Vertical and lateral variations in coccolithophore community structure across the subtropical frontal zone in the South Atlantic Ocean

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Marine Micropaleontology 67 (2008) 255 – 273 www.elsevier.com/locate/marmicro

Vertical and lateral variations in coccolithophore community structure across the subtropical frontal zone in the South Atlantic Ocean Babette Boeckel ⁎, Karl-Heinz Baumann Department of Geosciences, Universität Bremen, PO Box 33 04 40, 28334 Bremen, Germany Received 1 November 2007; received in revised form 28 January 2008; accepted 31 January 2008

Abstract In this study the coccolithophore compositions of 11 plankton depth stations along a N–S transect from the South Atlantic Subtropical Gyre to the Subantarctic Zone were examined qualitatively and quantitatively. The lateral and vertical distribution patterns of not only the most abundant taxa but also of the morphotypes of distinct species complexes, such as Calcidiscus leptoporus, Emiliania huxleyi, and Umbellosphaera tenuis were the focus. Geographic variation among morphotypes mirrors different ecological affinities of the members of a species complex. Multivariate statistics were used to infer the relationship between a set of known environmental data and species concentrations. The results of the detrended Canonical Correspondence Analysis (CCA) revealed the presence of distinct species assemblages. The Subtropical Gyre assemblage within the upper 50 m of the photic zone is mainly composed of Umbellosphaera irregularis, U. tenuis types III and IV, Discosphaera tubifera, Rhabdosphaera clavigera, S. pulchra and E. huxleyi var. corona, adapted to warm and oligotrophic conditions. In the deeper photic zone abundant Florisphaera profunda, Gephyrocapsa ericsonii and Oolithotus spp. are encountered, benefiting from higher nutrient concentrations in the vicinity of the nutricline. A well-defined Subtropical Frontal Zone (STFZ) association is clearly dominated by E. huxleyi types A and C throughout the upper 100 m of the water column. Secondary contributors in the upper photic zone are Syracosphaera spp. (mainly S. histrica, S. molischii), Michaelsarsia elegans, Ophiaster spp. and U. tenuis type II. This assemblage is associated with cooler, nutrient-rich waters. E. huxleyi type B is found deeper in the water column. Here it is accompanied by Algirosphaera robusta, G. muellerae, and S. anthos indicating a tolerance of lower light availability in environments with elevated productivity. C. leptoporus spp. leptoporus shows relatively high cell numbers in all sampled water levels throughout the STFZ. Interestingly, its coccoliths are often smaller 5 μm in lith diameter. The mean coccolithophore assemblages of a station were compared to the underlying surface sediment assemblages. For the most part, the distribution of the morphotypes is reflected in the sedimentary archive, thus proving their potential as paleoecological proxies. © 2008 Elsevier B.V. All rights reserved. Keywords: coccolithophore; coccoliths; morphotypes; ecology; surface sediments; South Atlantic

1. Introduction ⁎ Corresponding author. Tel.: +49 421 218 3947; fax: +49 421 218 7134. E-mail address: [email protected] (B. Boeckel). 0377-8398/$ - see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.marmicro.2008.01.014

Living coccolithophores belong to the phylum Haptophyta, division Prymnesiophyceae (Jordan and Chamberlain, 1997). As unicellular, photosynthetic organisms,

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they are bound to the sun-lit upper layer of the world oceans. According to the hydrographic conditions in the photic zone there are characteristic coccolithophore assemblages thriving in the upper 220 m of the water column (Winter et al., 1994). This phytoplankton group is capable of tolerating a wide range of ecological conditions (Brand, 1994). Besides their importance as primary producers in oligotrophic areas coccolithophores reach considerable importance in high productivity regions (e.g. Mitchell-Innes and Winter, 1987; Giraudeau and Bailey, 1995; Broerse et al., 2000). Their cell-covers, composed of calcite platelets, the coccoliths are preserved in the sedimentary record and store valuable information on palaeoenvironmental conditions from the photic zone (McIntyre and Bé, 1967; Roth, 1994; Baumann et al., 1999; Boeckel et al., 2006). Although plankton samples from the water column only provide snap-shots of the community structure, they provide essential information on the composition of coccolithophore assemblages, their distribution, and the ecology of different species necessary for the application of coccoliths in paleoceanographic reconstructions. In their fundamental work McIntyre and Bé (1967) established a latitudinal biogeographic nannoplankton zonation based on differences in assemblage composition. The boundary between their subtropical and temperate zones approximately parallels the Subtropical Front, where the warm and oligotrophic Subtropical Gyre waters meet the cold, nutrient-rich Antarctic waters. This study particularly focuses on the lateral and vertical coccolitho-

phore distribution patterns within the upper 150 m of the water column along a North–South transect across the Subtropical Gyre to the Subtropical Frontal Zone in the South Atlantic along a longitude of 13° to 24°W. The chosen sampling period covers austral late summer to fall, a season where the Subtropical Front occupies a rather southward position. During that phase nanophytoplankton (1–20 µm) usually dominates the algal communities at the frontal areas (Laubscher et al., 1993). Long-term time-series to assess the variability in plankton processes have been undertaken within the Atlantic Meridional Transect (AMT) programme (e.g. Aiken et al., 2000; Robinson et al., 2006). A number of regionally constrained plankton studies have focused on the phytoplankton composition in the surface-layer of frontal systems, such as the Eastern Atlantic Subtropical Front by Eynaud et al. (1999), the Weddell Sea by Winter et al. (1999) and the Australian sector of the Southern Ocean by Findlay and Giraudeau (2000). Since the elementary work by McIntyre and Bé (1967), who provided a vast amount of fundamental knowledge on the distribution patterns and ecology of living coccolithophores, the taxonomic concepts of several taxa have been thoroughly revised. DNA-based studies have revealed that biodiversity had been underestimated in most groups of pelagic organisms (De Vargas et al., 2002). Former taxonomic entities have been split up into species or subspecies based on molecular evidence and life-cycle associations (Geisen et al., 2002; Sáez et al., 2003; Geisen et al., 2004). These findings often originated from the

