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Deep-Sea Research I

Deep-Sea Research I 56 (2009) 703–715

0967-06

doi:10.1

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Passeig

Tel.: +3

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journal homepage: www.elsevier.com/locate/dsri

Mesoscale physical variability affects zooplankton productionin the Labrador Sea

L. Yebra a,�, R.P. Harris a, E.J.H. Head b, I. Yashayaev b, L.R. Harris b, A.G. Hirst c

a Plymouth Marine Laboratory, Prospect Place, Plymouth PL1 3DH, UKb Ocean Sciences Division, Bedford Institute of Oceanography, PO Box 1006, Dartmouth, NS, Canada B2Y 2A4c School of Biological and Chemical Sciences, Queen Mary, University of London, Mile End Road, London E1 4NS, UK

a r t i c l e i n f o

Article history:

Received 20 December 2007

Received in revised form

13 November 2008

Accepted 21 November 2008Available online 3 December 2008

Keywords:

AARS

Bio-physical interaction

Calanus finmarchicus

Enzyme activity

Growth

Labrador Sea

Zooplankton

Production

37/$ - see front matter & 2009 Elsevier Ltd. A

016/j.dsr.2008.11.008

responding author at: Instituto de Ciencia

Marıtim de la Barceloneta, 37-49, Barcelona,

4 932309608; fax: +34 932309555.

ail address: lyebra@icm.csic.es (L. Yebra).

a b s t r a c t

Surface distribution (0–100 m) of zooplankton biomass and specific aminoacyl-

tRNA synthetases (AARS) activity, as a proxy of structural growth, were assessed during

winter 2002 and spring 2004 in the Labrador Sea. Two fronts formed by strong

boundary currents, several anticyclonic eddies and a cyclonic eddy were studied.

The spatial contrasts observed in seawater temperature, salinity and fluorescence,

associated with those mesoscale structures, affected the distributions of both

zooplankton biomass and specific AARS activity, particularly those of the smaller

individuals. Production rates of large organisms (200–1000mm) were significantly

related to microzooplankton biomass (63–200mm), suggesting a cascade effect from

hydrography through microzooplankton to large zooplankton. Water masses defined the

biomass distribution of the three dominant species: Calanus glacialis was restricted to

cold waters on the shelves while Calanus hyperboreus and Calanus finmarchicus were

widespread from Canada to Greenland. Zooplankton production was up to ten-fold

higher inside anticyclonic eddies than in the surrounding waters. The recent warming

tendency observed in the Labrador Sea will likely generate weaker convection and less

energetic mesoscale eddies. This may lead to a decrease in zooplankton growth and

production in the Labrador basin.

& 2009 Elsevier Ltd. All rights reserved.

1. Introduction

Zooplankton plays a central role in the transfer ofenergy from primary producers to fish populations. Theirdistribution and production are important to the mainfisheries of the North Atlantic. One species, the copepodCalanus finmarchicus, has a particularly significant role.It accounts for 470% of the mesozooplankton biomasson the North Atlantic continental shelves in spring (Headet al., 2003), where its young stages (eggs and nauplii)provide an important food source for larval groundfish(e.g. haddock, Gaard and Reinert, 2002; cod, Heath

ll rights reserved.

s del Mar (CSIC),

08003, Spain.

and Lough, 2007) and its later stages for pelagic fish(e.g. herring, Prokopchuk and Sentyabov, 2006; mackerel,Olsen et al., 2007) and baleen whales (e.g. right whales,Laidre et al., 2007). Despite its dominance on thecontinental shelves in spring, C. finmarchicus is generallyregarded as an oceanic species; being less abundant in fallbecause it retreats to depth to overwinter in a dormantstate (Heath et al., 2008). In the Northwest AtlanticC. finmarchicus dominates the mesozooplankton biomassof the central Labrador Sea (Head et al., 2003), whichis thought to serve as a distribution centre to the adjacentshelves (Wiebe, 2001). To understand and predict thedynamics of zooplankton production in general, andC. finmarchicus production in particular, we need to knowhow environmental factors (physical mesoscale features,food availability) affect the distribution of planktonicbiomass and growth rates. Some key habitats have a

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L. Yebra et al. / Deep-Sea Research I 56 (2009) 703–715704

special interest as they present hydrological structureslike fronts and eddies, in which fish larvae obtainnourishment from enhanced concentrations of zooplank-ton (Rodriguez et al., 2004). Despite the Labrador Seabeing a region of high physical variability, there are only afew studies on the effects of hydrography on zooplanktonpopulations in the area (Kielhorn, 1952; ICNAF, 1968;Head et al., 2003), mainly focused on C. finmarchicus (Headet al., 2000; Heath et al., 2004).

