Is sedimentation of copepod faecal pellets determined by cyclopoids? Evidence from enclosed ecosystems

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1 Is sedimentation of copepod faecal pellets determined by cyclopoids? Evidence from enclosed ecosystems CAMILLA SVENSEN* AND JENS C. NEJSTGAARD NORWEGIAN COLLEGE OF FISHERY SCIENCE, UNIVERSITY OF TROMSØ, N-9037 TROMSØ AND DEPARTMENT OF FISHERIES AND MARINE BIOLOGY, UNIVERSITY OF BERGEN, HIB, PO BOX 7800, N-5020 BERGEN, NORWAY *CORRESPONDING AUTHOR: Vertical flux of faecal pellets was compared in 26 vertically stratified 27 m 3 (diameter 2 m, depth 9.3 m) in situ seawater enclosures deriving from four separate experiments on the Norwegian west coast. Sediment traps were mounted in the non-mixed lower layer at 8 m depth. The zooplankton community composition was natural in three of the experiments, while manipulated to include four concentrations of Calanus finmarchicus in one. Calanoid copepods such as C. finmarchicus, Paracalanus spp., Pseudocalanus spp. and Microcalanus spp. dominated the zooplankton biomass in all mesocosms, except in eight of the enclosures where the cyclopoid copepod Oithona spp. occupied up to 40% of the biomass. Vertical flux of faecal pellet carbon (FPC) showed a significant negative correlation with Oithona biomass. In order to determine the retention potential of Oithona, measured sedimented faecal pellet carbon (FPC sed ) was compared with estimated maximum and minimum egestion rates. FPC sed decreased with increased biomass of Oithona. When the contribution of Oithona to the total copepod biomass was high, FPC sed was reduced to a few per cent of the maximum calanoid egestion rate (E max ) and was significantly less than the expected minimum calanoid egestion rate (E min ) in four of the mesocosms. On the other hand, FPC sed increased towards E max when the fraction of calanoid copepods increased towards 0% of the total copepod biomass. The results were obtained in experiments characterized by an extensive range of physical and biological processes. We suggest that the biomass ratio between pellet-producing (calanoids) and pellet-reworking copepods (Oithona) may be used to predict relative pellet retention and/or sedimentation rates of calanoid faecal pellets in natural plankton. INTRODUCTION Phytoplankton aggregates and faecal pellets are considered to be the most important vehicles for the transport of carbon from the euphotic zone. However, investigations involving sediment traps often find that zooplankton faecal pellets comprise only a minor fraction of sedimented material [see (Turner, 2002) for a review], and that the vertical flux of copepod faecal pellets gradually decreases with depth (Viitasalo et al., 999; González et al., 2000). One mechanism that could be responsible for this is zooplankton modification and grazing on faecal pellets (Smetacek, 980; Lampitt et al., 990; Noji, 99; Wassmann et al., 999; Reigstad, 2000; Wexels Riser et al., 200). Both calanoid (Dagg, 993) and cyclopoid copepods (González and Smetacek, 994) are known to graze on detrital material. However, because of its feeding behaviour, Oithona sp. is considered very efficient in faecal pellet grazing (González and Smetacek, 994). This cyclopoid copepod is a true ambush feeder and most likely perceives prey by means of hydromechanical, instead of chemical, signals (Svensen and Kiørboe, 2000). Therefore, Oithona sp. feeds mainly on motile prey (Paffenhöfer, 993, 998; Sabatini and Kiørboe, 994; Nielsen and Sabatini, 996) and probably also on sinking faecal pellets (González and Smetacek, 994). Copepods of the genus Oithona are abundant in coastal and oceanic waters (González and Smetacek, 994; Atkinson, 996; Nielsen and Sabatini, 996) and may act as a coprophagous filter (González Journal of Plankton Research 25(8), Oxford University Press; all rights reserved

