. dilatata, C. murrayi, E. huxleyi morphotype B, U. tenuis type II, O. antillarum, S. pirus, P. vandelii, C. lecaliae, U. sibogae, P. aurisinae, H. spinosa, E. huxleyi morphotype A, C. mediterranea Hol, P. gaarderiae, C. gracillis, S.

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anthos Hol, Z. marsilli, Syracosphaera histrica HOL (“Calyptrolithophora papillifera”), H.

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carteri Hol and G. ornata, all show a preference for elevated salinity, temperature and pH

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and low NO3 and PO4 concentrations. All these species showed a maximum abundance in the ARFZ and STZ. Emiliania huxleyi type D, U. tenuis type IIIB, C. leptoporus subsp. small, C.

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leptoporus subsp. leptoporus, S. rotula and S. molischii show a preference for low NO3 and PO4 concentration and show a moderate relationship with increasing temperature and salinity

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conditions. E. huxleyi morphotypes C and B/C, S. protrudents, P. maximus show a preference for increasing NO3, PO4 and decreasing temperature, salinity conditions. Syracosphaera

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histrica HOL (“Calyptrolithophora papillifera”), H. vercellii, G. muellerae and A. acanthos

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show a weak relationship with increasing temperature, salinity and decreasing nutrient

Discussion

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concentrations.

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The study of the coccolithophore community in the upper 110m of the water column in the Indian sector of the Southern Ocean revealed a relationship between the oceanic parameters and the coccolithophore assemblages. We identified the ARFZ and the STZ as the regions with highest coccolithophore diversity whereas the SAZ and the PFZ were identified as the regions of highest coccolithophore standing stocks. Similar results were also obtained in other areas of the Southern Ocean (Mohan et al., 2008; Gravalosa et al., 2008; SaavedraPellitero et al., 2014; Malinverno et al., 2015). The PFZ forms a natural boundary where 14

ACCEPTED MANUSCRIPT coccolithophore diversity, coccosphere abundance and numbers of coccoliths all rapidly drop in southern direction. The decrease in the coccolithophore diversity and abundance (Winter et al., 1994; Mohan et al., 2008; Malinverno et al., 2015) and the occurrence of monospecific E. huxleyi abundance south of the PFZ has been recorded previously in various Southern Ocean regions (McIntyre and Bé, 1967; Eynaud et al.,1999; Findlay and Giraudeau, 2000; Mohan et

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al., 2008; Gravalosa et al., 2008; Hinz et al., 2012; Winter et al., 2014; Saavedra-Pellitero et

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al., 2014; Malinverno et al., 2015; Malinverno et al, 2016).

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The high coccolithophore abundance in the oceanic frontal zones (mainly at depths between 0-40m) of the Southern Ocean could be related to high temperature and elevated

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nutrient concentrations (Franks, 1992; Laubscher et al., 1993). The elevated coccolithophores

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diversity in the ARFZ and STZ and the increase in E. huxleyi abundance in the SAZ-PFZ are in agreement with the previous studies carried out in the Atlantic (Eynaud et al., 1999), Indian (Mohan et al., 2008), Pacific (Gravalosa et al., 2008; Saavedra-Pellitero et al., 2014;

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Malinverno et al., 2015; Malinverno et al., 2016) and Australian (Findlay and Giraudeau, 2000) sectors of the Southern Ocean. Previously, Mohan et al. (2008) identified three coccolithophore assemblages (subtropical, subantarctic and polar) in the Indian Sector of the

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Southern Ocean. They showed that increased nutrient concentrations south of the STF hinder

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the growth of coccolithophores, but that high nitrate concentrations at the PF correspond to increased abundances of the E. huxleyi populations. Our study is in agreement with the study of Mohan et al. (2008) which showed a decrease in coccolithophore diversity coinciding with an increase in nutrient concentration south of the STF and an increase in the abundance of E. huxleyi morphotypes B/C and C at the SAF and PF regions, coinciding with an increase in nitrate concentrations.

15

ACCEPTED MANUSCRIPT The coccolithophore abundance observed in this study is lower than that of northern high latitudes (eg. Bering Sea, 1000x103 coccospheres/l, Harada et al., 2012; Nordic Sea, up to 500x103 coccospheres/l, Baumann et al., 2000) but is comparable to the other sectors of the Southern Ocean (Findlay and Giraudeau, 2000; Mohan et al., 2008; Charalampopoulou,

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2011; Saavedra-Pellitero et al., 2014, Malinverno et al., 2015). In the present study, three assemblages were recognized based on the coccolithophore

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species diversity, abundance and the statistical analysis. (1) The first assemblage with high

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coccolithophore diversity and low abundance is found in the region between the ARFZ and STZ, (2) the SAZ assemblage is characterized by a reduced number of coccolithophore taxa

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Coccolithophore assemblage of ARFZ-STZ

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and an increased abundance and (3) the monospecific E. huxleyi dominate the PFZ.