The western region of the Labrador Sea is dominated bythe Labrador Current which is divided into two branches(Lazier and Wright, 1993): a smaller inshore branch at theupper continental slope and over the Labrador shelf, and anoffshore branch which forms the front between the cooler,fresher coastal waters and the warmer, saltier open oceanwaters. East of the offshore branch there is a cycloniccirculation bordered by the North Atlantic Current (NAC) inthe south. The NAC reaches the Labrador Sea as therelatively warm Irminger Current (Veron et al., 1999). Alongthe west shelf of Greenland, the West Greenland Current(WGC) flows north (Lazier and Wright, 1993), transportingfresh, cold water from the Nordic seas (Clarke, 1984;Dickson et al., 2007) and also small icebergs. The branchof the WGC that joins the Labrador Current shows highvariability in its salinity (Dickson et al., 1984). It is mostvariable near the shelf break between Greenland and theLabrador Sea because of eddies or shelf waves of about30 km in diameter that last for several days (Myers et al.,1989). Mesoscale physical phenomena such as fronts andeddies are common features in the Labrador Sea. Theirpresence depends on the seasonality of the interactingcurrents. Lazier and Wright (1993) found seasonal variationin upper level circulation (400 m and up) but not at greaterdepths (1000 m). Minimum velocities (0.06 m s�1) were inMarch and April while maximal ones (2.7 m s�1) wereobserved in October. However, Chanut et al. (2008)observed higher formation of eddies, known as IrmingerRings (Eden and Boning 2002), between December andMarch, followed by a strong seasonal peak of eddiesoriginating from the West Greenland boundary currentsystem in March and a later peak of convective eddies inApril.

In this study, we examine the contrasting hydrographyin winter (December 2002) and spring (May 2004)and the effects of mesoscale physical structures on thedistribution of zooplankton biomass, growth and produc-tion rates. We use aminoacyl-tRNA synthetases (AARS)activity as an index of zooplankton growth (Yebra andHernandez-Leon, 2004) and also, in spring, C. finmarchicus

egg production rates (EPR). The biochemical approachallowed us to study for the first time growth ratesof mixed zooplankton in the area (not just the dominantC. finmarchicus) during spring and winter.

2. Methods

2.1. Hydrography

From 1st to 9th December 2002, 17 stations weresampled across the Labrador Sea, following the World

Ocean Circulation Experiment (WOCE) line AR7W/L3(Fig. 1). From 15th to 30th of May 2004, 21 stationswere sampled along the same transect. A Seabird 9 CTDwas used to obtain profiles of temperature, salinityand fluorescence during both cruises. In addition, duringthe spring cruise, 129 XBTs were deployed to increaseresolution of the temperature profiles.

2.2. Zooplankton sampling

Vertical hauls (0–100 m, 0.5 m s�1) were made fromthe CCGS Hudson (cruises 2002-075 and 2004-016) with adouble Bongo net (63mm mesh, 0.34 m diameter) and aring net (200mm mesh, 0.75 m diameter). Zooplanktonfrom the ring net hauls were fractionated with sieves toobtain 200–450, 450–1000 and 41000mm size classes.The o200mm size fraction was obtained from the Bongohauls after sieving through a 200mm sieve to removelarger organisms. On the May 2004 cruise, the 63mmdouble net was substituted for a single 76mm mesh net(0.50 m diameter) to collect the o200mm fraction. Eachfraction was quickly rinsed with filtered sea water oncorresponding mesh (to remove phytoplankton andsmaller than desired zooplankton) and stored in liquidnitrogen (�196 1C) for later measurement of proteincontent and aminoacyl-tRNA synthetases activity (AARS,Yebra and Hernandez-Leon, 2004).

On the May 2004 cruise additional ring net hauls(0.75 m diameter) for taxonomic analysis were towedvertically (0–100 m) at every station of the transect. Onthe December 2002 cruise at stations with a water columndepth of 4500 m, zooplankton samples for taxonomicanalysis were collected using a Hydro-bios Multi-netsystem (0.5�0.5 m mouth) towed vertically (0–200 m).Both nets were fitted with 200mm mesh and retrieved at�1 m s�1. Samples were preserved in 4% formalin. Inspring all zooplankton categories were counted (cope-pods, chaetognats, amphipods, medusae, etc., data notshown), including individual stages of three Calanus

species (C. finmarchicus, C. glacialis, C. hyperboreus). Inwinter Calanus species were also counted but otherzooplankton taxa were not enumerated. Due to poorsample condition, C. finmarchicus copepodite stages IV–VIwere enumerated separately, while stages I–III werepooled together. We used these spring and wintertaxonomic data to compare Calanus abundances distribu-tion between seasons. Previously, Head and Pepin (2007)obtained significantly similar C. finmarchicus abundanceswhen using both gears at the same stations, even thoughdepth ranges were somewhat different (Multi-net: 0–100or 0–200 m versus ring net: bottom to surface, maximumdepth range sampled 0–1000 m; t-Student, t ¼ 0.78,n ¼ 84, p ¼ 0.43).

2.3. Calanus finmarchicus metabolism

We use metabolism here to refer to synthesis processessuch as protein synthesis and egg production. Whenpossible, additional ring nets were deployed (0–100 m) toobtain C. finmarchicus stages IV–VI copepodites from both

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Fig. 1. Upper layer currents in the Labrador Sea (modified from Yashayaev, 2007), indicating WOCE line AR7W/L3 stations and location of anticyclonic

eddy found in May 2004.

