Grazing by meso- and microzooplankton on phytoplankton in the upper reaches of the Schelde estuary (Belgium/The Netherlands

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Grazing by meso- and microzooplankton on phytoplankton in the upper reaches of the Schelde estuary (Belgium/The Netherlands
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  Grazing by meso- and microzooplankton on phytoplanktonin the upper reaches of the Schelde estuary(Belgium/The Netherlands) M. Lionard  a, *, F. Aze ´mar  b , S. Bouleˆtreau  b , K. Muylaert  a ,M. Tackx  b , W. Vyverman  a a University Gent, Biology Department, Sect. Protistology and Aquatic Ecology,Krijgslaan 281 - S8, B 9000 Gent, Belgium b Laboratoire d’Ecologie des Hydrosyste `mes (LEH), Universite´  Paul Sabatier,118 route de Narbonne, F-31062 Toulouse, Cedex 4, France Received 8 November 2004; accepted 18 April 2005Available online 5 July 2005 Abstract In contrast with the marine reaches of estuaries, few studies have dealt with zooplankton grazing on phytoplankton in the upperestuarine reaches, where freshwater zooplankton species tend to dominate the zooplankton community. In spring and early summer2003, grazing by micro- and mesozooplankton on phytoplankton was investigated at three sites in the upper Schelde estuary.Grazing by mesozooplankton was evaluated by monitoring growth of phytoplankton in 200  m m filtered water in the presence orabsence of mesozooplankton. In different experiments, the grazing impact was tested of the calanoı ¨d copepod  Eurytemora affinis , thecyclopoid copepods  Acanthocyclops robustus  and  Cyclops vicinus  and the cladocera  Chydorus sphaericus ,  Moina affinis  and  Daphniamagna /  pulex . No significant grazing impact of mesozooplankton in any experiment was found despite the fact thatmesozooplankton densities used in the experiments (20 or 40 ind. l  1 ) were higher than densities in the field (0.1 e 6.9 ind. l  1 ).Grazing by microzooplankton was evaluated by comparing growth of phytoplankton in 30 and 200  m m filtered water.Microzooplankton in the 30 e 200  m m size range included mainly rotifers of the genera  Brachionus ,  Trichocerca  and  Synchaeta , whichwere present from 191 to 1777 ind. l  1 . Microzooplankton had a significant grazing impact in five out of six experiments. They hada community grazing rate of 0.41 e 1.83 day  1 and grazed up to 84% of initial phytoplankton standing stock per day. Rotiferclearance rates estimated from microzooplankton community grazing rates and rotifer abundances varied from 8.3 to 41.7  m l ind.  1 h  1 . CHEMTAX analysis of accessory pigment data revealed a similar phytoplankton community composition after incubationwith and without microzooplankton, indicating non-selective feeding by rotifers on phytoplankton.   2005 Elsevier Ltd. All rights reserved. Keywords:  Schelde estuary; grazing; rotifers; mesozooplankton; phytoplankton; HPLC; CHEMTAX 1. Introduction In contrast to the downstream, marine reaches of estuaries, where the zooplankton community is usuallydominated by marine calanoid copepods (e.g. Castel andVeiga,1990; Soetaert and Van Rijswijk, 1993; Tackxet al., 1995; Roman et al., 2001), freshwater zooplank-ton species tend to become more important in the upperreaches of estuaries, where the water is fresh or slightlybrackish. In the upper reaches of estuaries, rotifers areoften numerically the dominant zooplankton group. * Corresponding author. E-mail address:  marie.lionard@ugent.be (M. Lionard).0272-7714/$ - see front matter    2005 Elsevier Ltd. All rights reserved.doi:10.1016/j.ecss.2005.04.011Estuarine, Coastal and Shelf Science 64 (2005) 764 e 774www.elsevier.com/locate/ECSS  Rotifers have been found to dominate the zooplanktoncommunity in the upper reaches of the Hudson Riverestuary (Pace et al., 1992), the Hawkesbury-NepeanRiver estuary (Kobayashi et al., 1996), Chesapeake Bay(Park and Marshall, 2000) and the Schelde estuary(Muylaert et al., 2000a; Tackx et al., 2004). In thisrespect, the upper reaches of estuaries strongly resemblethe lowland reaches of large rivers (e.g. Pourriot et