Fig. 1. Schematic map of the circulation in the upper levels of the South Atlantic (after Peterson and Stramma, 1991; Orsi et al., 1995; Belkin and Gordon, 1996). Locations of plankton stations indicated as circles. SEC = South Equatorial Current, SECC = South Equatorial Counter Current, BOC = Benguela Oceanic Current, NSTF = Northern Subtropical Front, SAC = South Atlantic Current, SSTF = Southern Subtropical Front, SAF = Subantarctic Front, ACC = Antarctic Circumpolar Current.

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detection of intra-specific, fine-scale morphological differences within major coccolithophore taxa, such as Calcidiscus leptoporus, Emiliania huxleyi, Umbellosphaera tenuis (e.g., Young and Westbroek, 1991; Kleijne, 1993). The various morphotypes of a species complex are likely to express distinct ecological preferences. So far fine-scale species-level diversity has mostly been disregarded in coccolithophore counts. Therefore the ecological tolerances inferred for major coccolithophore species seem rather broad. Only a few studies (Kleijne, 1993; Bollmann, 1997; Knappertsbusch et al., 1997; Renaud et al., 2002; Hagino and Okada, 2006; Boeckel et al., 2006) addressed the ecological affinities of the morphological varieties within a species complex. To reveal the complex relationship between coccolithophore taxa and environmental conditions, we applied multivariate analysis in this study. Particular attention is paid to the morphotypes of the species com-

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plexes of C. leptoporus, E. huxleyi, and U. tenuis in order to elucidate whether the respective morphotypes exhibit unequal environmental affinities. Furthermore, the results from the plankton assemblages are compared to surface sediment assemblages in order to evaluate their potential for paleoceanographic reconstructions. 2. Oceanographic setting Hydrographically the studied transect is under the influence of three large-scale regimes, subequatorial waters, the South Atlantic Subtropical Gyre and the Southern Ocean (Fig. 1). The proximity of Subantarctic Surface Water to the much warmer and saltier Subtropical Surface Water produces pronounced meridional property gradients (Fig. 2). The positions of the nutricline and thermocline vary accordingly (Fig. 3). The transition from nutrient-depleted subtropical to

Fig. 2. Mean austral summer hydrographic parameters, such as (a) temperature, (b) nitrate concentration, and (c) phosphate concentration within the upper 200 m of the water column in a N–S transect of the South Atlantic at 15.5°W. Sampling positions are indicated as circles.

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Fig. 3. Mean monthly temperature and nitrate profiles (http://ingrid.ldeo.columbia.edu/SOURCES/.NOAA/.NODC/.WOA01/) for most of the studied plankton depth station. The grey bar indicates the position of the nutricline.

fresh subantarctic waters is extending over a large area of up to 4–5° latitude within the Subtropical Frontal Zone (STFZ; Smythe-Wright et al., 1998). The STFZ is variable in space and time with strong latitudinal shifts to the south in austral summer and to the north in winter. Its position varies seasonally by 2.5° latitude in the midSouth-Atlantic (Smythe-Wright et al., 1998). In the South Atlantic a Northern (NSTF) and a Southern Subtropical Front (SSTF) have been identified extending from the Brazil Current to the Agulhas– Benguela area (Belkin, 1993). The continuity of the zonal double structure across the South Atlantic has been summarised by Belkin and Gordon (1996). SmytheWright et al. (1998) state that within a longitude of 15° and 5°W the NSTF lies between 35 and 37°S and the SSTF at approximately 39°S. The double structure of the STFZ results from variations in mixing between the Subantarctic and Subtropical waters as a consequence of the large-scale wind-field and convective and advective thermohaline processes (Belkin and Gordon, 1996). The South Atlantic Current flows primarily in the top 1000 m between both fronts following two eastward jets. The particular values of the properties within fronts may be subject to both temporal and downstream changes as a result of gradual modification of the adjacent water masses by non-frontal processes, such as air–sea interaction, and cross-frontal mixing (Belkin and Gordon, 1996). To the north of the STFZ, the oceanic circulation is mainly controlled by the anticyclonic motion and position of the South Atlantic High pressure field (Peterson and Stramma, 1991). Waters south of the STFZ belong to the eastward flowing Antarctic Circumpolar Current, which is driven by the world's strongest westerly winds approximately at 45°–55°S (Trenberth et al., 1990).