2 and Smetacek, 994). Pulses of sedimented faecal pellets would then be a result of leaks in the filter that could be caused by patchiness in horizontal distribution or local decimation of the scavengers by predators (González and Smetacek, 994). Studying faecal pellet grazing (coprophagy) in situ is difficult because of advective processes influencing both the zooplankton community and sedimentation of faecal matter, and process studies in the laboratory are rare (González and Smetacek, 994). Mesocosms represent a link between in situ and laboratory studies and have the following advantages: (i) the zooplankton community composition and abundance can be controlled; and (ii) there are no problems resulting from advection. Encouraged by the above-mentioned advantages, we investigated vertical faecal pellet fluxes in four different mesocosm experiments with different abundances and compositions of mesozooplankton. In particular we hypothesized that the cyclopoid copepod Oithona sp. (hereafter termed Oithona) has a strong regulating effect on the vertical export of faecal pellets. We further hypothesized that the retention of faecal pellets is dependent on the ratio between faecal pellet producers and potential consumers (in this respect the calanoid copepod:oithona ratio). METHOD The mesocosm Four mesocosm experiments (each consisting of four to eight enclosures) were conducted in the Raunefjord (60 N, 60 W), western Norway between 996 and 998 (Table I). Each experiment consisted of vertically stratified enclosures, 9.3 m deep (the lower.5 m being slightly conical) and 2 m in diameter (27 m 3 ). For a more detailed description of the location and general set-up see Svensen (Svensen et al., 200) and LSF/inst2.html. The overall objective for all experiments was to investigate the effect of macronutrients (nitrate, phosphate and silicate) on phytoplankton and zooplankton production and the vertical flux of biogenic matter. Briefly, as explained in Table I, experiments I and II (September 996 and April 997) were designed to test the effect of two levels of turbulence on the plankton community. In experiment III (April/May 998) we investigated the effect of copepod grazing by adding Calanus finmarchicus to the enclosures in low to moderate natural concentrations. In experiment IV (August 998) the effect of nutrient pulsing was studied by adding nutrients either all at once, in intervals or in constant supply. In all experiments, every mesocosm was fertilized with nitrate and phosphate (i.e. NP enclosures), while half received silicate in addition (i.e. NPS enclosures). The mesocosms were filled by pumping water from ~5 m depth outside the mesocosms with a large volume centrifugal pump optimized for low disturbance of the plankton. In experiments I, II and IV, the mesocosms were filled with unfiltered seawater, allowing a natural composition and abundance of zooplankton. In experiment III, the water was screened through a 90 µm mesh to remove all large zooplankton prior to the controlled addition of copepods. Stratification was created in all enclosures either by increasing the salinity in the lower 4 m (experiment II), or by adding fresher water to the upper layer (experiments I, III and IV). The increase in salinity was achieved by introducing filtered ( µm mesh) seawater saturated with NaCl from a large tank through tubes with outlet at 7 m depth in each mesocosm. The upper 4 m of the mesocosms were kept homogeneous by airlift systems, pumping water at 40 l min ( Jacobsen, 2000). This mixing system generated turbulence in the Table I: Description of the four mesocosm experiments providing data for this paper (26 enclosures in total) Exp. Timing Days Temp. ( C) Encl. Purpose of experiment range (average) I September () 6 Effect of turbulence and silicate on the plankton community II April (6) 4 Effect of turbulence and silicate on the plankton community III April/May (7.5) 8 Plankton community response to large calanoid grazers in concentrations ranging from low to normal IV August (4) 8 Effect of nutrients added in pulses compared with constant nutrient supply Exp. indicates the roman number by which the experiment is referred to in the text. Days gives the duration of the experiment. Encl. is the number of enclosures in each experiment. Temperature ( C) is given as range and average (in parentheses). All enclosures were fertilized with nitrate and phosphate, while in half of them dissolved silicate was also added. 98