L. Yebra et al. / Deep-Sea Research I 56 (2009) 703–715 705

cruises. Also, during December 2002, C. finmarchicus

copepodite Vs were taken from integrated 0 to 1000 mMulti-net tows. Groups of 20 individuals were staged andfrozen in liquid nitrogen for further analysis of proteincontent and AARS activity.

EPRs were determined in May 2004, at station 8 andevery second station from stations 11–25, as described inCampbell and Head (2000), based on the method of Runge(1985). In brief, �25 females were picked at random andplaced individually in Petri dishes containing 50 ml offiltered seawater. The females were incubated for 24 h inlaboratory incubators within 70.5 1C of surface watertemperatures. At the end of the 24 h period the femaleswere removed. The eggs were counted and average EPR

were calculated. No EPR were determined in December2002.

2.4. Biochemical assays

In the laboratory frozen samples were homogenized inTris–HCl buffer (20 mM, pH 7.8) and centrifuged (10 min,0 1C). AARS activity was assayed following the method ofYebra and Hernandez-Leon (2004), modified by Yebraet al. (2005b). In brief, 250ml of the sample supernatantwas added to a pre-warmed mixture containing 200 ml ofpyrophosphate (PPi) reagent (Sigma, P-7275) and 300 mlof Milli-Q water. The absorbance of the reaction mixture

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L. Yebra et al. / Deep-Sea Research I 56 (2009) 703–715706

was monitored at 340 nm for 10 min at 37 1C. Theaminoacylation of the tRNA releases PPi, which producesan oxidation of NADH. This is shown as a decrease inabsorbance (dA). The NADH oxidation rate (dA min�1)was converted to PPi release rate (AARS activity,nmPPi ml�1 min�1) with Eq. (1) in Yebra and Hernandez-Leon (2004). The AARS activity was corrected for the in

situ field temperature by applying an activation energy of8.57 kcal mol�1 (Yebra et al., 2005b) to the Arrheniusequation in order to obtain AARSin situ activity.

Protein content of all samples was assessed followingthe Lowry et al. (1951) method adapted for micro-assay byRutter (1967). Production rates of each size fraction werethen estimated as growth rates multiplied by biomass,where growth is specific AARSin situ activity (nmPPi mgprotein�1 h�1, named spAARSsitu thereafter) and biomassis protein content (mg protein m�3). Production is there-fore expressed as nmPPi m�3 d�1.

Fig. 2. Temperature (1C), salinity and relative fluorescence (mV) profiles alon

Labrador Shelf, LF: Labrador Front, Wb: West basin, Eb: East basin, GF: Greenla

gyres, C: cyclonic eddy. X-axis represents distance (km) to the Labrador coast.

Due to the high concentration of algae (Phaeocystis spp.)present at stations 16–28 during May 2004, we had todiscard several samples of the smaller fractions (o450mm)as we could not separate zooplankton from phytoplanktonby rinsing the sieves with filtered sea water.

3. Results

3.1. Hydrography

The study region showed two marked fronts duringboth winter and spring. The first, between the coldinshore Labrador Current and the main offshore LabradorCurrent, was 350 km off the Labrador coast (sts. 7–8,Fig. 2). The second front separated the warm IrmingerCurrent and the cold West Greenland Current, 100 km offWest Greenland (st. 26, Fig. 2). From Canada to Greenland

g the L3 line, from West to East in December 2002 and May 2004. LS:

nd Front, GS: Greenland Shelf, A: anticyclonic eddy, a: small anticyclonic

Inverted triangles denote CTD stations and dots XBT casts.

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Table 1Labrador Sea physical zonation according to surface temperature (ANOVA, po0.001), indicating: stations belonging to each zone, average (7SD) surface

temperature (1C) and relative fluorescence (mV), zooplankton biomass (mg protein m�3, all size fractions), spAARSsitu (nmPPi mg protein�1 h�1, all size

fractions) and production (nmPPi m�3 d�1, all size fractions) during December 2002 and May 2004.

Labrador Shelf Labrador Front West basin East basin Greenland Front Greenland Shelf

December

Stations 1–6 7–8 9–18 19–24 25–26 27–28

Temperature 0.3970.09 (3) 2.3470.45 (2) 3.7570.15 (9) 4.5970.37 (6) 2.8170.04 (2) 0.85 (1)

Fluorescence 0.1370.03 (3) 0.1370.02 (2) 0.1470.02 (9) 0.1070.01 (6) 0.0670.00 (2) 0.07 (1)

Biomass 5.3572.36 (3) 1.00 (1) 1.2370.54 (5) 0.8070.73 (3) 0.89 (1) 0.65 (1)

spAARSsitu 3.3472.22 (3) 5.48 (1) 4.0871.96 (5) 4.9372.68 (3) 1.66 (1) 4.25 (1)

Production 327.167139.57 (3) 89.54 (1) 127.82760.58 (5) 85.04757.24 (3) 40.25 (1) 16.49 (1)

May

Stations 1–6 7–8 9–15 16–24 25–26 27–28

Temperature �1.0670.02 (4) 2.3170.01 (2) 3.7170.12 (7) 4.1670.39 (9) 3.0072.64 (2) 0.7370.45 (2)

Fluorescence 0.3470.18 (4) 0.1170.06 (2) 0.3970.13 (7) 1.2270.53 (9) 1.4971.20 (2) 1.7870.28 (2)

Biomass 3.1572.43 (4) 1.0870.53 (2) 9.0477.22 (6) 6.4776.30 (8) – 0.14 (1)

spAARSsitu 1.5870.53 (4) 5.2772.45 (2) 2.6571.15 (6) 3.5371.97 (8) – 1.58 (1)

Production 49.40715.58 (4) 48.49716.57 (2) 389.657488.69 (6) 285.667271.03 (8) – 5.29 (1)

Number of stations sampled in parenthesis.

