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Marine Micropaleontology

Coccolithophore export production during the 1997–1998 El Nino

event in Santa Barbara Basin (California)

Bianca De Bernardia,b,T, Patrizia Ziverib, Elisabetta Erbaa, Robert C. Thunellc

aDepartment of Earth Sciences bArdito DesioQ, University of Milan, Via Mangiagalli 34, 20133, Milano, ItalybDepartment of Paleoecology and Paleoclimatology, Fac. of Earth and Life Sciences, Vrije Universiteit Amsterdam, The Netherlands

cDepartment of Geological Sciences, University of South Carolina, Columbia, South Carolina 29208, USA

Received 24 May 2004; received in revised form 18 January 2005; accepted 1 February 2005

Abstract

The response of coccolithophore export production to non-El Nino and El Nino conditions was monitored during a two

year period (26 March 1996–3 April 1998) in the centre of the Santa Barbara Basin (34814V N; 120802V W), California

borderland. During the 1997–1998 El Nino the seasonal cycle of the surface water conditions was altered by the presence

of a relatively warm, low-nutrient and low-salinity water mass. Throughout the studied period, the total mass flux is

dominated by lithogenic components with terrigenous input being highest during El Nino period. Although the annual

biogenic sediment fluxes were largely dominated by silica, with diatoms as the major contributor to the opal flux, the

coccolith flux was high during the entire studied period. During winter 1998 carbonate fluxes were unusually high for this

time of the year. Moreover, a strong positive correlation between organic carbon and opal flux indicates that siliceous

phytoplankton production is the most important factor controlling organic carbon flux in the Santa Barbara Basin. A

positive correlation between carbonate and organic carbon fluxes existed indeed during the final phase of El Nino, when

the correlation between organic carbon and opal fluxes is poor. The sinking coccolithophore assemblage was dominated by

Emiliania huxleyi, followed by Florisphaera profunda, Umbilicosphaera sibogae, Gephyrocapsa oceanica, Helicosphaera

carteri, Gephyrocapsa muellerae and Calcidiscus leptoporus. The intensification of El Nino 1997–1998 conditions altered

the typical hydrographic structure of the Santa Barbara Basin weakening the spring upwelling as reflected by reduced

diatom fluxes. In contrast, the coccolith flux was relatively high during El Nino, particularly for the tropical species G.

oceanica, that showed a pronounced increase in its flux when the spring upwelling was reduced under El Nino conditions.

In addition, we have found that this species has a strong correlation with nitrite, phosphate and iron availability in surface

water.

D 2005 Elsevier B.V. All rights reserved.

Keywords: coccolithophores; phytoplankton; sediment trap; Santa Barbara Basin; El Nino Southern oscillation

0377-8398/$ - s

doi:10.1016/j.m

T Correspondi

E-mail addr

55 (2005) 107–125

ee front matter D 2005 Elsevier B.V. All rights reserved.

armicro.2005.02.003

ng author. Fax: +39 0250315494.

ess: bianca.debernardi@unimi.it (B. De Bernardi).

B. De Bernardi et al. / Marine Micropaleontology 55 (2005) 107–125108

1. Introduction

Coccolithophores constitute one of the major

groups of marine phytoplankton and are most

abundant in the warm, stratified waters of low

latitude regions (Honjo and Okada, 1974; Cortes et

al., 2001). In coastal upwelling environments, several

studies (Winter, 1985; Ziveri et al., 1995a; Broerse,

2000) have shown that coccolithophores can be

important contributors to the phytoplankton com-

munity. Using a time series of sediment trap samples

collected from the Santa Barbara Basin (SBB) we

monitored the response of the coccolithophores to

seasonal hydrographic changes in this part of the

California Borderlands. During late 1997 and early

1998 the coastal ocean off western North America

was anomalously warm due to one of the strongest

episodes of El Nino (EN) ever recorded (McPhaden,

1999). Previous works in this basin, during this EN

anomaly, have shown a deepening of the thermo-

cline, warming of surface water and reduced nutrient

concentration altering the development of the plank-

ton communities (Lange et al., 1997; Kincaid et al.,

2000; Black et al., 2001).

Fig. 1. Bathymetric map of the SBB showing the locatio

In this paper we will discuss the coccolithophore

export production at 500 m water depth in the SBB

during a two-year period (26 March 1996–3 April

1998) in response to non-EN (1996) and EN (1997–

98) conditions. These fluxes are compared with

concurrent hydrographic data collected at the trap

site. The main hypotheses that we want to test are:

(1) is there a coccolithophore community change

reflecting the EN anomaly? and (2) can coccolith

ecology be used to reconstruct paleo-EN conditions

in this region?

2. Study site

The SBB is the northern-most basin of the

Southern California Borderlands (Fig. 1). Seasonal

changes in the position of the North Pacific High

and the adjacent continental thermal low result in

changes in wind speed and direction, which in turn

control the strength of the California Current. During

the spring and early summer, prevailing northerly

winds cause Ekman-induced strong upwelling (Hen-

dershott and Winant, 1996; Harms and Winant,

n of the sediment trap mooring used in this study.

B. De Bernardi et al. / Marine Micropaleontology 55 (2005) 107–125 109

1998). In our study period (March 1996–April 1998)

the upwelling interval was clearly identified by

isotherms shoaling (Fig. 2). During fall and winter,

the northerly component of the wind weakens,

upwelling is diminished and precipitation and runoff

are typically enhanced (Soutar and Crill, 1977;

Thunell et al., 1995). During EN anomalies the

California Current weakens and warm tropical–sub-

tropical waters propagate northward, along the west-

ern margin of North America.

2.1. ENSO’s indices

The oceanographic conditions of SBB are strongly

seasonal with winds controlling the intensity of the

California Current. Quasi-periodic anomalies to this

pattern are associated with the El Nino Southern

Oscillation (ENSO), the most important coupled

ocean–atmosphere phenomenon to cause global cli-

mate variability at interannual time scale. EN anom-

aly, representing the warm phase of ENSO, is a

disruption of the ocean–atmosphere system in the

tropical Pacific which has important consequences for

global weather patterns. EN conditions are usually

followed by La Nina (LN), a series of colder than

normal ocean waters in the equatorial Pacific.

