PRIMARY RESEARCH PAPER

The importance of protozooplankton as prey for copepodsin the coastal areas of the central Irish Sea

G. M. Figueiredo Æ D. J. S. MontagnesÆR. D. M. Nash

Received: 26 November 2008 / Revised: 1 April 2009 / Accepted: 14 April 2009 / Published online: 27 April 2009� Springer Science+Business Media B.V. 2009

Abstract This study evaluates food supply forcopepods, highlighting the trophic relationshipbetween copepods and protozooplankton. To test thehypotheses that protozooplankton prey are capable ofsustaining the copepod standing stock in the westernIrish Sea, the taxonomic and size composition of thesetwo groups and the size-speciÞc predation of cope-pods on protozooplankton were investigated. Proto-zooplankton and copepod samples were collected offthe southwest coast of the Isle of Man using 1.7 lNiskin water bottles and two nets (64 and 280lmmeshes), respectively. Copepod predation on proto-zooplankton was calculated using weight-speciÞcclearance rates from the literature, considering theavailability of prey that was accessible to a given sizeof copepod. Low protozooplankton biomass was

dominated by small cells (\60 lm), and high copepodbiomass was dominated by small species, which weremore efÞciently collected by a 64-lm mesh net.However, large copepods were only collected by a280-lm mesh net, suggesting that the combination ofthe two nets provided a better estimate of copepodbiomass. Predation by the copepod assemblage in theIrish Sea removed 1Ð47% and 0.5Ð22% of ciliates anddinoßagellates standing stock, respectively, resultingin 1Ð40% of the copepod feeding requirement per day.Contrary to our hypothesis, copepods could not meettheir feeding requirements by grazing only on themicrozooplankton prey (15Ð200lm), and other foodsources (i.e. nanoplankton) must be important addi-tional dietary components to copepods in the IrishSea.

Keywords Copepod� Protozoa� Predationpressure� Irish Sea

Introduction

Over the last 20 years the role of zooplankton (micro-and mesozooplankton) in pelagic food webs has beenrevisited. Since the microbial loop was described(Azam et al.,1983), studies have demonstrated theimportant role that microzooplankton play, particu-larly the protozooplankton, which can act as toppredators within microbial pelagic food webs (Sherr

Handling editor: S. M. Thomaz

G. M. Figueiredo (&)Laborato«rio de Zooplaöncton, Departamento de BiologiaMarinha, Universidade Federal do Rio de Janeiro - UFRJ,Ilha do Funda÷o, Rio de Janeiro, RJ CEP 21949-900, Brazile-mail: gmandali@biologia.ufrj.br

D. J. S. MontagnesSchool of Biological Sciences, University of Liverpool,Biosciences Building, Crown Street, Liverpool L69 7ZB,UK

R. D. M. NashInstitute of Marine Research, PO Box 1870, Nordnes,5817 Bergen, Norway

123

Hydrobiologia (2009) 628:227Ð239DOI 10.1007/s10750-009-9787-8

& Sherr, 2002; Calbet & Landry,2004). Protozoo-plankton may also graze upon phytoplankton andcontrol primary production (Landry et al.,1997;Verity et al.,2002). This role was previously mainlyattributed to copepods (Steele & Frost,1977), forwhich protozooplankton are also currently consideredto be an important food item (e.g. Tiselius,1989;Gifford & Dagg, 1991; Levinsen et al., 2000).However, copepod preferences for protozooplanktonare poorly understood (Calbet & Saiz,2005), sincethe proportions of protozooplankton and phytoplank-ton as food may depend on their relative availability,size and palatability (Stoecker & Capuzzo,1990;Nielsen & Ki¿rboe,1994; Ohman & Runge,1994;Broglio et al.,2004).

Thus to fully understand pelagic food web dynam-ics, there is a need to recognise and describe the linkbetween protozooplankton and copepods, as thistrophic link may explain discrepancies between thephytoplankton densities and metabolic demand andproduction rates of copepods (e.g. Dam et al.,1995;Saiz et al.,1999; Calbet et al.,2002). Even though theimportance of protozooplankton in pelagic food webshas been well established, studies targeting this groupin the Irish Sea are still rare (i.e. Graziano,1989;Edwards & Burkill, 1995; Montagnes et al.,1999;Figueiredo et al.,2005). In addition, although cope-pods are the focus of the majority of studies ofplankton dynamics, the small-bodied copepods areoften ignored inCalanus-dominated systems, becauseplankton nets with a coarse mesh are traditionally usedfor sampling (Levinsen et al.,2000). Considering thatin shallow coastal waters the planktonic system isoften dominated by small copepods and microbialcommunities (Williams et al.,1994), studies approach-ing these groups in the Irish Sea are necessary.Moreover, Gowen et al. (1998) suggested that hetero-trophic microplankton may be an alternative foodsource for copepods, responsible for the onset of theirproduction prior to the spring bloom in the Irish Sea.

