Deep-Sea Research II 48 (2001) 1957}1981
Coccolithophore ecology at the HOT station ALOHA, Hawaii
Mara Y. CorteH s*, JoK rg Bollmann, Hans R. Thierstein
Geological Institute, ETH-Zentrum, CH-8092 Zurich, Switzerland
Abstract
Cell densities of total coccolithophores and dominant taxa were determined in 183 samples from the upper
200 m of the water column at about monthly intervals between January 1994 and August 1996 at the HOT
station ALOHA, Hawaii. High cell densities were observed twice a year, in March (up to 41;10 cells l\)
and in September/October (up to 52;10 cells l\). In the intervening months, cell densities were extremely
low (0}20;10 cells l\), re#ecting a strong seasonality. The main production of coccolithophores took place
in the middle photic zone between 50 and 100 m water depth. In total 125 coccolithophore species were
identi"ed but only "ve constituted on average more than 30% of the community: Emiliania huxleyi,
Umbellosphaera irregularis, U. tenuis, Florisphaera profunda and Gephyrocapsa ericsonii. The generally low,
but seasonally dynamic coccolithophore cell density variability is compared with in situ measurements of
environmental parameters. Correlation analyses between cell density variability of the dominant taxa and
potentially controlling environmental parameters show signi"cant correlation coe$cients when the data set
was separated into upper and lower photic zone. Cell densities of all dominant taxa are most highly
correlated with temperature variability. U. irregularis is positively correlated in the upper photic zone,
whereas E. huxleyi and G. ericsonii are negatively correlated. In the lower photic zone, F. profunda cell
densities are positively correlated with light, which corresponds to the maximum bottom-up control (i.e. by
physical forcing) of any species encountered. The surprisingly low correlations of cell densities with nitrate
and phosphate may be caused by insu$cient sampling resolution, nutrient levels close to detection limits, or
both. 2001 Elsevier Science Ltd. All rights reserved.
1. Introduction
1.1. Purpose and goals
Coccolithophores are unicellular marine golden-brown algae (Prymnesiophyta) covered by
calcium carbonate platelets (coccoliths). Coccolithophores are a major group of primary producers
* Corresponding author. Fax: #41-1-632-1080.
E-mail address: [email protected] (M.Y. CorteH s).
0967-0645/01/$ - see front matter 2001 Elsevier Science Ltd. All rights reserved.
PII: S 0 9 6 7 - 0 6 4 5 ( 0 0 ) 0 0 1 6 5 - X
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M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
in the world's oceans, contributing about 15% of the average oceanic phytomass (Berger, 1976) and
up to 60% of the bulk pelagic calcite deposited on the ocean #oors (Honjo, 1996). Although
coccolithophores are considered to play an important role in the global bio-geochemical cycle in
the present and in the past (Holligan et al., 1987; Balch et al., 1991; Emiliani, 1992; Holligan, 1992;
Westbroek et al., 1994), little is known about their biology and ecology. Consequently, it is
important and necessary to improve our knowledge of the taxonomy, biogeography and ecology of
coccolithophores.
Thanks to the e!orts of scientists at the time-series station ALOHA, a phytoplankton and
environmental sampling program could be carried out at this station. The simultaneous acquisition
of environmental data and "lter samples provided a unique opportunity to identify processes
controlling the vertical, seasonal and inter-annual distribution of coccolithophores. We present
here one of the "rst multi-annual records of coccolithophore standing stocks throughout the photic
zone (0}200 m) in the North Paci"c Gyre, as a complementary study to that carried out by Haidar
and Thierstein (2001) at the Bermuda time-series station (BATS). We document the vertical,
temporal and inter-annual variability of total coccolithophore cell densities and dominant coccolithophore species during the period from January 1994 to August 1996. We then address the
following questions: Which environmental conditions in#uence the distribution of total coccolithophore cell densities? How does species composition respond to changes in environmental
parameters? What are the environmental `nichesa of the dominant coccolithophore species?
1.2. Time-series sampling at ALOHA, Hawaii
Station ALOHA, located approximately 100 km north of Oahu (22345N, 15830W; Fig. 1), is
representative of the Central North Paci"c Gyre (NPCG), an area with stable environmental
conditions and only low seasonal and interannual variability (Karl and Lukas, 1996 and references
therein). Since 1988, when this deep-water hydrostation was established, selected oceanic properties
supporting the World Ocean Circulation Experiment (WOCE) and the Joint Global Ocean Flux
Study (JGOFS) objectives have been routinely measured. On approximately monthly cruises,
measurements were taken of the thermohaline structure of the water column, water column
chemistry, currents, primary production and particle #ux (Chiswell et al., 1990; Karl et al., 1996b).
1.3. Previous work on coccolithophores
Much of our current knowledge of coccolithophores is based on the correlation of coccolith
distribution in marine surface sediments with environmental parameters measured in overlying
surface waters and, to a minor extent, on the analyses of living plankton or the culturing of
coccolithophores under di!erent environmental conditions in the laboratory. A comprehensive
overview of the current knowledge about coccolithophores is given by Winter and Sisser (1994),
and a short overview about coccolithophores in the North Atlantic is given by Haidar and
Thierstein (2001).
