Deep-Sea Research I 53 (2006) 689–712 Temporal variability in phytoplankton pigments, picoplankton and coccolithophores along a transect through the North Atlantic and tropical southwestern Pacific Yves Dandonneau a, , Yves Montel b , Jean Blanchot b , Jacques Giraudeau c , Jacques Neveux d a IRD, IPSL/LOCEAN (CNRS, IRD, MNHN, UPMC), 4 Place Jussieu, 75252 Paris Cedex 05, France b Centre IRD, BP 172, 97492 Sainte Clotilde, La Re´union, France c De´partement de Ge´ologie et Oce´anographie, UMR CNRS 5805 EPOC, Universite´de Bordeaux 1, 33405 Talence, France d Laboratoire Arago (UMR 7621), BP 44, 66651 Banyuls sur Mer Cedex, France Received 8 November 2004; received in revised form 9 November 2005; accepted 3 January 2006 Available online 7 March 2006 Abstract Biogeochemical processes in the sea are triggered in various ways by chlorophyll-containing phytoplankton groups. While the variability of chlorophyll concentration at sea has been observed from satellites for several years, these groups are known only from cruises which are limited in space and time. The Geochemistry, Phytoplankton and Color of the Ocean programme (GeP&CO) was set up to describe and understand the variability of phytoplankton composition on large spatial scales under a multi-year sampling strategy. It was based on sea-surface sampling along the route of the merchant ship Contship London which travelled four times a year from Le Havre (France) to Noume´a (New Caledonia) via New York, Panama and Auckland. Observations included the measurement of photosynthetic pigments, counts of picoplanktonic cells by flow cytometry (Prochlorococcus, Synechococcus, and picoeucaryotes) and counting and identification of coccolithophores. The results confirmed that tropical areas have low seasonal variability and are characterized by relatively high divinyl-chlorophyll a and zeaxanthin concentration and that the variability is strongest at high latitudes where the phytoplankton biomass and population structure are found to have large seasonal cycles. Thus, the spring bloom in the North Atlantic and an austral winter bloom north of New Zealand are marked by chlorophyll concentrations which are often higher than 0.5 mgl 1 and by high concentration of fucoxanthin (a pigment used as an indicator for diatoms), while summer populations are dominated by Prochlorococcus sp. and have low chlorophyll concentrations. Apart from this yearly bloom at temperate latitudes, fucoxanthin is scarce, except in the equatorial upwelling zone in the eastern Pacific Ocean, where it is found in moderate amounts. In this region, relatively high chlorophyll concentrations extend generally as far as 141S and do not respond to the seasonal strengthening of the equatorial upwelling during the austral winter. Prochlorococcus, which is known to dominate in oligotrophic tropical seas and to disappear in cold conditions, in fact has its minimum during the spring bloom in the North Atlantic, rather than during the winter. Coccolithophores are ubiquitous, showing a succession of species in response to oceanic conditions and provinces. 19 0 Hexanoyloxyfucoxanthin, the pigment generally considered as an indicator of coccolithophores, is relatively ARTICLE IN PRESS www.elsevier.com/locate/dsr 0967-0637/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr.2006.01.002 Corresponding author. E-mail address: [email protected] (Y. Dandonneau).
Transcript
ARTICLE IN PRESS
0967-0637/$ - see
doi:10.1016/j.ds
�CorrespondiE-mail addre
Deep-Sea Research I 53 (2006) 689–712
www.elsevier.com/locate/dsr
Temporal variability in phytoplankton pigments, picoplanktonand coccolithophores along a transect through theNorth Atlantic and tropical southwestern Pacific
Yves Dandonneaua,�, Yves Montelb, Jean Blanchotb,Jacques Giraudeauc, Jacques Neveuxd
aIRD, IPSL/LOCEAN (CNRS, IRD, MNHN, UPMC), 4 Place Jussieu, 75252 Paris Cedex 05, FrancebCentre IRD, BP 172, 97492 Sainte Clotilde, La Reunion, France
cDepartement de Geologie et Oceanographie, UMR CNRS 5805 EPOC, Universite de Bordeaux 1, 33405 Talence, FrancedLaboratoire Arago (UMR 7621), BP 44, 66651 Banyuls sur Mer Cedex, France
Received 8 November 2004; received in revised form 9 November 2005; accepted 3 January 2006
Available online 7 March 2006
Abstract
Biogeochemical processes in the sea are triggered in various ways by chlorophyll-containing phytoplankton groups.
While the variability of chlorophyll concentration at sea has been observed from satellites for several years, these groups
are known only from cruises which are limited in space and time. The Geochemistry, Phytoplankton and Color of the
Ocean programme (GeP&CO) was set up to describe and understand the variability of phytoplankton composition on
large spatial scales under a multi-year sampling strategy. It was based on sea-surface sampling along the route of the
merchant ship Contship London which travelled four times a year from Le Havre (France) to Noumea (New Caledonia)
via New York, Panama and Auckland. Observations included the measurement of photosynthetic pigments, counts of
picoplanktonic cells by flow cytometry (Prochlorococcus, Synechococcus, and picoeucaryotes) and counting and
identification of coccolithophores. The results confirmed that tropical areas have low seasonal variability and are
characterized by relatively high divinyl-chlorophyll a and zeaxanthin concentration and that the variability is strongest at
high latitudes where the phytoplankton biomass and population structure are found to have large seasonal cycles. Thus,
the spring bloom in the North Atlantic and an austral winter bloom north of New Zealand are marked by chlorophyll
concentrations which are often higher than 0.5 mg l�1 and by high concentration of fucoxanthin (a pigment used as an
indicator for diatoms), while summer populations are dominated by Prochlorococcus sp. and have low chlorophyll
concentrations. Apart from this yearly bloom at temperate latitudes, fucoxanthin is scarce, except in the equatorial
upwelling zone in the eastern Pacific Ocean, where it is found in moderate amounts. In this region, relatively high
chlorophyll concentrations extend generally as far as 141S and do not respond to the seasonal strengthening of the
equatorial upwelling during the austral winter. Prochlorococcus, which is known to dominate in oligotrophic tropical seas
and to disappear in cold conditions, in fact has its minimum during the spring bloom in the North Atlantic, rather than
during the winter. Coccolithophores are ubiquitous, showing a succession of species in response to oceanic conditions and
provinces. 190Hexanoyloxyfucoxanthin, the pigment generally considered as an indicator of coccolithophores, is relatively
front matter r 2006 Elsevier Ltd. All rights reserved.
ARTICLE IN PRESSY. Dandonneau et al. / Deep-Sea Research I 53 (2006) 689–712690
abundant at all times and in all regions, but its abundance is generally not tightly correlated with that of coccolithophores.
The regional differences revealed by these results are in overall agreement with Longhurst’s division of the ocean into
ecological provinces.
r 2006 Elsevier Ltd. All rights reserved.
1. Introduction
The decades from 1960 to 1980 were marked byan effort of the scientific community to collect largeamounts of chlorophyll a (Chl a) data, which are abulk indicator of phytoplankton biomass. The firstmodels to simulate biogeochemical fluxes in theglobal ocean used it to force the process ofphotosynthetic carbon fixation (Morel, 1991; Plattand Sathyendranath, 1991; Six and Maier-Reimer,1996). This key process, however, occurs in differentways in a variety of phytoplankton populations thatare not randomly distributed, as they need differenttrophic environments for active growth. Conse-quently, changes in the phytoplankton communitystructure depend on the nutrient potential of watersinduced by local (sometimes remote) climate condi-tions and ocean general circulation. Further re-search, coordinated by the Joint Global Ocean FluxStudy, found that this structure has significantbiogeochemical consequences. Striking examplesare the populations dominated by diatoms, colonialcyanobacteria (Trichodesmium), or calcareous coc-colithophores. The diatoms need silica and iron,and under suitable conditions, they make large anddense blooms, after which dead cells sink, trans-porting large amounts of carbon to depths (Lochteet al., 1993; Romero et al., 2001). Unlike almost allother photoautotrophs, Trichodesmium and someother oceanic cyanobacteria can obtain their nitro-gen requirements from abundant dissolved N2. Thisprocess, called diazotrophy, is thought to beresponsible for a greater drawdown of inorganiccarbon in surface oceanic waters than expected ifnew primary production used only the nitratesupplied by the ocean’s dynamics (Karl et al.,1997). The coccolithophores fix carbon in two ways:(1) like other algae, they synthesize organic matter,and (2) they build calcium carbonate tests, whichexerts a pressure on the ocean’s alkalinity andcapacity to dissolve atmospheric carbon dioxide(Robertson et al., 1994). These examples are ofintense but episodic events, some of which affect thecolour of the sea and can be detected from satellites(Subramaniam et al., 2002; Tyrell et al., 1999).