To understand the planktonic food web in thecoastal area of the Irish Sea in this study we giveemphasis to the link between small copepods andprotozooplankton and hypothesise that microproto-zooplankton prey (15Ð200lm) could sustain cope-pod stocks and production. Given the scarcity ofstudies on protozooplankton and small copepods inthe Irish Sea, the current study speciÞcally aimed to(1) describe the composition (species and sizes) of

these groups; (2) determine the size-speciÞc relation-ship between copepod and protozooplankton prey and(3) estimate, based on data from the literature, thepotential impact of copepod predation on micropro-tozooplankton prey during the spring and summer incoastal waters of the central Irish Sea.

Materials and methods

Sampling was conducted off the west coast of the Isleof Man using the University of LiverpoolÕs RVÔRoaganÕ during the spring and summer (23 April, 6,19 May, 1, 22 June, 12 July 1999) at three sites (seeFigueiredo et al.,2005). Temperature, salinity andßuorescence proÞles were determined from surface tothe bottom (*35 m) using a Seacat SBE-19 CTD(Seabird Inc.), equipped with a ßuoremeter (Minitra-cka, Chelsea Instruments), attached to a rosettesampler. Chlorophylla was determined by convertingthe ßuorescence reading, based on standard calibra-tions, and carbon values were estimated assuming acarbon:chlorophylla ratio of 40:1 (Geider et al.,1998).

At each station, protozooplankton were collectedat depths of*1, 15 and 25 m using a rosette sampler(1.7 l Niskin bottles), and copepods were collectedwith nets. To access all copepods stages and sizes,10 min horizontal hauls were conducted using aminiature version of a Gulf sampler (nosecone with a4.3 cm diameter aperture and a 64-lm mesh net)mounted on the top of the frame of a Gulf VII high-speed plankton net sampler with a 280-lm mesh netand a PRO-NET electronics system (details given inNash et al.,1998). Protozooplankton and copepodsamples were preserved with LugolÕs iodine (2% Þnalconcentration) and 4% Borax buffered formaldehyde,respectively.

Microprotozooplankton (cells[ 15 lm) sub-sam-ples (25Ð100 ml) were settled for 24 h following theUtermo¬hl method (Hasle, 1978), identiÞed, andcounted. To estimate protozooplankton biomass,linear dimensions were measured using an invertedmicroscope equipped with a video camera attached toa computer with image analysis software (Scionimage for Windows, Scion Corp., MD, USA), and thevolumes were calculated assuming simple geometricshapes. Carbon biomass of protozoa (dinoßagellatesand ciliates) was estimated using the biovolumeÐcarbon

228 Hydrobiologia (2009) 628:227Ð239

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regression provided by Menden-Deuer & Lessard(2000).

Species composition, abundance and biomass ofcopepod nauplii, copepodites and adults were deter-mined using a dissection microscope. The biomass ofcopepod nauplii was estimated by converting biovo-lume to the wet weight assuming a copepod density of1 mg mm-3 (Knutsen et al.,2001) and a dry weight of20% wet weight (Postel et al.,2000). Lengths andwidths of copepodites and adults were measured usingan image analysis system attached to a dissectionmicroscope (described above), and their dry weights(±1 lg) were determined after the specimens weredried (60�C, 24 h). Biomass of copepodites and adultswere determined based on estimates of abundance andwidth, and widthÐdry weight regressions determinedfor each sampling date. Dry weight was thenconverted to carbon assuming a 45% conversionfactor (Ki¿rboe et al.,1985).

Data analyses

The water structure was determined by calculating avertical stratiÞcation parameter (U = J m-3) and thenclassiÞed as stratiÞed (S, U[ 20 J m-3), mixed (M,U\ 10 J m-3) or transitional (T, 10 J m-3\ U[20 J m-3) (Simpson et al.,1979).

To estimate size-speciÞc ingestion rates, copepodsand protozooplankton sizes were expressed as equiv-alent spherical diameters [ESD= V/(0.523)0.33],whereV is the volume inlm3 and ESD is expressedin lm, according to Hansen et al. (1994). Copepodpredation on protozooplankton was calculated using aweight-speciÞc clearance rate at 14�C of 4 and 7 ml(lg C)-1 d-1 for small (15lm ESD) and largeciliates (50lm ESD), respectively (Tiselius,1989);these rates were divided by two when applied todinoßagellates, assuming the relative differencedescribed by Levinsen & Nielsen (2002). A Q10 of2.8 was applied to correct copepod clearance rates(Hansen et al.,1997). Ingestion rates (I= CR 9 [P])were, then, determined considering the size-speciÞccopepod clearance rates (CR) and the densities ofprotozooplankton [P], for the range of sizes thatcopepod are able to ingest. It was assumed that thesize ratio of copepod (predator): protozooplankton(prey) ranged from 33:1 to 10:1 ESD. These ratioswere determined from the literature and indicate therange of prey size that corresponds to±50% of the

maximum copepod clearance rate (see details inHansen et al.,1994).