The ARFZ-STZ shows the highest coccolithophore diversity, what can be linked to

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presence of warm highly saline waters with low nutrient concentrations. CCA analysis

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indicates a preference of most coccolithophore species for the warm, highly saline, oligotrophic regions (Fig. 4). Our observations corroborate the study of Mohan et al. (2008),

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who showed high coccolithophore diversity and abundance between 21°S-41°S (north of the

regions).

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STF) and a decrease of both diversity and abundance between 42°S-50°S (SAF and PF

Emiliania huxleyi is recognized as the most abundant and widespread coccolithophore species in these zones, comprising four different morphotypes (A, B, C and B/C). In the previous studies, different E. huxleyi morphotypes were reported from environmentally diverse regions (Okada and Honjo, 1973; Findlay and Giraudeau, 2000; Gravalosa et al., 2008; Mohan et al., 2008; Beaufort et al., 2011; Hagino et al., 2011; Henderiks et al., 2012; 16

ACCEPTED MANUSCRIPT Saavedra-Pellitero et al., 2014, Malinverno et al., 2015). The E. huxleyi morphotype A appears to prefer warm waters with low nutrient conditions, in agreement with studies by Hiramatsu and De Deckker (1996); Findlay and Giraudeau (2000) and Mohan et al. (2008). Emiliania huxleyi morphotype B was present only in the ARFZ in low abundance and was not recorded south of this zone. In contrast, replacement of ‘robust’ E. huxleyi morphotype A

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by rare E. huxleyi morphotype B was observed in the Pacific sector of the Southern Ocean

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south of the SAZ by Saavedra-Pellitero et al. (2014). In earlier studies the occurrence of E.

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huxleyi morphotype B was recorded in the northern hemisphere (Cook et al., 2011) and this morphotype was not reported in the Southern Ocean (Findlay and Giraudeau, 2000; Mohan et

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maximum abundance south of the STZ.

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al., 2008). Emiliania huxleyi morphotypes C and B/C were most abundant and observed in

The occurrence of Gephyrocapsa muellerae in the ARFZ and STZ and its absence at more southern stations indicates its preference to temperate waters. The presence of G.

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muellerae in the tropical and subtropical frontal regions, with temperature >14°C, and its absence <10°C in the Australian sector of the Southern Ocean was recorded previously by Findlay and Giraudeau (2000). The occurrence of G. muellerae in low abundance in the STZ

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and relatively high abundance in the surface sediments of the SAZ and PFZ was observed by

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Saavedra-Pellitero and Baumann (2015) in the Pacific sector of the Southern Ocean. In contrast, the preference of this species for colder waters (it can be found as far as 70°S) was observed by Samtleben et al. (1995); Winter et al. (1994) and Winter et al. (1999). In these previous studies, the presence of G. oceanica and/or G. ericsonii was recorded at and south of the STZ (Verbeek 1989; Eynaud et al., 1999; Mohan et al., 2008; Maliverno et al., 2015), but G. muellerae was not recorded. The discrete occurrence of G. muellerae in the STZ and south

17

ACCEPTED MANUSCRIPT of the STZ and its absence south of SAZ suggest a preference of this species for warm low nutrient conditions. Calcidiscus leptoporus subsp. small and C. leptoporus subsp. leptoporus showed comparatively similar distribution patterns in this study. Both subspecies dominated in the

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STZ and occurred as far as south of the SAZ. The preference of C. leptoporus subsp. small for warmer waters, equatorward of the STZ (Hiramatsu and De Deckker 1996) and a

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restricted occurrence in the subtropical gyre (Boeckel and Baumann 2008) was recorded

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previously. McIntyre et al., (1970) highlighted C. leptoporus as a mainly tropical species, present in waters of 20-30°C but also documented the presence of C. leptoporus in much

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colder waters until 6°C. High abundances of C. leptoporus south of the STZ region were

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observed in previous studies (Nishida 1986; McIntyre and Bé 1967; Findlay and Giraudeau 2000). We did not find coccospheres of C. leptoporus south of the SAZ, although it has been found there in previous studies (Findlay and Giraudeau, 2000; Malinverno et al., 2015). A

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low abundance of C. leptoporus throughout the study area and a rare occurrence at stations south of the SAZ and PFZ in the Indian Sector of the Southern Ocean was previously observed by Mohan et al. (2008). This species was observed in water samples and in surface

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sediments from the subantarctic and Polar Front regions of the Pacific sector of the Southern

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Ocean (Saavedra-Pellitero and Baumann, 2015). The observed occurrence of C. leptoporus in the SAZ and occurrence of coccoliths south of SAZ confirm its affinity for cold nutrient poor waters.