3 C. SVENSEN AND J. C. NEJSTGAARD FAECAL PELLET SEDIMENTATION DYNAMICS order of 8 W kg (Svensen et al., 200), and was thus within the range of what can be found naturally in the mixed upper layer ocean (Oakey and Elliott, 980). Zooplankton abundance Metazooplankton were collected by pump between filling each mesocosm (start concentrations), by weekly net hauls in the mesocosms during the experiment, and at the termination of the experiments by pumping the entire mesocosm content through a net. All nets had 90 µm meshes. Pump samples were collected with a 56 cm diameter net, while the net used for hauls in the mesocosms was smaller (30 cm diameter) to minimize the zooplankton removal from the mesocosm during the experiment. Samples were fixed with buffered formaldehyde (4% final concentration) and examined under a dissecting microscope (Wild M). Metazooplankton abundance was converted into carbon values using species- and stage-specific values from the literature (Nejstgaard et al., 200). Net and pump samples were pooled to calculate average abundance for the experimental period from each mesocosm. Vertical flux Vertical flux of particulate organic carbon (POC) and faecal pellets was measured with sediment traps immersed to a depth of 8 m. The traps consisted of transparent cylinders (height 0.45 m, inner diameter m, aspect ratio 6.25) mounted on a gimballed frame. The sediment traps were deployed for 48 h (experiments I and II) or 24 h (experiments III and IV), and no preservative was applied. POC was measured by filtering triplicate subsamples of sedimented material onto pre-combusted Whatman GF/F glass fibre filters and analysed on a Leeman Lab 440 elemental analyser, after fuming with HCl to remove carbonates. Subsamples for faecal pellet analysis (0 ml) were preserved with a Lugol mix of 2% final concentration (Rousseau et al., 990). Pellets were counted and measured (length and width) in a.0 ml chamber using a Rathenow (Zeiss, Jena) light microscope at 0 magnification. Faecal pellet carbon (FPC) was calculated from volumes, assuming cylindrical shape, and a volumetric carbon conversion factor of mg C mm 3 (Riebesell et al., 995). This rather high factor was chosen in order to avoid an underestimation of the sedimented faecal pellets. However, it is still realistic for a bloom situation in our geographic area (T. Noji, personal communication), and lies within reported factors for faecal pellets produced by similar calanoid communities (González and Smetacek, 994) in nearby fjords (González et al., 994). No attempt was made to distinguish between whole and fragmented faecal pellets. Sedimented faecal pellets are therefore presented in terms of FPC instead of absolute numbers. Estimation of copepod ingestion and egestion rates In order to estimate FPC production in the different experiments and enclosures, we calculated minimum and maximum ingestion and egestion rates for calanoid copepods. Comparing the potential FPC production with measured faecal pellet sedimentation rates is assumed to reflect the faecal pellet retention capacity of the zooplankton community. For instance, less FPC in the sediment traps than calculated from minimum carbon requirements (i.e. respiration) would mean that recycling processes or mechanical breakage were taking place in the water column. Only calanoid copepods (stages NIII CVI) were considered in the calculations because faecal pellets from cyclopoid copepods have been suggested not to make an important contribution to the vertical export of carbon (González and Smetacek, 994; Lane et al., 994). Nauplii were included because small faecal pellets with volume <6 4 µm 3 were recorded in the sediment traps, and these could have been produced by nauplii (Mauchline, 998). Minimum ingestion rates were calculated from weightspecific respiration rates according to Ikeda (Ikeda, 985): ln (R) = ln (CW ) T () where R is individual respiration rate (µl O 2 ind. h ), CW is copepod carbon weight (mg C ind. ) and T is temperature ( C). Respiration rates (R; ml O 2 ind. h ) were then converted to individual carbon requirements (CR; mg C ind. h ) according to Ikeda et al. (Ikeda et al., 2000): CR = R 0.97 (2/22.4) (2) Maximum ingestion rates were calculated according to Hansen et al., using a corrected version of the empirically obtained regression between predator volume and maximum specific ingestion rates (Hansen et al., 997). The zooplankton biomass was converted to biovolume assuming 0.45 g C (g DW) and 0.2 g C cm 3 and ingestion calculated using the regression by Hansen et al. (Hansen et al., 2000): log (I max ) = log(b) (3) I max is maximum ingestion (µg C ind. h ) at 20 C and b is copepod volume (cm 3 ). All rates obtained in µm 3 were converted to mg C m 2. The rate was then corrected for temperature with an overall Q of 2.8 (Hansen et al., 997), using the equation correlating temperature and biological process rate (r): 99