3. Materials and methods 3.1. Coccolithophore analyses The water samples were collected during METEOR cruises, M41/2 and 3 in March to May 1998 and M46/4 in February to March 2000. A total of 58 filter samples from 11 different depth stations were studied (Table 1). Water samples were taken from NISKIN bottles of a rosette at different water depths between 10 and 150 m. The surface water sample at a depth of 5 m was taken from the vessel's membrane and Kreisel-pump systems. Generally, 2 l of water was filtered through cellulose nitrate filters (25 mm diameter, 0.45 µm pore size) by Table 1 Sampling date and location of investigated plankton samples Cruise Station Date

Latitude Longitude (S) (W)

M41-2 II III

27.03.1998 8.14 09.04.1998 12.93

14.54 15.68

M41-3 VII

09.05.1998 19.10

17.25

III

29.04.1998 23.83

16.27

M46-4 X

08.03.2000 31.60

24.51

IX

02.03.2000 33.83

23.58

VIII

02.03.2000 35.71

22.73

VII

28.02.2000 38.43

21.53

VI V IV

26.02.2000 39.95 25.02.2000 44.00 21.02.2000 44.51

18.16 13.07 21.72

Sampling depth (m) 5, 20, 50, 90, 150 5, 10, 20, 50, 100, 150, 200 5, 10, 20, 50, 100, 150 5, 10, 20, 50, 100, 150 5, 20, 50, 100, 150 5, 20, 50, 100, 120 5, 10, 20, 50, 100, 150 5, 20, 50, 100, 150 5, 20, 50, 100 5, 20, 50, 100 5, 20, 50, 100, 150

B. Boeckel, K.-H. Baumann / Marine Micropaleontology 67 (2008) 255–273 Table 2 Numbers of coccoliths per sphere for distinct species Taxa

Table 2 (continued ) Taxa

No. of liths per sphere min max mean N

Heterococcolith/nannolith bearing spheres Acanthoica quattrospina Acanthoica spp. Algirosphaera robusta Alisphaera capulata Alisphaera unicornis Calcidiscus leptoporus spp. leptoporus Calcidiscus leptoporus small type Calciosolenia brasiliensis Calciosolenia murrayi Coronosphaera binodata Coronosphaera mediterranea Discosphaera tubifera Emiliania huxleyi type a Emiliania huxleyi type b Emiliania huxleyi type c Emiliania huxleyi var. corona Florisphaera profunda Gephyrocapsa ericsonii Gephyrocapsa muellerae Gephyrocapsa oceanica Gephyrocapsa ornata Gladiolithus flabellatus Hayaster perplexus Helicosphaera carteri Helicosphaera hyalina Helicosphaera pavimentum Michaelsarsia elegans Michelsarsia spp. Neosphaera coccolithomorpha Oolithotus antillarum Oolithotus fragilis Ophiaster spp. Pappomonas sp. type 4 Polycrater galapagensis Pontosphaera multipora Rhabdosphaera clavigera Rhabdosphaera xiphos Syracosphaera ampliora Syracosphaera anthos Syracosphaera bannockii Syracosphaera corolla Syracosphaera halldalii Syracosphaera histrica Syracosphaera lamina Syracosphaera molischii Syracosphaera nana Syracosphaera nodosa Syracosphaera noroitica Syracosphaera ossa Syracosphaera prolongata Syracosphaera pulchra Syracosphaera rotula Syracosphaera sp. aff. ossa Syracosphaera sp. type D

26 30 20

259

72 40 60

100 150 20 38 10 30 74 180 21 96 22 88 25 82 14 68 14 88 16 96 10 54 20 100 12 28 8 42 20 26 12 22 30 108 36 76 16 26 22 28 16 24 24 80 20 46 18 40 12 28 14 60 20 72 46 50 100 400 15 36 30 50 20 60 36 90 36 84 24 66 44 128 16 104 30 42 16 60 16 44 35 58 40 44 24 60 50 120 32 80 36 46 24 50 40 68

48 34 32 66 126 29 21 120 79 68 43 47 24 36 50 20 62 15 19 23 17 56 47 21 25 20 48 36 29 19 32 47 48 225 38 27 38 31 53 49 42 76 47 36 38 26 42 42 35 73 45 41 37 56

13 3 34 1 3 4 16 4 1 3 6 46 66 13 210 55 86 21 17 2 6 14 4 6 3 2 21 6 5 22 16 46 2 4 1 33 7 11 20 5 5 4 18 2 33 5 5 4 8 8 22 2 3 5

No. of liths per sphere min max mean N

Heterococcolith/nannolith bearing spheres Syracosphaera tumularis Tetralithoides quadrilaminata Turrilithus latericioides Umbellosphaera irregularis Umbellosphaera tenuis Umbilicosphaera anulus Umbilicosphaera foliosa Umbilicosphaera hulburtiana Umbilicosphaera sibogae Average HET sphere Holococcolith bearing spheres Antosphaera sp. aff. fragaria Calcidiscus leptoporus spp. leptoporus HOL Calyptrolithina multipora Corisphaera gracilis Corisphaeratyrheniensis Helicosphaera carteri HOL Helladosphaera conifera Helladosphaera pienarii Homozygosphaera sp. Homozygosphaera triarcha Poricalyptra aurisinae Poricalyptra isselii Syracosphaera anthos HOL Syracolithus quadriperforatus Syracosphaera pulchra HOL oblonga type Syracosphaera pulchra HOL pirus type Zygosphaera amoena Average HOL sphere

22

42

14 15 50

42 54 60

16 44

30 86

34 108 24 76 28 90 30 86

20 30 80 156 44 200 56

66

82 100 90 104

32 54 116 26 25 52 18 23 68 47

28 63 53 46 56 38 72 25 118 148 70 60.5 126 91 97 32 70

4 1 1 169 150 3 1 14 7

1 4 6 4 8 1 1 2 2 4 1 4 1 3 2 1

means of a vacuum pump immediately onboard. Without washing, rinsing or chemical conservation the filters were dried at 40 °C for at least 24 h and then kept permanently dry with silica gel in transparent film. A small filter piece (~ 0.5 cm2) was cut and mounted on an aluminium stub. The gold/palladium sputtered stubs were inspected qualitatively and quantitatively for coccolithophores using a Zeiss DSM 940A (Scanning Electron Microscope) at magnifications of 3000 or 5000×. The identification of the taxa is based on the taxonomy by Young et al. (2003). In a first step the coccoliths were counted on an arbitrarily chosen transect, aiming at a total number of 500 coccoliths. Apart from the coccospheres already encountered on the coccolith transect, up to 100 additional coccospheres were counted on a separate transect. In order to determine the number of coccoliths per coccosphere, the visible liths of an intact sphere were counted and doubled (Table 2). These numbers were then used to convert coccolith numbers into sphere units. The third step involved the assessment of the relative percentage of morphotypes in the plankton and the underlying surface