Syracosphaera is the most diverse genus, including species reported from different zones and various ecological habitats (Jordan and Chamberlain 1997). In this study, coccospheres of six Syracosphaera species and coccoliths of 19 Syracosphaera species were recorded, all showing an affinity to high temperature, salinity and low nitrate concentrations. 18

ACCEPTED MANUSCRIPT Our study supports the findings of Boeckel and Baumann (2008) and Malinverno et al. (2015), who showed members of the family Syracosphaeraceae contributing considerably to the frontal zone community. In the Pacific sector of the Southern Ocean, Saavedra-Pellitero et al. (2014) recorded 13 Syracosphaera species with relative coccosphere abundance up to 7.4%, and all being restricted to the SAZ. Findlay and Giraudeau (2000) documented ten

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Syracosphaera species in the Australian sector of the Southern Ocean. Our study

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corroborates the findings of Findlay and Giraudeau (2000) who showed the highest relative

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abundance of Syracosphaera species in tropical and subtropical waters and their absence south of the SAZ. Conversely, Mohan et al. (2008) indicated the rare occurrence of

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Syracosphaera spp. throughout their study region in the Indian Sector of the Southern Ocean.

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The maximum numbers of holococcolithophores observed in the ARFZ and the STZ confirm their preference for warm oligotrophic waters. The coccolithophore community in the Indian sector of the Southern Ocean is rather comparable in terms of abundance and

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species composition to those observed in the Atlantic and Australian Sectors of the Southern Ocean. However, in previous studies, high abundances of G. ericsonii, U. tenuis, Umbilicosphera irregularis, S. pulchra, Discosphaera tubifera, Michaelsarsia elegans,

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Coccolithus pelagicus, Ophiaster species etc. were observed in the SSTF and the SAF

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regions, but these species were either not observed, or present in low abundance, in our study. This difference could possibly be due to unfavorable conditions for these species in the Indian sector of the Southern Ocean. Coccolithophore assemblage in the SAZ and PFZ Coccolithophore diversity decreased and total coccolithophore abundance increased in the SAZ and PFZ. The increase in coccolithophore abundance is probably due to nutrient availability in the surface waters of the frontal zones as compared to surrounding areas, as 19

ACCEPTED MANUSCRIPT suggested previously by Gravalosa et al. (2008), Murphy (1995) and Pollard et al. (1995). The SAZ and PFZ assemblages are dominated by E. huxleyi morphotypes C and B/C. Compared to E. huxleyi morphotype A, these morphotypes are less calcified, delicate and consist of loosely attached coccoliths (Young et al., 2003; Mohan et al., 2008; SaavedraPellitero et al., 2014; Patil et al., 2014). The dominance of morphotypes C and B/C was

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previously recorded in various sectors of the Southern Ocean (Findlay and Giraudeau, 2000;

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Cubillos et al., 2007; Gravalosa et al., 2008; Mohan et al., 2008; Charalampopoulou, 2011;

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Patil et al., 2013; Malinverno et al., 2015), and a latitudinal shift of one E. huxleyi morphotype to another was previously recorded in various sectors of the Southern Ocean

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(Findlay and Giraudeau, 2000; Mohan et al., 2008). An increasing southward expanse of E.

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huxleyi has been observed in recent studies (Winter et al., 2014). In our study, the occurrence of E. huxleyi coccospheres was documented as far as the PFZ, but the presence of detached coccoliths was observed until 65°S. The occurrence of E.

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huxleyi morphotype C and B/C coccoliths at the southernmost station (S9), contrasting with the absence of coccospheres, suggests that coccoliths were either transported or that the E. huxleyi coccospheres in the southernmost station were very delicate and loosely attached and

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may therefore easily get broken during filtration. The decrease in E. huxleyi abundance and

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absence of other coccolithophore species south of the PF was attributed to low temperature, salinity and probably also low light intensity. The increase in diatom abundance in the high silicate regions has been suggested in previous studies as an explanation of the reduced coccolithophore abundance (Egge and Aksnes, 1992; Findlay and Giraudeau, 2000, Mohan et al., 2008). The recent increase in temperature, water stratification and decrease in oceanic pH is thought to affect biogeographic boundaries of marine organisms including coccolithophores. 20

ACCEPTED MANUSCRIPT Winter et al. (2013) compared the southernmost occurrence of E. huxleyi in the various studies carried out in the Southern Ocean (Hasle, 1960; McIntyre et al., 1970; Nishida, 1986; Winter et al., 1999; Findlay and Giraudeau, 2000; Eynaud et al., 1999; Gravalosa et al., 2008; Cubillos et al., 2007; Beaufort et al., 2011; Mohan et al., 2008; Patil et al., 2013) and hypothesize that this species may be more sensitive to recent environmental changes (ex.