L. Yebra et al. / Deep-Sea Research I 56 (2009) 703–715 707

we described six physical zones according to temperaturedifferences between water masses (Table 1, ANOVA,po0.001): Labrador Shelf, Labrador Front, West basin,East basin, Greenland Front and Greenland Shelf.

In addition, several mesoscale physical structures werefound. The December 2002 section showed several smallanticyclonic gyres in the East basin (a, sts. 19–21, Fig. 2),which caused warm surface waters to ‘‘sink’’ as deep as600 m. In the West basin we crossed the edge of a biggeranticyclonic eddy (A, st. 16, Fig. 2). The core of this eddyproduced a downward displacement of isotherms down to800 m depth (profile not shown).

In May 2004 we also found several anticyclonicgyres in the East basin (a, sts. 20–22, Fig. 2). To thewest there were two anticyclonic eddies. The first wascharacterised by deepening warm waters to 1500 mdepth, therefore we decided to perform an extra stationin its core (A, st. named eddy in all Figs.). The secondwas less intense (A, sts. 16–17) and extended theEast basin hydrographic zone to st. 16 (Fig. 2). In theWest basin we found a cyclonic eddy, which pumpedwaters from 1000 m depth up to the euphotic zone(C, st. 15, Fig. 2). A phytoplankton bloom (Phaeocystis

spp.) dominated the Greenland Shelf and the East basin(sts. 16–28, Fig. 2).

3.2. Zooplankton

Mean winter biomass on the Labrador Shelf wassignificantly higher than in the West and East basinzones together (t-Student, t ¼ 5.13, po0.001, Table 1) andshowed values similar to those found on the LabradorShelf in spring (t-Student, t ¼ 1.20, p ¼ 0.28, Table 1).During May the difference between the Labrador Shelf andthe basin was only significant for the smaller fractions(o450mm, t-Student, po0.02, Fig. 3B). Spring biomass ofthe 4450mm size categories was very variable with peaks

at stations 12–13 and 21. Mean zooplankton biomass(grouping all size fractions) in the Labrador basin(West and East zones together) was 7-fold higher in May(7.5776.56 SD mg protein m�3) than in December (1.0770.61 SD mg protein m�3) (t-Student, t ¼ �2.76, p ¼ 0.012).Winter biomass in the East basin was similar to thaton the Greenland Shelf (t-Student, t ¼ 0.05, p ¼ 0.96). Inspring, as we had to discard several spring shelf samplesdue to the Phaeocystis spp. bloom, we could not assessseasonal differences on the Greenland Shelf (Fig. 3).Biomass of the different size fractions was positively andsignificantly correlated during winter (Table 2), but not inspring. Temperature was negatively correlated with sizefractionated biomass during winter (Table 2), but onlywith the 200–450mm fraction during spring (R2

¼ 0.77,n ¼ 15, po0.001).

Winter spAARSsitu (nmPPi h�1 mg protein�1) werehighly variable along the transect; with higher values inthe basin (sts. 9–24, t-Student, t ¼ 2.97, po0.02) for the41000mm fraction, but with peaks at the frontal stations(sts. 8, 24) or over the Labrador Shelf (sts. 1–3) for thesmaller fractions (Fig. 4A). In spring the East basinpresented similar spAARSsitu as the West basin (p40.05,Table 1). Specific AARSsitu in the cyclonic eddy (st. 15,1.7772.20SD, C in Fig. 4B) was lower but not significantlythan the rest of the stations (sts. 9–14, 3.2072.53SD).Specific enzyme activities were not correlated with fieldtemperature, except for the 41000mm size fractionduring spring (R2

¼ 0.46, n ¼ 19, po0.05). Biomass andspAARSsitu were not correlated with fluorescence duringwinter or spring, except for winter biomass of organismslarger than 1000mm (Table 2).

Production in winter (nmPPi m�3 d�1) was concen-trated on the Labrador Shelf (Table 1), and was mainly dueto organisms o1000mm (Fig. 5A). In spring higher valueswere found in the Labrador basin (West and East zones,Table 1), where Calanus EPRs were generally high (Fig. 5).Unfortunately, total spring zooplankton production could

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1 4 6 8 10 12 14 16 18 20 22 24 26 28

1 4 6 8 10 12 14 16 18 20 22 24 26 28

1 4 6 8 10 12 14 16 18 20 22 24 26 28

LF Wb Eb GS LS GFLF Wb Eb GS

Fig. 3. Zooplankton biomass distribution (mg protein m�3, 0–100 m) of the o200, 200–450, 450–1000 and 41000mm size fractions during (A) December

2002 and (B) May 2004. LS: Labrador Shelf, LF: Labrador Front, Wb: West basin, Eb: East basin, GF: Greenland Front, GS: Greenland Shelf, A: anticyclonic

eddy, a: small anticyclonic gyres, C: cyclonic eddy. Filled circles and lines (41000mm panels, right scale axis) show the total abundance of Calanus spp.