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Table 3 Surface sediment samples investigated for morphotypes Surface sediment sample

Latitude

Longitude

Water depth (m)

GeoB2911 GeoB1903 GeoB5136 GeoB5140 GeoB5112 GeoB6429 GeoB6422 GeoB6418 GeoB6410

11.50° N 8.68° S 19.02° S 19.02° S 23.02° S 31.95° S 35.71° S 38.43° S 44.52° S

21.04° W 11.84° W 12.07° W 16.10° W 15.93° W 24.25° W 22.73° W 21.54° W 20.09° W

5020 3161 3227 3660 3841 4335 3972 4126 4038

sediment samples (Table 3). Therefore, 30 to 100 specimens of a species complex were counted. In badly preserved surface sediment samples, fragments of the delicate species, U. tenuis, were included. Most of the surface sediment samples have already been described for their coccolith composition in Boeckel et al. (2006). Coccolithophore concentrations were calculated following the formula (e.g. Andruleit, 1996): C¼

F N AV S

where C = absolute number of coccosphere units l− 1seawater; F = effective filtration area (mm2); N = number of

coccoliths counted; A = investigated filter area (mm2); V = filtered water volume (l); S = average species-specific number of liths per sphere. Data presented here are archived in the PANGAEA database (www.pangaea.de). 3.2. Multivariate analysis A detrended canonical correspondence analysis (CCA), included in the statistical package, CANOCO 4.5 for Windows (Ter Braak and Smilauer, 2002), was carried out for a summarised interpretation of species abundance data in relation to known environmental variables. This ordination technique is based on the assumption that species respond unimodally to changing environmental gradients. The ordination axes are constrained to be linear combinations of the environmental variables. The statistical significance of the species–environment canonical relationship was inferred from Monte Carlo permutation tests. For the CCA only those environmental variables were selected that best explain the assemblage composition. Therefore, parameters were omitted from further multivariate statistics, which in previous statistical examination had proven to be of minor importance, like salinity, or showed strong co-variation with other variables, like the co-varying concentrations of the macro-nutrients, phosphate and nitrate. Exclusively

Fig. 4. Total coccolithophore abundance (in sphere units), number of intact coccospheres, the Shannon diversity index, the number of species and the concentrations of the cells in their holococcolith-bearing stage are displayed in a latitudinal section at selected water depths.

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the latter one was chosen for further statistical analysis. While temperatures were measured in situ, monthly nutricline depth, nitrate and seasonal chlorophyll concentrations were extracted from the World Ocean Atlas (http://ingrid.ldeo.columbia.edu/SOURCES/.NOAA/. NODC/.WOA01/) for the respective sampling months and depths.

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The species incorporated in the multivariate analysis include not only the most abundant taxa, but also the constituents of the morphological groups that were sometimes rarely present in the studied material. Taxa with low concentrations below 1.5 × 103 sphere units l− 1 contributing less than 8% to the species assemblage were excluded from the analysis.

Fig. 5. Concentrations of those taxa most abundant within the Subtropical Gyre waters, such as U. irregularis, S. pulchra, U. tenuis types I and III, R. clavigera, D. tubifera, G. ericsonii, F. profunda, O. antillarum, and O. fragilis. The abundances of a species at different water depths are displayed in stacked diagrams.

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4. Results 4.1. Total coccolithophore abundance and species diversity Highest cell numbers (up to 179.4 × 10 3 sphere units l − 1 ) were encountered south of the NSTF within the frontal zone (Fig. 4). Within the upper 50 m of the water-column coccolithophore concentrations are higher in the frontal zone than in the Subtropical Gyre region. Mean coccolithophore concentrations in the Subtropical Gyre are about 25 × 103 sphere units l− 1, whereas average coccolithophore numbers add up to 82 × 103 sphere units l− 1 in the frontal waters. Only in the deeper waters (N150 m) higher numbers are encountered in the transitional zone between Gyre and STFZ (32 to

36°S). Lowest values (8.6 × 103 sphere units l− 1) are found in the deeper photic zone of the STFZ. An essentially analogous pattern is shown by the number of intact spheres. A total of 112 different taxa were identified in the studied samples. On average a coccolithophore assemblage is composed of 14 different species. The number of species ranges from 8 to 21 per sample. The Shannon diversity index, which takes into account the abundance of the species, indicates highest diversities in the southernmost Subtropical Gyre Station M46-4 IX (7–100 m samples) and the southernmost station of the study area M46-4 IV (20 and 50 m; Fig. 4). A remarkable decrease in diversity is recorded at the frontal zone with low values persisting further south. At the southernmost station the Shannon Index again indicates higher diversities.

Fig. 6. Concentrations of C. leptoporus morphotypes and E. huxleyi types A, B, C and variant corona. The abundances of a species at different water depths are displayed in stacked diagrams.