Recent models try to account for some of thefunctional variability of phytoplankton populationsby correctly simulating the role of diatoms, nitrogenfixing cyanobacteria, or Prochlorococcus (Bissetet al., 1999; Aumont et al., 2003; Le Quere et al.,2005). Data used to validate these models comefrom oceanographic cruises. They are scarce andlimited to some regions and seasons. We know verylittle about the distribution of other small algae suchas Chrysophytes, Cryptophytes, Chlorophytes, orsmall cyanobacteria. Apart from the genera Pro-
chlorococcus and Synechococcus, which can becounted automatically by flow cytometry (Vaulot,1989), these groups cannot be easily recognized, anddirect observation for given locations and seasons isgenerally lacking. However, the algae containphotosynthetic pigments that differ in proportionand sometimes in nature between groups. Inven-tories of these pigments can help to determine thepresence and relative abundance of various phyto-plankton groups (Williams and Claustre, 1991;Letelier et al., 1993; Mackey et al., 1996).
The Geochemistry, Phytoplankton and Color ofthe Ocean project (GeP&CO) was undertaken todescribe the time and space variability of phyto-plankton populations at the ocean surface inrelation with the observed variability of the ocean’sphysical and chemical conditions (http://www.lodyc.jussieu.fr/gepco). Measurements of photosyn-thetic pigments collected four times a year during 12GeP&CO cruises from Europe to the southwesterntropical Pacific (Table 1) reflect the various assem-blages of phytoplankton and their seasonal andregional changes. These long transects across suchcontrasted areas as the North Atlantic, the Car-ibbean Sea, the equatorial Pacific and the southsubtropical Pacific are of global interest. Pigmentdata are complemented by counts of picoplanktonand coccolithophores and by nutrient measure-ments. This article describes the main patterns ofvariability encountered during GeP&CO and dis-cusses them in relation to ancillary data such astemperature and nutrients. It focuses on thephytoplankton groups mentioned above, whichhave a specific impact on the biogeochemistry of
Y. Dandonneau et al. / Deep-Sea Research I 53 (2006) 689–712 691
the ocean and on their main diagnostic pigments.The work was organized according to Longhurst’s(1998) classification of ecological oceanic provinces,which is a recent synthesis of modern knowledge.GeP&CO is part of the PROcessus Oceaniques et
Flux (PROOF) programme, which is the Frenchcontribution to JGOFS. Financial support wasprovided by the French research institutes INSU/CNRS, IRD, CNES and IFREMER.
2. Material and methods
2.1. Sampling conditions at sea
The GeP&CO surveys (Fig. 1) were undertakenfrom a merchant ship, Contship London, during itsregular crossings. A cabin on the main deck wasmade available to the GeP&CO experiment, forfiltering seawater and conditioning and storingsamples. Seawater samples were taken every 4 h(i.e. at 6:00, 10:00, 14:00, 18:00 and 22:00, localtime; sampling at 2:00 was skipped). Seawatersamples were drawn from the outlet of a thermo-salinograph (http://www.legos.obs-mip.fr/umr5566/francais/obs/sss/) installed in the engine room at theintake of the cooling system, at a depth ofapproximately 5m, depending on the ship’s load.A high flow rate (several m3min�1) minimizesheating and contamination and thus ensures high-quality water for chemical and biological analyses.Each cruise lasted about 38 days, from Le Havre(France) to Noumea (New Caledonia). Sampleswere stored on board for another 45 days until theship returned to Le Havre. Then, it took from 1
week to 2 months before laboratory measurementswere taken. Storage thus generally lasted between 50days for samples that were taken just before the callat Noumea and then quickly processed in thelaboratory and 140 days when processing ofsamples from the eastern North Atlantic wasdelayed for about 2 months. All samples werestored at �80 1C, in order to preserve theirbiological and optical properties (Sosik, 1999).
2.2. Nutrients
Seawater samples (of 20ml, in polyethylene tubes,with an addition of mercury chloride, kept frozen at�80 1C until analysis) were processed on a four-channel Technicon AAII analyser. The process fordetermining phosphate, nitrate (nitrate+nitriteminus nitrite) and silicate concentration used thesame reactions as in Strickland and Parsons (1972).Final concentrations (mg l�l) were calibrated inrelation to reference material of NO2, NO3, PO4
and Si(OH)4.
2.3. Measurements of photosynthetic pigments using
HPLC
Seawater samples were filtered through WhatmanGF/F filters, 25mm in diameter, with a vacuumpressure of less than 0.25 atm. Filtering was stoppedafter 1 h, in order to avoid damage to the pigmentsthat may occur when filters are clogged andfiltration takes too long. Degradation of some Chla into chlorophyllide (Jeffrey and Hallegraeff, 1987)and also pheopigments (Suzuki and Fujita, 1986)
Fig. 1. Positions of observations used in this work, from the 12 GeP&CO cruises. Indications refer to the oceanic provinces defined by
Longhurst (1999): North Atlantic Drift Province (NADR), Gulf Stream (GFST), Caribbean Sea (CARB), Pacific North Equatorial
Countercurrent (PNEC), Pacific Equatorial Divergence (PEQD), South Pacific Subtropical Gyre (SPSG) and Archipelagic Deep Basins
(ARCH).
Y. Dandonneau et al. / Deep-Sea Research I 53 (2006) 689–712692
could occur during filtration and sometimes withinthe cells before being affected by added solvent(Neveux, 1988). A filtration time of 1 h is acompromise between the risk of degradation andthe need of enough pigments for a precise measure-ment. The volume filtered under such conditions isusually about 2.5 or 3 l in clear waters and some-times only 1.5 l in rich coastal waters. Chlorophyl-lides were not measured in our samples. However,Chl a estimates made by HPLC and spectro-fluorometry were in good agreement, which suggeststhat degradation of Chl a into chlorophyllide a wasnegligible. Furthermore, phaeopigments were mostoften found in negligible quantities. Filters werethen folded with the phytoplankton cells inside,inserted into a numbered plastic envelope andstored at �80 1C. They were recovered at the nextcall in Le Havre and transported to LOCEAN inParis and later to the Station Marine d’Arcachon incontainers packed with dry ice.
Measurements were made according to theGoericke and Repeta (1993) method with thehigh-performance liquid-chromatography equip-ment of the Laboratoire d’Oceanographie Biologique
in Arcachon. This equipment, a Thermo Separa-tions HPLC system, has a binary pump, a 3-mmpore size Licospher (endcapped) C-8 column,250� 4mm, maintained at 30 1C and a ThermoSeparations UV LP 6000 diode array detector. A
refrigerated automat can handle several samples,thus allowing measurements to be taken at night.Filters were extracted in 2ml of 100% methanol for1 h at 4 1C in darkness after ultrasonication (15 s).Extracts were filtered through 0.2-mm PTFE filtersto remove all solid particles and then loaded into theautomat at 2 1C. Ammonium acetate (2:1, v/v), 1M,was added just prior to injection. Pigments wereseparated at a flow rate of 0.6mlmin�1. Theproportion of solvents varies linearly during theseparation, programmed as follows (the three valuesare, respectively, for time given in minutes, %solvent A, % solvent B): (0;75;25), (1;50;50),(20;30;70), (25;0;100), (35;0;100), (40;75;25). SolventA consists of 70% methanol and 30% ammoniumacetate (1M) and solvent B of 100% methanol. Thecolumn was then restored to original conditions for10min. Pigments were detected by absorption at440 nm.
Numeric chromatograms were recorded andprocessed with the PC1000 Thermo Separationssoftware. Calibration used pigment standardspurchased from DHI Water and Environment,Horsholm, Denmark: peridinin, 190butanoyloxy-fucoxanthin (190BF), fucoxanthin, 190hexanoyloxy-fucoxanthin (190HF), prasinoxanthin, violaxanthin,diadinoxanthin, zeaxanthin, chlorophyll b (Chl b),divinyl-chlorophyll a (d-Chl a), Chl a and b caro-tene. As we had no standard of divinyl-chlorophyll
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b (d-Chl b), we identified its peak in the chromato-gram according to its relative position in theGoericke and Repeta (1993) method, and weestimated its concentration by assuming that itsextinction coefficient was identical to that of Chl b.However, separation of d-Chl b (or d-Chl a) fromChl b or (Chl a) was often uncertain and entailederrors.