A number of excellent studies on the composition and variability of total phytoplankton
communities in the North Paci"c have been carried out using light microscope techniques (Eppley
et al., 1973; Beers et al., 1975; Bienfang et al., 1984; Venrick, 1988, 1995, 1999) and pigment analyses
(Ondrusek et al., 1991; Campbell and Valuot, 1993; Letelier et al., 1993; Winn et al., 1995; Campbell
M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
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Fig. 1. Location of the JGOFS time-series station ALOHA at Hawaii with the general surface circulation patterns after
Pickard and Emery (1990). The symbols indicate the locations where coccolithophores have been studied in this area:
䊏"this study; 䢇"Beers et al. (1975) and Reid (1980); 䉭"Station 6, 䉱"station 7 and 䉲"station 10, in Okada and
Honjo (1973) and Honjo and Okada (1974); nml " nautical mile.
et al., 1997). Detailed taxonomic analyses of the calcareous phytoplankton were carried out in a few
additional studies (Beers et al., 1975; Reid, 1980; Okada and Honjo, 1973; Honjo and Okada, 1974).
In two pioneering studies, Okada and Honjo (1973) and Honjo and Okada (1974) identi"ed six
coccolithophore zones, each with its own species composition, along "ve north}south and
east}west transects in the North and Central Paci"c. These zones are associated with the Paci"c
current system. In addition, Reid (1980) documented the seasonal distribution of coccolithophores
in the North Paci"c Gyre from six cruises between 1972 and 1976. She reported a less strati"ed
community in winter than in summer, with di!erent species compositions than those presented by
Okada and Honjo (1973) and Honjo and Okada (1974).
2. Materials and methods
2.1. Plankton samples
Twenty-seven pro"les with a total of 270 plankton samples were collected from the following
water depth levels: 5, 10, 25, 50, 75, 100, 150, 200, 250 and 300 m between September 1993 and
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M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
September 1996 (cruises HOT 49}76) by the Hawaii Ocean Time-series (HOT) group at the School
of Ocean & Earth Sciences (SOEST), University of Hawaii. An average of 8 l of sea water was
"ltered on a 47-mm diameter Millipore威 or Nucleopore威 (HOT 61, 67}76) membrane "lter with
a pore size of 0.8 m immediately after arrival on deck using Nalgene and Gelman inline "lter
gaskets. A vacuum of less than 100 mmHg was applied with an electrical vacuum pump below the
"lters in order to prevent the disintegration of cells. After "ltering, samples were rinsed with 50 ml
of bu!ered distilled water (NH , pH 8.5) to remove sea salt. Filters were placed in labelled
petri-dishes, dried immediately in an oven at 403C and stored in a dry, dark and cool place until
they were analysed.
Before analysis, each "lter was examined by eye to verify an even distribution of material.
Because no coccolithophores were found in any sample from the "rst year (1994) at 250 and 300 m
water depth, with the exception of the sample HOT 56 250 m, only samples down to a depth of
200 m were analysed for 1995 and 1996. Therefore, a total of 183 samples from January 1994 to
August 1996 (cruises HOT 51}75) are presented in this study.
Counting was done with a Hitachi 2300 scanning electron microscope (SEM) at 1500; and
3000; magni"cation on a piece of "lter that was mounted onto an aluminium stub using carbon
tape and coated with 15 nm of gold. A total of 3.8 mm was analysed along a radial transect of 40
equidistant areas of observation, each 0.097 mm. This is equivalent to 25 ml water. Each area of
observation required 9;9 "elds of view at 3000; magni"cation (each 1200 m as calibrated with
a calibration grid), or 5;4 "elds of view at 1500; (each 4800 m). In samples with either
extremely low or high cell densities, only 20 "elds of observation were analysed because of time
constrains. A detailed description and discussion of the counting method is presented in CorteH s
(1998).
The chosen counting technique provides reproducible counts with a minimum error of $10%
and a maximum error of $26% for total coccolithophore cell densities higher than
5;10 cells l\. Reproducibility decreases considerably at lower cell densities. The detection limit
of the applied method is 120 cells l\ at a 95% con"dence limit when 25 ml of sea water are
analyzed. This corresponds to one cell in 12.5 ml or 20 "elds of observation.
2.2. Taxonomy
The identi"cation of the coccolithophore species was done according to the taxonomic classi"cation scheme published by Jordan and Kleijne (1994 and references therein). E. huxleyi consists of
the morphotype C (Young and Westbroek, 1991) and E. huxleyi var. corona. Our G. ericsonii
includes typical G. ericsonii, G. ornata, G. protohuxleyi and several intermediates. G. ericsonii is the
equivalent of Gephyrocapsa `minute morphotypea de"ned in Holocene sediments by Bollmann
(1997). Most of the taxa encountered are illustrated in the ETH microfossil database available at
htpp://www.emidas.ethz.ch.
2.3. Environmental data treatment
All environmental data used in this study were collected by the HOT group of SOEST as part of
the repeated measurements of selected oceanic properties for the WOCE and JGOFS programs.
These data are available on the World Wide Web at http://www.soest.hawaii.edu/HOT}WOCE.
M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
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The temperature and salinity measurements are from the same casts and depths as the water
samples. Nutrient concentrations and other environmental measurements used in this study are
from the same cruise, but from the cast in which primary production and pigments were analysed
by the HOT group. Missing data or data of questionable quality, where possible, have been
interpolated from values of the neighbouring levels (see Appendix A on CD-ROM).
Data for light were acquired from continuous surface incidence irradiance measurements using
an Li-COR威 LI-192S instrument and photosynthetic available radiation (PAR) measurements
using a Pro"ling Natural Fluorometer PNF-300, both collected during each cruise (Karl et al.,
1990). Here, we calculate downward irradiance as the average at each desirable depth level of
$2.5 m. The di!erence between calculated downward irradiance and surface irradiance, both
measured with the same instrument, was converted to percentage. This percentage was then
applied to the incidence irradiance measured with the Li-COR instrument to calculate the quantity
of light (PAR) in E m\ s\. For those cruises where PAR measurements were not available,
values from the previous month or from the same month but a di!erent year were used assuming
limited temporal variability in light incidence (Bienfang et al., 1984). These authors reported no
discernible temporal pattern in the pro"les of quantum scalar irradiance south of Oahu, Hawaii.