The 1997–98 EN event represents one of the most

intense EN in the last 120 years, with major climatic

impacts felt around the world (McPhaden, 1999).

There are a number of indices that quantify the

presence and intensity of EN (Wolter and Timlin,

1998). Two indices were used in this study (Fig. 2).

The first one is the Multivariate ENSO Index (MEI)

based on six main variables over the tropical Pacific:

sea level pressure, zonal and meridional components

of the surface wind, sea surface temperature, surface

air temperature and total cloudiness (all values are

normalized for each bimonthly period). Data on MEI

are available at: http://www.cdc.noaa.gov/people/

klaus.wolter/MEI/table.html. Positive values represent

the EN phase of ENSO.

The second index, Northern Oscillation Index

(NOI; Schwing et al., 2002a), is based on the

difference in sea level pressure anomaly at the North

Pacific High (northeast Pacific—358N, 1308W) and

near Darwin (Australia—108S, 1308E). The non-

normalized NOI data are available on line at: http://

www.pfeg.noaa.gov. NOI is negative during EN

conditions and negatively correlated with the MEI.

The strong correlation between these two independent

climatic indices confirms that the atmosphere and the

ocean are strongly coupled during EN and non-EN

conditions in the Northeast Pacific (Schwing et al.,

2002b).

Using the NOI and MEI indices, we have

subdivided the study interval into three main periods

(Fig. 2): I) period A (non-EN conditions), from March

1996 though February 1997; II) period B (transition

phase—rapid growth from neutral to EN), from March

1997 up to July 1997, and III) period C (EN mature

phase), from August 1997 up to April 1998. In this

last period the EN was very strong with a slight

weakening in October–December 1997.

2.2. Climatic and surface hydrographic settings

Surface water temperatures in SBB show a

distinct seasonal pattern (Fig. 2). During spring

upwelling in 1996 the upper 50 m of the water

column recorded temperatures between 15 and 10

8C. In contrast, the stratified surface waters in the

summer reached 19 8C (July–August). During EN

conditions, temperature, salinity and density of the

upper 75 m changed significantly (Shipe and

Brzezinski, 2001). Temperature anomalies were

exceptionally large between spring 1997 and summer

1998. Dever and Winant (2002) observed two peaks

in temperature anomalies (increase up to 4 8C): thefirst one in June 1997 and the second one from the

end of September 1997 to February 1998 (with

maximum in November 1997 through January 1998).

The 1997 spring was characterized by an intense but

short upwelling period (March–May) as shown by

shoaling of isotherms (Fig. 2). The first peak in the

temperature anomaly started in June 1997 with a

delay of about three months from the beginning of

EN as identified by NOI and MEI indices. This

temperature anomaly showed maximum amplitude at

the surface and decreased quickly with depth and

towards the north. The warmest sea surface waters in

this period occurred in October 1997 (21.1 8C; ~48C higher than the previous year) and identify the

mature phase of EN in SBB. The water temperature

decreased rapidly at the end of 1997 and early 1998.

Nutrient levels during the EN 97–98 were unusu-

ally low for this region. In a site near our trap location,

Fig. 2. Monthly Multivariate ENSO Index (MEI, outlined line) and Northern Oscillation Index (NOI, solid line) for January 1996–December

1998 (modified after Schwing et al., 2002b). Temperature time series (isotherms are in centigrade degree) for March 1996 through March 1998

based on bi-weekly CTD casts at the sediment trap mooring site. Time/depth plot of phosphate, nitrite and nitrate concentration (measured

quarterly) at CalCOFI station 82.47 in Santa Barbara Basin.

B. De Bernardi et al. / Marine Micropaleontology 55 (2005) 107–125110

B. De Bernardi et al. / Marine Micropaleontology 55 (2005) 107–125 111

Shipe et al. (2002) observed that nitrate concentrations

from the surface to 75 m depth were b2.0 AM/l in

November 1997, while during the fall–early winter of

the previous year nitrate concentrations ranged

between 10 and 20 AM/l. However, during spring

1997, when the nutrient concentrations were

dnormallyT high, the nitrate concentration was above

average (Fig. 2) and returned below average in August

1997. Between October 1997 and January 1998

dissolved silicon and phosphate concentrations in

the upper 75 m were also below average (b5 AM/l

and b0.45 AM/l, respectively; Shipe et al., 2002).

Moreover, there was an abrupt decrease in density in

June 1997 and an unusually low density and low

salinity water mass remained in the channel until the

spring 1998.

3. Materials and methods

Sediment trap samples were recovered from the

centre of the SBB (34814V N; 120802V W), using a

Mark VI instrument between 26 March 1996 and 8

April 1998. The sediment trap was recovered and

redeployed every 6 months. Two hiatuses (attributed

to clogging to the trap during two different periods)

exist in the data set, one of 19 days between 10 and 23

September 1996 and the other one of 58 days,

between 24 March and 21 May 1997. The mooring

was deployed in 540 m water depth, with the sediment

trap positioned ~50 m above the sea floor. The 52

samples used in this study represent two years of

sedimentation; each sample represents a two-week

collection period except for the interval from 22 May

1997 to 25 June 1997 when the sampling resolution

increased to 7 days. Hydrographic data (temperature,

conductivity and density) were collected at the trap

site with two- to four-week intervals using a Sea Bird

Seacat 19 Profile fitted with an oxygen sensor and a

transmissometer. Nutrient concentrations for CalCOFI

(Scripps Institution of Oceanography) station 82.47 of

cruises 9602, 9604, 9608, 9702, 9704, 9707, 9709,

9802, and 9804 (www.mlrg.ucsd.edu/calcofi.html)

were used to construct Fig. 2. We generated 45-days

by 5 m data matrix from the original CalCOFI data-set

by a linear interpolation algorithm used to preserve

true data points. Prior to trap deployment, in each

sample cup, a buffered sodium acid solution was

placed as poison. Upon recovery, samples were

refrigerated and poisoned with HgCl2. Organic

carbon, calcium carbonate, biogenic silica and litho-

genic particle were determined by the methods

described in Thunell (1998a). For the iron mass

determination in the sediment trap samples, we used a

sample aliquot equal to the one for coccolith flux

quantification (see below). For the sample preparation

and analysis of iron concentration, we followed the

method described for carbonate fine fraction in

Broerse (2000).