Protozooplankton production (PP= PB 9 PG,where PB is protozooplankton biomass and PG isprotozooplankton-speciÞc growth rate) was esti-mated. To determine ciliate-speciÞc growth rate weapplied the equation of Mu¬ller & Geller (1983),which includes the effects of temperature and cellvolume on growth rate. For dinoßagellates weapplied the equation of Hansen et al. (1997), whichonly considers cell volume at 20�C, and then weimposed aQ10 of 2.8 to estimate growth rates atambient water temperatures.

Copepod predation and protozooplankton produc-tion were integrated according to the water structure,i.e. temperature proÞles were used to divide the watercolumn, since temperature is the dominant factorinßuencing the stratiÞcation in the western Irish Sea(Prestidge & Taylor1995). Thus, when the waterstructure was mixed, equal weights were given to thebiomass determined at each depth sampled. Incontrast, when the water column was transitional orstratiÞed, it was divided into three unequal partsbased on temperature changes.

Results

ProÞles of hydrography and biomass of plankton

The stratiÞcation parameter (U values) tended toincrease from spring to summer (Fig.1) althoughthere were variations in water column structurebetween the sites, i.e. the water column was transi-tional at two sites and either mixed (Fig.1d) orstratiÞed at the other (Fig.1c, e). The total auto-trophic plankton determined from the CTD ßuore-metry showed two peaks: one during spring and otherin early summer (Fig.1b, e). Comparison betweenautotrophic plankton panels and the ciliates anddinoßagellates panels suggested that 15Ð200lmautotrophic/mixotrophic ciliates and dinoßagellatesrepresented a small component of the total auto-trophic biomass. Protozooplankton biomass variedover the sampling period, being low during earlyspring. Ciliate biomass increased at the end of thespring (Fig.1d, e) and decreased in July (Fig.1f),and during the summer dinoßagellate biomassincreased (Fig.1e, f). Copepod nauplii and copepods

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did not vary substantially over the sampling period,and higher biomass tended to occur between 15 and25 m. High biomass of the total autotrophic planktonoccurred before the water became stratiÞed. Incontrast, protozooplankton exhibited an increase inbiomass after the water column stratiÞed.

Taxonomic groups, size and biomassof microzooplankton

The total protozooplankton biomass was low duringthe Þrst three spring sampling periods (23 April, 6, 19

May), and cells of all sizes had a similar contributionto biomass (Fig.2). Over the following samplingdates the protozooplankton biomass increased Þrstdue to the 20Ð60lm ciliates in early June, then dueto dinoßagellates of all sizes in late June, and Þnallythe[40 lm dinoßagellates had high contribution inmid-July. The highest ciliate biomass was recorded inJune, and the dominant taxa of ciliates over thespring/summer were the autotrophicMyrionecta

rubra Lohmann (wide size range 15Ð59lm), fol-lowed by Strombidium wulffi Wulff, Strombidium

capitatum Leegaard, andLaboea strobila Lohmann.

219

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412101

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Biomass (mg C m-3)

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0 10 20 0 30 60 0 150 3000 500 1000

Not sampled Not sampled

Temperature Phytoplankton Ciliates Dinoflagellates Copepods

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Dep

th (

m)

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(5 - 9)

24

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(23-41)

19

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M. rubra

M. rubra

M. rubra

NC

NC

NC

T

T

T

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A

A

NPL

NPL

NPL

NPL

NPL

COP

COP

COP

COP

COP

a23/04

b06/05

c19/05

d01/06

e22/06

f12/07

°C

Fig. 1 Water columnproÞles of temperature (�C)and biomass (mg C m-3).Values are means of thethree sites, and bars are SE,except on the temperaturepanels, where proÞles of thethree sites are separated. Inthe temperature panels,values of the stratiÞcationparameter (U) are shownnear the respectivetemperature proÞle, andhorizontal lines indicatewhere the water columnswere divided. In the panelsT tintinnids, NC nakedciliates,NA non-armoureddinoßagellates,A armoureddinoßagellates,NPLcopepod nauplii,COPcopepodites and copepodsadults

230 Hydrobiologia (2009) 628:227Ð239

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The tintinnids ([60 lm) always occurred at a lowbiomass levels (Fig.2a). The dinoßagellates exhib-ited the highest biomass during the summer, and thedominant groups were Gymnodiniaceae andCera-

tium spp. over the whole sampling period. Highbiomass ofProrocentrum spp.,Protoperidinium spp.andDinophysis spp. also occurred during the summer(Fig. 2b). Gymnodiniaceae occurred predominantlyin the\40 lm size fraction;Prorocentrum spp. andDinophysis spp. occurred in the range of 40Ð60lm;andCeratium spp. occurred[60 lm size. In general,protozooplankton biomass was dominated by smallcells (\60 lm), except during the summer whenlarger dinoßagellates predominated.