Furthermore, Chiswell et al. (1990) showed, based on monthly pro"les, almost no seasonal change
in the light attenuation in the photic zone between October 1988 and November 1989 at station
ALOHA.
2.4. Statistical analyses
Stepwise multiple regression models were calculated under the assumption of a normal distribution of the data after log-transformation of cell densities and light as these variables showed skewed
distributions. Principal component analyses (PCA) calculations were based on a product}moment
correlation matrix. Environmental parameters were standardised by subtracting the mean and
dividing by the standard deviation (Sokal and Rohlf, 1995).
Weighted average abundances of dominant species with respect to the main environmental
parameters were calculated to obtain their optimal environmental conditions. The averages were
calculated after Sokal and Rohlf (1995) by multiplying each cell density (per species) by the
corresponding environmental parameter and dividing their sum by the sum of cell densities (per
species).
All statistical analyses were done using the Data Desk statistics package (Data Description Inc.).
For these analyses, values of zero were excluded as we are interested in the identi"cation
of the environmental variables that can contribute to the presence or increase of coccolithophore
cell densities. Because the variation of the environmental parameters at ALOHA is limited
compared to other oceanic areas where a particular taxon occurs, it should be kept in
mind that terms such as high, low, poor, rich, etc., are used with respect to the observations at
ALOHA only.
2.5. Terminology
The following terms are used in this paper:
Photic zone (PZ): depth between 0 and 200 m.
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M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
Upper photic zone (UPZ): zone that contains samples collected mainly from 0 to 100 m as
identi"ed by the results of the PCA (note that these groups are based on a PCA of environmental
conditions and not simply on depth).
Lower photic zone (LPZ): zone that contains samples collected mainly from 100 to 200 m as
separated by the PCA.
Preferred environmental conditions of a taxon: related to the environmental condition at which
a taxon was found to be most abundant. The term `preferreda environmental conditions of a taxon
refers only to its preference at ALOHA, which may be di!erent from that elsewhere.
2.6. Oceanographic conditions during 1994}1996
2.6.1. Variability of abiotic factors
Environmental conditions at ALOHA have been documented in several publications by members of the HOT group (Winn et al., 1994, 1995; Bingham and Lukas, 1996; Dore and Karl, 1996;
Letelier et al., 1996; Karl et al., 1996a, b). We brie#y present the variability of the main abiotic
factors in the photic zone from 1994 to 1996.
2.6.2. Physical characteristics
At station ALOHA sea-surface temperature varied seasonally from 22.7 to 26.83C over the
period of study. Temperatures showed minor interannual changes throughout the photic zone
(Fig. 2a).
Sea-surface salinity, unlike temperature, did not show a persistent seasonal signal (Karl et al.,
1996b). Occasional invasions of low-salinity waters ((34.6) down to 100 m water depth, which
had been observed between 1988 and 1996, also occurred during the phytoplankton sampling
period in February and April 1995, as well as in June and July 1996 (Fig. 2b).
The mixed-layer depth (MLD) was determined for this location as the depth at which the
temperature was 13C lower than at the sea surface (Hastenrath and Merle, 1987). The MLD varied
seasonally: in winter, when a deepening of the mixed layer occurred, it was located at 125 m in both
years (Fig. 2c). In summer and fall, when the water is more strati"ed, the MLD was at &50 m.
Additionally, some interannual variation in the strati"cation gradient was observed during
summer and fall.
Incident solar irradiance varied from 200}300 E m\ s\ in winter to more than 500 E m\ s\
in summer (Fig. 2d). The 1% level of light was on average around 94$8 m depth. In winter, this
level was located at 90$1 m and in late spring around 104$1 m depth. The light intensity
(downward irradiance) was on average 4.6$1 E m\ s\ at this depth level.
2.6.3. Nutrients
The most important nutrients for coccolithophores are assumed to be nitrate and phosphate
(Brand, 1994 and references therein). At ALOHA, they were usually below the detection limit of the
autoanalyzer method in the photic zone (Karl and Lukas, 1996). Nanomolar concentrations in
these waters have been measured using a chemiluminescence method for nitrate and nitrite and
a magnesium-induced coprecipitation method for phosphate (Tupas et al., 1993; Karl and Tien,
1992). The detection limit of nitrates was 0.002 mol kg\, and the precision was $0.001 mol.
The detection limit of phosphate was 0.01 mol kg\ with a precision of 1}3% (Tupas et al., 1993).
M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
1963
Fig. 2. Physical characteristics and distribution of nutrients in the photic zone (0}200 m) at the time-series station
ALOHA, Hawaii from January 1994 to August 1996: (a) temperature; (b) salinity; (c) mixed-layer depth (MLD); (d) light;
(e) nitrate and (f) phosphate. Note: For those cruises where no downward irradiance measurements were available, values
were extrapolated from the previous month or from the same month but a di!erent year under the assumption that there
is limited temporal variability of light attenuation. Nitrate corresponds to the sum of nitrate and nitrite.
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M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
In this study, the sum of nitrite and nitrate is referred to as `nitratea. The measured concentrations
of nitrite were lower than those of nitrate below 100 m, and both nitrate and nitrite occurred in very
low concentrations in the upper 100 m (Dore and Karl, 1996).