4 log (r t ) = log (r 0 ) + log [Q (t t 0 )/] (4) Minimum ingestion rates were converted into minimum egestion rates by assuming 80% assimilation efficiency (i.e. assuming that 20% of the ingested C was egested) (Hasset and Landry, 990). Reversibly, maximum egestion rates were calculated from maximum ingestion rates assuming 20% C assimilation efficiency (Hasset and Landry, 990). This procedure should ensure that the possible range of FPC production was not underestimated. Spearman rank correlations were calculated for sedimentation rates of FPC and calanoid and cyclopoid biomass (performed in StatView 5.0., SAS Institute Inc.). Statistical differences between estimated and observed sedimentation rates were tested with a two-tailed t-test (performed in Excel version 8.0). Copepod biomass was log-transformed before analysis. RESULTS Zooplankton biomass Total average zooplankton biomass in the four experiments ranged from 8 to 4 mg C m 3 in experiment I, mg C m 3 in experiment II, 2 53 mg C m 3 in experiment III and mg C m 3 in experiment IV (Figure ). Hence, the highest variation in total biomass Other zooplankton Calanoid copepods Oithona spp. 60 Experiment I 60 Experiment II mg C m -3 mg C m LT-I LT-II HT-I LTS-I LTS-II HTS-II Experiment III LT-I HT-I LTS-I HTS-I Experiment IV 0 Z0 SZ0 Z SZ Z2 SZ2 Z3 SZ S S2 S3 S4 Fig.. Contribution of calanoid copepods, Oithona spp. and other zooplankton (mg C m 3 ) in experiments I IV. The group other zooplankton consisted of >20 different taxa of merozooplankton (see text for further details) and is not included in further analyses. Each experiment consisted of different enclosures, as indicated by abbreviations. S indicates that silicate has been added. Experiments I and II: LT, low turbulence; HT, high turbulence. Roman numbers represent replicate number. Experiment III: Z0, Z, etc. indicate the concentration of calanoids added to the enclosures, where 0 is the lowest and 3 the highest concentration. Experiment IV: the numbers 4 indicate how frequent the nutrients were added to the enclosures. represents once, 2 twice, 3 three times and 4 continuous supply. 920

5 C. SVENSEN AND J. C. NEJSTGAARD FAECAL PELLET SEDIMENTATION DYNAMICS was found in experiment III where zooplankton >90 µm were first removed, after which late copepodites of C. finmarchicus were added in different concentrations to six of the eight enclosures. Calanus finmarchicus was the dominant species in experiments II and III, while the smaller Paracalanus spp. and Microcalanus spp. dominated in experiment I, and Pseudocalanus spp. together with other calanoids dominated the zooplankton biomass in experiment IV. In experiment I, the average biomass of the cyclopoid copepod Oithona was 25 and 39% in experiment IV (Table II; Figure ), and it outnumbered all other zooplankton (data not shown). Other zooplankton (>90 µm) made up 2 8% of the total biomass (Figure ), except in the filtered mesocosms with the lowest copepod additions in experiment II (Z0, SZ0, Z and SZ, where they made up 5, 56, 9 and 27% of the very low biomass left in the mesocosms, respectively). This group consisted of >20 different taxa and were mostly meroplankton (such as mollusc, annelid and echinoderm larvae) and rotifers that were neither expected to produce a substantial amount of faecal pellets in the size range analysed here, nor to be coprophagous. Most of these were assumed to be non-feeding, or to ingest only small sized prey at relatively low body mass specific rates (Hansen et al., 997; Rouse, 2000). Thus, this group was not included in the further analysis of the data. Sedimentation of FPC and POC related to cyclopoid biomass The relationship between faecal pellet carbon sedimentation (FPC sed ) and biomass of calanoid copepods and Oithona is shown in Figure 2. Statistically significant correlation was found between the biomass of calanoid copepods and FPC sed (r = 0.398, P < 0.05), but no statistical significance was found between FPC sed and biomass of Oithona (r = 0.365, P > 0.05). However, it should be noted that the statistically significant correlation between FPC sed and calanoid biomass was due to one single data-point in Figure 2, showing a very high flux of FPC. No correlation was found between biomass of calanoid copepods and Oithona (data not