2.4. Spectrofluorometric measurements of
chlorophyllous pigments
Filtration and filter storage were done in the sameway as above for the HPLC measurements, themain difference being that the filtered volume wasonly half a litre, which usually took less than 10min,thus minimizing pigment degradation. Measure-ments were taken at LOCEAN in Paris with a F-4500 Hitachi spectrofluorometer. Filters are firstground in 10ml glass tubes with 6ml of 90%acetone with a scratched glass rod, and extraction isallowed overnight at 2 1C in darkness. The extractedcontents of each tube were centrifuged, then 1mlwas transferred to a square 1 cm� 1 cm quartz celland fluorescence emission excitation spectra weremeasured in the spectrofluorometer, operating inratio mode. The measurement process was para-meterized as follows: the excitation wavelengthvaried from 390 to 480 nm, with a 3-nm step andexcitation slit adjusted to 5 nm, and emission wasmeasured from 620 to 720 nm in steps of 4 nm , withan emission slit adjusted to 10 nm. This yielded31� 26 ¼ 806 fluorescence measurements for eachsample.
The concentration of chlorophyllous pigmentswas then computed according to Neveux andLantoine (1993), given that each one of these 806fluorescence values is the sum of the contribution ofn distinct pigments, with unknown concentrationsC1, C2yCn. The solution is given by the Ci valuesthat minimize:
Q2 ¼X480
lexc¼390
X720lem¼620
Flexc;lem �Xn
i¼1
CiF�i;lexc;lem
!2
,
(1)
where F is the fluorescence of the sample atwavelengths lexc and lem, and F�i is the specificfluorescence of pigment i (fingerprint) determinedon pigment standards. The main improvement tothe method first described by Neveux and Lantoine(1993) is an increase in the number of fluorescence
measurements, of which there are now 806 insteadof 24, thus discriminating more efficiently betweenpigments whose emission–excitation fluorescencespectra differ only slightly.
We used n ¼ 13 pigments: Chl a, Chl b, chlor-ophyll c2 , chlorophyll c3, d-Chl a, d-Chl b,corresponding phaeopigments and a fictitious pig-ment with a flat fluorescence excitation–emissionspectrum that accounts for the background signaland turbidity of the extract. Numerically minimiz-ing Q2 by linear least-squares approximation some-times gave small negative concentrations for somepigments. In such cases, these pigments were set to anull concentration, and the computation wasrepeated without them until only positive concen-trations are found. The measurements were cali-brated with pigment standards purchased from DHIWater and Environment, Horsholm, Denmark. Thed-Chl b was prepared, isolated and quantified byJacques Neveux.
2.5. HPLC vs. spectrofluorometric determination of
chlorophyllous pigments
Chlorophyllous pigments were thus estimated inparallel by HPLC and by spectrofluorometry. Thetwo techniques should give unbiased estimates sincethey both discriminate the various pigments and arecalibrated in relation to the same standards. Bothsubsets are included in the GeP&CO database.Comparative tests of 24 duplicate samples from aGeP&CO cruise, that were shared with HerveClaustre at the Laboratoire d’Oceanographie de
Villefranche (LOV) showed tight relationshipsbetween our HPLC measurements of carotenoidsand their estimates. However, it became obviousthat the GeP&CO HPLC measurements of d-Chl a
were inconsistent and did not reproduce the majortrends that one might expect from a large-scalesurvey, such as high %dChl a in oligotrophic areasor in summer in temperate regions. Indeed, theGeP&CO HPLC determinations of d-Chl a showedno correlation with those made at LOV (Fig. 2a).On the contrary, the GeP&CO spectrofluorometricdeterminations of d-Chl a were in close agreementwith those made at LOV (Fig. 2a: r2 ¼ 0:93,slope ¼ 1:17). There was also a close agreementbetween the GeP&CO spectrofluorometric and theLOV HPLC determinations of Chl a (Fig. 2b:r2 ¼ 0:98, slope ¼ 1:07). The problem arose from animprecise separation of Chl a and d-Chl a in theGeP&CO HPLC instrumentation and method. In
ARTICLE IN PRESS
Fig. 2. Comparisons of GeP&CO measurements of mono- and divinyl-chlorophyll a by spectrofluorometry and by HPLC with HPLC
measurements at the Laboratoire d’Oceanographie de Villefranche sur mer. For this test, three filtrations were made on 24 seawater samples
taken during the GeP&CO cruise K.
Y. Dandonneau et al. / Deep-Sea Research I 53 (2006) 689–712694
principle, the Goericke and Repeta method sepa-rates these two pigments. In fact, in our chromato-grams, the two absorption peaks were more or lessmingled and accurate separation was not possible.This problem did not affect the measurement ofcarotenoid pigments. Consequently, for chlorophyl-lous pigments, we prefer here to use the GeP&COspectrofluorimetric determinations. Total chloro-phyll a (Tchla), which is the sum of Chl-a and d-Chl-a, as well as the percentage of d-Chl a
(%dChla ¼ 100� d-Chl a (Chl a+d-Chl a)�1), arecomputed from the spectrofluorometric determina-tions. The effects on our results should be small,given their tight agreement with the HPLC esti-mates made at LOV.
2.6. Partitioning total chlorophyll a into size
categories using pigment concentrations
The size structure of the planktonic communityhas a strong influence on the export of particulateorganic carbon to depth (Boyd and Newton, 1995),and some global biogeochemical models (Aumontet al., 2003) include small and large phytoplanktonin order to better represent this export. In addition,the optical properties of the phytoplankton are alsoa function of the average size of planktonic cells(Bricaud et al., 2004). Knowledge of the sizestructure of the phytoplankton is thus useful topredict the efficiency of the biological carbon pump,to validate biogeochemical models, and to under-stand the variability of sea colour. Such knowledge,
however, is difficult to obtain routinely at sea.Quantitative pigment inventories provide a guess atthis size structure, by using pigments that indicatephytoplankton groups (Vidussi et al., 2001). Thebasic assumptions are as follows:
�
fucoxanthin and peridinin are diagnostic pig-ments for diatoms and dinoflagellates, whichdominate the microplankton (420 mm), � nanoplankton (2–20 mm) is characterized by
alloxanthin, 190BF and 190HF, which are abun-dant in most microflagellates,
� picoplankton (o2 mm) is assessed from zeax-
anthin and Tchlb.
Estimations of percentages of each size categorywere made with weighting coefficients (Bricaud etal., 2004), determined empirically, that maximizethe correlation coefficient between the weighted sumof these seven pigments (DPw) and Tchla, in orderto account for differences in diagnostic-pigments toChl a ratios in phytoplankton classes:
ARTICLE IN PRESSY. Dandonneau et al. / Deep-Sea Research I 53 (2006) 689–712 695
We did not consider alloxanthin, which was notmeasured on cruises 1–4. This probably does notchange the results much, as alloxanthin concentra-tion is generally lower than that of 190HF or 190BFby a factor 10 or 20, except in some coastal areas,which were not considered in this work. AllocatingTchlb, which is present in large nanoplanktonicchlorophytes, to the picoplankton may lead toerrors. However, Chl b and d-Chl b occur mainlyat depth and have a very small impact on thepresent estimates of picoplankton, since theirconcentration in the GeP&CO surface samples issmall. There are certainly many exceptions to thesepigment/size relationships, such as the tiny diatomsChaetoceros socialis and Nitzschia spp., or zeax-anthin-containing microplanktonic Trichodesmium,or 190BF and 190HF present in golden-brownflagellates of picoplanktonic size. Allocating onepigment to a class of algae may also lead to errors(see fucoxanthin for diatoms and 190HF forcoccolithophorids in the discussion section). Thisapproach corresponds to generally admitted proper-ties of algal groups (Jeffrey et al., 1997) and is onlyintended to provide the dominant trends at theregional and seasonal scales.