In the top 100 m nitrate was homogeneously distributed, with concentrations lower than
0.10 mol kg\, and showed no seasonal or interannual variability (Fig. 2e). However, from 100 to
200 m, nitrate concentrations increased up to 3 mol kg\ and varied seasonally. Karl et al. (1996b)
reported that the nitricline varied between 200 and 600 m due to nutrient injection events in late
winter (Karl et al., 1996a). The nitracline ('1 mol kg\) varied seasonally and was shallow in
winter and fall, and deep in spring and summer (Winn et al., 1995).
Phosphate concentrations varied from 0.02 to 0.34 mol kg\. Concentrations higher than
0.1 mol kg\ were usually measured below 150 m but also were detected above 100 m in fall 1994
and winter}spring 1995 (Fig. 2f ) during short periods of nutrient injection (Karl et al., 1996a). In
contrast to nitrate, phosphate showed a detectable seasonal variation.
3. Results
3.1. Total coccolithophores
Total coccolithophore abundances showed both vertical and seasonal variations in the water
column (Fig. 3a). Highest cell densities occurred in the middle photic zone from 75 to 100 m. No
coccolithophores were found in any sample from the "rst year (1994) at 250 and 300 m water depth,
with the exception of the sample HOT 56 at 250 m in which 29 cells were identi"ed. In general, only
isolated coccoliths were encountered below 200 m. For 1995 and 1996, therefore, only samples
down to a depth of 200 m were analysed. Cell densities varied from a maximum of 52;10 cells l\
in October 1995, at a depth of 75 m, to 0 cells l\ in 5 samples.
Cell densities were less than 30;10 cells l\ between 5 and 50 m and below 100 m (Fig. 3a).
However, two exceptions were observed, one in March 1995 and a second in August 1996, when
concentrations of more than 40;10 and 38;10 cells l\ were measured at 50 m, respectively.
Coccolithophore concentrations higher than 30;10 cells l\ occurred only between 75 and
100 m, and were restricted to late-winter/early-spring and late-summer/early-fall in both years,
re#ecting a clear seasonal signal.
3.2. Dominant coccolithophore taxa
In total, 125 coccolithophore taxa including 36 holococcolithophore species were identi"ed at
species level during the sampling period (CorteH s, 1998). Only a few of the observed species are
common (average '1;10 cells l\). The dominant taxa (i.e. '5;10 cells l\) were Emiliania
huxleyi, Umbellosphaera irregularis, U. tenuis, Florisphaera profunda and Gephyrocapsa ericsonii.
The temporal cell density variability of the dominant taxa is shown in Fig. 3b}f, and Appendices
A and B (see CD-ROM) contain all relevant statistical data. E. huxleyi was always present during
the sampling period, but it showed clear abundance peaks in late winter and early spring. The peak
value (20;10 cells l\) in 1995 was more than double that observed in 1994 (8;10 cells l\) and
four times higher than that observed in 1996 (6;10 cells l\, Fig. 3b). U. irregularis showed the
M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
1965
Fig. 3. Distribution of total coccolithophore cell densities and dominant species cell densities in the photic zone from
January 1994 until August 1996 at station ALOHA: (a) total coccolithophore cell density; (b) E. huxleyi; (c) U. irregularis;
(d) U. tenuis; (e) G. ericsonii; (f) F. profunda. Contouring was done by interpolation between three grid points.
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M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
highest cell densities in summer and fall, with values in 1994 (20;10 cells l\) double those of 1995
and 1996 (10}12;10 cells l\, Fig. 3c). U. tenuis showed a peak in late winter and summer}fall. Its
peak cell densities varied from 9;10 cells l\ in winter 1994 to 16;10 cells l\ in summer 1994
(Fig. 3d). G. ericsonii showed a similar seasonal pattern to that of U. tenuis, but the overall cell
densities were lower (Fig. 3e). The highest cell densities of F. profunda were observed mainly in
summer, with values of up to 15;10 cells l\ at 150 m depth (Fig. 3f). However, a peak of
14;10 cells l\ occurred at 100 m in winter 1995. Its peak in summer 1995 was less pronounced,
but a peak (17;10 cells l\) was observed in early fall at 100 m depth.
The temporal distribution of relative abundances of the dominant coccolithophore species
identi"ed in this study did not re#ect the temporal patterns of their cell densities. Only species with
high cell densities at distinct depth levels tended to show high relative abundance within the
coccolithophore community (CorteH s, 1998).
The community structure of coccolithophores changed seasonally at all depth levels. The winter
community in the upper and middle photic zone was characterised by E. huxleyi, U. tenuis and G.
ericsonii, while in summer and fall U. irregularis was the most prominent species within the upper
photic zone. G. ericsonii became abundant in the middle photic zone mainly during 1994. In the
lower photic zone, winter and summer communities were characterised by F. profunda. All of these
species occurred together with numerous less abundant coccolithophore taxa that will be the topic
of a future publication.
4. Ecological analyses and interpretation
4.1. Total coccolithophore cell densities
Scatter plots of total coccolithophore cell densities and environmental parameters were
used to check whether there were any dominant ecological controls (Fig. 4). Coccolithophores
at low cell densities occurred over a wide range of environmental conditions, while high cell
densities (3;10 cells l\ or more) were generally found at a `narrowa range of environmental
conditions, which were: 20}253C water temperature; 34.9}35.2 salinity; 0.004}0.07 mol kg\
nitrate; (0.025 mol kg\ phosphate and 2}25 E m\ s\ light intensity. From Fig. 4 it is
obvious that there are no simple linear relationships between single environmental parameters and
cell densities.