al.,1982; Gosselain et al., 1994). Rotifers have a shortgeneration time compared to crustacean zooplanktonand are therefore well adapted to survive in ecosystemslike rivers and estuaries, which often have a short re-tention time. Freshwater crustacean mesozooplanktonlike cladocera or cyclopoid copepods may occasionallybecome abundant in the upper reaches of estuaries, butrarely during prolonged periods.Despite the fact that the upper reaches of estuariestend to be very turbid they often show dense phyto-plankton blooms. Phytoplankton biomass in upperestuarine reaches is often higher than in the marinereaches. Itis not unusual forchlorophyll a  concentrationsin the upper reaches of estuaries to exceed 50  m g l  1 (e.g. Schuchardt and Schirmer, 1991; Muylaert et al.,2005). While many studies have dealt with zooplanktongrazing on phytoplankton in the marine zone of estuaries (e.g. Heinle et al., 1977; Tackx et al., 1995;Roman et al., 2001), much less is known about thefate of phytoplankton in the upper estuary. Park andMarshall (2000) suggested that rotifers may play animportant trophic role in the upper reaches of estuaries.Grazing experiments carried out in the freshwater tidalPotomac River seem to confirm this hypothesis (Sellneret al., 1993). In the lowland reaches of rivers, of whichthe upper reaches of estuaries form a downstream con-tinuation, rotifers were found to graze a considerablefraction of phytoplankton production or standing stock.In the River Meuse, rotifers grazed up to 113% of phytoplankton standing stock per day (Kobayashi et al.,1996; Gosselain et al., 1998). Using riverine ecosystemmodels, rotifers were predicted to exert a significantcontrol on phytoplankton during summer (Seine river:Billen et al., 1994; Meuse river: Everbecq et al., 2001; Rhine river: Schol et al., 2002).The Schelde estuary is one of the few Europeanestuaries with an extensive freshwater tidal zone in itsupper reaches. This freshwater tidal zone is character-ized by the occurrence of dense phytoplankton bloomsand a zooplankton community that is dominated byrotifers (Tackx et al., 2004). The first goal of this studywas to determine whether zooplankton can exerta significant grazing pressure during phytoplanktonblooms in the upper reaches of the Schelde estuary. Theexperiments were carried out during the spring and thesummer blooms at three sites representative of riverine,freshwater tidal and oligohaline conditions. Grazing bymesozooplankton and microzooplankton (dominatedby rotifers) were determined separately to evaluate therelative roles of rotifers and mesozooplankton inphytoplankton grazing. Using CHEMTAX analyses of HPLC derived pigment data phytoplankton groupsselective grazing on the major was evaluated. 2. Materials and methods 2.1. Study site The Schelde estuary (Fig. 1) is a macrotidal coastalplain estuary situated in Western Europe. In contrast tomany other European estuaries, where locks have beenconstructed at the freshwater seawater interface, theSchelde estuary still possesses an extensive freshwatertidal zone in its upper reaches. In these upper reaches,dense phytoplankton blooms occur during spring andsummer. The spring bloom tends to be mainly importedfrom the tributary river Schelde while the summerbloom reaches its maximum within the upper estuary.These phytoplankton blooms are dominated by diatomsbut chlorophytes can be co-dominant in the tributaryrivers and near the head of the estuary in summer(Muylaert et al., 2000b). The zooplankton community inthe upper estuary is dominated by rotifers, whichfrequently attain abundances of about 1000 ind. l  1 (Soetaert and Van Rijswijk, 1993; Muylaert et al.,2000a; Tackx et al., 2004). Mesozooplankton densitiesrarely exceed 20 ind. l  1 . The crustacean zooplankton inthe freshwater tidal reaches and river is dominated bythe cyclopoid copepod  Acanthocyclops robustus  withother cyclopoid copepods or cladocera like  Cyclopsvicinus ,  Bosmina longirostris ,  Moina  spp. and  Daphnia spp. often being codominant. Towards the brackishreaches of the estuary, the calanoid copepod  Eurytemoraaffinis  replaces