For the coccolith analysis, aliquots of each sample

were wet split (1/6400) by a rotary precision splitter

(McLane WSD-10-deviation between aliquot b4%).

Two aliquots for each sample were selected for

coccosphere and coccolith flux quantification. For

coccolith analyses, the organic matter was oxidized

following the procedure described in Bairbakhish et

al. (1999). Each aliquot was then wet sieved under 32

Am mesh and the b32 Am fraction was filtered on

Millipore filter (HTTP 0.45 Am pore size; 47 mm

diameter). For coccosphere analysis we used the un-

oxidized aliquot (1/6400) b32 Am, and used a similar

filtering procedure. A portion of the filter was

mounted on a glass slide and fixed with Canada

balsam. For quantitative analysis of coccolithophores

we used a Leitz Laborlux microscope with parallel

and crossed nicols at �1250 magnification. Cocco-

liths and coccospheres were counted along several

parallel scans from the border to the center of the

filter, on an area of 3 and 14 mm2, respectively. The

numbers of coccoliths and coccospheres counted were

extrapolated for the entire samples using the method

described in Ziveri et al. (1999). The uniformity in the

coccolithophore distribution on the filter surface was

tested on representative samples from different pro-

duction episodes (during non-EN and EN periods) by

counting in various areas of the filter, ranging from

the border to the centre (deviation b6%). To check the

sieving efficiency, the taxonomic composition and to

evaluate coccolith preservation we used scanning

electron microscopy (SEM).

Using temperature, nitrite, nitrate, phosphate and

iron concentrations, we calculated the environmental

variables, in accordance with Legendre and Legendre

(1998). To avoid collinearity, we first used a Principal

Component Analysis (PCA) method on our environ-

mental data, applying Canoco software for Windows

B. De Bernardi et al. / Marine Micropaleontology 55 (2005) 107–125112

V4.5. The derived theoretical axes were tested in a

multiple linear regression analysis against the data for

the species of interest. The partial regression coef-

ficient (Beta) of this analysis was then multiplied by

the theoretical values of the matrix of the environ-

mental variables, as derived in the PCA. Ultimately,

this derived partial regression coefficient (RC) for the

separate environmental values indicates the explan-

atory value for the species data.

4. Biogenic and non-biogenic fluxes in SBB

4.1. Seasonal total particulate flux, foraminiferal and

siliceous plankton fluxes and coccolithophore export

production

The particulate flux in SBB is clearly controlled by

strong variability in seasonal atmospheric and oceanic

conditions. A significant amount of temporal varia-

bility exists in both total mass flux and fluxes of the

individual particulate component. Total mass flux

varied by an order of magnitude (0.94–9.09 g�2 d�1)

between March 1996 and April 1998 (Table 1, Fig. 3).

High terrigenous flux during fall and winter is due to

increased river input associated with the rainy season

(Soutar and Crill, 1977; Thunell et al., 1995). The

Santa Clara and Ventura rivers deliver over 90% of the

terrigenous sediment into SBB, and the source rocks

are mainly clastic (Fleischer, 1972). The biogenic opal

flux (mainly diatoms in Lange et al., 1990;) is highest

in spring and dominates the annual biogenic sediment

flux (Thunell, 1998a; Lange et al., 2000) in both years

(Fig. 3).

Twenty-eight coccolithophore species were identi-

fied during this study, but 7 species largely dominate

the coccolith assemblage. Coccolith and coccosphere

fluxes were dominated by Emiliania huxleyi, followed

by Floriphaera profunda, Umbilicosphaera sibogae,

Gephyrocapsa oceanica , Helicosphaera carteri ,

Gephyrocapsa muellerae and Calcidiscus leptoporus.

The remaining species contribution was b1% to the

coccolith assemblages.

4.1.1. Period A: (non-EN condition: March 1996–

February 1997)

During 1996–1997, the particulate flux patterns

reflected the seasonal hydrography of the basin; fluxes

were high during spring and summer and low in

winter (Fig. 3), similar to the patterns observed in

previous studies in the California Borderlands (Sautter

and Thunell, 1991; Thunell, 1998b). The biogenic

opal flux (mainly diatoms; Lange et al., 2000) was

highest during the spring upwelling and dominates the

annual biogenic particle flux. Organic matter, C vs. N

ratios and organic carbon isotopic composition

indicate that carbon is derived primarily from a

marine source phytoplankton (Thunell, 1998a).

Organic carbon flux always account for less than

5% of the total flux.

The planktonic foraminiferal and siliceous plank-

ton fluxes show both seasonal and interannual

variability in response to environmental changing

in SBB (Kincaid et al., 2000). Lange et al. (1997)

observed that fluxes of diatoms, radiolarians and

silicoflagellates in the SBB show a distinct seasonal

pattern: radiolarians in late summer and fall, silico-

flagellates in winter and diatoms in spring (Fig. 4).

During non-EN interval the foraminiferal population

increases quickly (Fig. 4), about one month after

spring upwelling. Foraminiferal maximum flux

occurs in late June–August 1996 when the surface

water was warm and strongly stratified (Kincaid et

al., 2000).