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oceanic carbonate chemistry, increased availability of aqueous CO2). In the present study, we

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did not observe a southward expansion of E. huxleyi into polar waters as coccospheres were

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not documented south of the PFZ at temperatures below 1°C. Earlier, Patil et al. (2013) showed phytoplankton community structure changes during early to late austral summer

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related to seasonal changes in nutrient availability. We hypothesize that, the differences in coccolithophore species biogeographic distribution and abundance between our present and

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previous studies may be largely due to difference in sampling periods and seasonal changes in physico-chemical factors. Regional factors such as eddies and circulation patterns may also

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influence coccolithophore community structure in the different regions of the Southern Ocean

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and may cause their transport in to Antarctic coastal waters. The occurrence of large number of detached coccoliths of species for which no

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complete spheres were observed indicates that these species either existed at the study

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location or were transported from surrounding areas. Extensive studies need to be carried out in this regard to understand residence times of detached coccoliths in the water column and their transport by physical vectors. Moreover, the difference in species composition and standing stocks between the different zones in the austral summer period is probably governed by a combination of environmental factors rather than by single factor. Though temperature is observed to be the prime parameter responsible for increase in coccolithophore diversity at ARFZ and STZ, the limitation of nutrients in the surface waters may reduce their 21

ACCEPTED MANUSCRIPT standing stock. Conversely, the increase in E. huxleyi morphotypes B/C and C abundance in the SAZ and PFZ suggests that these morphotypes are adapted to low temperature and are capable to attain high standing stocks in nutrient rich waters. In this study, we did not find any significant relationship between coccolithophore species and pH.

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Conclusions

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Based on our observations the following conclusions can be drawn:

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1. A total of 39 taxa were recorded as complete coccospheres and 85 as coccoliths. E. huxleyi (86.7%) is the most abundant coccolithophore, whereas G. muellerae (2.6%),

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Syracosphaera rotula (1.5%), Umbellosphaera sibogae (1%), Syracosphaera spp. (2.3%), C. leptoporus subsp. small (1%), C. leptoporus spp. leptoporus (0.7%), P.

MA

galapagensis (1.5%), Syracosphaera histrica HOL (“Calyptrolithophora papillifera”) (1.1%), H. carteri Hol (0.6%) were commonly found, especially in the northern part

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of the investigated transect.

2. Maximum coccolithophores abundance was documented in the SAF and PF regions

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(up to 750x103 coccospheres/l). The number of coccospheres decreased towards the south of the PF where monospecific assemblages of E. huxleyi morphotypes C and

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B/C were found. At the southernmost station, only coccoliths of E. huxleyi morphotypes C and B/C were observed, whereas this station was devoid of coccospheres.

3. Most of the coccolithophore species recorded in this study were restricted to the ARFSSTF region and were documented in the upper 40m of the water column. Temperature and nutrient concentrations were identified as the most prominent factors

22

ACCEPTED MANUSCRIPT influencing coccolithophore diversity and distribution in the Indian sector of the Southern Ocean. 4. Coccolithophore biogeography of the Indian Sector of the Southern Ocean is comparable to other Southern Ocean sectors. Occurrence of different biogeographic

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boundaries of coccolithophore assemblages is due to seasonal variation and different timing of the sampling campaigns. The recent biogeographic coccolithophore

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distribution in different frontal zones of the Indian sector of the Southern Ocean

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provides valuable information for future paleoceanographic reconstructions.

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5. The poleward expansion of E. huxleyi as suggested in the previous studies was not observed in the present study.

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Acknowledgement

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The authors are thankful to the Secretary of the Ministry of Earth Sciences (MoES),

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Government of India and the Director of the ESSO-National Centre for Antarctic and Ocean Research for supporting the Southern Ocean expedition. We would also like to thank the chief scientist, Dr. N. Anilkumar and the expedition members for the support extended for

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our sampling needs. We gratefully acknowledge Captain Satishraja Rangaraja, Ebin James

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and other crew members of ORV Sagar Nidhi, for their support during the expedition. The authors would like to thank editor and both reviewers for their valuable comments. Dr. Shramik

would

like

to

thank

DST

Inspire

for

providing

funding

(DST/INSPIRE/04/2015/001969). This is NCAOR Contribution No. XXXX.

Appendix The supplementary data associated with this article can be found in the Appendix.

23

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ACCEPTED MANUSCRIPT Verbeek, J.W. 1989. Recent calcareous nannoplankton in the southernmost Atlantic. Polarforschung 59 (1/2), 45-60. Westbroek, P., Brown, C.W., van Bleijswijk, J., Brownlee, C., Brummer, G.J., Conte, M., Egge, J., Fernández, E., Jordan, R., Knappertsbusch, M., Stefels, J., Veldhuis, M., van

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der Wal, P., Young, J., 1993. A model system approach to biological climate forcing. The example of Emiliania huxleyi. Global and Planetary Change, 8, 27-46.

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Sea. Deep-Sea Research I, 46(3), 439-449.

