MARINE ECOLOGY PROGRESS SERIES Vol. 78: 123-129,1991 Published December 16 Mar. Ecol. Proy. Ser.

Grazing pressure of the calanoid longicornis on a Phaeocystis dominated spring bloom in a Dutch tidal inlet

F. C. ~ansen',W. H. M. van ~oekel~

'NetherlandsInstitute for Sea Research, PO Box 59, 1790 AB Den Burg, The Netherlands 'University of Groningen, Dept of Marine Biology, PO Box 14, 9750 AA Haren, TheNetherlands

ABSTRACT Between 30 March and 11 May 1990, total copepod abundance and the abundance. b~omassand gut fluorescence of Temora longlcornls were determined and related to the abundance and succession of development in a Dutch tidal inlet Gut plgment values were h~ghest In females and lowest In young copepodites, but weight-spec~f~cpigment concentrations were about slrnilar Pigment levels measured In the guts were relatively high at the beginning and end of the penod of investigation when dom~natedthe phytoplankton community, dnd low dunng the Phaeocystls dom~natedperiod, when ambient chlorophyll concentrations were h~ghest For the latter period, calculated ingestion rates In T longlcornls were low and estimated dally consumption amounted to less than 1 % of the phytoplankton standing stock, suggeswg a negl~giblegrazlng Impact on the development of the Phaeoc)/stls bloom In splte of the low grazrng on phytoplankton. T long]- corms biomass increased by one older of magnitude The discrepancy between low giazlng pressuie and copepod development is explained by assumlng that T long~cornlsscvltched to heterotrophic food a bloom of ciliates present during the Phaeocystls dominated period

INTRODUCTION scientists within a joint EEC project. A major question to be answered is the ultimate fate of Phaeocystis and Copepod grazing has traditionally been regarded as In this context the possible role of in con- having an important function in coupling phyto- trolling Phaeocystis blooms. plankton to higher trophic levels, leading to fish The literature concerning copepod grazing on production (Steele 1974). Increased nutrient Inputs Phaeocystis is contradictory. On the one hand, Phaeo- into North Sea coastal waters in the past 2 decades cystis 1s regarded as unsuitable food (e.g. Schnack correlate not only with an increase in phytoplankton 1983, Daro 1986, Verity & Smayda 1989).This holds for biomass but also with a shift in its community compo- the colonies, because they are sticky and partly too sition towards flagellates (Cadee 1986, Radach et al. large (up to ca 20 mm), as well as for the small flagel- 1990). In particular since 1973, blooms of the prym- lates (3 to 8 pm) which are at the lower end of the size nesiophyte Phaeocystis sp. have increased (e.g.Cadee spectrum of retainable algae for most herbivorous 1986), which has been reported to cause nuisances and copepods. Possible negative effects on copepods by possible econonlic drawbacks in fishery (e.g. Savage the release of antibacterial acrylic acid (Sieburth 1960) 1932) and tourism (Lancelot et al. 1987). Environ- and DMS (Glbson et al. 1990) have not yet been mental problems are suspected from diinethylsulfide studied in detail. On the other hand, Phaeocystis (DMS) release (Turner et al. 1988 and references cited ingestion by copepods has been reported (e.g. Lebour therein) and mass production and sedimentation 1922, Estep et al. 1990) and recent laboratory studies (Wassmann 1990) of organic matter, for which the quantifying grazing (Huntley et al. 1987, Tande & impact on the benthic and pelagic food web structure B6mstedt 1987, Hansen et al. 1990) indicate that is still unclear. Since 1988, Phaeocystis bloom copepods are potential Phaeocystis consumers. In this dynamics have been studied by a group of European respect, the calanoid copepod Temora longicornis

0 Inter-ResearchIPrinted in Germany 124 Mar. Ecol. Prog. Ser. 78: 123-129, 1991

seems to be a promising candidate, because of its high abundance during spring in North Sea coastal waters (e.g. Fransz & van Arkel 1983 and references cited therein) and its ability to feed on Phaeocystis colonies (Weisse 1983) and single cells (F. Hansen unpubl. obs.). There are strong indications that food quality and composition have a major impact on copepod grazing activity (e.g. Cowles et al. 1988, Estep et al. 1990, Klein Breteler et al. 1990, F. Hansen unpubl.). Differ- ences in food quality and composition may also be responsible for contradictions in reports regarding copepod grazing on Phaeocystis in laboratory and field studies. Direct estimates of copepod grazing on a Phaeocystis bloom in the field are scarce and contra- dictory. This study measures Temora longicornis grazing activity in the course of a Phaeocystis domi- nated spring bloom in the field by means of the gut fluorescence method, in order to evaluate the im- portance of T longicomis for Phaeocystis bloom dynamics.