Period A is characterized by high coccosphere

fluxes which occurred during the fall season (average

coccosphere flux of 64.9�105 m�2 d�1), with

maximum fluxes in November 1996 and a daily

average throughout this interval of 47.2�105 m�2

d�1 (Fig. 5). High coccolith fluxes characterized the

fall season as well (1028.3�106 coccoliths m�2 d�1)

but the seasonality was more pronounced in cocco-

sphere than in coccolith fluxes (Figs. 5 and 6). This

difference may be due to the fact that a coccosphere

represents a complete organism. In contrast, the

number of coccoliths constituting the coccosphere

(and covering the cell) is variable (Ziveri et al., 1995a;

Young et al., 2003) and consequently, is less reliable

in seasonal signal. In addition, sediment resuspension

from storms, waves and downslope processes can

easily transport fine material including coccoliths

from the shelf to the centre of SBB (Thunell,

1998a), contributing to coccolith flux in the trap.

Coccolith and coccosphere fluxes were dominated by

E. huxleyi which represents 80% of the total coccolith

flux, followed by F. profunda (5%), U. sibogae (4%),

Table 1

Comparison of means, maxima and minima of biotic and water physical parameters measured in the SBB

March 1996–February 1997 March 1997–July 1997 August 1997–April 1998 Reference Sample type

Period A (non-El Nino condition) Period B (transitional phase) Period C (mature El Nino)

Average Minima Maxima Average Minima Maxima Average Minima Maxima

Temperature (8C) (upper 5 m) 14.8 April 12.8 August 17 16.4 April 12 July 19.9 17.2 April 13.75 October 21.09 this study SBB CTD cast

Nitrite (NO2) at 20 m (AM/l) 0.11 February 0.01 April 0.15 0.35 March 0.27 April 0,43 0.12 October 0.01 February 0.25 see capt method CalCOFI station 82.47

Nitrate (NO3) at 20 m (AM/l) 4.2 February 2.8 April 6.5 8.3 June 1.8 April 14.8 1.8 October 0.1 April 8 see capt method CalCOFI station 82.47

Phosphate (PO4) at 20 m (AM/l) 0.42 0.27 0.63 0.39 0.34 0.43 0.3 0.22 0.43 see capt method CalCOFI station 82.47

Chlorophyll (mg m�2) Average Feb 1996–April 1997 68 Average February 1997–April 1998 29 Shipe et al.,

2002

CalCOFI station 82.47

Iron flux (mg m�2 day�1) 18.9 June 9.81 February 35.91 37.1 May 19.43 May 51.02 40.7 October 21.89 February 113.16 this study sed. trap

Total mass flux (g m�2 day�1) 2.01 February 0.94 May 3.57 3.061 June 2.4 March 3.8 3.49 January 1.8 February 9.09 this study sed. trap

Terrigen flux (g m�2 day�1) 1.27 February 0.59 May 2.28 1.873 June 1.58 March 2.27 2.8 January 1.4 February 7.73 this study sed. trap

Carbonate flux (g m�2 day�1) 0.14 December 0.062 June 0.244 0.225 May 0.158 June 0.294 0.23 January 0.124 March 0.545 this study sed. trap

Organic carbon (g m�2 day�1) 0.09 February 0.04 April 0.198 0.144 June 0.110 June 0.182 0.1 January 0.051 February 0.183 this study sed. trap

Opal flux (g m�2 day�1) 0.37 January 0.143 April 0.962 0.617 July 0.328 March 1.02 0.23 January 0.09 October 0.4 this study sed. trap

Diatom flux

(num 105�m�2 day�1)

6.1 June 0.219 November 30.8 2.5 June 0.12 March 8.45 0.4 February 0.026 November 0.87 Lange et al.,

2000

sed. trap

Silicoflagellates flux

(num 103�m�2 day�1)

3.12 May 0.04 October 15.3 1.46 June 0.22 May 3.9 1.03 February 0.073 March 2.45 Lange et al.,

2000

sed. trap

Radiolarian flux

(num 104�m�2 day�1)

1.2 May 0.53 December 2.50 2.1 May 1.7 May 2.93 0.46 December 0.11 October 2.90 Lange et al.,

2000

sed. trap

Foraminiferal flux

(individuals�m�2 day�1)

b2000 Jan.1997 b1000 November ~6600 ~7500 March ~2000 May ~13000 ~1000 October b200 August ~4000 Black et al.,

2001

sed. trap

Coccolith species flux (num 106�m�2 day�1)

Total coccolith 1037.9 171.1 1571.3 1431.1 355.7 3237.9 1833.1 694.7 2783.8 this study sed. trap

E. huxleyi 835.8 43.6 14.25 1146.6 283.6 2791.1 1287.5 433.4 1962.1 this study sed. trap

F. profunda 51.4 8.1 86.5 91.8 16.7 177 116.4 5.56 215.2 this study sed. trap

U. sibogae 42.2 0.7 258.8 30.8 50.3 77.9 70.2 – 281.1 this study sed. trap

G. oceanica 33.4 7.3 144 74.7 7.6 173.3 261.4 19.1 808.1 this study sed. trap

H. carteri 30.1 3.35 71.4 28.8 6.9 106.5 38.9 9.7 71.9 this study sed. trap

G. muellerae 20.6 8.1 51.9 28.5 9.3 62.8 28.6 6.7 57.3 this study sed. trap

C. leptoporus 7.9 1.01 43.6 16 3.3 38.7 18.4 4.5 38.2 this study sed. trap

Coccosphere species flux (num 105�m�2 day�1)

Total coccosphere 47.2 8.6 87.6 54.7 24.7 102.4 26.4 6.4 51.2 this study sed. trap

E. huxleyi 37.4 8.6 79.7 34.6 10.9 74.9 15.8 4.5 27.4 this study sed. trap

F. profunda 0.6 – 2.9 0.1 – 0.7 0.3 – 1.8 this study sed. trap

U. sibogae 1.8 – 5.7 0.9 – 3.6 0.3 – 1.8 this study sed. trap

G. oceanica 1.2 – 5.7 12.1 1.8 29.2 7.3 0.9 21 this study sed. trap

H. carteri 3.3 – 12.9 1.3 – 5.4 0.7 – 2.7 this study sed. trap

G. muellerae 1.2 – 4.3 3 – 10.1 0.5 – 1.8 this study sed. trap

C. leptoporus 0.2 – 1.4 0.3 – 1.8 0.5 – 2.7 this study sed. trap

B.DeBern

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al./Marin

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paleo

ntology55(2005)107–125

113

Fig. 3. Total mass, terrigenous, iron, carbonate, organic carbon and opaline silica fluxes for the period March 1996 through April 1998.