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Winter, A., Elbrächter, M., Krause, G., 1999. Subtropical coccolithophores in the Weddell

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Winter, A., Henderiks, J., Beaufort, L., Rickaby, E.M., Brown, C.W., 2014. Poleward expansion of the coccolithophore Emiliania huxleyi. Journal of Plankton Research,

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36(2), 316-325.

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Winter, A., Jordan, R.W., Roth, P.H., 1994. Biogeography of living coccolithophores in

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ocean waters. In: Winter, A., Siesser, W.G. (Eds.), Coccolithophores. Cambridge University Press, Cambridge, pp. 161-177.

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Young, J.R., Geisen, M., Cros, L., Kleijne, A., Sprengel, C., Probert, I., Ostengaard, J., 2003. A guide to extant coccolithophore taxonomy. Journal of Nannoplankton Research,

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Special Issue 1. International Nannoplankton Association, London. 125pp.

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Fig. 1. Location of water samples. Red dots represent vertical profile stations (S1-S9) and white dots represents surface water samples collected during the austral summer of 2010. Location of fronts after Orsi et al. (1995), Anilkumar et al. (2006) and Luis and Sudhakar, (2009). ARF, Agulhas Retroflection Front; SSTF, Southern Subtropical Front; SAF, Subantarctic Front; PF, Polar Front. The different oceanographic frontal zones are indicated as, ARFZ, Agulhas Retroflection Frontal Zone; STZ, Subtropical 32

ACCEPTED MANUSCRIPT Zone; SAZ, Subantarctic Zone; PFZ, Polar Frontal Zone; AZ, Antarctic Zone. SST image source- SST image source — http://oceancolor.gsfc.nasa.gov/cgi/l3. The white dotted contour is the sea ice extent in November 2009 inferred from monthly HadISST global sea ice data

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(http://badc.nerc.ac.uk/view/badc.nerc.ac.uk__ATOM__dataent_hadisst).

Fig. 2 Plots showing abundances of total coccospheres, total coccoliths and number of species (shaded area) observed both as coccospheres and coccoliths.

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Fig. 3a. Densities of major coccolithophore taxa between surface and 110m water depth. 35

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Fig. 3b. Physico-chemical parameters [temperature (°C); salinity; NO2, PO4, NO3, SiO4 (values in μM); and pH] measured during the austral summer of 2010 in the Southern Indian Ocean.

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Fig. 4. Ordination diagram based on Canonical Correspondence Analysis (CCA) of the

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coccolithophore community in the study region. The variables (temperature, salinity, nitrate, nitrite, phosphate, silicate and pH) are indicated by arrows, labeled temp, sal,

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NO2, NO3, PO4, SiO4 and pH respectively.

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ACCEPTED MANUSCRIPT Table 1. Sample locations, sampling depths, number of coccospheres and coccoliths documented per litre, in situ temperature and salinity Sampling Collection Latitude Longitude depth Total Total Temperature Station date (°S) (°E) (m) coccospheres/l coccoliths/l (°C) Salinity

S6

5-Feb-10 5-Feb-10 6-Feb-10

91 124 120 83 38 18 115 143 79 144 56 33 42 92 251 56 122 94 75 42 286 105 142 174 106 46 765 642 97 83 66 18 232 85 758 914 279 235

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4-Feb-10

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S5

84 104 22 6 18 15 15 89 32 83 23 22 24 9 155 18 38 38 29 7 130 23 40 46 36 39 707 362 49 28 36 11 40 28 742 745 168 139

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2-Feb-10

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S4

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2-Feb-10 2-Feb-10

surface 20 40 60 80 110 surface surface 20 40 60 80 110 surface surface 20 40 60 80 110 surface 20 40 60 80 110 surface 20 40 60 80 110 surface surface surface 20 40 60

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S3

57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3

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S2

1-Feb-10 1-Feb-10

39 39 39 39 39 39 40 41 41 41 41 41 41 42 43 43 43 43 43 43 44 44 44 44 44 44 45 45 45 45 45 45 46 47 48 48 48 48

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31-Jan-10

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S1

18.4 18.0 17.9 16.8 15.8 15.0 17.5 16.5 16.6 16.5 16.5 16.2 15.3 16 11.6 16.7 16.7 16.6 15.9 15.1 12.4 11.8 12.0 12.0 8.5 7.5 11.1 11.1 11.2 9.4 9.8 9.1 10.5 10.5 7.2 7.2 7.2 7.2 38

35.30 35.38 35.39 35.42 35.43 35.44 35.33 35.40 35.43 35.44 35.45 35.45 35.45 35.4 35.37 35.41 35.47 35.48 35.48 35.49 33.95 34.02 34.08 34.17 34.21 34.25 33.93 33.94 34.02 34.07 34.34 34.51 33.82 33.76 33.72 33.72 33.72 33.73

ACCEPTED MANUSCRIPT

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189 149 104 18 18 548 523 554 97 232 98 56 13 1 246 237 466 35 212 2 9 6 1 0 0 0 0 0 0 1 3 0 0 0