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Cells in their holococcolith-bearing stage are encountered in the upper 100 m of the water column (Fig. 4). They occur only sporadically in the studied samples with highest cell numbers of 7.4 × 103 sphere

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units l− 1 in the upper 5 m of the STFZ. Apart from that, holococcolith-bearing cells are mostly found in the Gyre waters where they reach a maximum of 3.0 × 103 sphere units l− 1.

Fig. 7. Concentrations of taxa most abundant within the frontal waters, such as Ophiaster spp., M. elegans, S. histrica, S. molischii, S. anthos, U. tenuis types II and IV, A. robusta, G. muellerae, U. sibogae, and U. foliosa. The abundances of a species at different water depths are displayed in stacked diagrams.

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4.2. Coccolithophore species 4.2.1. Assemblage composition Out of 112 taxa observed, only 16 species, not including morphotypes or subspecies, reach considerable cell numbers. These species occur in cell concentrations of at least 1.5 × 103 sphere units l− 1 and contribute a minimum of 8% to the assemblage in at least

one sample. According to their lateral and vertical distribution patterns these taxa can be roughly assigned to certain communities. The upper to middle photic zone Subtropical Gyre community (5 to 50 m, latitude: 8°–34°S; Fig. 5) is dominated by Umbellosphaera irregularis (maximum concentration: 26.0 × 103 sphere units l− 1). Significant contributors to the assemblage are E. huxleyi var. corona,

Plate I. Scanning electron micrographs of different Calcidiscus leptoporus coccospheres. A scale bar is displayed on each graph. 1–2. C. leptoporus small type from M46-4 VII (5 m) and M41-2 II (90 m). 3–4. C. leptoporus spp. leptoporus from M41-2 II (90 m). 5. C. leptoporus spp. leptoporus with liths of different sizes from M46-4 VI (5 m).

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Syracosphaera pulchra, Rhabdosphaera clavigera, Discosphaera tubifera, U. tenuis types IV and III. These secondary species reach maximum numbers at the transition to the STFZ (Fig. 5). In the lower photic zone of the Subtropical Gyre Florisphaera profunda is the predominant coccolithophore species (maximum concentration: 27.7 × 103 sphere units l− 1). Important accessory species are Gephyrocapsa ericsonii, Oolithotus antillarum and Oolithotus fragilis (Fig. 5). Abundant E. huxleyi morphotypes, types C, A and var. corona, are encountered in the upper photic zone of the STFZ (Fig. 6), accounting for up to 75% of the assemblage. Members of the family Syracosphaeraceae, such as Michaelsarsia elegans, Ophiaster spp., Syracosphaera histrica, Syracosphaera molischii, and Syracosphaera anthos, contribute considerably to the frontal zone community (Fig. 7). E. huxleyi type B, Gephyrocapsa muellerae and Algirosphaera robusta characterize the deeper photic zone (50 to 150 m) of the SFTZ (Figs. 6, 7).

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4.2.2. Distribution of morphological variants, subspecies or species of distinct taxa 4.2.2.1. Calcidiscus leptoporus. Both proven subspecies of C. leptoporus, i.e. C. leptoporus spp. leptoporus and C. leptoporus spp. quadriperforatus, and C. leptoporus small type which is likely to be a subspecies (Sáez et al., 2003; Young et al., 2003) were observed in the studied plankton transect. The most abundant morphotype is C. leptoporus spp. leptoporus with maximum cell concentrations of 6.8 × 103 sphere units l− 1 (Fig. 6). It is continuously recorded in all water depths of the STFZ south of 40°S. Its liths with moderately curved elements are described to range from 5 to 8 µm in diameter whereas C. leptoporus small type produces liths smaller 5 µm with kinked, serrated sutures along the elements (Kleijne, 1993; Knappertsbusch et al., 1997; Geisen et al., 2002). Although overlapping ranges in coccolith diameter between the different morphotypes are well known (Kleijne, 1993; Knappertsbusch et al., 1997; Quinn et al., 2004), in the STFZ waters the increased occurrence of

Plate II. Scanning electron micrographs of different Emiliania huxleyi coccospheres. A scale bar is displayed on each graph. 1. E. huxleyi type A from M46-4 VII (5 m) 2. E. huxleyi var. corona from M41-3 VII (20 m). 3. E. huxleyi type B/C from M41-2 II (90 m). 4. E. huxleyi type B from M46-4 VI (10 m).

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C. leptoporus spp. leptoporus liths smaller than 5 µm is striking (Fig. 6). These small-sized liths exhibit smooth element sutures and have been observed to appear on the same sphere as “regular”-sized liths (Plate I, Fig. 5). Notably none of the observed spheres were exclusively composed of coccoliths of C. leptoporus spp. leptoporus smaller than 5 µm, displaying possibly an enhanced production of liths smaller 5 µm in the frontal waters. Neither C. leptoporus small type nor C. leptoporus spp. quadriperforatus show a clear distribution pattern. They both appear consistently across the transect in low numbers (maximum: 2.5 × 103 sphere units l− 1). 4.2.2.2. Emiliania huxleyi. The characteristics of the well-established morphological groups of E. huxleyi have been described in detail by Young and Westbroek (1991) and Young et al. (2003). The discrimination between E. huxleyi var. corona and type A, was sometimes difficult, because of the occasionally weakly developed elevated “corona” around the central area of the former (compare Plate II, Figs. 1 and 2). On complete coccospheres of E. huxleyi var. corona the central “corona” is not always well developed on each coccolith. Sometimes there is simply a white, slightly embossed ring visible around the central area. Apart from the collar, another criterion to distinguish both forms was the mostly smaller central area to distal shield area ratio of E. huxleyi var. corona (Fig. 8). Highest cell concentrations of all morphological groups of E. huxleyi were encountered in STFZ waters. E. huxleyi type A basically appears at all investigated stations with maximum cell concentrations of 41.4 × 103 sphere units l − 1 (Fig. 6). A restricted distribution is shown by E. huxleyi type B, mainly confined to the deeper waters (100 m) of the STFZ. Here highest abundances of 66.1 × 10 3 sphere units l − 1 are recorded. E. huxleyi type C was not only observed to be the most abundant (maximum: 73.3 × 10 3 sphere units l − 1 ) of morphological E. huxleyi groups, but also of all studied taxa. The latitudinal proliferation of E. huxleyi var. corona stretches from the northernmost station to 36°S with a maximum abundance of 65.9 × 10 3 sphere units l − 1 . Due to poor preservation in the southernmost stations, also a number of E. huxleyi specimens were unidentifiable to subspecies level.