B. De Bernardi et al. / Marine Micropaleontology 55 (2005) 107–125114

G. oceanica (3%), H. carteri (3%), G. muellerae (2%)

and C. leptoporus (1%) (Fig. 7). F. profunda was the

second most abundant species in this study, with high

coccosphere fluxes in fall when the water column was

stratified and the thermocline was deep (Fig. 5). A

bloom of U. sibogae occurred during the late summer

period, with a maximum of coccolith flux in

September (258.8�106 coccoliths m�2 d�1) when

Fig. 4. Average daily fluxes of silicoflagellates, radiolarians, diatoms and foraminiferal fluxes from January 1996 to April 1998.

B. De Bernardi et al. / Marine Micropaleontology 55 (2005) 107–125 115

the column water was strongly stratified; the super-

ficial layer was warm (16 8C upper 25 m) and the

other phytoplankton groups were less abundant (Fig.

6). Fluxes of G. oceanica remained relatively low

during period A, with a minor increase in early 1997

(Fig. 5). H. carteri coccosphere and coccolith fluxes

were highest during the spring period of both years

(1996 and 1997), with maximum fluxes in March

1996 (daily average coccoliths 71.4�106 m�2 d�1)

and, February 1997 (daily average 10�105 cocco-

spheres m�2 d�1; Fig. 6) when upwelled waters

entered the basin increasing primary productivity (Fig.

Fig. 5. Coccolith (bars, scale at left) and coccosphere (line, scale at right) fluxes for the total and the major individual species of

coccolithophores in the SBB. The three main ENSO phases are also indicated.

B. De Bernardi et al. / Marine Micropaleontology 55 (2005) 107–125116

6). C. leptoporus shows low fluxes throughout period

A, except for a brief peak in July 1996 (43.6�106

coccoliths m�2 d�1).

4.1.2. Period B: (transitional phase: March 1997–

July 1997)

During this period biogeochemical fluxes increase

more than 50% and are dominated by the lithogenic

components. Starting from March 1997 foraminiferal

total flux increases enormously, reaching a peak

value of nearly 13,000 individuals m�2 d�1 at the

end of May (Fig. 4). At this time the foraminiferal

flux was more than four times greater than values

measured during the 1996 upwelling season (Black

et al., 2001).

During period B (March–June 1997) the average

coccolith flux was 1431.1�106 coccoliths m�2 d�1

and the coccosphere flux was slightly higher than

the previous period (56.1�105 coccospheres m�2

d�1) (Fig. 5). Period B is mainly characterized by

elevated fluxes of G. oceanica coccospheres. This

species shows a pronounced increase in coccosphere

flux after March 1997, with maximum flux recorded

in June 1997 (29.2�105 coccospheres m�2 d�1)

Fig. 6. Coccolith (bars, scale at left) and coccosphere (line, scale at right) fluxes of U. sibogae, H. carteri, G. muellerae, and C. leptoporus

during the experiment in SBB. The three main ENSO phases are also indicated.

B. De Bernardi et al. / Marine Micropaleontology 55 (2005) 107–125 117

contributing up to 50% of the total coccosphere

flux.

F. profunda average coccolith flux was slightly

higher with respect to non-EN period (more than

25%). The other coccolithophore species fluxes did

not show a significant change compared with the

previous period.

4.1.3. Period C: (mature El Nino: August 1997–April

1998)

Throughout period C, the total mass flux is

dominated by lithogenic components (50–80%; Fig.

3) with terrigenous input being highest during EN

period, up to 8 vs. 1–2 g m�2 d�1 for the non-EN

period (Table 1). During winter 1998 carbonate

fluxes were unusually high. Moreover, a strong

usually positive correlation between organic carbon

and opal flux indicates that siliceous phytoplankton

production is the most important factor controlling

organic carbon flux in SBB. However, a positive

correlation between carbonate and organic carbon

fluxes existed indeed during the final phase of EN,

when the correlation between organic carbon and

opal fluxes is poor (Fig. 3). In particular, high value

Fig. 7. Relative abundances (a) of the most abundant coccolithophore species and cumulative (b) abundance of minor species (normalized

100%) in coccolith flux.

B. De Bernardi et al. / Marine Micropaleontology 55 (2005) 107–125118

in organic carbon flux coincided with a February

1998 peak in the carbonate flux (mainly delivered

by foraminiferal and coccolithophores, Thunell,

1998a; Kincaid et al., 2000) and high abundances

of tintinnids of genus Stenosella (Lange et al.,

2000).

During EN 97–98 a 20% decrease in radiolarian

flux (Lange et al., 1997) is paralleled by a major

decrease in the diatoms flux and an increase in the

abundance of warm water species. Moreover, the

fall–winter peak in silicoflagellates fluxes, occurring

annually from 1993 to 1996 (Kincaid et al., 2000), is

not observed. Finally, benthic diatoms increased in

winter 1998, probably reflecting the intense storm

activity, high precipitation, and lateral advection into

the central basin during the EN period (Lange et al.,

2000). Compared to the previous year, during fall

and winter 1997, there was a change in foraminiferal

population marked by a significant increase in warm-

water species (Globigerina rubescens and Globiger-

inoides ruber), generally absent under normal con-

dition (Black et al., 2001).