MATERIAL AND METHODS

Samples were collected from the Marsdiep (Fig. l),a eutrophicated and well-mixed tidal part of Dutch coastal waters. A detailed description of the hydro- graphy of this area was given by Postma (1954). To follow phytoplankton and development, quantitative surface water samples were taken frequently between 30 March and 11 May 1990, always at high tide. During this period, water temp- erature remained low until 24 April (8 to 10 "C), with Fig. l Location of the Marsdiep area (asterisk ~ndicates position of sampling site) a subsequent rise to 14 "C in mid-May. Chlorophyll a (chl a) concentration in the samples was measured by applying the spectrophotometric stored in the dark in Petri dishes at -24 OC for 2 to 4 mo. method of Lorenzen (1967). Cell number and species Copepods were collected from the gauzes and sorted composition of phytoplankton were determined with for species under a dissecting microscope. Temora the Utermohl sedimentation technique (Utermohl longicornis specimens were further sorted for sex and 1958) in samples fixed with Lugol. Cell volumes of developmental stage, and their lengths measured. Phaeocystis and species were determined by Young copepodite stages (stage 5 C4) were distin- n~icroscopical size measurements. Phytopiankton guished from older copepodites (stage C5 pius C6), carbon was calculated by assuming that the chl a ratio which were separated into males and females. Phaeocystisldiatoms equals the biovolume ratio Temora longicornis gut fluorescence was determined Phaeocystisldiatoms in the samples and by applying a as described by Baars & Oosterhuis (1984) with minor carbon/chl a ratio of 25 in diatoms (Riemann et al. modifications. Copepods were homogenized using a 1982) and 29 in Phaeocystis (Lancelot-van Beveren Potter grinder. After 2 h of extraction in the dark at 1980). The Phaeocystis colonies in the samples were all 5 'C, the solution was filtered through a GF/F filter of the globosa-type (Jahnke & Baumann 1987). mounted on a syringe. In the filtrate, chlorophyll a and To collect copepods, 60 1of water collected by bucket phaeopigment concentrations were measured and gut was poured into plastic bottles and gently filtered over fluorescence was taken as the sum of chlorophyll a a floating 300 pm gauze. Retained plankton were plus phaeopigments, expressed as ng chl a equivalent rinsed on pieces of 200 pm gauze and mmediately per copepod. In preliminary experiments background deep-frozen by means of liquid nitrogen. Gauzes were fluorescence and changes in pigment concentration Hansen & van Boekel: Grazing pressure of a copepod 125

due to storage and freezing were found to be negligible. Gut pigment content (chl a plus derived phaeo- pigments) is expressed as ng chl a weight equivalent per copepod or per mg ash-free dry weight, calculated from size-weight relationships given by Klein Breteler & Gonzales (1988). Temora longicornis body carbon was taken as 40 % ash-free dry weight (Omori 1969). Copepod ingestion rates were calculated from gut fluorescence and temperature-dependent rates of gut clearance given by Dam & Peterson (1988).