shown). In all four experiments faecal pellets with diameters of µm dominated the total FPC flux (data not shown). Small pellets <30 µm in diameter that could potentially have been produced by protists and cyclopoids (Martens, 978; Gowing and Silver, 985) made an insignificant contribution to the total FPC flux in all experiments. Most likely, C. finmarchicus was the producer of the µm size group as it contributed 85 0% of the total FPC flux in experiment III, where this species made up almost 0% of the copepod biomass (Figure ). This indicates that the calanoid copepods were the main producers of sinking faecal pellets, as assumed in the calculations of ingestion rates. Estimated ingestion and egestion rates Maximum calculated ingestion rates differed by more than two orders of magnitude, from 2 mg C m 2 day in experiment III to 328 mg C m 2 day in experiment IV (Table II). The difference between the experiments is naturally a function of the biomass of calanoid copepods (because they provide the basis for the calculations) and the average temperature in the experiments. The minimum ingestion rates provide a guideline of the absolute minimum grazing impact from calanoids, assuming no significant use of stored energy. Consequently, this rate will also indicate the minimum amount of faecal pellet-derived carbon in the sediment traps (that is unless remineralization or mechanical breakage has taken place). On the other hand, the maximum ingestion and egestion rates are estimates of the maximum expected contribution of FPC to the vertical flux. Thus, Table II: Range of (average concentrations within each experimental enclosure) calanoid copepod (NIII CVI, mg C m 3 ) and Oithona (CI VI) biomass and relative contribution of Oithona to total zooplankton (i.e. Oithona + calanoid copepods) biomass Exp. Calanoids Oithona sp. % Oithona POC ± SD Min. I Max. I Min. E Max. E (mg C m 3 ) (mg C m 3 ) (biomass) (mg C m 2 ) (mg C m 2 day ) I ± II ± III ± IV ± Suspended biomass of POC (mg m 2 day ) and calculated minimum and maximum ingestion (Min. I and Max. I) and egestion rates (Min. E assuming 80% assimilation efficiency and Max. E assuming 20% assimilation efficiency) in experiments I IV are given. All ingestion and egestion rates are in mg C m 2 day. 92

6 Fig. 2. Biomass of calanoid and cyclopoid (Oithona) copepods (mg C m 3 ) and vertical flux of POC and FPC (mg m 2 day ). Note different scales on the x-axes. the expected sedimentation rate of FPC would lie somewhere between minimum and maximum egestion rates. Faecal pellet carbon flux versus estimated egestion and zooplankton composition In experiments I III, the range of expected egestion rates was in good agreement with FPC sed (Figure 3). The rates of FPC sed were significantly higher than E min in experiments I, II and III (P = 0.002, n = 8, two-tailed paired t-test). Calculated E max in experiments II and III (dominated by Calanus) was not significantly different from FPC sed (P = 0.63, n = 2). In experiment I (dominated by smaller calanoids, but with a significant contribution of Oithona; see Table II) FPC sed was significantly lower than E max (P = 0.006, n = 6). Furthermore, in experiment IV, FPC sed was either significantly lower than E min in the nonsilicate mesocosms (Figure 3, mesocosms 4, P = 0.025, n = 4, two-tailed paired t-test), or merely approaching the E min (not significantly different, P = 0.44, n = 4) in the silicate fertilized mesocosms (S S4), respectively. Thus, the largest difference between predicted and measured FPC sedimentation was found in experiment IV with Oithona biomass almost as high as the biomass of calanoid copepods (39%). FPC sed increased towards the expected E max when the fraction of Oithona to total copepod biomass decreased (Figure 4A). On the other hand, when the contribution of Oithona was 39%, FPC sed was reduced to a few per cent of E max. The data were well described (r 2 = 0.68, P < 6 ) by a logarithmic regression between the fraction of Oithona, and the FPC sed /E max ratio (Figure 4A). A similar trend was found for the relation between FPC sed /E min and the biomass of Oithona (Figure 4B). In five of the enclosures in experiment IV with high biomass of Oithona, the vertical flux of FPC was even lower than expected from the minimum carbon requirements (i.e. FPC sed /E min < ), indicating unrealistically low sedimentation rates of copepod faecal pellets. DISCUSSION Comparing all 26 mesocosm enclosures, we found that when the relative biomass contribution of calanoids was close to 0% (i.e. Oithona biomass approaching zero), the measured FPC sedimentation was virtually identical to the estimated production of faecal pellets (FPC sed /E max ~; see Figure 4A). This is in good agreement with previous mesocosm experiments (Nejstgaard et al., 997, 200) where Calanus feeding at similarly high food concentrations showed FPC egestion rates slightly below 922