PT

RI

109 97 24 15 15 361 325 314 63 153 63 2 16 4 162 144 276 20 124 1 11 9 2 0 0 0 0 0 0 0 0 0 0 0

SC

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80 110 surface surface surface surface 20 40 60 80 110 surface surface surface surface 20 40 60 80 110 surface surface surface surface surface surface surface surface surface 20 40 60 80 110

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S9

12-Feb-10 12-Feb-10 13-Feb-10 13-Feb-10 14-Feb-10 14-Feb-10 15-Feb-10 15-Feb-10 18-Feb-10

57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 57.3 41.09 41.09 41.09 41.09 41.09 41.09

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S8

9-Feb-10 9-Feb-10 10-Feb-10 11-Feb-10

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S7

7-Feb-10 7-Feb-10 8-Feb-10 8-Feb-10

48 48 49 50 51 52 52 52 52 52 52 53 54 55 56 56 56 56 56 56 57 58 59 60 61 62 63 64 65.49 65.49 65.49 65.49 65.49 65.49

6.5 4.6 7 5 5 4.4 4.2 3.4 3.3 3.2 2.3 4 3.5 3 2.7 2.6 2.6 2.6 2.0 0.6 3 2 1.5 2 1.5 1.5 1 1.5 -0.7 -0.6 -0.6 -0.7 -0.6 -1.5

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33.74 33.80 33.69 33.78 33.77 33.87 33.88 33.88 33.88 33.88 33.91 33.83 33.86 32.82 33.94 33.95 33.95 33.95 33.95 34.00 32.38 32.54 33.63 33.59 33.22 33.69 33.69 33.67 33.56 33.59 33.69 33.75 33.90 34.33

ACCEPTED MANUSCRIPT Table 2 Criteria utilized for the identification of oceanic fronts Adopted property indicators for the identification of oceanic fronts Temperature (°C) Salinity

Frontal Structure

References

Consistent value of surface salinity ~35.5

Belkin and Gordon (1996); Holiday and Read(1998); Kostianoy et al. (2004)

Agulhas Return Front (ARF)

35.39-35.54 at surface; 34.9035.57 at 200m depth

Holiday and Read (1998); Belkin and Gordon (1996); Sparrow et al. (1996); Kostinoy et al. (2004)

9°C-10°C at surface; 4.8°C-8.4°C at 200m

Subantarctic Front (SAF2)

8°C-9°C at surface, 4° isotherm at 200m depth

Polar Front (PF1)

4°C-5°C at surface, northern limit of the 2°C isotherm below 200m

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Subantarctic Front (SAF1)

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Polar Front (PF2)

2°C-3°C at Surface

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34.04-35.35 at surface; 34.6-35 at 100m; 34.42-34.92 at 200m 33.85-34.0 at surface; 34.1134.40 at 200m

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Southern Subtropical 11°C-17°C at surface, Front (SSTF) 10°C-12°C at 100m

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17°C-19°C at surface; 10° isotherm from 300 to 800m

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Northern Subtropical 21°C-22°C at surface Front (NSTF)

Consistent value of surface salinity ~33.85 south of the SAF 33.8-33.9 at surface

33.8-33.9 at surface

Holiday and Read (1998); Belkin and Gordon (1996); Sparrow et al. (1996); Kostianoy et al. (2004) Holiday and Read (1998); Belkin and Gordon (1996); Sparrow et al. (1996); Kostianoy et al. (2004); Park et al. (1993) Holiday and Read (1998); Peterson and Whitworth (1989); Kostianoy et al. (2004) Holiday and Read (1998); Belkin and Gordon (1996); Sparrow et al. (1996); Kostianoy et al. (2004) Holiday and Read (1998); Kostianoy et al. (2004)

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ACCEPTED MANUSCRIPT Table 3. Two-way ANOVA to evaluate the variation in abundance, species richness, evenness and species diversity of coccolithophores in the sampling locations. Values in bold indicate significant differences. SS

df

MS

F

P-value

F crit

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472061.2 5 94412.23 5.383519 0.000896 2.485143 485195 7 69313.57 3.952358 0.002812 2.285235 613804.5 35 17537.27 1571061 47

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2.163531 5 0.432706 0.942931 0.465623 2.485143 26.20533 7 3.743618 8.157898 7.12E-06 2.285235 16.06132 35 0.458895 44.43018 47

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0.367349 5 0.07347 2.265938 0.069254 2.485143 1.521259 7 0.217323 6.702615 4.62E-05 2.285235 1.134825 35 0.032424 3.023433 47

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0.192813 5 0.038563 1.843889 0.129723 2.485143 1.794144 7 0.256306 12.25539 8.46E-08 2.285235 0.731982 35 0.020914 2.718939 47