A principal component analysis among the environmental parameters known to a!ect coccolithophore densities revealed that 86% of the total variance within the sample set could be
explained by two components (Table 1). The "rst component explains 56% of the variance, and it is
characterised by positive loadings of temperature and light and a negative loading of nitrate. The
second component explains 29% of the variance, and is characterised by a positive loading of
salinity and a negative loading of phosphate (Fig. 5a). Thus, the "rst component appears to
represent parameters that change mostly with depth, and the second parameters that change also
with time. Loadings of the two factors in 183 individual samples separate these into two groups
mainly related to depth (Fig. 5b and c). These results suggest that the important and potentially
controlling parameters and their variability in the UPZ are distinctly di!erent from those in the
LPZ. Thus the sample data set was divided into two groups based on the PCA analysis. The "rst
M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
1967
Fig. 4. Cell density distribution of coccolithophores with respect to various environmental parameters.
group (133 shallow samples) is characterised by temperatures higher than 223C, a salinity range
from 34.3 to 35.3, nitrate usually lower than 0.01 mol kg\, phosphate lower than 0.2 mol kg\,
and light higher than 10 E m\ s\. The second group (50 deep samples) is characterised by
temperatures lower than 223C, a salinity range from 34.7 to 35.4, nitrate concentrations usually
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M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
Table 1
Principal component factor loadings (eigenvectors) of environmental parameters
Variable
Temperature
Salinity
Nitrate
Phosphate
Light
Variance explained by components
Percent of total variance explained
Component loadings
F1
F2
F3
0.93
!0.37
!0.88
!0.77
0.67
2.81
56.30
!0.07
0.84
!0.34
!0.59
!0.55
1.46
29.30
!0.05
0.38
0.17
!0.01
0.49
0.41
8.30
Fig. 5. Principal component analysis of environmental parameters. (a) Component loading vectors: the "rst component
relates to temperature and light versus nutrients, the second component is related to salinity versus everything else. (b)
Ordination of samples as a function of the two main factors obtained from the PCA. The samples can be grouped into
two clusters that correspond to the upper (䊐) and lower photic zone (䉭). (c) Ordination of samples as a function of time
and water depth. 䊐"UPZ and 䉭"LPZ.
M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
1969
higher than 0.01 mol kg\, phosphate concentrations up to 0.4 mol kg\ and light intensities
lower than 10 E m\ s\.
For further ecological analysis and interpretation, the two sample groups were treated separately.
A Pearson product}moment correlation for the UPZ shows no improvement over the analyses of all
samples. For the LPZ, however, total cell densities show high and signi"cant correlations with most
of the environmental parameters (see Appendix C on CD-ROM). High positive correlation coe$cients (r'0.6) were obtained with light and temperature, and negative correlation coe$cients
(r'0.5) were obtained with nitrate and phosphate. Variability of total cell densities cannot be related
to a single environmental parameter, and varying coccolithophore cell densities are likely the result of
several factors operating at the same time with di!erent intensities on di!erent taxa.
Multiple regression models (MR) were tested to explain the variability of total coccolithophore
cell densities in the upper and lower photic zone.
In the UPZ, the variance of coccolithophores cell densities could be explained by 12% (R )
with the following equation:
log(CD) "3.98#4.97phosphate!0.24log(light).
3.8
Both, phosphate and light explained 6% of total variance.
In the LPZ, a high multiple correlation coe$cient was obtained (R "0.68) for the following
equation:
log(CD) "39.24#0.47log(light)!0.23nitrate!1.0salinity.
*.8
Light explained 50% of the variance, nitrate 16% and salinity 2%.
4.2. Dominant taxa
Here we document the environmental conditions at which each of the major taxa was found
separately. In general, the distribution of these taxa with respect to environmental parameters
showed characteristic patterns (Figs. 6}10; Table 2).
Fig. 6. Distribution of cell densities of E. huxleyi with respect to temperature and phosphate. Pearson correlation
coe$cients for the upper and lower photic zone are given in the plots.
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M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
Fig. 7. Distribution of cell densities of U. irregularis with respect to temperature, phosphate and light. Pearson
correlation coe$cients for the upper and lower photic zone are given in the plots.
4.2.1. E. huxleyi
This species was found over a wide range of environmental conditions, but it was only abundant
at a narrow temperature range (22}243C), low nitrate concentrations ((0.1 mol kg\) and at
light intensities between 5 and 100 E m\ s\. The highest cell densities ('19;10 cells l\)
were found in two samples (HOT 61, 50 m and HOT 61, 75 m) collected in winter 1995 during
a period of relatively low salinity and relatively high nutrient concentrations (see Fig. 2b, e and f).
These samples were characterised by temperatures of 22}233C, a salinity of 35.0, light intensities
less than 25 E m\ s\, nitrate concentrations up to 0.02 mol kg\ and phosphate concentrations of 0.11 mol kg\. E. huxleyi represented more than 20% of the community in almost all the
samples in which it was present, excluding those samples collected in fall, in which temperatures
were higher than 243C.
Multiple regression models for E. huxleyi cell densities with respect to environmental parameters
were calculated for the UPZ and LPZ because this species was present in both zones. In the UPZ
67% of the variance of E. huxleyi could be explained by
log(E.hux) "9.28!0.29temperature#7.48phosphate.
3.8
M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
1971
Fig. 8. Distribution of cell densities of U. tenuis with respect to temperature, phosphate and light. Pearson correlation
coe$cients for the upper and lower photic zone are given in the plots.
Temperature and phosphate explained 50 and 17% of the variance, respectively. In the LPZ only
31% of the variance (R ) of E. huxleyi can be described by the following equation:
log(E.hux) "3.16!0.20nitrate.