Copepods size, stage, species compositionand biomass

The two net samplers (64 and 280-lm mesh size)collected different copepod sizes; the 64-lm meshnet collected a higher abundance of\65-lm widecopepods than the 280-lm mesh net (Fig.3). How-ever, the 64-lm mesh net did not collect copepodslarger than 65-lm wide, which were caught by the280 lm net. The total copepod biomass was deter-mined by combining portions of the biomass ofcopepods collected using the 64lm (copepods\65-lm wide) and 280lm (copepodsC65-lm wide)mesh nets. Taxonomic composition of copepods

Cili

ate

biom

ass

(µg

C L

-1)

b

a

Din

ofla

gella

te B

iom

ass

(µg

C L

-1)

23 April 6 May 19 May 1 June 22 June 12 July

Sampling date

0

2

4

6

8

10

15-1

920

-39

40-5

9>

60

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9>

60

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-39

40-5

9>

60

15-1

920

-39

40-5

9>

60

15-1

920

-39

40-5

9>

60

Tintinnids

Strombidium capitatum

Strombidium wulffi

Laboea strobila

Leegaardiella spp.

Myrionecta rubra

Strombidium spp.

Others

8-13

9-22

20-4

550

-95

8-13

9-22

20-4

550

-95

8-13

9-22

20-4

550

-95

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550

-95

Length (µm)

ESD (µm)

0

4

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20

15-1

920

-39

40-5

9>

60

15-1

920

-39

40-5

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15-1

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-39

40-5

9>

60

15-1

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-39

40-5

9>

60

15-1

920

-39

40-5

9>

60

15-1

920

-39

40-5

9>

60

Ceratium spp. Prorocentrum spp.Dynophysis spp.PeridinaleGimnodiniaceaProtoperidinium spp.

13-1

815

-39

24-5

245

-60

13-1

815

-39

24-5

245

-60

13-1

815

-39

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-60

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-39

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-60

13-1

815

-39

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-60

13-1

815

-39

24-5

245

-60

Length (µm)

ESD (µm)

spp.

sp.

spp. spp.

spp.

spp.

Fig. 2 Biomasscontribution of thedominant species ofprotozoaa ciliates andbdinoßagellates, the mean(n = 3 sites) of totalprotozoan biomass (?SE)for size classes (lm), andthe equivalent ESD for eachsampling date. Note thedifferent scales ofY-axes

Hydrobiologia (2009) 628:227Ð239 231

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\65 lm andC65-lm wide are described in Table1.Nauplii and copepodites dominated the copepodassemblage in numbers, and the taxonomic composi-tion of copepods changed over spring to summer at alldevelopmental stages. In the samples collected withthe 64-lm mesh net, densities ofAcartia clausi

Giesbrecht nauplii and copepodites began to increasein the late spring, and during the summer they attainedas high densities asCentropages hamatus Lilljeborg,Oithona similis Claus andParacalanus parvus Claus.

Nauplii and copepodites ofPseudocalanus elongatus

Boeck occurred in high densities in the spring anddecreased during the summer, whileTemora longi-

cornis Mu¬ller nauplii and copepodites occurred overthe whole sampling period (spring/summer) but in lownumbers. High densities of adultP. elongatus andT. longicornis occurred during the spring and werereplaced by high densities ofA. clausi, O. similis andP. parvus in the summer. The 280-lm mesh netmainly collected copepodites and adults ofCalanus

spp. during the early spring and summer, but alsocollected A. clausi, C. hamatus, P. elongatus andT. longicornis during early spring (Table1). Com-parison between these two nets (Table1) indicatedthat some species of copepods in the adult stage (e.g.Calanus spp.) were not collected by the 64-lm meshnet, while copepod nauplii in general and adults ofP. parvus and O. similis Claus did not occur in the280-lm mesh net samples.

Adult copepods ofCalanus spp., Centropages

hamatus, Pseudocalanus elongatus and Temora lon-

gicornis collected by the 280-lm mesh net ([65-lmwide) provided a low contribution to the totalcopepod biomass, where small copepods predomi-nated (Fig.4).

The analysis of copepod biomass per size classindicated that the occurrence of larger copepods

1

10

100

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100000

0.05-0.14

0.15-0.24

0.25-0.34

0.35-0.44

0.45-0.54

0.55-0.64

0.65-0.74

0.75-0.84

0.85-0.94

Width (mm)

No

orga

nism

s m

-3

Fig. 3 Mean (?SE) of the densities of copepods at each sizeclass collected using the 64lm (black bars) and 280lm(white bars) mesh nets for all samples (n = 45)

Table 1 Density (organism l-1) in each stage (nauplli, copopodites and adults) of the dominant copepod species collected using netsof 64 and 280-lm mesh size

Copepodspecies

Meshsize(lm)