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Source of Variation Abundance (N) Depth Station Error Total Species richness (d) Depth Station Error Total Species evenness (J') Depth Station Error Total Species diversity (H') Depth Station Error Total

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ACCEPTED MANUSCRIPT

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ACCEPTED MANUSCRIPT Plate. 1. (A) Emiliania huxleyi morphotype A, (B) Emiliania huxleyi morphotype B/C, (C) Emiliania huxleyi morphotype C, (D) Emiliania huxleyi type D, (E) Gephyrocapsa muellerae, (F) Gephyrocapsa ornata, (G) Calcidiscus leptoporus spp. leptoporus, (H) Calcidiscus leptoporus small type, (I) Syracosphaera molischii, (J) Umbellosphaera tenuis type II, (K) Polycrater galapagensis, (L) Poricalyptra aurisinae, (M) Helicosphaera carteri

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HOL (solid), (N) Poricalyptra gaarderiae, (O) Homozygosphaera vercellii.

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ACCEPTED MANUSCRIPT Appendix

Table 1. List of coccolithophore species found as coccospheres or coccoliths in the study. (ARFAgulhas Retroflection Front; SSTF- Southern Subtropical Front; SAF- Subantarctic Front; PFPolar Front) Sr. Occurrence as Occurrence Occurrence of coccospheres Coccolithophore species No coccospheres as coccoliths ARF SSTF SAF PF

T P

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

Emiliania huxleyi morphotype A Emiliania huxleyi morphotype B Emiliania huxleyi morphotype C Emiliania huxleyi morphotype B/C Emiliania huxleyi type D Emiliania huxleyi var. corona Acanthoica acanthos Acanthoica biscayensis Acanthoica cidaris Acanthoica quattrospina Algirosphaera cucullata Algirosphaera robusta Alisphaera extenta Alisphaera unicornis Alveosphaera bimurata Calcidiscus leptoporus spp. small Calcidiscus leptoporus

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Calcidiscus quadriperforatus

+ + + + + + +

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C C

A

+ +

+ + + + + +

+

C S U

N A

M

+ + + + + + + + + +

+ + + + +

+ +

I R

+

max coccosphere nos x103/l 17.98 15.33 659.14 292.60 20.02

+

+

+ + +

+ + +

+ + +

+

+ +

1.74 1.05

+ +

15.29 3.40

+ +

max coccolith nos x105/l 8.58 2.60 847.99 370.41 27.46 0.30 37.11 1.84 7.14 1.06 5.07 14.35 5.61 0.05 8.44 21.01 0.42 44

ACCEPTED MANUSCRIPT 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45

Calciopappus caudatus Calciosolenia brasiliensis Calciosolenia murrayi Coronosphaera mediterranea Cyrtosphaera aculeatae Cyrtosphaera lacaliae Discosphaera tubifera Gephyrocapsa mullerae Gephyrocapsa ornata Helicosphaera carteri Michaelsarsia adriaticus Michaelsarsia elegans Oolithotus antillarum Oolithotus fragilis Ophiaster formosus Ophiaster hydroideus Palusphaera vandelii Papposphaera sp. type 4 Polycrater galapagensis Pontosphaera discopora Pontosphaera multipora Prymnesium neolepis Rhabdosphaera clavigera Rhabdosphaera xiphos Syracosphaera anthos Syracosphaera anthos BCs Syracosphaera corolla

+ + + + +

+ +

+

D E

T P E

C C

A

+ + + + +

+

+ + + + + + + + + + + + + + + + + + + + +

+

1.57 + +

+ +

M

+

T P

I R

C S U

N A + +

+

+

+

+

1.77 0.73 4.72 3.45

1.10 3.40

1.05 +

+

5.26

2.44 3.11 2.58 2.80 0.31 0.27 6.39 1.80 0.69 9.23 41.37 2.03 8.06 8.35 17.60 3.03 4.44 0.05 0.45 0.04 0.72 0.89 21.51 2.67 8.32 1.43 45

ACCEPTED MANUSCRIPT 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72

Syracosphaera delicata Syracosphaera dilatata Syracosphaera exigua Syracosphaera exigua BCs Syracosphaera halldalii Syracosphaera histrica Syracosphaera marginaporata Syracosphaera molischii Syracosphaera nana Syracosphaera nodosa Syracosphaera nodosa type C Syracosphaera nodosa type A Syracosphaera nodosa type A XCs Syracosphaera ossa type 1 Syracosphaera ossa type 2 Syracosphaera pirus Syracosphaera protrudens Syracosphaera pulchra Syracosphaera rotula Syracosphaera rotula XC Syracosphaera tumularis Umbellosphaera irregularis Umbellosphaera tenuis type I Umbellosphaera tenuis type II Umbellosphaera tenuis type IIIa Umbellosphaera tenuis type IIIb Umbilicosphaera foliosa