In period C the average coccolith flux is

relatively high (1833.1�106 coccoliths m�2 d�1)

but the coccosphere flux was lower (26.4�105

coccospheres m�2 d�1) than in the previous two

periods. The assemblages during period C are

characterized by an increase in G. oceanica

(12%), with E. huxleyi still being the dominant

species (71%). The other species present during this

period were F. profunda (7%), U. sibogae (4%), H.

carteri (2%), G. muellerae (1%) and C. leptoporus

(1%) (Fig. 6). From July 1997 to April 1998, when

the surface water temperatures were above average

(anomalies of up to 3–4 8C), coccolith and cocco-

sphere fluxes of G. oceanica are consistently high

(daily average 7.2�105 coccospheres m�2 d�1 and

261.4�106 coccoliths m�2 d�1). During mature EN

period, F. profunda was the third most important

species and showed a significant increase (~70%

with respect to previous year) in its coccolith flux

(Table 1). Helicosphaera carteri and G. muellerae

coccosphere fluxes remained relatively low during

this period. Umbilicosphaera sibogae was slightly

higher on average coccolith flux than the previous

year and showed a peak in its coccolith flux in

November. The coccolith flux of C. leptoporus was

higher on average than during non-EN and transi-

tional periods (Fig. 6), with maximum values in

July 1997 (38.7�106 coccoliths m�2 d�1).

B. De Bernardi et al. / Marine Micropaleontology 55 (2005) 107–125 119

4.2. Iron flux

Iron is one of the most abundant elements on Earth

but its concentration in seawater is very low (Johnson

et al., 1997). There is strong evidence that phyto-

plankton growth is limited by iron availability, as

demonstrated in studies in open-ocean waters (Martin

et al., 1994; Coale et al., 2004) and in coastal

upwelling areas (Hutchins and Bruland, 1998; John-

son et al., 1999). In the present study we used the iron

flux in the fine fraction (b20 Am) to observe the

relationship between iron availability and coccolitho-

phore flux. The iron flux was relatively low during

1996 (Table 1; Fig. 2). In early 1997 the iron flux

became significant and remained high for all 1997

(N42% higher than in previous year), reaching a peak

in February 1998 (Fig. 2).

It has been hypothesized that elevated iron

concentration in coastal regions may arise from river

input, resuspended sediment (Johnson et al., 1999) or

atmospheric deposition (Martin and Gordon, 1988). In

this study we found a strong correlation between iron

and lithogenic fluxes (r=0.88), as a result of excep-

tionally intense winter storm activity along the West

Coast (Lynn and Bograd, 2002) in December 1997–

February 1998. This pattern suggests that river input

and runoff from the continent to the basin play an

important role for the iron distribution in this area and

presumably phytoplankton fertilization.

5. Discussion

5.1. Plankton export production response to EN

97–98

The supply of sediments in the SBB is controlled by

seasonal changes in primary productivity and local

climatic changes which control the sedimentation in

the basin. During 1996–1998, the particulate flux

patterns reflected the seasonal hydrography of the

basin. The total mass flux was dominated by lithogenic

components with terrigenous input being three times

greater during EN than in the non-EN period. This

pattern reflects the higher rainfall, runoff, and down-

slope transport into the SBB. Samples collected during

this period contained many pollen grains, plant debris

and estuarine benthic foraminifers, further indicating

that considerable amounts of material were flushed

into the basin (Thunell et al., 1995; Lange et al., 2000).

The biogenic flux and species composition of the

plankton (foraminiferal, coccolithophore and sili-

ceous) community reflect both seasonal and interan-

nual variability in response to environmental changing

in SBB (Thunell et al., 1995; Lange et al., 1997;

Thunell, 1998a; Kincaid et al., 2000).

In non-EN years production maxima of diatoms

occur during spring upwelling, followed by radio-

larians in late summer–fall and, silicoflagellates in

winter. This characteristic seasonal trend was altered

during the EN 97–98 event. In fact, the warm water

incursions into the SBB and the diminished upwelling

are reflected by a decrease in total siliceous flux and a

change in assemblage composition with an increase in

percentage of warm species. In previous sediment trap

experiments in SBB it was found that EN events

reduced biogenic opal export production and

increased siliceous microfossil diversity (Lange et

al., 1997; Kincaid et al., 2000). In other coastal

locations, where the diatoms dominated during

seasonal upwelling such as S. Pedro and Cariaco

Basins, EN events are reflected by a decrease in total

annual silica flux and primary productivity (Sautter

and Thunell, 1991; Tedesco and Thunell, 2003). The

foraminiferal population increases quickly, circa one

month after upwelling period, probably due to

utilization of the diatoms as food (Kincaid et al.,

2000). Maximum foraminiferal fluxes occurred in

August 1996 when surface waters were strongly

stratified and sea surface temperatures were high.

During EN 97–98, relatively warm surface waters

(N20 8C) in the basin are reflected by the increased

fluxes of bwarmer-waterQ foraminifera (G. ruber and

G. rubescens), generally absent during non-EN

conditions (Black et al., 2001). Similar variations in

foraminiferal population during EN anomaly were

found in previous years (Lange et al., 1997; Kincaid et

al., 2000) and in other coastal basins characterized by

seasonal upwelling, such as San Pedro Basin (Sautter

and Thunell, 1991), the Gulf of California (Sancetta,

1995) and the more distant Cariaco Basin (Tedesco

and Thunell, 2003).

When the EN anomaly dominates the hydrographic

conditions of SBB, the annual coccolith flux increases

more than 46% with respect to the previous year. In

fact, the presence of warm water masses and the

B. De Bernardi et al. / Marine Micropaleontology 55 (2005) 107–125120

weakening of the spring upwelling allowed coccoli-

thophores to flourish and to adapt to eutrophic

conditions while outcompeting with diatoms limited

by silica depletion (Ziveri et al., 1995b, 2000).