the cyclopoid copepods and cladocera.This species has recently moved upstream into thefreshwater tidal zone, possibly due to improved waterquality (Appeltans et al., 2003).For the experiments, water and zooplankton werecollected in 2003 in spring (March) and early summer(June) at three sites situated at the upper reaches of theSchelde estuary (Fig. 1): the river Schelde just before itenters the estuary, the freshwater tidal reaches of theestuary in Dendermonde and the oligohaline reaches inAntwerpen. March and June were representative for thetwo phytoplankton blooms that occur annually in theupper Schelde estuary. Water and zooplankton forthe experiments were sampled from the river bank usingbucket hauls. A quantitative mesozooplankton sample(50 l) was collected by means of a 200  m m mesh sizeplankton net. Salinity and temperature were measuredin situ using an YSI 650 MDS multimeter with an YSI600 R sensor. 765 M. Lionard et al. / Estuarine, Coastal and Shelf Science 64 (2005) 764 e 774  2.2. Experimental setup Grazing rates of meso- and microzooplankton onphytoplankton were estimated by comparing phyto-plankton growth rates in the presence and absence of grazers. Phytoplankton was separated from micro- andmesozooplankton by filtration over a 30  m m nylon mesh.Exploratory tests had demonstrated that this filter didnot significantly retain phytoplankton. Mesozooplank-ton was separated from microzooplankton by filtrationover a 200  m m nylon mesh. Microzooplankton grazingon phytoplankton was estimated by comparing phyto-plankton development in the  ! 200  m m and  ! 30  m mfiltrates. Microzooplankton therefore only includedgrazers in the 30 e 200  m m size range. Mesozooplanktongrazing on phytoplankton was estimated by comparingphytoplankton development in  ! 200  m m filtrates withand without added mesozooplankton. Mesozooplanktonwas collected at each sampling site by filtering 200 e 300 lof water through a 200 e m m mesh size plankton net. Aknown number of individuals were picked out usinga wide-bore pipette and a dissecting microscope to beadded to the treatments. Two mesozooplankton treat-ments were set up for each experiment. If two specieswere co-dominant in the mesozooplankton community,the grazing impact of these two species was assessedseparately. If only one species was dominant, this specieswas added to the treatments in different densities. Thetreatments were incubated in 1 l polycarbonate bottlesduring 1 day. Three replicates were prepared for eachtreatment. The bottles were incubated in a temperatureand light controlled incubator. Temperature was setwithin approximately 1   C of the field temperature(10   C in March and 20   C in June). Light intensity wasset at 22  m mol m  2 s  1 , which corresponds to the meanunderwater irradiance at Dendermonde in spring.The mean underwater irradiance was estimated froma typical spring surface irradiance, the vertical lightextinction coefficient and mean water column depth.The mean underwater irradiance experienced by phyto-plankton will have been different at the other two sitesand in summer. Therefore, growth rates measured in theexperiments cannot be extrapolated to the field situa-tion. In March, light was (accidentally) suppliedcontinuously while a 12 h dark e 12 h light cycle wassupplied in June. Bottles were incubated on a rotatingtable (100 rpm) to keep the phytoplankton in suspen-sion. All bottles were sampled for phytoplankton andmicrozooplankton at the start and at the end of theexperiment.Phytoplankton pigments were sampled by filtering50 e 100 ml water over 25 mm GF/F filter. Filters werequickly dried between blotting paper and stored frozenat   80   C until analysis. Microzooplankton was sam-pled by filtering 50 e 100 ml water over a 30  m m nylonmesh. Samples were fixed with formalin at a final GentAntwerpen 10 km N NorthSea Schelde 4°20’ Schelde 4°20’51°10’51°00’4°00’ Dendermonde FGBNLB 51°20’ Fig. 1. Map of the Schelde estuary indicating the position of the sampling sites with black points. The grey arrows indicate the position of upper limitof tidal influence.766  M. Lionard et al. / Estuarine, Coastal and Shelf Science 64 (2005) 764 e 774  concentration of 4%. Samples for quantification of ciliates were fixed according to the Lugol-formalin-thiosulphate method (Sherr et al., 1989). In themesozooplankton treatments, mesozooplankton indi-viduals added to the bottles were collected on a 200  m mmesh at the end of the experiment for identification upto the species level. Mesozooplankton was fixed in a 4%formalin solution. 