7 C. SVENSEN AND J. C. NEJSTGAARD FAECAL PELLET SEDIMENTATION DYNAMICS FPC sed E max E min Experiment I Experiment II Sedimented material (mg C m -2 d - ) 0. 0, LT-I LT-II HT-I LTS-I LTS-II HTS-II Experiment III 0. 0, LT-I HT-I LTS-I HTS-I Experiment IV 0. 0, Z-0 SZ-0 Z- SZ- Z-2 SZ-2 Z-3 SZ , S S2 S3 S4 Fig. 3. Daily sedimentation rates of faecal pellet carbon (FPC sed ) and calculated minimum (E min ) and maximum (E max ) egestion rates in experiments I IV. All rates are in mg C m 2 day. Note the logarithmic y-axes. See text for further details on calculations. For enclosure abbreviations, see legend to Figure. (~%) our estimated E max in experiments II and III. Furthermore, our estimated maximum ingestion rates are very similar to (~80 % of ) maximum values reported for C. finmarchicus in the North Atlantic during phytoplankton blooms at comparable temperatures (Gamble, 978; Ohman and Runge, 994). This also suggests that the calanoids were feeding and egesting pellets near estimated maximal rates during the present experiments. The good correspondence between our estimated rates of E max and rates obtained from field and laboratory experiments also confirms that the empirical regression by Hansen et al. (Hansen et al., 997) appears realistic. Also, the concentrations of carbon were relatively high in all enclosures (Table III), suggesting that the assumptions regarding respiration and egestion at foodsatiated rates were reasonable. When the biomass of Oithona was increasing, the rate of FPC sed /E max decreased. This may indicate that Oithona acted as a filter for sinking faecal pellets in these experiments. We therefore suggest that the biomass ratio between pellet-producing (calanoids) and pellet-reworking copepods (Oithona) may be used to predict relative pellet retention and/or sedimentation rates of calanoid faecal pellets in natural plankton. By extrapolating the regression in Figure 4A, a zooplankton biomass consisting of 50% Oithona implies that only ~% of the FPC produced will contribute to the carbon flux (i.e. a retention capacity of 99%). However, zooplankton other than Oithona may also ingest faecal pellets, especially when food is scarce (i.e. oligotrophic conditions). When such zooplankton are important contributors they should be included in the calculations. 923

8 FPC sed /E min FPC sed /E max 0. 0, 00. 0, A f(x) = 0.98 exp (-0.09 x) n = 26 r 2 = 0.68, p < -6 B f(x) = 2.83 exp (-0.08 x) n = 26 r 2 = 0.62, p < , Percentage Oithona biomass Fig. 4. (A) Relationship between the biomass percentage of Oithona (Oithona/[(Oithona + calanoids) 0]), and the ratio of faecal pellet carbon sedimentation (FPC sed )/estimated maximal (E max ) calanoid egestion rates. (B) Same as for (A), but shows the ratio of faecal pellet carbon sedimentation (FPC sed )/estimated minimum (E min ) calanoid egestion rates. Cross represents experiment I, square represents experiment II, circle represents experiment III and diamond represents experiment IV. One mesocosm (SZ-0 in experiment III) deviated significantly from the rest, showing an FPC sed /E max ratio of We believe this may be due to an underestimation of E max. The SZ-0 enclosure, which was pre-screened for zooplankton >90 µm, had the lowest biomass of calanoid copepods, only 0.86 mg C m 3. This very low biomass makes the E max estimate very sensitive to zooplankton sampling error and the underlying assumptions for the calculation of ingestion rates. We are aware that results obtained experimentally may not necessarily be directly comparable with the real world. As the sediment traps in these experiments were positioned at a depth of 8 m, and because the FPC flux generally decreases with depth (Riebesell et al., 995; González et al., 2000), the sedimentation rates presented here should be regarded as maximum rates. On the other hand, the short sedimentation distance would