+

+

+ + +

T P E +

C C

A

D E

+ +

+ + + + + + + + + + + + + + +

+

+

+

+

1.32

+

0.65

+

2.10 1.07

+

5.75

+

+

T P

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C S U

N A

M

+ + + + + + + + + + +

1.57

+

2.00 +

6.47

0.03 4.83 2.10 15.08 8.49 0.26 2.89 3.91 20.00 3.22 9.12 3.32 1.65 2.61 1.83 0.14 1.83 15.11 0.83 3.21 1.28 0.82 7.09 0.17 4.72 0.33 46

ACCEPTED MANUSCRIPT 73 74

Umbilicosphaera hulburtiana Umbilicosphaera sibogae

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undescribed heterococcolithophore A (Young et al., 2003) Syracosphaera histrica HOL (“Calyptrolithophora papillifera”) Corisphaera gracilis Corisphaera tyrheniensis Coronosphaera mediterranea HOL gracillima type Helicosphaera carteri HOL solid ("Syracolithus catilliferus") Homozygosphaera spinosa Homozygosphaera vercellii Poricalyptra aurisinae Poricalyptra gaarderiae Poritectolithus maximus Syracosphaera anthos HOL (Periphyllophora mirablis) Zygosphaera marsilli

76 77 78 79 80 81 82 83 84 85 86 87

+ +

+

+

4.39

+ +

+ +

+ +

+

+

+

+

+

+

+ + + + +

+ + + + +

PT

E C

7.55

+

D E

+ +

2.42 6.59

+

+

I R

+ +

N A

C S U

M

+ + + +

+

+

+

+

+ + + + +

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+ +

3.59 2.52 1.30

20.35 6.09 3.25

1.36

3.66

1.43 1.50 1.37 0.88 1.00 0.62

20.09 12.90 17.11 4.20 8.52 7.09

0.85 0.83

4.86 2.78

C A

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ACCEPTED MANUSCRIPT Table 2. ANOVA (two-factor without replication) for species abundance, species richness, species evenness and species diversity during the study period

Summary 0 20 40 60 80 110

T P

Species abundance (N)

Species richness (d)

Species evenness (J')

Species diversity (H')

CN

Sum

Ave

Var

Sum

Ave

Var

Sum

Ave

Var

Sum

8 8 8 8 8 8

2430 1753 990 363 527 257

303 219 123 45 65 32

74966 62999 13328 1732 2884 1087

9.5 12.6 11.1 9.6 7.3 8.7

1.1 1.5 1.3 1.2 0.9 1.1

0.65 1.51 1.36 0.53 0.33 1.63

3.0 4.7 4.5 5.1 3.9 3.7

0.3 0.6 0.6 0.6 0.5 0.4

0.01 0.03 0.05 0.05 0.06 0.16

2.5 3.8 3.6 3.3 2.6 2.8

0.3 0.5 0.4 0.4 0.3 0.3

0.02 0.08 0.07 0.03 0.04 0.11

0.01 0.03 0.03 0.02 0.03 0.02 0.03 0.10

3.8 3.5 3.2 3.5 1.0 1.2 1.2 1.3

0.6 0.6 0.5 0.6 0.1 0.2 0.2 0.2

0.02 0.04 0.03 0.03 0.02 0.02 0.01 0.01

D E

T P E

A

C C

C S U

M

N A

S1 6 249 41 1721 11.9 1.9 0.70 4.5 0.7 S2 6 273 45 1000 10.2 1.7 0.83 4.2 0.7 S3 6 285 47 2917 12.4 2.0 1.25 3.7 0.6 S4 6 314 52 1505 12.3 2.0 0.51 3.7 0.6 S5 6 1193 198 79657 3.8 0.6 0.15 1.5 0.2 S6 6 2000 333 101551 3.4 0.5 0.14 1.8 0.3 S7 6 1279 213 18649 2.9 0.5 0.01 2.2 0.4 S8 6 727 121 10168 1.8 0.3 0.04 3.2 0.5 (CN= Count; Ave= Average; Var= Variance) (Species abundance Sum- nos x103)

I R Ave

Var

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Table 4. Interset correlations between environmental variables and site scores

Temperature Salinity NO2 PO4 NO3 SiO4 pH

Envi. Axis 1 0.632 0.7 -0.318 -0.419 -0.508 -0.191 0.392

T P

I R

Envi. Axis 2 -0.021 0.084 -0.156 0.236 -0.223 -0.163 -0.054

C S U

N A

D E

M

T P E

C C

A

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ACCEPTED MANUSCRIPT Highlights

1. 39 species as complete coccospheres and coccoliths of 85 species were documented. 2. Maximum coccolithophore diversity occurs at SSTF, SAF and lowest at south of PF zone 3. E. huxleyi morphotypes C and B/C dominates south of SAF zone 4.

T P

I R

Poleward expansion of E. huxleyi as suggested in the recent studies was not recorded.

C S U

N A

D E

M

T P E

C C

A

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