2.7. Flow cytometry counts of picoplankton
Seawater samples of volume 1.5ml in cryotubeswere preserved with 1% glutaraldehyde, and after15min they were stored at �80 1C to awaitlaboratory analysis. The flow cytometry measure-ments were performed within 2 h after thawing on0.1ml water volumes with a FACScan flow cyt-ometer (Becton-Dickinson) equipped with two lightscatter sensors (right angle and forward angle) andthree fluorescence sensors (green, orange and red).Filtered seawater served as a sheath fluid and 1 mmfluorescent beads were used as standards (Blanchotand Rodier, 1996). The data were treated with theBecton-Dickinson LYSYS II software and analysedwith the cytowin software (Vaulot, 1989) to identifyand count Prochlorococcus spp. (low forward anglediffusion, relatively low red fluorescence, nullorange fluorescence), Synechococcus spp. (orangefluorescence, medium red fluorescence, forward andright angle diffusion) and undifferentiated phyto-planktonic picoeucaryotes (hereafter referred to aspicoeucaryotes, high red fluorescence, high diffu-sion, null orange fluorescence). Under high irradi-ance conditions, Prochlorococcus cells often had redfluorescence that was too weak and were not
detected. In such environments, low counts of thisspecies do not necessarily mean that it is notabundant. Hence, we shall not consider these resultshere and will describe the variability of Prochlor-
ococcus spp. using only the abundance of its specificpigment d-Chl a.
2.8. Counts of coccolithophores
Seawater of volume 1.5 l was filtered onboardthrough Millipore nitrocellulose AA filters (0.8-mmpore size, 25-mm diameter). The filters were thenstored in flat circular biopsy boxes and kept drywhile awaiting identification and counting. Intactcoccospheres were counted under a polarizedoptical microscope, with a magnification of 1250,according to the procedure of Giraudeau and Bailey(1995). The taxonomic composition of the cocco-lithophore population and total standing stocksexpressed in cellsml�1 was obtained after countingof the specimens in a minimum of 30 view-fields,extrapolating the counted specimens to the entireeffective filtration area and correcting for thevolume of filtered seawater.
3. Results
The data collected during the 12 GeP&CO cruises(Table 1) cover several oceanic regions. We orga-nized here the large set of measurements accordingto the division of the ocean into oceanic provinces.We adopted the limits proposed by Longhurst(1998) for the ‘North Atlantic Drift’ (NADR), forthe ‘Gulf Stream’ (GFST), for the ‘Caribbean’(CARB) and for the ‘Archipelagic Deep Basins’(ARCH) provinces while changing the other onesslightly:
�
we fixed the limit between the ‘Pacific NorthEquatorial Current’ (PNEC) and the ‘PacificEquatorial Divergence’ (PEQD) provinces at21N, instead of 51N, basing it on a higher sea-surface temperature (SST) which characterizesPNEC and extends as far southward as 21N, � we extended PEQD farther south than 51S, as
suggested by relatively high chlorophyll andnutrient concentrations and CO2 partial pressuresouthward to 121S (Dandonneau and Eldin,1987; Dandonneau, 1995),
� we discarded the region between 121S and 161S,
which is episodically influenced by the equatorialupwelling (Dandonneau and Eldin, 1987) or by
ARTICLE IN PRESS
Fig
in t
(%
mu
thi
nan
(Sy
Y. Dandonneau et al. / Deep-Sea Research I 53 (2006) 689–712696
the Tahiti island mass and thus is not alwayssubject to the oligotrophic regime that prevails inthe ‘South Pacific Subtropical Gyre Province’(SPSG),
� similarly, we discarded the region of SPSG south
of 301S, where perturbations of oceanic currentsinduced by New Zealand islands and verticalmixing consecutive to winter cooling give differ-ent conditions to that of SPSG,
� furthermore, we discarded all observations that
were close to the coast (in the English Channel,along the east coast of North America, nearPanama and near New Zealand) or collected in atransition zone.
All these provinces represent different regimes ofupper mixed layer formation and seasonal cycles ofphytoplankton growth and the many conditionsthat may be encountered in the world ocean.Finally, 980 out of the total of 1500 observationsof the GeP&CO programme were retained (Fig. 1).
We used quarterly observations made fromNovember 1999 to August 2002 and we computedthe average observations in each province for each
. 3. Time variations detected by GeP&CO cruises in NADR. Plots co
his province for each cruise. From top to bottom: first panel, total ch
dChla, thin line), concentration of fucoxanthin (Fuco, bold dotted
ltiplied by 10); second panel, sea-surface temperature (SST, bold dot
n line) and phosphate (PO4, thin dotted line, multiplied by 10); third
oplankton (grey) and microplankton (white) to Tchla (pie charts), ce
n, thin line).
cruise (phytoplankton pigments, nutrients, countsof picoplankton: Figs. 3, 5–7 and 9–11). The abun-dance of coccolithophores (cell numbers, averaged)was also described in the oceanic provinces listedabove with the exception of the CARB and ARCHprovinces, for which coccolithophore counts havenot yet been processed; data described here arelimited to one seasonal cycle (GeP&CO A–D). Anadditional dataset related only to the Pacific wascomputed to provide information on interannualvariability in coccolithophore standing stocks anddiversity within a single season (boreal fall 1999,2000 and 2001, corresponding to the GeP&COcruises A, E and I).
3.1. North Atlantic Drift province
Phytoplankton pigment and nutrient concentra-tions revealed a high seasonal variability in thisprovince (Fig. 3). The maximum each year occurs inthe boreal spring for Tchla which amounts to1 mg l�1. During the year 2000, however, the springbloom was weak in late April on the GeP&CO_cruise C and fucoxanthin (a proxy for diatoms,
rrespond to average values of �12 observations at the sea surface
lorophyll a (Tchla, bold line), percentage of divinyl-chlorophyll a
line, multiplied by 10) and zeaxanthin (Zeax, thin dotted line,
ted line), concentrations of nitrate (NO3, bold line), silicate (SiO2,
panel, pigments-estimated contribution of picoplankton (black),
ll numbers of picoeucaryotes (Peu, bold line), and Synechococcus
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which generally characterize the spring bloom) wasstill abundant in summer, suggesting that the bloomoccurred late during that year or was partly over-looked, considering the low sampling frequency.The spring bloom was marked by high fucoxanthincontent, high contribution of the microplankton tophytoplankton biomass (30–50%), relatively lowcontribution of picoplankton (despite relatively highnumbers of picoeucaryotes) and low abundance ofProchlorococcus as suggested by low %dChla. Thehighest %dChla was found in autumn each year.The contribution of nanoplankton to phytoplank-ton biomass varied between 30% and 60%.Coccolithophore cells were equally abundant duringspring and summer 2000 (ca. 80 cellsml�1), thoughcomposed of different species (Fig. 4): a heavilycalcified morphotype of Emiliania huxleyi (‘‘closed’’E. huxleyi) which has been reported previously onlyin the Bay of Biscay (Beaufort and Heussner, 2001),dominated the spring 2000 population in the
Fig. 4. Average coccolithophore standing stocks and concentrations
GFST (bottom) provinces. The vertical error bars are the standard dev
NADR province. Nutrients peaked in winter, afterconvective mixing with deep waters, except inJanuary 2002, when winter mixing had not yetbrought nutrient concentrations to the levels of 2000or 2001. All major nutrients were generally ex-hausted in summer, but silicates still remained at thesurface (1.5 mmol l�1) in July and October 2001.
3.2. Gulf Stream
Our observations in this province clearly corre-sponded to what is expected in temperate regions,with a clear Tchla maximum in spring of about1.5 mg l�1 and a minimum in summer or autumn(Fig. 5). The spring maximum corresponded to amaximum of fucoxanthin and, in most cases, ofpicoeucaryotes. Microplankton contributed to morethan 50% of this maximum. %dChla was null inwinter and spring and culminated in summer orautumn (25–30%). Zeaxanthin and % Pico were at
of 190hexanoyloxyfucoxanthin (190HF) in the NADR (top) and
iation of estimates of total standing stocks.
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Fig. 5. Time variations detected by GeP&CO cruises in GFST. Plots correspond to average values of �11 observations at the sea surface
in this province for each cruise. Symbols and scales are the same as in Fig. 3.