5.2. Coccolithophore export production in upwelling

regions

The coccolith fluxes recorded in SBB are com-

pared with the fluxes measured by sediment traps in

other settings (Table 2). Annual coccolith fluxes in

SBB are of the same order of magnitude as those

estimated in areas of high fertility, such as the West

Pacific (Tanaka and Kawahata, 1991), Northeast

Atlantic (Beaufort and Heussner, 1999; Ziveri et al.,

2000) and Arabian Sea (Andruleit et al., 2000). The

high values reported for the Arabian Sea, two times

Table 2

Comparison of coccolith fluxes recorded by sediment trap studies in vari

Reference Region Location Settings

This work Pacific Santa

Barbara Basin

348 N 1208 W upwelling

This work Pacific Santa

Barbara Basin

348 N 1208 W upwelling

Broerse, 2000 Central Pacific 128 S 1358 W oligotrophic

Tanaka and Kawahata,

1991

West Pacific 28 S 1358 W Equatorial

Counter Cu

Ziveri and Thunell,

2000

Pacific Guaymas

basin

278 S 1118 W upwelling

Ziveri and Thunell,

2000

Pacific Guaymas

basin

278 S 1118 W upwelling

Broerse, 2000 Indian Somalia 108 S 538 E upwelling

Andruleit et al., 2000 Indian NE Arabian

Sea

248 S 658 W High Fertili

Sprengel et al., 2000 Atlantic Gran

Canaria

298 S 158 W upwelling

Sprengel et al., 2000 Atlantic Gran

Canaria

298 S 15 8W upwelling

Ziveri et al., 2000 Northeast Atlantic 488 N 218 W upwelling

Beaufort and

Heussner, 1999

Northeast Atlantic

Bay Biscay

448 N 28 W upwelling

Andruleit, 1997 Atlantic Norwegian

Sea

698 N 08 W Norwegian

Current

Andruleit, 1997 Atlantic Greenland 728 N 78 W Jan Mayen

Current

EN=El Nino; W-EN=weak El Nino; No-EN=No El Nino.

T =defined by http://www.cpc.ncep.noaa.gov/products/analysis_monitor

higher than those found in SBB, seem to be positively

correlated to lithogenic fluxes and do not seem to

represent real production phases exclusively, but also

resuspension and lateral advection processes. In

addition, the coccolith fluxes recorded in oligotrophic

regions are four times lower (Broerse, 2000) than

those found in this experiment. Coccolith fluxes

reported for other upwelling areas in the Pacific

(Guaymas Basin, Ziveri and Thunell, 2000), Atlantic

(Gran Canaria, Sprengel et al., 2000) and Indian

(Somalia, Broerse, 2000) are definitely much lower.

These different results can be explained by the effect

of resuspension on coccolith fluxes. More congruous

data are needed (e.g. coccolith vs. coccosphere fluxes)

before tracing a better picture of coccolithophore

production/fluxes and separate local, regional and

global changes.

ous settings

RemarksT Average

coccolith

flux (num�106 m�2 d�1)

Deployment time Trap

depth (m)

No-EN 994 Mar 1996 Feb 1997 540

strong EN 1640 Mar 1997 Apr 1998 540

EN 222 Feb 1992 Jan 1993 1292

rrent

EN 1800 June 1991 March1992 1592

W-EN 240 Jan–1991 Dec–1991 700

EN 310 Jan–1992 Dec–1992 700

No-EN 488 June1992 Feb 1993 1032

ty No-EN ~3000 March 1995 Feb 1996 590

No-EN 425 Jan–1995 Dec–1995 1000

No-EN 689 Jan–1996 Dec–1996 1000

No-EN 900 Apr–1989 Apr–1990 1000

No-EN 889 June 1990 Aug 1991 1900

EN 4 Aug 1991 July 1992 500

EN b1 Aug 1991 July 1992 500

ing/ensostuff/ensoyears.html.

B. De Bernardi et al. / Marine Micropaleontology 55 (2005) 107–125 121

5.3. Coccolithophore ecology in SBB

Both E. huxleyi and G. oceanica may respond

positively to nutrient enrichment, such as in equato-

rial and coastal upwelling areas, and marginal seas

(Okada and Honjo, 1975; Broerse, 2000). G.

oceanica usually dominates in tropical and sub-

tropical regions (McIntyre et al., 1970; Andruleit et

al., 2000, 2003), while E. huxleyi is the most

cosmopolitan coccolithophore species. The relatively

high flux of E. huxleyi during weak LN (period A—

Fig. 5) shows the preference of this species for cool

upwelling conditions. In contrast, the abrupt increase

in G. oceanica coccosphere flux during period B,

and its relative high contribution to the coccolith

assemblage during period C, shows a clear associ-

ation of this species with warm water (up to ~3 8Cduring EN than during non-EN, in the upper 20 m).

Several studies discussed the relationship between

G. oceanica and E. huxleyi, and proposed their ratio

Fig. 8. Correlation plot of G. oceanica coccosphere fluxes versus phosph

March 1996 to April 1998. Pearson correlation coefficient for the EN (RE

as a proxy for surface water fertility (Cheng and

Wang, 1997; Broerse, 2000). In our study, it appears

that the main oceanographic parameter controlling the

distribution of G. oceanica is temperature, since

nitrate and phosphate are relatively high throughout

the study period. E. huxleyi and G. oceanica fluxes

are negatively correlated, especially in coccosphere

flux (Fig. 5). In contrast, Ziveri and Thunell (2000)

found that in the Gulf of California E. huxleyi and F.

profunda prefer EN conditions, while G. oceanica

dominated during weak or non-EN conditions. In the

Arabian Sea, both E. huxleyi and G. oceanica

responded clearly to monsoon-induced nutrient fertil-

ization (Broerse, 2000). In our study, although it

seems that the main oceanographic parameter con-

trolling G. oceanica is temperature, its increase in

abundance is also strongly related to increased nitrite

(NO2) concentration (partial regression coeffi-

cient=0.48 and 0.45; respectively at 20 m depth;

Fig. 8).

ate (AM/l), nitrate (AM/l), nitrite (AM/l) at 20 m water depth from

) and non-EN (R ) period are given in the plots.