Nauplii Copepodites Adults

23Apr

06May

19May

01Jun

22Jun

12Jul

23Apr

06May

19May

01Jun

22Jun

12Jul

23Apr

06May

19May

01Jun

22Jun

12Jul

Acartia clausi 64 2.4 0.3 27.4 17.6 43.6 0.8 0.7 1.0 6.2 7.7 0.1 0.2 0.7

280 0.1 0.1

Calanus spp. 64 3.1 0.2 0.1 0.2 0.5 1.4 1.5 0.4 0.1 0.8

280 0.6 0.5 0.9 0.5 0.1 0.1

Centropageshamatus

64 0.6 0.5 1.4 5.0 10.0 0.1 0.1 0.5 4.7 0.1 0.1

280 0.1 0.1 0.1

Oithona similis 64 3.5 2.5 5.6 13.5 30.8 5.0 3.4 7.3 15.3 42.1 0.4 0.1 0.8

280

Paracalanusparvus

64 0.5 0.1 0.6 0.9 44.1 1.2 1.0 1.2 0.2 15.4 0.3 0.3 0.1 0.5

280

Pseudocalanuselongatus

64 21.2 7.5 2.0 2.5 2.8 7.1 3.7 9.7 0.1 1.5 1.2 0.4

280 0.1 0.1 0.7 0.2 0.4

Temoralongicornis

64 5.2 3.9 2.5 9.9 1.8 1.2 1.6 1.3 0.3 0.2 2.1 0.2

280 0.1 0.2 0.4 0.3 2.2 0.1

232 Hydrobiologia (2009) 628:227Ð239

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(45Ð64lm wide) in May was composed of copepo-dites and adults ofCalanus spp., P. elongatus andT. longicornis, while during the late spring and

summer copepods 15Ð34lm wide exhibited thehighest biomass; i.e.A. clausi, O. similis and P.

parvus (cf. Table1, Fig. 4). Copepod size was alsoexpressed in equivalent spherical diameters (ESD) andused for describing the size-speciÞc ingestion rates ofcopepods on protozooplankton prey (see below).

Copepod predation

Copepod predation pressure on protozooplankton wasestimated considering (1) the weight-speciÞc clear-ance rate of copepods feeding on ciliates anddinoßagellates and (2) the densities of prey in deÞnedsize that are accessible to the respective copepodsize-class; for clarity, both were expressed as ESD(Fig. 4). Copepod predation for all size classesincreased from late spring to summer (Fig.4dÐf),and, in general, the highest predation impact wasexerted by the 25Ð44lm wide copepods, which weremainly composed ofCalanus spp.,P. elongatus andT. longicornis copepodites in the spring andA. clausi,O. similis andP. parvus copepodites and adults in thesummer.

Protozooplankton production was similar (April/May) or higher (June/July) than copepod predation(Fig. 5). Copepod predation on ciliates was higherthan on dinoßagellates, except in the summer, mainlydue to the high densities of dinoßagellates (seeFigs.2b, 5).

200

160

120

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40

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0

5 15 25 35 45 55 65 75 14 24 34 44 54 64 74 84 Width (µm)

ESD (µm) copepod

ESD (µm) prey

77 215 346 473 588 699 793 869 153 310 430 533 627 725 848 969

3 8 12 15 18 22 25 28 12 26 39 50 61 71 82 92

3

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Cop

epod

bio

mas

s (µ

gC L

-1)

Cop

epod

pre

datio

n

a

23/04

b06/05

c

19/05

d01/06

e22/06

f12/07

Fig. 4 Mean (?SE) of copepod biomass (bars, left y-axis) ateach size class (width and ESD,lm) and their respective mean(±SE) predation rate on protozoa prey (dots, right y-axis) foreach sampling date (n = 3 sites). Note that, for each size ofcopepod the corresponding ESD of the prey is given

0

2

4

6

8

10

Cop

epod

pre

datio

n/P

rey

prod

uctio

n

C D C D C D C D C D C D

23 April 6 May 19 May 1 June 22 June 12 July

Sampling date

Fig. 5 Mean (bars, ?SE) of total copepod predation(lg C L-1 d-1) on ciliates (C) and dinoßagellates (D) andprey production (dots, ±SE) (lg C L-1 d-1) for each samplingdate (n = 3 sites)

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Discussion

Hydrography and protozooplankton composition

Increasing plankton biomass has been related to thesummer water stratiÞcation of the Irish Sea (Burkartet al.,1995; Edwards & Burkill, 1995; Gowen et al.,1995, 1998) that starts in the deeper offshore watersoff the west of the Isle of Man and tends to encroachinshore from May onward (Nicholas,1995; Lee et al.,2007; current study). During the spring and summer,the protozooplankton (15Ð200lm) biomass was 1Ð30 lg C l-1 in the current study, which is similar tothat found in the southwestern of the Irish Sea (1Ð41 lg C l-1) where stratiÞcation occurs earlier(Edwards & Burkill, 1995). Edwards & Burkill(1995) described a higher and earlier peak (Apriland May) of protozooplankton biomass with a highercontribution of larger cells than in our study, i.e. apeak in June and July. These differences may be dueto the late and weak stratiÞcation off the west coast ofthe Isle of Man.