(103 ind m�2) in December 2002 (0–200 m) and in May 2004 (0–100 m).

L. Yebra et al. / Deep-Sea Research I 56 (2009) 703–715708

not be fully assessed as there was a lack of data fororganisms o450mm due to the Phaeocystis spp. bloom(sts. 16–28, Fig. 5B).

In winter, the biomass of the o450mm fractionswas significantly correlated with production of the largerorganisms (200–1000mm, Table 2). However, production

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Table 2Correlation coefficients (r) between temperature (1C), relative fluorescence (mV), zooplankton biomass (mg protein m�3) and production (nmPPi m�3 d�1)

for the different size fractions (mm) during December 2002..

Size fraction Biomass Production

o200 200–450 450–1000 41000 o200 200–450 450–1000 41000

Temperature �0.79�� (13) �0.79�� (14) �0.56� (14) �0.63� (14) �0.63� (11) �0.73� (11) �0.67� (14) �0.19 (13)

Fluorescence 0.23 (13) 0.24 (14) 0.43 (14) 0.60� (14) 0.46 (11) 0.19 (11) 0.46 (14) 0.60� (13)

Biomass o200 – – 0.92�� (10) 0.89�� (13) 0.35 (12)

200–450 0.64� (13) – – 0.72� (14) 0.08 (13)

450–1000 0.93�� (13) 0.53� (14) – – 0.46 (13)

41000 0.83�� (13) 0.70� (14) 0.92�� (14) –

�pp0.05, ��pp0.001. Number of stations sampled in parenthesis.

L. Yebra et al. / Deep-Sea Research I 56 (2009) 703–715 709

of the 41000mm fraction was not related to the biomassof the smaller size fractions. In spring, only biomasso200mm was correlated with production of the200–450mm size fraction (R2

¼ 0.88, n ¼ 9, po0.001),but both size fractions were undersampled due to thePhaeocystis spp. bloom. Winter production o1000mm wascorrelated with temperature but not with fluorescence. Incontrast, production of organisms larger than 1000mmwas related to fluorescence but not to temperature(Table 2). In spring only production of the 200–450 umsize fraction was correlated (negatively) with temperature(R2¼ 0.37, n ¼ 9, po0.05).

3.3. Calanus spp.

In May, on average, copepods represented 92% ofthe zooplankton abundance (data not shown) and thegenus Calanus was on average 61% of the total copepodabundance, ranging from 24% to 94% (Table 3). InDecember only two Calanus species were found and theirabundances were notably lower than in May. Calanus

abundance reflected the biomass distribution patternof the 41000mm zooplankton size fraction (Fig. 3). Alsothe species distribution varied according to the differentwater masses, showing C. hyperboreus and C. glacialis

linked to cold shelf waters, whilst C. finmarchicus wasmore abundant in the basin and on the Greenland Shelf(Fig. 6).

Protein content (mg protein ind�1) of winter C. fin-

marchicus CVs caught in the 0–100 m layer was higherthan that of CVs from the 0–1000 m depth range(t-Student, po0.003, Table 4). Surface winter CV proteincontents were also higher than those of spring CVs(t-Student, po0.015). Enzyme activities were higher, butnot significantly, in the surface CVs compared to the0–1000 m C. finmarchicus CVs during winter (t-Student,p40.05). However, spAARSsitu was significantly higher inspring than in 0–1000 m winter CVs (t-Student, po0.015,Table 4). C. finmarchicus female (0–100 m) biomass andspAARSsitu were not significantly different betweencruises (t-Student, p40.05). Spring EPR (eggs female�1

d�1) were high in the central basin. However, the highestrates were found at stations affected by both the warm

Irminger Current and the Phaeocystis spp. bloom (sts.24–26, Fig. 5B). Female EPR was not linearly correlatedwith fluorescence. As data seemed to follow an Ivlevfunction we applied this form and obtained a significantrelationship (EPR ¼ 39.07(1�exp(�4.86?Fluorescence)),R2¼ 0.45, n ¼ 9, p ¼ 0.046). EPR did not correlate with

temperature (p40.05).

4. Discussion

Environmental conditions affect zooplankton directly(e.g. temperature, salinity, turbulence) and indirectly, byaffecting food abundance and distribution (phytoplank-ton, microplankton). We studied zooplankton productionfrom small organisms (microplankton, o200mm) to largeones (mesozooplankton, 200–2000mm) by looking atdifferent size fractions in relation to the hydrography ofthe Labrador Sea under two different situations: winterand spring. The Labrador Sea is characterised by a varietyof water masses (see review by Yashayaev, 2007) makingthe hydrography in the area complex. Along the AR7W/L3transect we encountered four water masses, two fronts,several anticyclonic eddies and a cyclonic one.