B. De Bernardi et al. / Marine Micropaleontology 55 (2005) 107–125122

Many authors have found a relationship between

phytoplankton growth and iron availability in open-

ocean waters (Martin et al., 1994; Coale et al., 1996)

and in coastal upwelling areas (Hutchins and Bru-

land, 1998). In Monterey Bay, during March 1997,

Johnson et al. (1999) found high concentrations of

iron in the California Current System in the upper 50

m. This iron fertilization probably further induced

increased rates of biomass production (Schulz et al.,

2004). In our study, we observed high coccosphere

fluxes of G. oceanica during the same period and we

hypothesize an effect of the iron fertilization on this

species. The statistical analyses (PCA and multiple

regression) of the environmental variables indicated

that Fe from the sediment samples and surface

concentration in PO4 (0 m), were explaining mostly

the variation of G. oceanica (Fig. 8). The derived

regression coefficient between coccolith (cocco-

sphere) flux and Fe (Fig. 9) is 0.76 (0.48), and

between coccolith coccosphere) flux and PO4 (Fig.

8) is 0.69 (0.46). Recent studies (Sanudo-Wilhelmy

et al., 2001) have also suggested that Fe availability

may control phytoplankton productivity in oceanic

regions where surface seawater is relatively rich in N

and P (Martin and Gordon, 1988; Martin et al.,

1991).

F. profunda lives almost exclusively in sub-tropical

and tropical regions in the lower photic zone between

50–200 m (Okada and Honjo, 1973; Okada, 1992;

Okada and Matsuoka, 1996; Malinverno et al., 2003),

and has a depth range of approximately 10–80 m in

Arabian Sea (Andruleit et al., 2003). The distribution

Fig. 9. Correlation plot of G. oceanica coccosphere and coccolith fluxes v

regression coefficient (RC) is given in the plots.

of F. profunda is controlled mainly by light, temper-

ature, water transparence and, to a lesser extent, by

nutrients (Haidar and Thierstein, 2001; Cortes et al.,

2001). The abundance of this species in fossil

assemblages has been used to reconstruct the depth

of the nutricline in the equatorial Atlantic (Molfino

and McIntyre, 1990) and primary productivity in

Equatorial Indian Ocean (Beaufort and Heussner,

1999). In this study the F. profunda flux shows an

increase during the mature EN phase, when the water

column was strongly stratified. In the Southern

California Bight and Gulf of California, F. profunda

was one of the most abundant coccolithophore species

(Ziveri et al., 1995a; Ziveri and Thunell, 2000). In

particular, this species was most abundant during the

strong EN 1992–1993 period and has been suggested

as a paleo-El Nino indicator in this region.

U. sibogae has been shown to prefer oligotrophic

waters with temperatures N15 8C (Okada and

McIntyre, 1979; Ziveri et al., 2004). The abundance

of this species decreases in upwelling areas (Kleijne,

1993). In our trap experiment U. sibogae increases

during the summer in both years, but with more

intensity during EN summer. This increase seems to

be connected with the presence of an unusually low

salinity and high temperature water mass that

remained in the channel from June 1997 until the

spring of 1998 (Shipe et al., 2002). In Southern

California Bight, this species was associated with the

warm poleward flowing California Countercurrent

(Winter, 1985). Similarly, high abundances were

observed in the Southern California Bight during

ersus iron concentration measured in sediment trap samples. Partial

B. De Bernardi et al. / Marine Micropaleontology 55 (2005) 107–125 123

EN when the surface waters were warmer and

oligotrophic (Ziveri et al., 1995b). Observations of

coccolithophore distributions in the Atlantic suggest

that H. carteri prefers warm water in the mesotro-

phic eastern equatorial tropical divergence (Ziveri et

al., 2004 and references therein).

6. Conclusions

During a two-year sediment trapping project in

SBB significant changes in planktonic community

(coccolithophore, foraminifera, and siliceous plank-

ton) fluxes occurred in response to changes in

hydrography. Specifically, the flux patterns suggest

that these trends are driven by both annual and

interannual changes in the upper water column

associated with EN. Seasonal coccolith fluxes are

observed, with flux maxima in fall during March 1996

to March 1998.

In the SBB, the EN97–98 is marked by the

presence of a warm low salinity and low nutrient

surface water mass. This is reflected by reduced opal

fluxes and by an increase in total planktonic fora-

miniferal fluxes. Coccolithophore assemblages were

largely dominated by E. huxleyi, followed by F.

profunda, U. sibogae, G. oceanica, H. carteri, G.

muellerae and C. leptoporus. More oligotrophic

conditions resulted in relatively high coccolith fluxes

during EN period. G. oceanica, a subtropical species

often associated with high nutrient conditions, was

present in the SBB during the whole study-period, but

shows a strong increase at the onset of EN event. This

increase was correlated to high temperature of the

upper water column (~3 8C during EN with respect to

non-EN period), to high concentrations of nitrite

(NO2) and phosphate and, to iron fertilization. The

observed increase in abundance of G. oceanica during

strong EN events could be used as a paleo-EN

indicator in the SBB. Moreover, this taxon is

indicative of warm surface waters and fertilization

by iron and NO2. F. profunda was the second most

abundant species, showing an increase in its coccolith

fluxes during the EN condition, when the water

column was strongly stratified and nutrients were

available. U. sibogae prefers oligotrophic conditions.

In fact, it characterizes the summer period in both

years with a better incidence during EN.

Acknowledgements

We are grateful to Babette Boeckel and an

anonymous reviewer for constructive comments on

the manuscript, to Steven Kools and Lothar Kuijper

for helping with statistical analyses. Agostino Rizzi

(CNR-IDPA Milano) and Saskia Kars (Vrije Univer-

siteit, Amsterdam) are thanked for operating the SEM,

and Eric Tappa for sampling. The sediment trapping

program was supported by grants from NSF (OCE-

0117112) and NASA (NAG5-11253) to R. Thunell.

Appendix A. Supplementary materials

Supplementary data associated with this article can

be found, in the online version, at 10.1016/j.marmicro.

2005.02.003.

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