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a maximum when temperature was high, in summeror autumn. Nanoplankton accounted for about25% of the phytoplankton throughout the sampledperiod, which was a smaller value than in NADR.The abundance of some of the largest contributorsto nanoplankton, the coccolithophores, seems tohave been particularly intense during the micro-plankton-dominated spring season, peaking to130 cellsml�1 in the spring of 2000 (Fig. 4). Thisaverage value was, so far, the highest recorded inthe GeP&CO coccolithophore dataset. Nutrientconcentrations culminated in winter or spring, withmaxima of only 4 mM for nitrate (compared to 6 mMin NADR).
3.3. Caribbean Sea
In this province, SST is higher than 25 1C all yearround, with a maximum in May (Fig. 6), andnutrient conditions are oligotrophic. Tchla hasalways been very low there, averaging 0.13 mg l�1,and the seasonal cycle is uncertain (Fig. 6).Fucoxanthin was practically non-existent, excepton one occasion, in early May 2000, when itsrelative abundance might indicate an episode ofmicroplankton growth. %dChla was about 30–40%
and zeaxanthin was relatively high, averaging0.06 mg l�1. The picoplankton always dominated,and its contribution to total phytoplankton biomasswas greater than 60% (except in May 2000).Nutrient concentration was low for all 12 cruises.Numbers of picoeucaryotes were less than1000 cells l�1 most of the time, while those ofSynechococcus fluctuated between 1000 and10 000, with no clear seasonal signal.
3.4. Pacific North Equatorial Countercurrent
As for the CARB province, the SST was higherthan 25 1C all year round, with a maximum in May(Fig. 7). Tchla averaged 0.27 mg l�1, in which10–40% was due to d-Chl a. Nanoplankton andmicroplankton were more abundant than in CARB,as indicated by fucoxanthin in detectable amountsmost of the time. Coccolithophore populationssteadily increased from 20 to 40 cellsml�1 betweenNovember 1999 and August 2000 (Fig. 8) and wereoverwhelmingly dominated by the Gephyrocapsa
oceanica. Boreal autumn appears to be the seasonwith the lowest abundance for this group asdepicted by the steadily low total standing stocksrecorded in October–November 1999, 2000 and
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Fig. 6. Time variations detected by GeP&CO cruises in CARB. Plots correspond to average values of �7 observations at the sea surface in
this province for each cruise. Symbols and scales are the same as in Fig. 3. Note: the vertical scale for Synechococcus and picoeucaryotes is
in thousands of cellsml�1.
Fig. 7. Time variations detected by GeP&CO cruises in PNEC. Plots correspond to average values of �8 observations at the sea surface in
this province for each cruise. Symbols and scales are the same as in Fig. 3.
Y. Dandonneau et al. / Deep-Sea Research I 53 (2006) 689–712 699
2001. Zeaxanthin, which characterizes picoplank-ton, was almost 0.1 mg l�1. The picoplanktonrepresent about 50–60% of total phytoplankton
biomass. Synechococcus was ten times more abun-dant than eukaryotic picoplankton. Nutrient con-centration was generally low, though non-null.
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Fig. 8. Average coccolithophore standing stocks and concentrations of 190hexanoyloxyfucoxanthin (190HF) in the PNEC (top), PEQD
(middle) and SPSG (bottom) provinces. The vertical error bars are the standard deviation of estimates of total standing stocks.
Y. Dandonneau et al. / Deep-Sea Research I 53 (2006) 689–712700
However, nitrate concentration was higher than2 mM in April 2001 and July 2002.
3.5. Pacific Equatorial Divergence
In this province, the equatorial upwelling bringshigh nutrient concentrations to the surface (nitrateand silicate concentrations are, respectively, about6 and 2.6 mM). However, the Tchla average wasonly 0.19 mg l�1 (Fig. 9) and the maximum did notexceed 0.21 mg l�1. These waters are well known asHigh-Nutrients Low-Chlorophyll waters (HNLC).Phytoplankton biomass is dominated by the pico-plankton (about 50%) and by the nanoplankton(30%), while microplankton never exceeded 25%.Fucoxanthin had a low concentration indeed,
around 0.01 mg l�1. Picoeucaryotes varied by afactor of 4, and their maximum in the boreal springof 2001 was not detected in the Tchla record.
SST exhibited a slight but clear seasonal cycleduring the sampled period (during which no ElNino occurred), with a maximum in April and aminimum in August and November. However, thisseasonal cycle had no or little effect on otherproperties: Tchla, d-Chl a, Fuco, Zea, % Micro, %Nano and % Pico remained remarkably steady allthe year round. The exceptions were coccolitho-phores, which showed a clear maximum in standingstocks close to 60 cellsml�1 in October–November,i.e. during the period of maximum upwelling inthe PEQD province (Fig. 8). The coccolithophorepopulations were moderately diverse and were
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Fig. 9. Time variations detected by GeP&CO cruises in PEQD. Plots correspond to average values of �22 observations at the sea surface
in this province for each cruise. Symbols and scales are the same as in Fig. 3. Note: the vertical scale for picoeucaryotes and Synechococcus
is in thousands of cellsml�1.
Y. Dandonneau et al. / Deep-Sea Research I 53 (2006) 689–712 701
dominated by the opportunistic and occasionallyblooming species E. huxleyi.
3.6. South Pacific Subtropical Gyre
In this province (Fig. 10), highly oligotrophicconditions affected all the variables of the ecosys-tem: Tchla was low all year round(average ¼ 0.07 mg l�1, maximum ¼ 0.12 mg l�1 inJuly 2002), and %dChla was always greater than30. Fucoxanthin was found to have very lowconcentrations, while the zeaxanthin average was0.04 mg l�1, so that the picoplankton (�75%)strongly dominated the microplankton (�10%).Nanoplankton only contributed to total phyto-plankton biomass by �15% in general. SST wasat a minimum in July and at a maximum in January.Tchla also followed a low-amplitude seasonal cycle,in opposition to that for temperature. Coccolitho-phore standing stocks hardly went beyond20 cellsml�1, with the maximum and minimumvalues occurring, as in the PNEC province, duringthe boreal summer and autumn, respectively (Fig.8). The computed average values for the successive1999, 2000 and 2001 October–November periodspointed to a steady increase in coccolithophorestanding stocks.
3.7. Archipelagic Deep Basins
This province is located at about the samelatitude as the previous one, and nutrient concen-trations are low all the year and do not exhibitstrong seasonal variations. However, there areclearly seasonal variations for all biological vari-ables. In the austral winter (August), we observedmaxima in Tchla concentration (August: 0.27, 0.23and 0.49 mg l�1 in 2000, 2001 and 2002), fucoxanthinand nanoplankton and microplankton percentage(total 50%) when the SST was at minimum.Prochlorococcus represented 20% of Tchla. In theaustral summer (January), the proportion of Pro-chlorococcus increased to 40% of Tchla, which wasthen at its minimum (0.09, 0.07 and 0.08 mg l�1), andtotal picoplankton reached 75%. %dChla mirroredexactly the variations of Tchla (Fig. 11). Synecho-coccus were occasionally very abundant (in Decem-ber 1999, August 2000 and May 2001).
4. Discussion
Although the sampling frequency was relativelylow, the Gep&CO observations from 1999 to 2002covered a wide range of oceanic conditions, and thedata collected reflect some of the changes in the
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Fig. 11. Time variations detected by GeP&CO cruises in ARCH. Plots correspond to average values of �7 observations at the sea surface
in this province for each cruise. Symbols and scales are the same as in Fig. 3.
Fig. 10. Time variations detected by GeP&CO cruises in SPSG. Plots correspond to average values of �15 observations at the sea surface
in this province for each cruise. Symbols and scales are the same as in Fig. 3. Note: the vertical scale for picoeucaryotes and Synechococcus
is in thousands of cellsml�1.
Y. Dandonneau et al. / Deep-Sea Research I 53 (2006) 689–712702
physical and chemical forcing and in the phyto-plankton community structure. These data showedseasonal variability in various provinces. They also
made it possible to formulate a wide range ofquestions on how the composition of the phyto-plankton responds to the variability of the ocean.
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4.1. Nutrient– chlorophyll relationship
Nitrate, phosphate and silicate have long beenconsidered to be the main limiting nutrients forprimary production. In agreement with this state-ment, the nitrate exhausted SPSG had a very lowchlorophyll concentration (Fig. 10), while the high-est chlorophyll records in the GeP&CO data werefor the North Atlantic in spring, coincident withhigh nitrate concentration (Figs. 3 and 5).