The limits between the main currents (Inshore andOffshore Labrador Currents, Irminger Current and WestGreenland Current) promoted permanent marked frontsseparating both shelves from the basin. Temperaturechanges along the transect reflected the big differencesbetween water masses present in the Labrador Sea,ranging from low values on the shelves (o1 1C) to hightemperatures (2–5 1C) in the basin. The presence of thefronts affected zooplankton distribution. In the study areaCalanus was the most abundant genus. Calanus glacialis

was restricted to cold waters on the shelves whileC. hyperboreus and C. finmarchicus had widespreaddistributions from Canada to Greenland, as previouslyreported by Head et al. (2003). Fronts can also affectgrowth and enhance biomass development of planktonicpopulations (Le Fevre, 1986; Clark et al., 2001; Olson,2002; Yebra et al., 2004, 2006a). The Labrador Front wasassociated with enhanced spAARSsitu in the o450mmfractions during both seasons. Also, the Labrador Shelfwas the most productive area during December for the

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1 34 6 8 10 12 14 16 18 20 22 24 26 28 5 7 9 11 13 15 17eddy 20 22 24 26 28

1 34 6 8 10 12 14 16 18 20 22 24 26 28 5 7 9 11 13 15 17eddy 20 22 24 26 28

1 34 6 8 10 12 14 16 18 20 22 24 26 28 5 7 9 11 13 15 17eddy 20 22 24 26 28

LF Wb Eb GS LS GFLF Wb Eb GS

Fig. 4. Zooplankton spAARSsitu distribution (nmPPi mg protein�1 h�1, 0–100 m) of the o200, 200–450, 450–1000 and 41000mm size fractions during (A)

December 2002 and (B) May 2004. LS: Labrador Shelf, LF: Labrador Front, Wb: West basin, Eb: East basin, GF: Greenland Front, GS: Greenland Shelf A:

anticyclonic eddy, a: small anticyclonic gyres, C: cyclonic eddy.

L. Yebra et al. / Deep-Sea Research I 56 (2009) 703–715710

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<200 um

A a

10

10

20

30

40

50

60<200 um

CA A a

0

10

20

30

40

50

60

200-450 um

A a05

10152025303540

260200-450 um

CA Aa

05

1015202530354045

450-1000 um

A a0

20

40

60

80

100

120

140

160450-1000 um

C

A

A

a

0

20

40

60

80

100

120

140

160

>1000 um

A a

0

100

200

300

400

500

600

700>1000 um

C

A

A

3 5 7 9 11 13 15 17eddy20 22 24 26 28

3 5 7 9 11 13 15 17eddy20 22 24 26 28

3 5 7 9 11 13 15 17eddy20 22 24 26 28

3 5 7 9 11 13 15 17eddy20 22 24 26 28

0

100

200

300

400

500

600

1300

0510152025303540455055

EP

R (e

ggs·

fem

ale-1

·day

-1)

Pro

duct

ion

(nm

PP

i·m-3

·d-1

)

LS GF

a

4 6 8 10 12 14 16 18 20 22 24 26 28

1 4 6 8 10 12 14 16 18 20 22 24 26 28

1 4 6 8 10 12 14 16 18 20 22 24 26 28

1 4 6 8 10 12 14 16 18 20 22 24 26 28

LF Wb Eb GS LS GFLF Wb Eb GS

Fig. 5. Zooplankton production distribution (nmPPi m�3 d�1, 0–100 m) of the o200, 200–450mm, 450–1000mm and 41000mm size fractions during (A)

December 2002 and (B) May 2004. LS: Labrador Shelf, LF: Labrador Front, Wb: West basin, Eb: East basin, GF: Greenland Front, GS: Greenland Shelf, A:

anticyclonic eddy, a: small anticyclonic gyres, C: cyclonic eddy. Filled circles and lines (41000mm right panel, right scale axis) show average Calanus

finmarchicus female EPR (eggs female�1 d�1).

L. Yebra et al. / Deep-Sea Research I 56 (2009) 703–715 711

organisms o1000mm, having higher production than inspring. This was probably due to the combination offactors: (1) it had the highest biomass concentration,

(2) temperatures were higher in winter than in spring and(3) the fact that most of the Calanus were overwintering atdepth (Table 5). This later factor would reduce both the

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L. Yebra et al. / Deep-Sea Research I 56 (2009) 703–715712

predation pressure on the smaller fractions as well as thecompetition for phytoplankton resources, which wererelatively high over the Labrador shelf in winter.

Table 3Total copepod and Calanus species abundance (103 ind m�2) found in the

0–200 m layer during December 2002 and in the 0–100 m layer during

May 2004, range and average along the AR7W/L3 transect.