*.8
4.2.2. U. irregularis
This species was common in the UPZ and it was usually found under the following conditions:
22}273C water temperature, 34.2}35.3 salinity, low nitrate concentration ((0.04 mol kg\), wide
phosphate range (0}0.22 mol kg\) and light intensity from 0 to 225 E m\ s\. U. irregularis
was dominant ('50% of the community), mainly at high temperature ('253C), very low nitrate
()0.001 mol kg\) and low to moderate phosphate concentrations (0.025}0.12 mol kg\).
Cell densities of U. irregularis were positively correlated with temperature and light, both of
which are highly correlated with each other (Fig. 7). A mere 18% of total variance of U. irregularis
could be explained with the following equation:
log(U.irr) "!1.09#0.19temperature!0.34log(light)#3.26phosphate.
3.8
Temperature explained 10.5%, light 4.4% and phosphate 3.1% of the variance.
1972
M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
Fig. 9. Distribution of cell densities of G. ericsonii with respect to temperature, phosphate and light. Pearson correlation
coe$cients for the upper and lower photic zone are given in the plots.
4.2.3. U. tenuis
Although U. tenuis was a frequently occurring taxon, cell densities higher than 5;10 cells l\
occurred only at a narrow range of environmental parameters: temperatures between 22 and 243C,
a salinity range of 34.8}35.2, low nitrate concentrations ((0.01 mol kg\), a wide phosphate
range (0.01}0.22 mol kg\) and low light (25 E m\ s\). U. tenuis was dominant at a salinity
higher than 35.0, when phosphate varied from 0.02 to 0.07 mol kg\.
Cell densities of U. tenuis showed a weak negative correlation with temperature and light in the
UPZ (Fig. 8). In the UPZ 21% (R ) of the total variance of this species is explained by
log(U.ten) "5.54!0.10temperature!0.27log(light)#3.78phosphate.
3.8
Temperature explained 16%, phosphate 1.9% and light 3.1% of the total variance.
4.2.4. G. ericsonii
This species was commonly associated with U. tenuis and E. huxleyi. It was present over
a relatively narrow range of environmental conditions. Its highest cell densities occurred at 233C,
high salinity (35.0}35.2), low nitrate concentrations ((0.03 mol kg\) and low light intensities
M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
1973
Fig. 10. Cell densities of F. profunda with respect to temperature, nitrate and light. Pearson correlation coe$cients for the
upper and lower photic zone are given in the plots.
Table 2
Environmental parameters controlling the variability of the dominant coccolithophore taxa as obtained by multiple
correlation analyses
Species
Environmental parameters
Temperature
E. huxleyi
U. irregularis
U. tenuis
G. ericsonii
F. profunda
x
x
x
x
Salinity
Light
o
x
Nitrate
o
Phosphate
R
o
o
o
0.67
0.18
0.21
0.46
0.63
(x) refers to the environmental parameter that explains the largest proportion of the variance in cell density; (o)
indicates the second and (-) the third environmental parameter in the regression model. The adjusted coe$cient of
determination (R ) was preferred as it only improves if the added variable in the multiple regression equation is
signi"cant.
M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
1974
(5}10 E m\ s\). Phosphate was low ((0.07 mol kg\) except in one sample in which it was
higher than 0.2 mol kg\. The relative abundance of G. ericsonii increased to 30% at conditions
similar to those with high cell concentrations.
Forty-six percent of the variance of this taxon can be explained by the following equation:
log(G.eric)"10.37!0.32temperature#3.62phosphate!0.28log(light).
Temperature explained 42% of the variance, phosphate and light 2%.
4.2.5. F. profunda
This species was common around 100 m water depth. High cell densities ('5;10 cells l\)
occurred when temperature and light were low (21}223C and (10 E m\ s\, respectively),
salinity was '35.0 and nutrient availability was high (nitrate 0.3 mol kg\ and phosphate
0.02}0.22 mol kg\). This taxon was relatively abundant ('20%) in almost all the samples in
which it was present, even when its cell density was low.
For the LPZ 63% of the variance is explained by the equation
log(F.prof )"3.88#0.42log(light)!0.21nitrate.
Light explained 53% of the variability and nitrate 10%.
5. Discussion
5.1. Abiotic (bottom-up) control
Coccolithophores in the upper 200 m are in#uenced mainly by the availability of nutrients
(nitrate and phosphate) and light (Brand, 1994). This is, in general, con"rmed by our results.
However, the individual in#uence of these parameters on coccolithophore cell densities varies with
water depth. In the UPZ, coccolithophores are apparently in#uenced by temperature and the
availability of phosphate, whereas in the LPZ, light and nitrate seem to control the presence/absence of coccolithophores. The results of the PCA and the multiple regression models
con"rm the existence of the two-layers model proposed by Dugdale (1967) for oligotrophic areas.
In that model phytoplankton growth, including coccolithophores, is limited mainly by nutrients in
the upper and light in the lower photic zone.
Multiple regression analysis supports the division of the photic zone into a nutrient- and
a light-limited system. Furthermore, it is obvious that in this region relatively small variations in
nutrient supply or in temperature (bottom-up e!ect) play a decisive role in the population
dynamics of coccolithophores. The unexplained variance of coccolithophore cell densities may be
due to forcing by abiotic parameters other than those monitored here (including vitamins and trace
metals) or to biotic processes such as grazing, competition with other phytoplankton groups or
viral infections (Carlucci and Bowes, 1970; Brand et al., 1983; Sunda, 1988/1989) or to randomness.
Mesozooplankton grazing on phytoplankton seems to be responsible for only a small amount of
loss of phytoplankton standing stocks at ALOHA (Landry et al., 1996). In addition, phytoplankton
might react with a time lag to environmental changes (Sommer, 1989). However, this e!ect could
not be tested in our data set because of the limited temporal resolution of the sampling period (on
average 30 d).