However, the highest nitrate concentrations en-countered during the whole experiment were not inthe North Atlantic, but rather in PEQD, where theywere associated with chlorophyll concentrationsthat barely exceeded 0.2 mg l�1 (Fig. 9). The HNLCcharacter of the equatorial Pacific has long beenknown (Thomas, 1979; Dugdale and Wilkerson,1991). This anomaly is now explained by lack ofiron in this area, which is remote from continentalsources (Martin, 1992; Gordon et al., 1997).Grazing may also play an important role (Landryet al., 1997; Le Borgne et al., 2003). Stronglimitation of phytoplankton growth in PEQD isespecially obvious on a Tchla vs. nitrate scatterplot(Fig. 12) for which nitrate concentrations observedduring GeP&CO were markedly higher in thisprovince than in any other. By comparison, theNorth Atlantic in winter had similar or often largerchlorophyll concentrations (Figs. 3 and 5) in spite ofsevere light limitation caused by short days, cloudcoverage and a deep mixed layer. The HNLC
Fig. 12. Chlorophyll versus nitrate concentration in the North Atlan
compared to the HNLC Pacific Equatorial Divergence (solid squares).
character of the equatorial Pacific contrasted withall other provinces described here. The neighbour-ing PNEC region had lower nitrate content, butchlorophyll was higher on average (Figs. 7 and 9).Iron input from river outflows in this low-salinityprovince may explain the difference between the twoareas.
4.2. Seasonal variability
The regions for which seasonality in chlorophyllconcentration was most strongly marked are thosein the temperate North Atlantic: NADR andGFST. In our GeP&CO data, these two provinceslooked very similar, in terms both of the phase ofthe seasonal cycle and of the magnitudes of thevariables. The patterns of seasonal variabilitycorresponded to the well-known succession ofevents that occurs each year in temperate regions.Nutrients were high in winter (January), while Tchla was only 0.2–0.3 mg l�1 in NADR, as expectedwhen irradiance is low and the mixed layer is deep,but was near 1 mg l�1 in GFST. The chlorophyllmaximum was in spring (Figs. 3 and 5). Themechanisms that trigger the spring bloom ofphytoplankton in such areas have been demon-strated by Sverdrup (1953). Stratification of theupper layers together with a seasonal increase ofirradiance are key processes for the initiation of thebloom, as well as the grazing pressure in response tothe increased phytoplankton biomass (Siegel et al.,
tic (open squares) and in oligotrophic provinces (solid circles)
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2002). The GeP&CO cruises in April captured thephytoplankton spring bloom, which was marked bya fucoxanthin maximum. Oppositely, in summerand autumn (July and October, respectively), therewas a maximum in the percentage of d-Chl a and inzeaxanthin.
In ARCH (Fig. 11), loss of heat to the atmo-sphere and consecutive cooling of the ocean surfacemixed layer during the austral winter is known toentrain nutrients from depth into the photic layer,resulting in a chlorophyll maximum (Dandonneauand Gohin, 1984; Longhurst, 1998). This maximumwas detected in August 2000, 2001 and 2002 andexceeded 0.20 mg l�1 on average in the GeP&COdata. It corresponded to the minimum of %dChlaand to a weak fucoxanthin maximum. Farthersouth, the GeP&CO data were strongly influencedby coastal processes near New Zealand, which wereresponsible for high chlorophyll concentration,mostly contributed by microplankton, with amaximum in spring (Chang et al., 2003). In thisprovince, which extends from 231S to 351S, %dChlaand % Pico were relatively high all year long.Nutrient levels remained low throughout the year,probably because the upward entrainment flux wasslow and nutrients were immediately taken up bynew production.
The other provinces are located between thetropics, and seasonal cycles are weaker. CARB isknown as an area where dinitrogen fixationcontributes significantly to new production (Coleset al., 2004). A chlorophyll maximum in winter hasoften been reported to occur either at the Bermudatime series station located to the northeast (Menzeland Ryther, 1961; Johnson and Howd, 2000) or inthe neighbouring Gulf of Mexico (Muller-Karger etal., 1991; Dandonneau et al., 2004). The GeP&COdata did not suggest any clear seasonal cycle in thisprovince (Fig. 6), except for SST (27 1C in Februaryand April, 28 1C in August and November). Isolatedevents, such as the maximum of fucoxanthin inApril 2000 in CARB (Fig. 6), dominated thevariability here rather than a possible seasonalcycle. Similarly, the high value of %dChla fromMay 2000 to February 2001 in PNEC (Fig. 7)dominated the 3-year long GeP&CO record in thisprovince. A longer time series would be needed toisolate the seasonal variability from noise in CARBand PNEC. By contrast, the permanently oligo-trophic SPSG (Fig. 10) had higher averagechlorophyll concentrations in May (0.077 mg l�1)and August (0.088 mg l�1) than in November
(0.047 mg l�1) or February (0.054 mg l�1) and thusexhibited a small but clear seasonal cycle, which hadalready been pointed out by Longhurst (1998) andby Dandonneau et al. (2004). A similar pattern hasbeen described for the North Atlantic subtropicalgyre by Neuer et al. (2002) and Bahamon et al.(2003). Furthermore, the contribution of d-Chl a toTchla, as well as the zeaxanthin concentration,culminated in the austral winter, indicating thatProchlorococcus sp. and picoplankton had contrib-uted to this maximum. It is, however, unlikely thatnutrients are entrained upwards into the photiclayer in this very oligotrophic province where thewater column is permanently stratified and thepycnocline and nutricline are always deep. Rather,the slight winter chlorophyll maximum observed byGeP&CO might, at least partly, be a response of thephotosystem antenna to less intense irradiance(Cloern et al., 1995).
PEQD is known as the site of the interannual ElNino anomaly that dominates its possible seasonalvariability (Murray et al., 1994). However, no suchevent occurred during the GeP&CO sampling. It isalso known for its permanent upwelling along theequator, which intensifies each year from July toDecember when trade winds reinforce seasonally(Wyrtki and Kilonsky, 1984). The variations of SSTshown in Fig. 9 respond to this latter pattern.Nitrate available for primary production variedbetween 4 and 8 mmole l�1 but was not well phasedwith this upwelling reinforcing and seasonal cool-ing. This discrepancy in the nitrate–temperaturerelationship probably results from the removal ofnitrate by the phytoplankton. In spite of suchimportant relative variations of nitrate, Tchlaremained remarkably constant throughout the1999–2002 observed period, as well as %dChla,zeaxanthin and the proportions of pico-, nano- andmicroplankton (Fig. 9). This evenness of theequatorial Pacific ecosystem has already beenemphasized by Longhurst (1998) and probablyresults from iron limitation that persists throughoutthe year, giving this province the HNLC characterdiscussed above (Fig. 12).
4.3. Oceanic provinces
The ocean’s ability to support the growth of thephytoplankton is basically the same in all areas:there are nutrients in abundance at depth and lightat the surface. Biogeochemical variability arisesfrom the history and properties of the surface mixed
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layer. Areas with a permanently nutrient-exhaustedsurface layer differ strongly from those that aresupplied with nutrients, either seasonally at highlatitudes or continuously such as in upwellings.CARB, PNEC, SPSG and ARCH on the one sideand NADR, GFST and PEQD on the other sidecorrespond to this division between nutrient-depleted and nutrient-supplied areas. In addition,SPSG and PEQD differ from the other provinces,because they receive no, or very little, atmosphericiron. Given these limiting conditions for phyto-plankton growth and their spatial distribution, theframework offered by Longhurst (1998), whodivided the ocean into provinces, is convenient forthis study. Even CARB and ARCH differedmarkedly, the latter being located at higher latitudesand subject to a seasonal cycle that cannot be seenin CARB (Figs. 6 and 11). It was less easy todifferentiate between NADR and GFST. These twoprovinces exhibited chlorophyll and fucoxanthinmaxima in spring and still contained abundantfucoxanthin in July, and the nutrient maximum wasin spring and winter (Figs. 3 and 5). Based onobjective criteria for a given data set, Hooker et al.(2000) identified NADR-type water masses as farsouth as 321N. The most obvious differencesbetween the two provinces can be seen here in thecoccolithophore population data (see Section 4.4)and in the variations in size of the phytoplankton(derived from its photosynthetic pigments): nano-plankton (2–20 mm in size) accounted for about40% of the total phytoplankton biomass at allseasons in NADR, while it accounted for only 25%in GFST. This lower relative contribution ofnanoplankton in GFST was balanced by relativelyhigher microplankton levels in winter and springand higher picoplankton levels in summer andautumn. Longhurst (1998) emphasized the genera-tion of eddies in GFST and the consequences ofthese eddies on the ecosystem. However, theseasonal cycles that he worked out for these twoprovinces do not differ markedly. The differencesbetween them cannot be drawn from the GeP&COquarterly data alone, and they might result from alag in the phase of the spring bloom in the easternor western North Atlantic. They may also bedue to the route taken by the ship (Fig. 1), sinceGeP&CO sampled the very south of NADR and thenorth of GFST. Generally, with only a few minorchanges (for the shifted boundaries of PEQD,see the results section), the oceanic provincesdefined by Longhurst (1998) provided a pertinent
and useful framework for analysing the GeP&COdata.