December 2002 May 2004

Range Avg7SD Range Avg7SD

All copepods – – 12.95–107.10 36.68727.27

All Calanus 0.60–5.52 2.2271.28 3.50–90.83 23.49724.31

C. finmarchicus 0.52–5.48 2.2071.28 1.70–83.77 20.53723.59

C. hyperboreus 0–0.16 0.0370.04 0.14–9.37 2.5573.02

C. glacialis 0 0 0–2.63 0.4070.75

Decem

10

1

2

3

4

5

6

C. hypC. fin

Ma

C

30

20

40

60

80

100

C. glaC. hypC. fin

Abu

ndan

ce (1

03 in

d·m

-2)

LS LF Wb

LS LF Wb

4 6 8 10 12 14

5 7 9 11 13 15

Fig. 6. Calanus species abundance distribution (103 ind m�2) along L3 line d

finmarchicus (C. fin), C. hyperboreus (C. hyp) and C. glacialis (C. gla). LS: Labrador

Front, GS: Greenland Shelf, A: anticyclonic eddy, a: small anticyclonic gyres, C:

Production of the largest size fraction (41000 um) wasrelated to fluorescence both in winter (derived fromspAARSsitu) and in spring (assessed as C. finmarchicus

EPR). This is consistent with previous studies (Campbelland Head, 2000; Head pers. comm.) describing a positiverelationship between EPR and phytoplankton concentra-tion in the region. In May, C. finmarchicus production washighest on the Greenland Shelf. This was probably due tothe coupling of warmer Irminger waters and the Phaeo-

cystis spp. bloom that dominated the eastern LabradorSea. Enhancements of phytoplankton (Munk et al., 2003;Holliday et al., 2006) and zooplankton biomass (Headet al., 2003; Yebra et al., 2006a) in frontal areas have beenpreviously observed at high latitudes, suggesting that thefront between the cold Greenland Current and the warmIrminger Current may have promoted the phytoplanktonbloom.

ber 2002

A a

y 2004

AA

a

Eb GF GS

Eb GF GS

16 18 20 22 24 26 28

17 eddy 20 22 24 26 28

uring (A) December 2002 (0–200 m) and (B) May 2004 (0–100 m). C.

Shelf, LF: Labrador Front, Wb: West basin, Eb: East basin, GF: Greenland

cyclonic eddy.

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Table 4Individual biomass (mg protein ind�1) and spAARSsitu (nmPPi mg protein�1 h�1) of Calanus finmarchicus late stages from the upper 100 m layer, compared

to those from the 0–1000 m Multi-net tows during December 2002.

0–100 m layer 0–1000 m layer

Females CV CIV Females CV

December

Biomass 43.478.4 (3) 42.476.6 (4) 35.3 (1) 32.375.1 (17)

spAARSsitu 6.572.3 (3) 3.972.2 (4) 4.3 (1) 1.571.3 (5)

May

Biomass 52.7735.5 (6) 28.175.4 (4) 24.978.8 (3)

spAARSsitu 4.471.6 (6) 5.172.1 (4) 10.278.4 (3)

No. of samples in parenthesis, each sample contained 20 individuals.

Table 5Percentage of Calanus finmarchicus late stages present on the upper

0–200 m layer, relative to those in the 0–1000 m water column (100%) at

stations sampled with the Multi-net during December 2002.

Station Females CV CIV

13 18.75 13.36 40.00

16 21.43 16.00

19 30.00 12.68 44.44

21 33.33 9.85

24 33.33 4.26 71.43

Average 27.37 11.23 51.96

L. Yebra et al. / Deep-Sea Research I 56 (2009) 703–715 713

The East basin zone showed high variability. Duringboth cruises, the near shelf area had numerous smallanticyclonic gyres. In spring, they most likely wereIrminger Rings, as they had low salinity in their uppercore (0–200 m) and higher salinity and temperaturebetween 200–1000 m depth (Hatun et al., 2007), andwere found north of 581N (Chanut et al., 2008). Also, bothin winter and spring, the East basin was dominated byintense anticyclonic eddies, probably originating in theGreenland boundary current (Chanut et al., 2008). Thesetrapped warm waters from the Irminger Current andtransported them to the West basin. Mesoscale eddiesare known to affect plankton biomass and productivity(Le Fevre, 1986; Olson, 2002; Yebra et al., 2004). Theirpresence explains the high variability of mean zooplank-ton biomass observed in the Labrador basin. Anticycloniceddies are characterised by sinking phyto- and bacter-ioplankton, and by concentrating zooplankton withintheir cores (Hernandez-Leon et al., 2001; Yebra et al.,2004). Cyclonic eddies act like small upwellings increas-ing primary production (Arıstegui et al., 1997). However,due to the upward pumping of waters, the enhancedzooplankton biomass and production is displaced to theiredges (Hernandez-Leon et al., 2001; Yebra et al., 2004,2005a). Despite the similar temperatures observed inspring inside adjacent cyclonic and anticyclonic eddies;production was clearly different within them. The antic-yclonic eddy (st. 16) had 3.9-fold more production in itscore than the contiguous cyclonic eddy (st. 15). On the

same cruise, to the east, the anticyclone named eddy had3–10 fold higher production than the surrounding waters,and the same was observed at station 21 due to thepresence of anticyclonic gyres. In winter, the areadominated by anticyclonic warm eddies also presentedenhanced mesozooplankton growth rates.