Protozooplankton composition changed over theperiod of study; there was a peak of ciliates duringthe spring replaced by an increase in dinoßagellatebiomass during the summer. This pattern was alsodescribed for other temperate waters (e.g. Nielsenet al., 1993; Nielsen & Ki¿rboe,1994). The proto-zooplankton assemblages was primarily composed ofoligotrich ciliates in the genusStrombidium, theautotrophic ciliateMyrionecta rubra (=Mesodinium

rubrum), and dinoßagellates in the class Gymnodini-ales and the genusCeratium. Similar results weredescribed for the Irish Sea in a larger spatial-temporalscale study (Edwards & Burkill,1995) and in otherareas, i.e. Southampton Water (Leakey et al.,1992),Plymouth coastal waters (Pilling et al.,1992) and thenortheastern Atlantic (Burkill et al.,1993). Thus, ourresults appear to be representative of the Irish Sea ingeneral and should be applicable to other understud-ied regions of this water body.

Copepods composition

The dominant copepod species werePseudocalanus

elongatus, Acartia clausi and Temora longicornis;Calanus spp. were less abundant. Previous studiesconducted in the Irish Sea (Scrope-Howe & Jones,1985; Nicholas, 1995; Gowen et al.,1997, 1998,

1999) showed a similar taxonomic composition of thecopepod assemblage. With regard toCalanus spp.,both recently and in the early 1900s, there has beenlarge intra- and interannual variation in abundance inthe Irish Sea (Gowen et al.,1997; Nash & Geffen,2004). Temporal changes in composition of copepodspecies over the spring and summer sampling resultedin changing copepod sizes, but in general smallcopepod species dominated the assemblage. Thesmall size of the available prey may be one of thereasons for the dominance of small-sized copepods inthe Irish Sea (see below), and possibly the size ofcopepods will inßuence higher trophic levels (e.g.Þsh larvae).

In the current study, higher (2- to 10-fold) copepodbiomass was found, compared with other studiesconducted in the Irish Sea and areas of the North Sea(e.g. Scrope-Howe & Jones,1985; Ki¿rboe &Nielsen, 1994). The high numbers and biomass ofcopepods found was due to the use of both small andlarge mesh nets, which were not used in previousstudies. This is clearly revealed if only Gulf VII (280-lm mesh net) samples are considered such valuesindicate copepod densities similar to those previouslydescribed for the Irish Sea (Scrope-Howe & Jones,1985; Nicholas, 1995). It is, therefore, likely thatprevious studies underestimated nauplii, copepodites,and some small adults densities. Using a 64-lmmesh, Pepin & Penney (2000) also found microzoo-plankton concentration to be 5Ð10 times higher thanthose described in other coastal ecosystems; this wasalso attributed to the sampling gear. In fact, copepoddensities determined using nets with mesh sizes[200 lm seem to generally underestimate abun-dance (Hopcroft et al.,1998), and this may be moreserious in environments where small species aredominant, such as the Irish Sea. Here, the gear Þttedwith a 64-lm mesh accessed the adult stage of allcopepods species, except the largeCalanus spp.,which, despite being rare, were collected using the280-lm mesh net. Therefore, the combination of thenets of different mesh sizes was essential for theestimate of copepod biomass, and we stronglyrecommend this approach for future work, especiallywhere small copepods are expected to be abundant.

In general, although the present study was con-ducted over a short period and a limited area, theplankton community was similar to that described inlarger scale studies in the Irish Sea (e.g. Scrope-Howe

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& Jones,1985; Edwards & Burkill, 1995; Nicholas,1995; Gowen et al.,1998; Montagnes et al.,1999).Thus, copepod predation on protozooplanktonassessed here is likely to be applicable to other areasof the Irish Sea.

Copepod predation on protozooplankton

To estimate predation by the whole copepod assem-blage, differences between copepod clearance rateson ciliates and dinoßagellates were considered;however, there is debate as to whether there aredifferences in clearance rates. For example, Calbet &Saiz (2005) examined the few studies that consideredciliates and dinoßagellates as prey and found nosigniÞcant differences between copepod clearancerates on these groups. However, other studies haveshown that copepods graze on ciliates and dinoßag-ellates at different rates (e.g. Tiselius,1989; Stoecker& Capuzzo,1990; Ki¿rboe & Nielsen,1994; Levinsen& Nielsen,2002; Jakobsen et al.,2005). According toKi¿rboe et al. (1996), prey encounter rate is animportant determinant of feeding, and therefore mostmotile prey will increase their encounter rates withpredators. Based on these considerations we assumedthat copepod clearance rates on ciliates are 2-foldhigher than on dinoßagellates, following Levinsen &Nielsen (2002) estimates. Besides predator and preysizes and swimming speed, shape of swimming pathsand the ability to escape can affect encounter ratesand the outcome of the encounter (Broglio et al.,2001). Thus, a prey may be missed by some copepodspecies and preferred by others. The ciliateMyrio-

necta rubra, which has an ability to ÔÔjumpÕÕ, appearsto escape from the small copepods (Jonsson &Tiselius, 1990) and contributes signiÞcantly to thediet of others (Fileman et al.,2007). Given thevariability of data and lack of knowledge on thesubject we have taken a parsimonious approach:functional groups of copepod and protozoa wereanalysed and only the implications of predator andprey sizes and motility were considered. SpeciÞc preypreferences were beyond the aims and ability of thepresent multi-species study.