30 2 6 10 14 18 2226 30 4 8 12 April May RESULTS Fig. 3. Phaeocystis biovolume fractionof total phytoplankton Between 30 March and 9 April 1990, the phyto- biomass in Marsdiep. Vertical lines indicate period of plankton community in the Marsdiep was dominated Phaeocystis dominance by large diatoms (Biddulphia sinensis, Thalassiosira spp.). In the first half of April, both chl a and Phaeo- number. Other copepods mainly consisted of Pseudo- cystis cell concentration increased, with peaks on 13 calanus elongatus, which appeared in higher concen- and 15 April respectively (Fig. 2). At the peak of tration during May. An attempt was made to esti- the Phaeocystis bloom, cell concentration exceeded mate T longicornis production from biomass increase 67 X 106 cells 1-' while the chlorophyll concentration in the larger copepodites by the application of an amounted to 55 pg chl a I-' Thereafter, Phaeocystis exponential growth model (Fig. 5). The significant cell density and chlorophyll concentration declined regressions for females (1) and males (2),(r12 = 0.80; sharply. Between 11 and 24 April, phytoplankton r,'= 0.74; nl, n2 = 9; p], p2 < 0.01), yielded minimum biomass was dominated by Pl~aeocystis(Fig. 3). In the P/B ratios (including mortality, see 'Discussion') of second half of April small diatom species (Plagio- 15 O/O d-l, indicating good growth during the Phaeo- gramma brockmanni, Asterionella spp.) became cystis dominated period. increasingly important. Cerataulina bergonii domi- Gut fluorescence of males and females (C5 + C6) and nated the phytoplankton community after 24 April. In smaller copepodites did not resemble the course of the the latter period, chlorophyll concentration decreased chlorophyll concentration in the water (Figs. 2 & 6), but further down to 11 ,ug chl a 1-'. appeared to be inversely correlated with Phaeocystis Copepod abundance remained low until mid-April, dominance (Fig. 3). During the Phaeocystis attributed reaching significantly higher concentrations in the chlorophyll increase, gut fluorescence declined, being latter part of the investigation period (Fig. 4). Gener- lowest while Phaeocystis dominated the phyto- ally, Temora longicornis was the dominant copepod, plankton community. Thereafter in May, while the comprising on average 80 % of the total copepod phytoplankton community was mainly composed of

chl a re0 a, 2 6M0 3 other copepods cells - - 5000 Temora

%:

302 5 91214172022242714 711 April May April May Fig. 2. Phytoplankton spring development in the Marsdiep Fig. 4. Abundance of Ternora longicomjs and other copepod from 30 March to 12 May 1990: chlorophyll a and Phaeocystis species in the Marsdiep in spring 1990 (mean concentrations cell concentrations of all stages concentrated on 300 pm gauze) 126 Mar. Ecol. Prog. Ser. 78. 123-129, 1991

C5+C6 females U g 1 C5+C6 females C5+C6 males A C5+C6 males 0 smaller copepodites

April

Fig. 5. Biomass of male and female C5 and adult Temora Fig. 7. Temora longicornis. Weight-specific gut fluorescence longicornjs in the Marsdiep in spnng 1990 (mean concen- of 3 age and sex classes In the hlarsdiep during sprlng trations of all stages concentrated on 300 pm gauze). Expo- 1990 (mean concentrations of all stages concentrated on nential growth curves fitted according to: B, = B, (?"'.R - "'l', 300 pm gauze) where Bo, B,: biomass at the beginning/end of studied period t (in days); P: production; m: mortality. (For results, see text) ranged between 6 and 26 ng chl a 1-' d-l. This is less than 1 O/oof the phytoplankton standing stock present. several small diatom species, gut fluorescence showed Thus it is concluded that grazing by 7: longicornls did an increase of a factor of about 4. not have a significant impact on the dynamics of the Generally females showed highest gut fluorescence, spring Phaeocystis bloom. Considering the small males lower, and copepodites the lowest gut fluores- biomass of the other copepods, this probably also holds cence (Fig. 6). However, after correcting for body size for the whole copepod community. differences, by expressing gut fluorescence per unit ash-free dry weight (AFDW),the gut fluorescences of the different sexes and stages were almost the same or DISCUSSION rather higher in the smaller stages (Fig. 7). In the diatom dominated periods, calculated ingestion rates The gut fluorescence method (Mackas & Bohrer were much higher in April/May compared to 1976) allows the study of undisturbed grazing by March/April (Table l), partly due to the higher gut copepods in the field and has therefore been widely evacuation rates in the latter period with higher water implemented for the last 15 yr. The uncertainty in the temperature. determination of gu.t passage times suggests that one Total daily phytoplankton ingestion by Temora has to be cautious deriving absolute ingestion figures longicornis was low, especially during the Phaeocystjs from gut fluorescence measurements (e.g. Penry & dominated period. In this period, total ingestion Frost 1990 and references cited therein). However, Kiarboe et al. (1982, 1985) and Peterson et al. (1990) have shown good agreement of this method with esti- 0.8- C5+C6 females U mates obtained by the measurement of the decrease of P A C5+C6 males Q chlorophyll and cells during incubation experiment as P o smaller copepodites 8 0.6 - well as good correlation between ingestion measured P5 with the gut fluorescence technique and egg pro- duction. Thus, for studying daily feeding rhythms or I 0.4 - U seasonal differences, as presented here, the gut fluo- rescence method may still be regarded as a useful tool. 0.2 - Many authors have reported diel feeding rhythms in Sf copepods (e.g. Mackas & Bohrer 1976, Stearns 1986, m Tiselius 1988) although such rhythms may also be o.O!.l.l.l.l.,.l'l.l.I.I.I 30 2 6 10 14 18 2226 30 4 8 12 absent (Roman et al. 1988). Baars & Fransz (1984) and April May Dam (1986) found gut pigment content in Temora longicornis to be about twice as high at night as during Fig. 6. Temora long~corn~s.Gut fluorescence of 3 age and sex classes in the Marsdiep during spring 1990 [mean concen- the day. It has been proposed that light intensity is an trations of all stages concentrated on 300 pm gauze) important factor in controlling diel feeding rhythms Hansen & van Boekel: Grazing pressure of a copepod 127