Fig. 8. Morphometric studies on coccoliths of the E. huxleyi species complex.

4.2.2.3. U.tenuis. Based on Kleijne (1993), Young et al. (2003) differentiated between U. tenuis types I, II, IIIa, IIIb, and IV according to the development of the ornamentation of the macroliths and their central areas. In some cases the differentiation between types II and III is not unambiguously possible. All macroliths with ribs protruding teeth-like into the central area and well developed papillae were assigned type II (Plate III, Figs. 3–4). Those umbelloliths where the ribs almost cover the entire central area were included into type III (Plate III, Figs. 5–6). In contrast to Young et al. (2003), we refrained from further subdividing type III, because differences in the degree of calcification and central area closure appeared rather blurred. U. tenuis is preferentially found in samples of the upper water column (5 to 50 m; Figs. 5, 7). The different U. tenuis morphological groups exhibited distinct lateral and vertical distribution patterns. Type I occurred only in the northernmost station of the study area in very low concentrations (maximum: 0.7 × 103 sphere units l− 1). While U. tenuis type II was restricted to the STFZ waters where it reached high cell numbers (35.1 × 103 sphere units l− 1), type III was most abundant in the Subtropical Gyre waters (13.6 × 103 sphere units l − 1 ). Elevated abundances (34.4 × 103 sphere units l− 1) of U. tenuis type IV, the second most abundant U. tenuis type, prevailed in the

Plate III. Scanning electron micrographs of different Umbellosphaera tenuis types. A scale bar is displayed on each graph. 1. U. tenuis type I coccosphere from M41-2 II (10 m) 2. Single U. tenuis type I coccolith from M41-2 II (90 m). 3. U. tenuis type II coccosphere from M46-4 VI (20 m) 4. Single U. tenuis type II coccolith from M46-4 VI (10 m). 5. U. tenuis type III coccosphere from M41-2 II (50 m) 6. Single U. tenuis type III coccolith from M41-3 III (50 m). 7. U. tenuis type IV coccosphere from M46-4 VII (5 m) 8. Single U. tenuis type IV coccolith from M46-4 VII (5 m).

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NSTF. This type also appeared in deeper water levels (100 m) of the Subtropical Gyre, where relatively high concentrations of intact coccospheres were detected. 4.2.2.4. Umbilicosphaera foliosa and Umbilicosphaera sibogae. Species of the genus Umbilicosphaera occurred only rarely in the samples studied (Fig. 7). The cooccurrence of U. foliosa with U. sibogae is striking. In 75% of cases when U. foliosa appeared, it was accompanied by U. sibogae. Maxima of both species were found in the middle to lower photic zone (50 to 150 m). While U. sibogae reached higher cell numbers (2.7× 103 sphere units l− 1) in the deeper gyre and transitional waters, U. foliosa occurred in highest abundances (0.9× 103 sphere units l− 1) in the frontal zone. 5. Ecological analysis and interpretation 5.1. Ecological affinities inferred from multivariate statistics and distribution patterns In order to infer the underlying gradients that control coccolithophore distribution, measured environmental parameters were related to species and those members of species complexes with abundances of more than 1.5 × 103 sphere units l− 1 in at least one sample. The Monte Carlo test indicates a highly significant relationship between coccolith data and environmental variables for the first axis (p = 0.005) and all canonical axes (p = 0.005). The eigenvalue (0.598) of the first axis is high compared to the rest, implying that the first axis represents a strong gradient (Table 4). Both main CCA axes only explain 19% of variance in species data thus representing 64.5% of the species–environment relationship (Table 4). This result implies that besides the included environmental parameters there are other unidentified more important variables to account for species variation. Potential controls could include the availability of light and micronutrients, water turbulence, and synecological dependencies. A potential error might lie in the use of the WOA data-sets. These data might not represent the actual hydrographic situation at the specific sampling moment Table 4 Summary of the CCA Axes