Copepod ingestion rates were estimated based onspeciÞc weight clearance rate determined for onecopepod species,Acartia clausi (Tiselius, 1989;Levinsen & Nielsen,2002). Using this clearancerate, determined for only one species, may have

introduced a source of bias to our estimates. How-ever, A. clausi was one of the dominant speciescollected over the period of study, and it seems tohave a similar feeding behaviour to the other copepodspecies found in the Irish Sea, i.e. Þltration, as forTemora, Pseudocalanus, Paracalanus, and raptorialas for Centropages and Oithona, depending on theprey size (see Hansen et al.,1994). In addition,correcting copepod clearance rates using aQ10 doesnot account for the effect of the interaction betweentemperature and food concentration as demonstratedfor other predators, e.g. ciliates (Montagnes et al.,2008). Thus, we recognise that these estimates are asimpliÞcation of copepod feeding physiology. How-ever, despite these potential limitations the clearancerates determined here were in the range described inthe literature. For instance, the clearance rates of thedominant copepod size (25Ð44lm wide) on ciliates(0.2Ð5 ml copepod-1 h-1) and dinoßagellates (0.1Ð2.5 ml copepod-1 h-1) were similar to the clearancerates estimated in other studies, i.e. 0.2Ð6 ml cope-pod-1 h-1 for ciliates and 0.05Ð4.9 ml cope-pod-1 h-1 for dinoßagellates (Vincent & Hartmann,2001; Calbet & Saiz,2005). Thus, we consider ourestimates a good Þrst approximation that can beapplied to our further analysis.

Copepod ingestion rates were estimated consider-ing the availability of prey that was accessible to agiven size of copepod. According to our estimates,the predation of copepod assemblage in the Irish Seawould remove 1Ð47% and 0.5Ð22% of ciliates anddinoßagellates standing stock, respectively. Otherstudies have demonstrated high variability (0Ð200%)of copepod predation impact on the ciliate standingstock (Nielsen & Ki¿rboe,1994; Fileman et al.,2007). Here, the lower predation impact of copepodon protozoa may be attributed to (1) the low densitiesof protozoan cells and (2) the dominance of smallcopepods that feed on small cells, i.e.\50 ESD (lm);these small copepods and respective prey have lowmotility, which, as stated above, inßuences encounterrates between predator and prey (Ki¿rboe et al.,1996)and, therefore, the clearance rates. Although weconsidered a wide spectrum of the preferred size ofprey (i.e.±50% of the optimum size; Hansen et al.,1994), protozoan availability was low in the studiedarea. Copepod predation during the spring, when thehigh densities of larger copepods and low densities ofprotozooplankton occurred, was similar to protozoa

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production, suggesting that copepods could exert asigniÞcant top-down control on protozoan stocks, assupported by others (Gifford & Dagg,1991; Nielsenet al.,1993; Nielsen & Ki¿rboe,1994). At the end ofthe spring and in the summer, the copepod assem-blage removed nearly half of the protozoan produc-tion, despite its increase in production and biomass.Thus, even when protozoan production increased,copepods appeared to exert a predation impact onmicroprotozoa prey. This predation may be evenmore important if our estimates of protozoan pro-duction were overestimated due to using optimisticmaximum growth rates equations (see Mu¬ller &Geller, 1983; Hansen et al.,1997).

Contrary to our hypothesis, copepods could notmeet their feeding requirements by grazing only onthe microprotozooplankton prey (15Ð200lm) incoastal areas of the Irish Sea. At the microprotozoandensities found off the west coast of the Isle of Man,copepods of several sizes and stages would ingest\1to 9% of their speciÞc body carbon d-1 (Fig. 6), butaccording to the literature, for copepods to maintainsustainable growth they require 22Ð70% of their bodycarbon d-1 (Dam & Lopes,2003; Maar et al.,2004).Therefore, the Irish Sea copepods would obtain only1Ð40% of their feeding requirements by feeding onlyon microprotozooplankton. Similar results weredescribed for the Celtic Sea, where ingestion ofprotozooplankton accounted for 3Ð19% and 40Ð52%of the daily carbon requirement ofCalanus

helgolandicus Claus andPara-, Pseudocalanus spp.populations, respectively (Fileman et al.,2007).Moreover, even using the highest ingestion ratesfound here and the biomass of copepod females of thewestern coast of the Irish Sea given in Nicholas(1995), we have calculated that females would ingestonly 5Ð8% of their speciÞc body carbon d-1. Assum-ing a copepod growth yield of 26% (Straile,1997),ingesting these percentages of carbon would givegrowth rates of*2% (speciÞc female body carbond-1 or weight-speciÞc egg production d-1). ThespeciÞc egg production rate found in other studies onsimilar species was*10% body C d-1 (Baûmstedtet al.,1999; Maar et al.,2004), which is higher thanour estimate of potential egg production based onmicroprotozooplankton prey alone. Therefore, if theIrish Sea copepods feed exclusively on microproto-zooplankton, egg production would be limited.