Table 1 Temora longicornis grazing pressure on the 1990 phytoplankton spring bloom before, during and after the Phaeocystis dominated period. Arithmetic means of weight-specific gut fluorescence (GF), gut passage time (GPT), specific daily ration (SDR),'T: longicornis biomass (TB], total phytoplankton ingestion by 7: longicornis (TPI),phytoplankton standing stock (PSS) and grazing pressure (GP) as ratio TPI/PSS for copepodite stages C5 + C6 females (f'),C5 + C6 males (m') and younger copepodites (c')

Date Group GF G PT SDR TB TPI PSS G P (ng chl a equiv. (min) (mg C mg (mg C m-3) (mg C m-' d.') (mg C m-" (%) mg body C-') body C-' d-')

29 Mar f ' to m' 12Apr c' Sum

13 Apr f ' 14.0 to m 15.5 24 Apr C' 18.1 Sum

25 Apr f' 37.7 to m' 41.3 11 May c' 55.5 Sum

(e.g. Stearns 1986 and references cited therein). In the obtained from growth experiments with T longicornis highly turbid Marsdiep area, copepods are exposed to cultures in the presence of excess food (Klein Breteler low light levels during daytime as well. Hence, they et al. 1990). During the Phaeocystis bloom, the calcu- might exhibit a much less pronounced daily feeding lated daily ration of T. longicornis, as based upon gut rhythm than copepods in other areas. Sampling took fluorescence measurements, amounted to only a small place at high tide, thus varying regularly between percentage of its body carbon, quite insufficient to 07:OO and 19:OO h with 3 shifts from evening to cover its food demand. Even on the basis that T longi- morning sampling in the course of this study. However, cornis fed solely on Phaeocystis colonies with a C/chl a neither an increase in gut fluorescence coinciding with ratio ranging between 55 and 245 (Lancelot & Billen these shifts was observed, nor could the observed 1990) and converted the mucus with the same gross variation of gut fluorescence be correlated to sampling growth efficiency (which is unlikely because it has a time. Daro (1986) likewise reported that T longicornis low nitrogen content), a considerable gap between lost its feeding rhythm during a Phaeocystis bloom. autotrophic food intake and energy demand would still Dlel feeding rhythms were not investigated in this remain. study and day-night differences in feeding could have In order to explain the high growth rates, the led to an underestimation of daily ingestion and hypothesis is put forward that Temora longicornis consumption rates calculated. However, this would not switched to a heterotrophic food source, at least during affect the major conclusions drawn in this paper. the Phaeocystis dominated period. We here consider 2 The observed spring increase in Temora longicornis major possibilities for this food source: detritus, prob- abundance is in accordance with previous studies in ably coated with bacteria, and microzooplankton. the Marsdiep area (Fransz & van Arkel 1983, Kuipers Unfortunately, there is very little information on the et al. 1990). The estimate for T longicornis production quality and quantity of detritus in the Marsdiep and to in April (Fig. 5) was made under the assumption that what extent detritus might be utilized by T longicornis. biomass accumulation in the older stages reflected the However, during the Phaeocystis dominated period a average copepodite growth in the sampled waters. bloom of ciliates was present exceeding copepod Fransz (1976) showed a similar spring development of biomass (R. Bak unpubl.). Protozoa are judged to be T. longicornis in different areas along the Dutch coast. high-quality food for zooplankton (see review by Assuming a daily mortality of about 10 % (e.g. Bakker Stoecker & Capuzzo 1990), in contrast to Phaeocystis & van Rijswijk 1987 and references cited therein), no for which a biochemical investigation reports a low advection, and a gross growth efficiency between nutritional value (Claustre et al. 1990). If copepod l? % (Harris & Paffenhofer 1976) and 35 % (e.g. Berg- grazing on Phaeocystis is affected by the availability gren et al. 1988), the observed growth of T longicornis and quality of alternative food sources, this might would require an ingestion of 70 to 140 % of body explain why most laboratory studies indicate that weight daily. This value agrees well with rates Phaeocystis, when offered alone or in mixture with 128 Mar. Ecol. Prog. Ser.