M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
1975
5.2. Ecological preferences of the dominant taxa
5.2.1. E. huxleyi
This taxon occurred in high concentrations when nitrate concentrations were very low, as was
also observed by Strickland and Eppley (1970). However, the multiple regression model indicates
that temperature is an important factor that explains more than 40% of the variance of E. huxleyi
cell densities at ALOHA. The optimum temperature of this species is 233C (Fig. 11), well within the
optimum range known from culture experiments that varied between 18 and 243C (Paasche, 1967,
1968; Brand, 1982; Fisher and Honjo, 1991). Tyrrell and Taylor (1996) proposed high light
intensities, low phosphate and calm conditions as main parameters fostering the blooming of E.
huxleyi in the North Atlantic. At ALOHA, such conditions were present during late summer and
fall. Temperatures, however, may have been too high ('243C) for optimum development of E.
huxleyi. Such a temperature limitation also is suggested by the distribution of relative abundance of
this taxon. When the temperature increased to more than 243C this species never reached more
than 30% within the coccolithophore community. The high concentrations observed in the second
year may be a result of the special conditions in the system produced partially by the shallow lens of
low-salinity waters observed from February until April 1995, together with the unusually high
phosphate concentrations associated with a winter injection event (February 1995).
Three morphotypes of E. huxleyi were encountered: A, C and var. corona (Young and Westbroek,
1991). Morphotypes A and C co-occurred, whereas E. huxleyi var. corona only occurred at high
concentrations in two samples (HOT 67 at 75 and 100 m) characterised by phosphate depletion.
This suggests that the ecological requirements of types A and C are the same and that both are
di!erent from those of E. huxleyi var. corona.
Fig. 11. Ecological preferences of dominant coccolithophore taxa. The preferences were determined by weighted
averages of the environmental parameters with the corresponding cell densities in all the samples where the taxon was
observed. Ranges are not given, as all the dominant species, except F. profunda, were observed throughout the spectrum
of environmental conditions (see Appendix A on CD-ROM).
1976
M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
5.2.2. U. irregularis
This species was present throughout the year, but it occurred at high concentrations only at
temperatures '223C. This is within the optimum range reported for the Atlantic and Paci"c
Oceans by McIntyre and BeH (1967) and Okada and McIntyre (1979). U. irregularis was the
dominant species in the community ('50%) at temperatures '253C and at the lowest nitrate
concentrations ()0.01 mol kg\) (Fig. 11). U. irregularis is considered one of the most oligotrophic coccolithophore species. Its abundance peaks occurred when phosphate concentrations
were relatively high (fall 1995). Simple correlations showed the negative relationship with nitrate
also previously reported by Kleijne et al. (1989).
5.2.3. U. tenuis
At ALOHA, this species occurred preferentially at intermediate temperatures (22}243C; Fig. 11),
clearly below the range preferred by U. irregularis as also reported by other authors in the Central
North Paci"c (Okada and McIntyre, 1977) and in the Western North Atlantic (Okada and
McIntyre, 1979; Haidar and Thierstein, 2001). Although this species has been found at high
concentrations at 293C or more in the Gulf of Aden and Red Sea (Kleijne et al., 1989; Kleijne, 1993),
high cell densities or relative abundances were not found at ALOHA at temperatures above 253C
(Fig. 11). This taxon appears restricted to low light intensities ((30 E m\ s\), usually occurring between 50 and 75 m depth. Comparably low light conditions have been reported for this
species at Bermuda (Haidar and Thierstein, 2001). U. tenuis is a characteristic species of oligotrophic conditions. It prefers waters that are almost nitrate-depleted ((0.02 mol kg\) .
5.2.4. G. ericsonii
The presence of this species was restricted to a narrow range of environmental conditions. G.
ericsonii often co-occurred with E. huxleyi and U. tenuis, overlapping their ecological niches (Fig.
11). Maximum concentrations occurred at 233C, in agreement with evidence from the Atlantic
(Okada and McIntyre, 1977). G. ericsonii was observed at lower temperatures (16}203C) in the
Southern California Bight (Ziveri et al., 1995). G. ericsonii seems to be mostly nitrate-limited
because it #ourished mainly at concentrations between 0.3 and 0.5 mol kg\, rather than phosphate-limited, because high cell densities ('5;10 cells l\) occurred at all phosphate concentrations measured at ALOHA. However, its highest concentrations in the upper photic zone coincided
with an increase in phosphate during 1994 (compare Fig. 2f and 3e). Apparently, G. ericsonii does
not have a narrow preferential salinity range. It was frequent at 35.0 or more, but it was also
present at salinities as low as 34.3. In the Central Red Sea, Winter et al. (1979) reported the presence
of G. ericsonii at very high salinities (max. 41).
5.2.5. F. profunda
This taxon was usually present at or below 100 m depth where light intensity is very low
((5 E m\ s\; Fig. 11). The light requirements of this taxon are much lower than those of most
coccolithophores (Okada and Honjo, 1973; Reid, 1980; Brand, 1994). The multiple regression
model con"rms that the distribution of F. profunda is mainly in#uenced by light and to a minor
degree by nutrients. F. profunda was present throughout the year, and its highest cell densities
occurred at the same time as the highest cell densities of the most important taxa from the upper
layers, E. huxleyi in winter and U. irregularis in late summer and fall, both of which also responded
M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
1977
to slightly elevated phosphate contents. The relative abundance of F. profunda in sediments has
been associated with water transparency (Ahagon et al., 1993), i.e. this species was more abundant
when very few coccolithophores were present in the upper layers (Haidar and Thierstein, 2001).