2.3. Analysis of samples Phytoplankton biomass and community compositionwere investigated by means of HPLC pigment analysis.Pigments were extracted from the filters in 90% acetoneby means of sonication (tip sonicator, 40 W for 30 s).Pigment extracts were filtered over a 0.2  m m nylon filterto remove particulates. Pigments were injected intoa Gilson HPLC system equipped with an Alltimareverse-phase C18 column (25 cm ! 4.6 mm, 5  m m par-ticle size). Pigments were analysed according to themethod of  Wright and Jeffrey (1997), which is anadaptation of the method of  Wright et al. (1991) formarine phytoplankton. This method uses a gradient of three solvents: methanol 80% e ammonium acetate 20%,acetonitrile 90% and ethyl acetate. Three detectors wereconnected to the HPLC system: an Applied Biosystems785A Programmable Absorbance Detector to measureabsorbance at 785 nm, a Gilson model 121 fluorometerto measure fluorescence of chlorophylls and theirderivates and a Gilson 170 diode array detector tomeasure absorbance spectra for individual pigmentpeaks. Pigments were identified by comparison of retention times and absorption spectra with purepigment standards (supplied by DHI, Denmark).Mesozooplankton added to the bottles, the quanti-tative mesozooplankton samples and microzooplanktonpresent in the  ! 200  m m filtrates were identified andenumerated using a dissecting microscope. Identificationwas based on Ruttner-Kolisko (1972), Pontin (1978) andSegers (1995). Ciliates were counted using an invertedmicroscope. Ciliates were identified up to class levelFoissner et al. (1999). Samples for microzooplanktonand ciliates were stained with Bengal Rose to aid indistinguishing between plankton and detritus. 2.4. Data analyses One-way ANOVA was used to compare densities of potential grazers of phytoplankton and concentrationsof total chlorophyll  a  at the end of the experimentsbetween the treatments.The CHEMTAX software was used to calculate thecontribution of different algal groups to total chloro-phyll  a  using concentrations of accessory pigments. Thissoftware package was developed specifically for theanalysis of phytoplankton pigment data (Mackey et al.,1996). The CHEMTAX software makes use threematrices: (1) a matrix containing concentrations of allmarker pigments in the samples; (2) an initial matrixcontaining marker pigment to chlorophyll  a  ratios for allalgal groups; and (3) a ratio limit matrix defining limitson the theoretical marker pigment to chlorophyll  a  ratios.The CHEMTAX program optimizes the contribution of different algal groups to total chlorophyll  a  based onmeasured pigment concentrations (matrix 1), using thepigment ratio matrix (matrix 2) as a starting point andallowing pigment ratios to vary according to constraintsdefined in the limit matrix (matrix 3). The initial pigmentratio matrix (Table 1) was obtained from previousmonitoring studies of phytoplankton pigments in theSchelde estuary in which biomass of major phytoplank-ton groups estimated by means of HPLC-CHEMTAXanalyses was verified with data obtained by microscop-ical analyses (M. Lionard, unpublished data). Pigmentdata were processed separately using CHEMTAX foreach experiment.Community grazing rates and individual clearancewere calculated according to Walz (1978) and Frost (1972). Grazing rates were calculated as  g Z ln ð C  t = C  zt Þð 1 = t Þ  where  C  t  and  C  zt  are the concentra-tions of the prey at the end of the incubation period,respectively in the absence and in the presence of thepredator, and  t  is the incubation time (in days). Thepercentage of initial phytoplankton biomass grazed perday was calculated as 100    