It is interesting to note that the smaller fractions(o450mm) were more affected by temperature thanthe large ones; indicating that small size organisms (e.g.microplankton, copepod nauplii) are more influenced bythe changing physical structure along the transect.In winter, biomass distributions of all the size fractionswere closely related and biomass of smaller organisms(o200mm) was significantly correlated with the produc-tion rate of the species with sizes between 200 and1000mm. We suggest that the effect of hydrography mightbe transmitted through the food web towards the largeranimals. However, production of the 41000mm fraction(mainly Calanus spp.) was not related to the biomass ofsmaller organisms but to fluorescence. In spring, the mainfeature seemed to be the interaction between eddies andthe Phaeocystis spp. bloom. The phytoplankton bloom wasadvected and trapped by anticyclonic gyres, whichextended it towards the central basin. Unfortunately, thelack of data from the small size fractions prevents us fromknowing whether hydrography and the bloom had acascading effect on the biomass and production such asthat observed in winter. Nevertheless, we did comparewinter and spring metabolism of the dominant species inthe area: C. finmarchicus. In winter, C. finmarchicus CVcopepodites from the 0–1000 m layer had lower spAARS

situ than from the surface (0–200 m). Head and Pepin(2007) observed during the same December 2002 cruisethat CVs in the basin were almost absent from the surfacelayers and were mostly at depths between 200 and 900 m.So, in our 0–1000 m depth tows most CVs would havebeen residing at depths 4200 m (84–95%, Table 5)and hence dormant. A significant reduction in C. finmarch-

icus spAARSsitu with increasing depth was previouslydescribed in the Irminger Sea when CVs underwentdormancy (Yebra et al., 2006b). Interestingly, springsurface spAARSsitu activity of CVs did not differ fromthe winter surface values, suggesting that the near-surface CVs remained active in winter. This implies

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a change in their dietary habits towards predation onitems other than phytoplankton, if the CVs are to survivethrough the winter. Such activity is consistent withprevious studies showing the ability of Calanus speciesto prey significantly on ciliates, cyanobacteria or copepodeggs and nauplii in the absence of phytoplankton blooms(Harris, 1996; Meyer-Harms et al., 1999; Ohman andHirche, 2001; Eiane et al., 2002; Irigoien et al., 2003;Bonnet et al., 2004).

In conclusion, we found that hydrography affectedthe biomass distribution and production of zooplanktonpopulations in the Labrador Sea. Surface variability ofhydrography in the Labrador basin is the result of seasonaltransport of eddies from the boundary regions. Theseeddies can be of surface origin (wind forcing) or mid-depth origin (convective mixing) (Lilly and Rhines, 2002).Beaugrand et al. (2002) suggested that hydrodynamics(and warm currents) were the key factors controllingpelagic diversity in the Labrador region. It is vital tounderstand how changes in climate will modify hydro-graphy in the area in order to predict accurately how thesechanges will affect plankton populations. The changes inLabrador Sea water temperatures observed in the lastdecades (0.5–1.0 1C, Yashayaev, 2007) and the furtherincreases predicted by different models (see Bindoff et al.,2007) could affect zooplankton growth and abundancedirectly (Tittensor et al., 2003) but also through theireffects on vertical stratification, baroclinic currents and,ultimately, rates of formation and properties of mesoscaleeddies. Recent increases in temperature have decreaseddensity or added buoyancy to the upper layers. This islikely to increase vertical stratification over the upper-to-mid-depth part of the Labrador Sea water column(Yashayaev, 2007) and to affect the frequency of con-vective and boundary current formed eddies in theLabrador Sea (Lilly and Rhines, 2002). This would in turnreduce the open ocean deep convection in the basin(Chanut et al., 2008; Guemas and Salas-Melia, 2008). Also,given the positive effect that mesoscale eddies have onphytoplankton and zooplankton biomass and growthrates, we suggest that any reduction in the recurrenceand strength of either convective eddies or those arrivingfrom the Greenland Slope into the central Labrador basinmay decrease zooplankton production in the region. Inaddition, we have shown that small organisms are verysensitive to the presence of mesoscale features and tochanges in temperature. Therefore, to predict what couldhappen to larger animals which may rely on the smallersize fractions for survival (e.g. Calanus spp. and theirpredators), we should focus on the complex mechanismlinking hydrographic conditions with the changes in smallplankton (o200mm) and their physiology.

Acknowledgements

We thank the crew and colleagues working on boardCCGS Hudson during both cruises. We especially thankS. Alvarado for his voluntary work during cruise 2004-016,C.B. Augustin and two anonymous referees for theirhelpful comments on the manuscript, and R. Almeda for

his help with statistical analysis. This work was fundedby the Spanish Ministry of Education, Culture and Sportgrant to L. Yebra (EX-2002-0456), and by the NERC MarineProductivity Thematic Programme (Grants NER/T/S/2001/01256 and NE/C508418/1). This work is a contribution tothe Plymouth Marine Laboratory Core Strategic ResearchProgramme and to the Marine Productivity UK-GLOBECProgramme. Completion of this work was funded by theEuropean Social Fund (I3P programme, CSIC).

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