Furthermore, relative abundance changes of F. profunda were used as an indicator for past changes
in water turbidity or productivity in several deep-sea cores from the Equatorial Atlantic (Mol"no
and McInyre, 1990) and from the Equatorial Indian Ocean (Beaufort et al., 1997). However, at
ALOHA F. profunda peaks tended to develop simultaneously with peaks of E. huxleyi, U.
irregularis and U. tenuis in the overlaying surface waters.
5.3. Ecological niche partitioning
Each of the dominant coccolithophore species responded di!erentially to the environmental
parameters. These responses, presented by weighted averages of cell density abundance with
respect to the various environmental parameters, suggest a well-di!erentiated coccolithophore
community structure, not only with respect to water depth but also with respect to temporal
(seasonal and interannual) environmental variability (Fig. 11).
Most of the species present preferred temperatures above 223C. U. irregularis thrived at
temperatures higher than 243C. F. profunda preferred temperatures below 213C. Both species
represent the end members of the environmental variable spectrum. U. irregularis was dominant
under the most oligotrophic conditions: high temperature and low-nitrate concentrations. U. tenuis
thrived at intermediate temperatures below the range preferred by U. irregularis. It preferred
intermediate depths and lower light intensities. High cell densities of this species occurred when
nutrients, mainly phosphate, were injected. F. profunda occurred at low light intensities, usually at
or below 100 m depth, and also at times of elevated nutrient concentrations. Its highest cell
densities coincided with those of the most important taxa from the upper layers, E. huxleyi in winter
and U. irregularis in late summer and fall, suggesting that not only light intensity but also nutrient
supply is an important limiting factor for this taxon. G. ericsonii preferred intermediate temperatures. Its distribution was similar to that of E. huxleyi with which it was frequently associated.
A similar coccolithophore community structure was observed at the Climax area (Venrick, 1999).
Within LPZ, U. irregularis and U. tenuis were present and F. profunda was characteristic for the
deep photic zone. The cosmopolitan species, E. huxleyi, was preferentially found in the middle
photic zone around 100 m. As in ALOHA, E. huxleyi was usually correlated with G. ericsonii
(Venrick, pers. Comm.).
5.4. Comparison between HOT and BATS
At station ALOHA cell densities were generally lower than in the North Atlantic Central Gyre.
Haidar and Thierstein (2001) reported cell densities of up to 100;10 cells l\ at the Bermuda
time-series station, which is twice as high as the maximum at ALOHA. Furthermore, there is
a larger seasonal variation in coccolithophore cell densities than at station ALOHA. At BATS
coccolithophore densities increased mainly in the upper 50 m during springtime whereas at station
ALOHA, increased cell densities of coccolithophores occurred twice a year, in winter and summer/fall, at 75}100 m depth. In winter the mixed layer deepened at station ALOHA resulting in
increased nutrient supply into the photic zone (Fig. 2c, e and f ). In summer and fall when the
1978
M.Y. Corte& s et al. / Deep-Sea Research II 48 (2001) 1957}1981
surface waters are strati"ed, there are nutrient injection events of short duration (Fig. 2e and f; Karl
et al., 1996b). At BATS a deepening of the mixed layer that is much stronger than at ALOHA
occurred only once a year, during winter/spring, resulting in high nitrate concentrations that
reached the surface waters. Maximum nitrate concentrations at BATS during spring were 65 times
higher than at ALOHA, but the corresponding cell density was only "ve times higher. On the other
hand, phosphate concentrations at ALOHA were twice as high as at Bermuda for the same period.
The highest cell density (30;10 cells l\) in the upper 5 m at ALOHA occurred when nitrate was
depleted, but coincided with an increase of phosphate (0.18 mol kg\). Although the environmental conditions at ALOHA and BATS are di!erent, the relative ecological niche partitioning is
exactly the same for the dominant taxa.
6. Conclusions
During the sampling period of this study (January 1994}August 1996), no coccolithophore
blooms of millions of cells per litre occurred as in the North Atlantic. Although coccolithophore
abundances occasionally increased (e.g., E. huxleyi) during periods when upper waters were well
mixed, they never attained characteristic bloom quantities ('10 cells l\).
The environmental parameters considered in this study show a strong di!erentiation between
the upper and lower photic zone. This separation is re#ected in the taxonomic composition and cell
density of coccolithophores. Separate analyses of coccolithophore taxa of the upper and lower
photic zone revealed distinct responses to environmental parameters. In the upper photic zone,
coccolithophores are mostly in#uenced by temperature and availability of phosphate more than
nitrate concentrations. In contrast, the important variables in the lower photic zone are light and
temperature.
Seasonal temperature variations seem to be an important controlling factor for the dynamics of the
main coccolithophore taxa in the upper photic zone. In winter, when temperatures are lower than
233C, E. huxleyi, U. tenuis and/or G. ericsonii were abundant. In summer/fall, the dominant species in
the upper photic zone changed to U. irregularis and to a lesser degree to U. tenuis when temperatures
increased to more than 243C, and to F. profunda almost exclusively in the lower photic zone.
Measured changes of the abiotic environmental parameters such as light and temperature alone
appeared to explain more than 50% of the variance of most of the dominant taxa.
Acknowledgements
We thank D. Karl, D. Hebel, L. Tupas, L. Fujieki and the sta! of the Hawaiian time-series group
for the collection of water samples during cruises HOT 49}76 and for the generous access to
environmental data. We are grateful to E. Venrick and an anonymous reviewer for their valuable
comments. This project was supported by the Swiss National Science Foundation.
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