4.4. Coccolithophorids
Changes in species and diversity of coccolitho-phore populations observed during the GeP&COtransects in the North Atlantic (Fig. 4) and Pacific(Fig. 8) are in agreement with the division intobiogeographical provinces defined by Longhurst(1998) according to differences in physical environ-ment and algal dynamics. The relative abundance ofcoccolithophore species across the NADR andGFST provinces (April 2000) on the one hand andacross the PNEC, PEQD and SPSG provinces(February 2001) on the other hand revealed twomarkedly different situations (Fig. 13). The NorthAtlantic record during the boreal spring in 2000showed two sub-domains within NADR: an easternone between 101W and 201W with Gephyrocapsa
muellerae as the dominant species and a western onedominated by a heavily calcified morphotype of E.
huxleyi (‘‘closed’’ E. huxleyi). These two subdo-mains also differed by their latitude, the formercorresponding to a temperate regime at about45 1N, while the latter was closer to the subtropicalgyre. The GFST province had higher speciesdiversity, which probably resulted from the routeof the ship being close to a highly dynamical frontalarea with meanders and subsequent intrusions ofsubpolar- and subtropical-thriving species. Thisdistribution of coccolithophore species generallycorresponded to the results published by Okada andMcIntyre (1979). Our record of changes in cocco-lithophore species in the equatorial and SouthPacific Central gyre (Fig. 13, February 2000) canbe seen as a dataset complementary to the uniquerecord published by Okada and Honjo (1973) forthe North and equatorial Pacific: the succession ofcoccolithophore groups of species identified alongthe GeP&CO route was symmetrical to the oneobserved in the northern hemisphere, with G.
oceanica, E. huxleyi and Umbellosphaera irregularis
dominating the populations in PNEC, PEQD andSPSG, respectively. This pattern of distribution ofcoccolithophore species therefore seems to be validfor the whole tropical and subtropical Pacific.
The coccolithophorids often dominate the Hap-tophytes in the open ocean. The microscopic enu-merations of coccolithophore cell abundance andmeasurements of 190HF concentration, a markerpigment for Haptophytes ( ¼ Prymnesiophytes),
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Fig. 13. Distribution of coccolithophore species (wt%) across the North Atlantic (top, boreal spring 2000) and Pacific (bottom, boreal
winter 2000) in surface water along the GeP&CO route. The grey box refer to the regions not considered in the present study (outside the
core of NADR, GFST, PEQD and SPSG provinces).
Y. Dandonneau et al. / Deep-Sea Research I 53 (2006) 689–712706
offers an opportunity to evaluate how tightly theconcentration of this diagnostic pigment is corre-lated to the abundance of this group. A crude globalcomparison (Figs. 4 and 8) showed poor agreementbetween the two variables. The agreement improvedin provinces characterized by high coccolithophorestanding stocks such as in GFST (Fig. 4) wherepeak concentrations of 190HF up to 0.12 mg l�1 inApril 2000 were associated with the highest cocco-lithophore standing stocks (around 130 cells ml�1).The general disagreement between the two variableswas possibly caused by changes in pigment ratios indifferent coccolithophorid species or in other groupscontaining 19’HF (Jeffrey and Wright, 1994); theseasonal evolution of the nearly monospecific (G.
oceanica) coccolithophore populations in the PNECprovince (Fig. 8) was indeed a good match with theevolution of 190HF concentrations, suggesting thatspecies diversity has to be considered in this respect.190HF content might be more tightly related to the
total volume of coccolithophore cells than to cellnumbers. The coccolithophore volume in 1mlvaries between 5 and 28 mm3. As a test we plotted(Fig. 14a) the distribution of coccolithophorestanding stocks, the calculated biovolumes basedon our microscopic observations and 190HF acrossthe Pacific region during February 2000. Biovo-lumes showed large-amplitude changes (larger thancell numbers) across this oceanic domain, especiallyin the southern part of PEQD. In this province,large-amplitude changes were only imperfectlytraced by changes in 190HF, while the large-scaletrends of this diagnostic pigment fit relatively wellwith the trends in both biovolumes and cell numbersin the nearby SPSG and PNEC provinces. The sametropical-Pacific-wide survey indicated that the lar-gest discrepancy between both sets of data occurredin the mesotrophic PEQD province, where peakvalues of 190HF concentrations were barely asso-ciated with high coccolithophore biovolumes or
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Fig. 14. Comparative records of coccolithophore standing stocks, biovolumes and 190HF concentrations along the GeP&CO route across
the Pacific during the boreal winter 2000 (a). The grey box refers to the region not considered in the present study (outside the core of
PEQD and SPSG provinces). Lack of correlation in the PEQD region between standing stocks of coccolithophores and 190HF
concentrations is highlighted in the scatter-plot (b).
Y. Dandonneau et al. / Deep-Sea Research I 53 (2006) 689–712 707
standing stocks (Fig. 14b). This suggested that theoverall imperfect agreement between pigment andcells concentrations (or biovolumes) of coccolitho-phores could also be a consequence of organic-scaleproducing Haptophytes such as Phaeocystis orothers, which are known to also contain 190HF(Belviso et al., 2001). They are successful in a widerange of coastal or open ocean eutrophic domainsand might well be involved in the peak 190HFconcentrations recorded in surface waters of thePEQD province (Fig. 14b). A relatively great
abundance and diversity of prymnesiophytes in thepicoplanktonic community of the Pacific equatorialupwelling were inferred from 18S rDNA sequences(Moon-van der Staay et al., 2000) at 1501W (littlewest from the PEQD province described here). Inthis case, 190HF was also the main carotenoid.
4.5. Diatoms
Diatoms are the most efficient among thephytoplankton in exporting carbon to depth, and
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fucoxanthin is often considered as the diagnosticpigment for this group of algae (Blain et al., 1999),even though some other groups of algae maycontain it, such as the Chrysophyceae, the Prymne-siophyceae, the Raphidophyceae (Jeffrey et al.,1997) or the Bolidophyceae (Guillou et al., 1999).As expected, fucoxanthin was abundant during thespring bloom in NADR and GFST (Figs. 3 and 5)and remained present in significant amounts in theseprovinces during the rest of the year. In contrast, itwas practically not found in the very oligotrophicSPSG (Fig. 10). Between these extremes, it occurredin relatively large amounts sporadically in PNEC(Fig. 7) and was found in abundance in CARB inMay 1999 (Fig. 6). Such brief peaks of fucoxanthinsupport the hypothesis that new production intropical areas might result from the growth ofdiatoms (Goldman, 1993). In ARCH, fucoxanthinwas present during each austral winter (0.026, 0.015and 0.038 mg l�1 in August 2000, 2001 and 2002),when Tchla was at a maximum (Fig. 11). Thisconfirmed that nitrate is entrained into the surfacemixed layer in winter (Dandonneau and Gohin,1984) and that the resulting new production is atleast partly due to diatoms. According to Chavez(1989), who found that the equatorial Pacific wasdominated by small cells in all circumstances, highfucoxanthin concentrations did not occur in PEQDin spite of high nitrate and silicate contents:measurements in this province indeed indicatedvery low concentrations averaging only 0.011 mg l�1
(Fig. 9), bringing additional evidence that phyto-plankton growth is strongly limited in this HNLCarea. Blooms of diatoms (Archer et al., 1997) or high-growth-rate events (Bender and McPhaden, 1990) arethus certainly the exception in this province.