other phytoplankton, is appropnate food, whereas selection by copepods: dlscrimination on the basis of food field studies indicate grazing to be depressed dunng quality. Mar. Biol. 100: 41-49 Phaeocystis blooms (Daro 1986, van Rijswijk et al. Dam, H. G. (1986). Short-term feeding of Ternora longicornis Miiller in the laboratory and the field. J. exp. mar. Biol. 1989). Laboratory grazing studies on copepods have Ecol. 99: 149-161 shown higher feeding rates on ciliates compared to Dam, H. G.. Peterson, W. T. (1988). The effect of temperature phytoplankton (Stoecker & Sanders 1985, Willlamson on the gut clearance rate constant of planktonic copepods. & Butler 1986, Stoecker & Egloff 1987), as well as pos- J exp mar. Biol. Ecol. 123. 1-14 Daro, M. H (1986). Field study of the diel, selective and itive selectivity for ciliates in mixtures with phyto- efflclency feeding of the manne copepod Temora longi- plankton (Wiadnyana & Rassoulzadegan 1989). cornis in the Southern Bight of the North Sea. In: van Ciliates are thought to be the major predator on Grieken. R.. Wollast, R. (eds.) Proc. of the Conference Phaeocystis single cells (Weisse & Scheffel-Moser 'Progress in Belgian Oceanographic Research'. Brussels, 1985. p. 250-263 1.990). If copepods are able to control ciliate abundance Estep, K. W., Nejstgaard, J C., Skjoldal, H. R , Rey, F. (1990). they may indirectly have a considerable impact on Predation by copepods upon natural populations of Phaeo- Phaeocystis bloom dynamics. Whether copepod cystls pouchetii as a functlon of the physiological state of grazing enhances or depresses Phaeocystjs develop- the prey. Mar. Ecol. Prog. Ser. 67(3):235-249 ment will then depend on the availability and type of Fransz, H. G. (1976). The spring development of calanoid copepod populations in the Dutch coastal waters as alternative food sources. We are continuing research related to primary production. In: Persoone, G.. Jaspers, E. on this topic and suggest that further grazing studies (eds.) Population dynamics of marine organisms in should concentrate more on heterotrophic microzoo- relation with nutrient cycling In shallow waters. Proc, 10th plankton and its possible function as a link between Eur. Mar. Biol. Symp., Vol 2. Universa Press, Wetteren, phytoplankton and larger zooplankton. p. 247-269 Fransz, H. G.. van Arkel. W. (1983). Fluctuation and suc- cession of common pelagic copepod species in the Dutch Wadden Sea. In: Boutler, J. (ed.) Proc. 17th Eur. Mar. Biol. Acknowledgements. This work was financially supported by Symp. Oceanol. Acta Vol. spec., p. 87-91 the EEC and is a contribution to the EEC research project on Gibson, .l. A. E., Garrick, R. C.. Burton, H. R.. 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This article was submitted to the editor Manuscript first received: May 17, 1991 Revised version accepted: October 31, 1991