100 e  ln ð  g Þ . The individualclearance rate was calculated as  F  Z  g ð V  = P Þ , where  P  isthe density of predators and  V   is the bottle volume. For P  the average density of predators during the incubationperiod was used, which was calculated according toMarin et al. (1986):  P Z ð P t    P o Þ = ln ð P t = P o Þ  where  P t  is Table 1Initial matrix with accessory pigments to chlorophyll  a  ratios in the major algal groups used in the CHEMTAX analysesPeridinin Fucoxanthin DiatoxanthindiadinoxanthinAlloxanthin Lutein Zeaxanthin Echinenone Chlorophyll  b Chlorophytes 0 0 0 0 0.162 0.025 0 0.229Cryptophytes 0 0 0 0.212 0 0 0 0Cyanophytes 0 0 0 0 0 0.036 0.085 0Diatoms 0 0.701 0.160 0 0 0 0 0Dinophytes 0.760 0 0.302 0 0 0 0 0Euglenophytes 0 0 0.333 0 0 0 0 0.372767 M. Lionard et al. / Estuarine, Coastal and Shelf Science 64 (2005) 764 e 774  the final predator density and  P o  is the initial predatordensity. 3. Results As shown in Table 2 salinity was ! 0.5 in spring, aswell as in summer, in Gent and Dendermonde. InAntwerpen, salinity was ! 0.5 in spring but was 1.75 insummer, which is indicative of oligohaline conditions.Temperature was 9.5   C at all sites in spring and variedbetween 21.5 and 23.5   C in summer. In spring,chlorophyll  a  concentration was highest in Gent anddecreased in downstream direction towards Dender-monde and Antwerpen. In summer, chlorophyll  a  con-centration was highest in Dendermonde and was lower inthe river in Gent and in the oligohaline reaches inAntwerpen. The contribution of different algal groups tototalchlorophyll a wasassessedbymeansofCHEMTAXanalysis of accessory pigment concentrations. In Gentand Dendermonde in spring and in Dendermonde insummer diatoms dominated the phytoplankton commu-nity with at least 78% of total chlorophyll  a . In Gent insummer, chlorophytes were dominant (58% of totalchlorophyll  a ) with diatoms being co-dominant. InAntwerpen, diatomsandchlorophyteswereco-dominantin spring as well as in summer, with both groupscontributing 60 e 80% to total chlorophyll  a . In spring,euglenophytes contributed 11% to total chlorophyll  a  inGent and 18% in Antwerpen. The contribution of otheralgal groups to total chlorophyll  a  was always ! 10%.Total mesozooplankton density was  ! 1 ind. l  1 inspring and summer in Gent and in spring in Dender-monde. Highest mesozooplankton densities were ob-served in Dendermonde in summer (about 7 ind. l  1 )and in Antwerpen in spring (about 9 ind. l  1 ). Cyclopoidcopepods ( Acanthocyclops robustus ,  Cyclops vicinus )dominated the mesozooplankton community at all sites Table 2Environmental conditions and phytoplankton and zooplankton biomass or abundance and community composition at the sampling sites at the timeof the experiments. n.d. indicates that no data were collected and  e  indicates zero abundance or biomassSpring SummerGent Dendermonde Antwerpen Gent Dendermonde AntwerpenAbiotic factors T   (  C) 9.47 9.45 9.54 23.7 23.1 21.51Salinity 0.35 0.34 0.43 0.36 0.34 1.75ph 9.58 7.76 7.64 7.37 7.43 7.53O 2  (%) 82 65 35 49 41 22PhytoplanktonChl  a  ( m g l  1 ) 92.2 8.7 2.9 28.8 214.9 12.9Diatoms (%) 78 79 27 35 89 43Chlorophytes (%) 4 8 37 58 7 41Euglenophytes (%) 11 3 18 1 0 5Dinoflagellates (%) 6 4 0 1 0 0Cryptophytes (%) 1 4 9 1 3 7Cyanophytes (%) 1 1 9 4 0 5MicrozooplanktonRotifers (ind. l  1 ) 1157 191 860 1777 1433 796 Brachionus calyciflorus  (%) 53 31 33 34 1 1 Brachionus angularis  (%) 5 6 2 18 15 3 Polyarthra  sp. (%) 11 7 7 0 9 0 Syncheata  sp. (%) 5 11 35 1 3 18 Trichocerca  sp. (%) 0 0 0 17 55 74Other rotifers (%) 26 45 23 30 17 4 Copepod nauplii   (ind. l  1 )  e  9.5 140  e  190 7Ciliates (ind. ml  1 ) n.d. 80.8 46.5 75.4 55.3 31.7Mesozooplankton (ind. l  1 ) Acanthocyclops robustus  e e e  0.2 6.9  e Chydorus sphaericus  0.1  e  0.5  e e e Cyclops vicinus  0.4 0.5 4.1  e e e Daphnia pulex  e e e e e  0.2 Daphnia magna  e e e e e  0.2 Eurytemora affinis  e e  4  e e  1.5 Moina affinis  e e e  0.8  e e 768  M. Lionard et al. / Estuarine, Coastal and Shelf Science 64 (2005) 764 e 774
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