4.6. Picoplankton
The picoplankton is composed of tiny cells (lessthan 2 mm in diameter) that are well adapted toassimilate nutrients at low concentrations and thatsink very slowly. Their contribution to exportproduction is thus small and their photosynthesis,respiration and source of food for grazing con-tribute to the microbial loop (Azam et al., 1983).The GeP&CO database contains two kinds ofmeasurements for estimating the biomass of pico-plankton: direct cell counts by flow cytometry orindirect estimates via diagnostic pigments: zeax-anthin for Cyanobacteria, d-Chl b for Prochlor-ophytes and Chl b for Prochlorococcus and small
chlorophytes (Chlorophyceae, Prasinophyceae). Asmentioned in Section 2, flow cytometry GeP&COcounts failed to detect Prochlorococcus sp. in welllighted surface tropical waters. Given this gap,picoplankton biovolume computed as the sum ofSynechococcus (1 mm in diameter) and picoeucar-yotes (1.7 mm in diameter) and biomass estimatedwith the diagnostic pigments were not tightlycorrelated (r2 ¼ 0.32). The abundance of Synecho-coccus and of picoeucaryotes generally varied asfor Tchla. There were some regional specificities:Synechococcus was most abundant in PNEC and inARCH (Figs. 7 and 11), where their averageconcentration often exceeded 50 000 cellsml�1
(i.e. more than in the productive NADR and GFST,as shown in Figs. 2 and 4). Picoeucaryotes weremore abundant relatively to Tchla in PEQD(Fig. 9) than in other provinces and exhibited highconcentrations occasionally, such as in May andNovember 2001 in PNEC (Fig. 7), in May 2001 inSPSG (Fig. 10), or in December 1999, August 2001,or May 2001 in ARCH (Fig. 11).
It is generally considered that Prochorococcus sp.is characteristic of warm waters and practicallydisappears from temperate waters in winter, whentemperature decreases below 13 1C (Partensky et al.,1999). Our measurements of significant amounts ofd-Chl a in winter in the North Atlantic (Figs. 3 and5) did not confirm this assumption. Prochlorococcus
sp. was detected by flow cytometry in NADR attemperatures ranging between 11 and 15 1C eachwinter and spring, when irradiance was low and didnot depress its fluorescence. Then, its abundancewas positively correlated to SST. However, whileaverage SST in April was approximately equal tothat in January (13.54 and 13.52 1C, respectively, in2001, 14.36 and 14.03 in 2002; no data in 2000),Prochlorococcus sp. was less abundant in April(797 cellsml�1 vs. 6590 in 2000, 1250 vs. 6240 in2001 and 2790 vs. 18 400 in 2002). Thus, it seemsthat Prochlorococcus sp. tends to vanish duringFebruary and March when the temperature reachesits minimum and that it does not respond to thetemperature increase in spring, contrary to the welladapted diatoms. In the tropical provinces, d-Chl a
contributed much more to Tchla. This contributionwas smaller in regions where nutrients are nottotally exhausted (22% in PNEC and PEQD) thanin oligotrophic ones (32% in ARCH, 35% inCARB and 39% in SPSG). This confirmed thatProchlorococcus sp. is better adapted to oligotrophicenvironments than the other species.
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High zeaxanthin-to-Chl a ratios generally char-acterize populations which are adapted to highirradiance and a low nutrients regime (Demmig-Adams and Adams, 2000). PNEC is the provincewhere we found zeaxanthin to be most abundant(0.089 mg l�1). In ARCH, it seemed to vary in phasewith Tchla and fucoxanthin, as if zeaxanthin-containing algae benefited from the supply ofnutrients that occurs in winter; variations, however,were very small, and average concentration was0.054 mg l�1. In CARB and PEQD, zeaxanthin didnot vary much, and its average was 0.056 and0.062 mg l�1, respectively. SPSG, the most oligo-trophic province and a well lighted one, had verylow phytoplankton biomass, and zeaxanthin con-centration was only 0.039 mg l�1. In spite of itshigher biomass, NADR had even less zeaxanthin,averaging only 0.023 mg l�1. GFST exhibited amplevariations of zeaxanthin, from nearly null concen-tration in winter and spring to about 0.060 mg l�1
when fucoxanthin was at a minimum. Thus,zeaxanthin was present only when irradiance washigh (in agreement with its photoprotectant role andalso because community structure is composed ofcells rich in zeaxanthin in summer), and in suchconditions its abundance is positively related tophytoplankton biomass.
5. Conclusion
GeP&CO is one of the few series of cruises thathave sampled the ocean on long tracks on aseasonal basis. The biannual Atlantic MeridionalTransects from England to the southern Atlantic(Barlow et al., 2002) are another such series, andmeasurements are still being pursued. They includeoceanographic stations and focus on the validationof products derived from satellite-detected seacolour. HPLC pigments have also been sampledmonthly through the North Pacific along thecommercial ship track from Canada to Japan(Obayashi et al., 2001). The GeP&CO cruises werescheduled for 3 years and ended in 2002. Theirfrequency was higher than that of the AtlanticMeridional Transect, with cruises every 3 months,and the duration of the experiment is longer thanthat of the Japan-to-Canada transect. The range ofoceanic conditions covered was different, withGeP&CO cruises sailing mostly in oceanic waters,with only a small portion of their track in coastalwaters (along the east coast of North America). TheGeP&CO and North Pacific cruises had to adapt to
the conditions of a commercial ship, sampling beinglimited to the sea surface as a result and to a varietyof parameters that could be handled by a singleoperator onboard. We did our best in the GeP&COso that all parameters were measured on all cruisesby the same protocols, in order to build a coherentdatabase with as few gaps as possible. Finally, it waspossible to organize the GeP&CO programme withno major problems occurring, and the resultingdatabase covered every 3 months a very largesection across the world ocean through a varietyof oceanic provinces. We have demonstrated herethat the GeP&CO data are generally in agreementwith current knowledge of the regional and seasonalvariability of the ocean. Our results have beenorganized according to Longhurst’s (1998) divisionof the ocean into provinces. Generally, the descrip-tion and timing of the annual bloom and successionof phytoplankton made by this author has beenconfirmed by the GeP&CO data. The GeP&COdata also included many parameters that were notroutinely sampled in the past, such as lightabsorption spectra by phytoplankton and coloureddissolved organic matter, surface seawater reflec-tances or accessory photosynthetic pigments mea-sured by HPLC or spectrofluorometry. We are alsoworking on excitation–emission fluorescence spectrathat contain information on the fluorescence ofphycoerythrin, and we are processing these spectrato derive phycoerythrin concentration from allGeP&CO observations.
The detailed GeP&CO pigment inventories reflectthe phytoplankton assemblages. They have beenused to evidence relationships between satellite-detected sea-colour anomalies and dominant phy-toplankton groups (Alvain et al., 2005). Knowledgeof dominant phytoplankton groups indeed makes itpossible to better understand how chemical ele-ments vary and how they are advected or exportedin the ocean. Deriving phytoplankton groups frompigment inventories is not a simple matter andrequires a profound knowledge of the ecology ofthese groups and of pigment ratios inside them. Forinstance, the common assumption that 190HF is aproxy for coccolithophores has been shown here tobe questionable. Nevertheless, the information thatquantitative pigment inventories contain makes itpossible to describe the phytoplankton populationswith much more insight than allowed by only bulkChla determinations or scarce identifications ofspecies. Finally, with the addition of nutrient andcarbonate data, GeP&CO has built up a convenient
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and homogeneous dataset that should prove veryuseful for validating global biogeochemical models,which now include more and more functional typesof plankton.
(The GeP&CO data can be obtained from http://www.obs-vlfr.fr/proof/).
Acknowledgements
We are especially grateful to Philippe Gerard,Joel Orempuller, Remi Chuchla, Denis Diverres andFranc-ois Baurand who ensured the GeP&COsampling and measurements on M.S. Contship
London. We are also grateful to the successivecaptains, officers and crew of Contship London forkindly helping to solve all difficulties during thecruises and to the owner and manager of the ship,respectively M.S. ‘‘Alexandra Rickmers’’ Schiffsbe-teiligungsgesellschaft mbH & Co. and MarineConsulting & Contracting Gmbh in Hamburg.During the first operational years of GeP&CO,Yves Montel and Jean Blanchot were, respectively,at the Station Marine d’Arcachon and at the StationBiologique de Roscoff.