The low density of microprotozooplankton in thecoastal areas of the Irish Sea indicates that, to obtaintheir food requirements, copepods must also feed onphytoplankton. Indeed, it was also demonstrated thatthe low biomass of microzooplankton meant that themesozooplankton had to switch their diet from proto-zoa to phytoplankton in the northern North Sea(Widdicombe et al.,2002). Moreover, in the CelticSea,Para-, Pseudocalanus spp. andCalanus helgo-

landicus only met their food requirements whenfeeding on protozooplankton and phytoplankton, andC. helgolandicus only occurred when chlorophyll-a

levels were at their highest (Fileman et al.,2007). It haslong been stressed that diatoms are an important fooditem for copepods (e.g. Joint et al.,2001; Koski,2007),and for the western Irish Sea it was shown that smallspecies of copepod are important grazers of the springphytoplankton bloom, including diatoms (Gowenet al., 1999). Although here copepod grazing ondiatoms was not assessed, diatom biomass was similaror, on some occasions, lower than that of the micro-protozoa (i.e. 5Ð14 mg C m-3; Figueiredo,2003). Asdiatoms will be cleared at similar or lower rates to theprotozoa (Wiadnyana & Rassoulzadegan,1989; Jons-son & Tiselius,1990), it is unlikely that the micro-plankton alone (i.e. diatom and protozoa, 15Ð200lm)sustains copepod growth in the coastal area of the IrishSea.

The results described here suggest that copepodsare food limited by the microplankton (15Ð200lm)prey, which, according to the predator:prey ratio

% o

f bod

y ca

rbon

inge

sted

d-1

0

2

4

6

8

1023 April06 May19 May01June22 June12 July

0 10 20 30 40 50 60 70 80 90 100

Width (µm)

1 2 4 53

Fig. 6 Percentage of speciÞc body carbon ingested per day forall copepod sizes (width,lm) on each sampling date.Verticalbars indicate the size of copepod females (1ÑAcartia clausi,2Ñ Pseudocalanus elongatus, 3Ñ Centropages spp., 4ÑTemoralongicornis and 5ÑCalanus spp.)

236 Hydrobiologia (2009) 628:227Ð239

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described in Hansen et al. (1994), would be theoptimum prey size for copepods from the westernIrish Sea. Therefore, copepod productivity may bebottom-up controlled in the Irish Sea. This issupported by other studies that indicate food limita-tion for copepods (Runge,1985; Halsband-Lenket al., 2001; Ceballos & A«lvarez-Marque«s, 2006).However, before we conclude that Irish Sea copepodsare food limited further studies need to be undertakenon (1) behavioural and metabolic mechanisms thatpermit marine metazooplankton to persist in contin-uously food-limited environments (cf. Paffenho¬feret al., 2007), (2) plankton patchiness and (3) theimportance of nanoplankton (either auto- or hetero-trophic) as a copepod food source. In fact, other foodsources, such as cells\15 lm, may be importantadditional dietary components for copepods in theIrish Sea, but there is some doubt as to whether smallphytoplankton (\10 lm) can sustain or supplementthe copepod diet (Tiselius & Jonsson,1990; Ki¿rboe& Sabatini,1994; Fileman et al.,2007). In particular,the largeCalanus spp., for instanceC. finmarchicus

Gunnerus seem to obtain optimal reproductive outputby feeding on algae\8 lm when they occur at highdensities of*100 lg C l-1 (Baûmstedt et al.,1999).Here, total phytoplankton biomass occurred in den-sity similar or higher than 100lg C l-1 (Fig. 1) andwas dominated by cells\15 lm. The high biomass ofnanophytoplankton and, possibly, also of nanozoo-plankton (not estimated here) associated to ourconclusions that copepod cannot Þnd their foodrequirements ingesting only microprotozooplanktonsuggests that cells\15 lm may be an important foodsources for copepods from the Irish Sea. Clearly, thisis an area of study that requires continued attention.

Acknowledgements This research was supported by theConselho Nacional of Desenvolvimento Cientõ«Þco (CNPq/Brazil), through a PhD fellowship to GM Figueiredo. Weacknowledge the Arctic Agency, Poland, for the copepodidentiÞcations. We are grateful to the crew of RV ÔÔRoaganÕÕwho helped in the sampling program and to Jean Valentin,Betina Kozlowsky-Suzuki and an anonymous referee for thevaluable comments.

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