1

2

3

4

Eigenvalues 0.598 0.277 0.041 0.027 Species–environment correlations 0.907 0.844 0.759 0.730 Cumulative percentage variance of 13.0 19.0 19.9 20.5 species data Cumulative percentage of species– 41.2 64.5 0.0 0.0 environment relation

within a highly variable system, like the STFZ (Belkin and Gordon, 1996). The triplot (Fig. 9) shows temperature, water depth, and nutricline depth as the variables that best explain variation in species composition (Table 5). Additionally the first CCA axis is negatively correlated to nitrate concentration. The second axis is delineated by depth and anticorrelated to chlorophyll content. Besides the apparent relation to sampling depth, the distribution of the sample scores is also linked to features of the main oceanographic regimes, gyre and frontal waters respectively (Fig. 9). In the following we will discuss the relation of the species assemblages to the applied environmental variables within four assemblages. 5.1.1. Subtropical Gyre association (upper photic zone, 5–20 m) In the CCA triplot (Fig. 9) a group of species is correlated to warm temperatures and low nutrient levels. These conditions describe the upper photic zone of the Subtropical Gyre, where the nutricline is very deep (Figs. 2, 3). U. tenuis types III and IV are present in this Subtropical Gyre association. Although U. tenuis types III and IV are similar ecologically (Figs. 5, 13), the distribution of the latter extends towards deeper water levels, indicating a slightly higher tolerance for cooler temperatures. Furthermore, the community is characterized by elevated abundances of U. irregularis, R. clavigera, S. pulchra, and D. tubifera. High abundances of U. irregularis are found in the upper to middle photic zone (5–50 m) with a deep nutricline, which fits with its designation as an indicator of oligotrophic conditions (Brand, 1994). In contrast to U. irregularis, R. clavigera and D. tubifera appear to benefit from increased equatorward nutrient input by STFZ waters, in water depths between 5 and 20 m within the transitional zone between the two systems (Fig. 5). Of all Syracosphaera spp. observed, S. pulchra appears to have the greatest preference for warm, oligotrophic conditions. 5.1.2. Subtropical Gyre association of the middle to lower photic zone (50–200 m) In ascending order, G. ericsonii, O. antillarum, C. leptoporus small type, O. fragilis and F. profunda preferentially thrive in intermediate to deeper water in environments with a deep nutricline. In contrast to the distribution of O. fragilis which is restricted to the gyre waters, F. profunda follows the trend of the nutricline towards shallower water levels in the STFZ (Fig. 5). A. robusta, U. sibogae and E. huxleyi var. corona plot in the upper right quadrant of the CCA triplot (Fig. 9). From the CCA diagram they all appear to occupy an intermediate position between the lower photic zone taxa,

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Fig. 9. The triplot is the graphical expression of the results of the detrended CCA. Environmental gradients are displayed as arrows pointing in the direction of greatest change. Species centroids are marked as triangles, whereas samples are represented by circles and squares.

F. profunda and O. fragilis, of the Subtropical Gyre and the more fertile environment of the STFZ. E. huxleyi var. corona-variant seems best adapted to oligotrophic conditions of all E. huxleyi variants. Earlier studies by Cortés et al. (2001) and Hagino and Okada (2006) corroborate this interpretation. 5.1.3. Subtropical Front association (upper photic zone, 5–20 m) Elevated concentrations of U. tenuis type II, M. elegans and Ophiaster spp. precisely at the NSTF correspond to elevated chlorophyll levels characterizing a more highly productive environment. Small to medium Syracosphaera spp. (mainly S. histrica, S. molischii) are very abundant here. However, the most dominant taxon is E. huxleyi, especially types A and C. Multilayered coccospheres were often detected in the frontal waters. 5.1.4. Subtropical Frontal Zone association of the lower photic zone (50–200 m) The deeper photic zone of the STFZ is dominated by E. huxleyi, in particular E. huxleyi type B. Although highest cell concentrations of C. leptoporus spp. leptoporus were found in the middle photic zone, similar to E. huxleyi type A, this taxon is very common in all water depths throughout the STFZ. Its affinity for fertile waters has already been suggested by Boeckel et al. (2006) and Hagino and Okada (2006). It is accompanied

by G. muellerae in this high-nutrient environment. Plotting farther from the aforementioned taxa, in the CCA diagram, are the centroids of C. leptoporus spp. leptoporus liths smaller 5 µm and S. anthos which are linked to the cooler temperatures of the STFZ. 5.2. Comparison of morphotype distribution in the plankton and sediment assemblages Despite the combined influences of biological destruction, dissolution, and transport by currents, the principal signal of the living communities is conserved in the underlying surface sediments (McIntyre and Bé, 1967; Baumann et al., 2000; Malinverno et al., 2003). Thus, sediment assemblages generally reflect oceanic conditions in the photic zone steering species distribution (Boeckel et al., 2006). The relative proportions of the different morphotypes of a species complex in the water column and in surface Table 5 Interset correlations between environmental variables and site scores Environmental parameters

Axis 1

Axis 2

Temperature Nutricline depth Depth Chlorophyll Nitrate

0.832 0.719 − 0.071 − 0.187 − 0.361

0.285 0.239 0.834 − 0.541 0.361

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Fig. 10. The relative proportion of C. leptoporus morphotypes within the upper 100 m of the water column (above) are compared with their percentages in the underlying surface sediments (below). The geographical positions of the surface sediments are listed in Table 3.

sediments are compared, in order to evaluate their potential for paleoceanographic reconstructions. While C. leptoporus spp. leptoporus appears in almost all plankton stations, small C. leptoporus spp. leptoporus (b 5 µm) are confined to Subantarctic waters (Fig. 10). Small liths of this type are likewise present in the underlying sediments. This observation suggests a generally enhanced production of these liths in the Subantarctic

region. In contrast, the occurrence of C. leptoporus small type is restricted to gyre and equatorial waters, where it is the sole morphotype present in the south-equatorial station M41/2 II. Similarly, in the sediments underlying equatorial water masses C. leptoporus small type is the prevailing form. To procedurally replicate these findings in future studies, emphasis should be on the biogeography of morphotypes, noting subtle fine-scale

Fig. 11. The relative proportion of E. huxleyi morphotypes within the upper 100 m of the water column (above) are compared with their percentages in the underlying surface sediments (below). The geographical positions of the surface sediments are listed in Table 3.

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Fig. 12. The relative proportion of U. tenuis morphotypes within the upper 100 m of the water column (above) are compared with their percentages in the underlying surface sediments (below). The geographical positions of the surface sediments are listed in Table 3.

differences between liths smaller 5 µm. Percentages of C. leptoporus spp. quadriperforatus are generally higher in the sediments than in the water column. This might be due to the higher preservational potential of their large and heavily calcified coccoliths or the enhanced production of C. leptoporus spp. quadriperforatus in another, unsampled period. E. huxleyi var. corona appears underrepresented in the surface sediments (Fig. 11), surprising due to its consistent and abundant occurrence in samples taken throughout the year. It is thus likely that its underrepresentation results from mis-identification due to the overall bad preservation of the “corona” in coccoliths of the sediment assemblage, which are then hardly distinguishable from E. huxleyi type A coccoliths. Type B and C coccoliths are likewise found in both plankton and sediment assemblages. Due to the bad preservational state of E. huxleyi coccoliths in the sediments underlying Subantarctic waters, type B and C coccoliths were probably merged as unidentified E. huxleyi specimens. Although the proportion of E. huxleyi type B and C within the sediment assemblages underlying Subantarctic waters is low compared to that in the plankton assemblages, highest percentages of types B and C are mainly confined to the Subantarctic sediments, thus reflecting the general trend observed in the plankton samples. The broad distributional pattern of U. tenuis morphotypes in the water column corresponds remarkably well to the surface sediment assemblages below (Fig. 12). Occurrence of type I was confined to the warm equatorial water masses. This is reflected by the equatorial surface

sediments where this morphotype is the dominant form. The prevailing morphotypes within the Gyre waters, types III and IV, likewise dominate the assemblages in the sediment. In both plankton and sediment assemblages of the frontal zone, U. tenuis type II is the predominant form. Consequently, the differentiation of U. tenuis morphotypes may serve as an important distinction in unravelling paleoecological questions. 6. Conclusions The present study was conducted to provide information about coccolithophore standing stock across the STFZ. Based on our data the following conclusions can be drawn: (1) Absolute abundances range from 8.6 × 103 sphere units l− 1 in the deeper photic zone of the STFZ to 179.4 × 103 sphere units l− 1 in the upper STFZ. Of 112 identified taxa, only 14 species contribute significantly to the species community. (2) The vertical and lateral distribution of the coccolithophore assemblages is controlled by the contrasting oceanographic characteristics in the study area, i.e. the stratified, warm, nutrient-depleted gyre waters and the productive frontal system. Implications for the ecological affinities of the species are inferred from their distribution patterns and multivariate statistics. (3) Geographical variation among morphotypes reflects different ecological affinities of the members of a

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species complex. This observation is shown via the CCA. For example, U. tenuis III and IVare found in more oligotrophic gyre waters, whereas U. tenuis II is confined to cooler, nutrient-rich environments. (4) The relative proportions of the morphotypes of a plankton station were compared to the underlying surface sediment assemblages. The comparison revealed a good correspondence between both types of assemblages, reflecting the broad trends of relative morphotype proportions in both sample sets. The preservation of the fine-scale morphostructures of E. huxleyi types may impair their application to paleostudies. In contrast, the great potential of U. tenuis morphotypes for paleoceanographic reconstructions could be demonstrated. Acknowledgements We are grateful to the officers and crews of the research vessel “Meteor” and to the scientific crews of the various cruises for their assistance. H. Heilmann, M. Geisen (AWI Bremerhaven) and F. Hinz (AWI Bremerhaven) assisted in SEM work. This research was funded by the Deutsche Forschungsgemeinschaft (Research grant Ba 1648/11 and Research Center “The Ocean in the Earth System" project A9). References Aiken, J., Rees, N., Hooker, S., Holligan, P., Bale, A., Robins, D., Moore, G., Harris, R., Pilgrim, D., 2000. The Atlantic Meridional Transect: overview and synthesis of data. Progress in Oceanography 45, 257–312. Andruleit, H., 1996. A filtration technique for quantitative studies of coccoliths. Micropaleontology 42 (4), 403–406. Baumann, K.-H., Cepek, M., Kinkel, H., 1999. Coccolithophores as indicators of ocean water masses, surface-water temperature, and paleoproductivity — examples from the South Atlantic. In: Fischer, G., Wefer, G. (Eds.), Use of proxies in paleoceanography: Examples from the South Atlantic. Springer Verlag, Berlin, Heidelberg, pp. 117–144. Baumann, K.-H., Andruleit, H., Samtleben, C., 2000. Coccolithophores in the Nordic Seas: comparison of living communities with surface sediment assemblages. Deep Sea Research Part II: Topical Studies in Oceanography 47, 1743–1772. Belkin, I.M., 1993. Frontal structure of the South Atlantic. In: Voronina, N.M. (Ed.), Pelagicheskie Ekosistemy Yuzhnogo Okeana. Nauka, Moscow, pp. 40–53. Belkin, I.M., Gordon, A.L., 1996. Southern Ocean fronts from Greenwich Meridian to Tasmania. Journal of Geophysical Research 101 (C2), 3675–3696. Boeckel, B., Baumann, K.-H., Henrich, R., Kinkel, H., 2006. Coccolith distribution patterns in South Atlantic and Southern Ocean surface sediments in relation to environmental gradients. Deep-Sea Research I 53, 1073—1099.

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