result in a similarly short exposure time for Oithona. It should also be mentioned that the mesocosm experiments were not specifically designed to test the effect of Oithona on sedimentation rates of faecal pellets. Consequently, alternative hypotheses must also be considered. For instance, mechanical break-up of faecal material may have occurred because of the elevated dissipation rates caused by the air-lift systems providing circulation in the upper part of the enclosures. However, this does not explain the observed differences in FPC sed between experiments I III and IV, as all mesocosms were subject to the same treatment. Also, since turbulence was generated in experiments I and II but not in III and IV, this should have been reflected in FPC sed if the water movements destroyed faecal material. Alternatively, the low rates of FPC sed in experiment IV could reflect differences in food availability for the calanoid copepods, hence directly affecting the production of faecal pellets. The average availability of phytoplankton carbon differed somewhat between the four experiments, but relative variations between NP and NPS treatments were larger than those between experiments (Table III). Although unfortunately the present experiments cannot provide direct evidence, we believe that the most plausible explanation of the low rates of FPC sed in experiment IV was coprophagy by Oithona. High retention rates of faecal pellets in the upper m of the ocean have been reported when cyclopoid copepods are abundant (González et al., 2000; Wexels Riser et al., 200). For instance, a retention capacity of 98% of produced faecal pellets was demonstrated in the upper 200 m in a study off the Iberian shelf, North West Spain (Wexels Riser et al., 200), co-occurring with high abundance of small copepods (Halvorsen et al., 200). Unfortunately, few studies have been addressing the specific role of Oithona in the coprophagous filter. Oithona appear especially well adapted for faecal pellet grazing. The clearance rate of Oithona, and hence its capacity to act as a coprophagous filter, may be highly variable as it seems to be related to the strength of the signal caused by the movements (sinking or swimming) of the prey particle (Kiørboe and Visser, 999). Both an idealized model and laboratory observations have suggested clearance rates between 5 and 00 ml day for Oithona similis grazing on faecal pellets produced by Acartia tonsa and C. finmarchicus (Kiørboe and Visser, 999). In mesocosm experiment IV the average concentration of Oithona (adult females and males) was ~3 5 individuals per enclosure (~ ind. l ). Thus, this species could have been able to clear m 3 day 924

9 C. SVENSEN AND J. C. NEJSTGAARD FAECAL PELLET SEDIMENTATION DYNAMICS Table III: Experiments I IV. Average biomass (mg C m 3 ) of total phytoplankton, diatoms, nondiatoms (mainly flagellates and dinoflagellates) and microzooplankton (mainly ciliates) in the NP (nitrate, phosphate treated) and NPS (nitrate, phosphate and silicate treated) enclosures, respectively Exp. Nutrients Total Diatoms Non-diatoms Microzooplankton phytoplankton (mg C m 3 ) (mg C m 3 ) (mg C m 3 ) (mg C m 3 ) I a NP NPS II NP NPS III NP NPS IV NP NPS a Nejstgaard et al. (200), and unpublished data. (depending on the signal strength created by the prey ), corresponding to times the enclosure volume above the sediment trap (25 m 3 ) daily. Cyclopoid copepods may also retard vertical flux of carbon in the water column through the utilization of detritus (aggregates and faecal material) and the production of small faecal pellets with low settling rates, which are mainly recycled near surface layers (González et al., 2000). Using average rates for whole experiments, ~800 mg m 2 more POC was present in experiment IV (Oithona dominated) than in experiment III (consisting of almost 0% C. finmarchicus) (Table II). Although no direct evidence is available, it is tempting to speculate that the relatively high concentrations of suspended POC in experiment IV could represent fragmented FPC. It should, however, be noted that some of the fragmented material could dissolve and enter the pool of dissolved organic carbon. CONCLUSIONS Data from the experiments, characterized by an extensive range of physical and biological processes, suggest that Oithona may regulate vertical flux of biogenic matter. The differences among the experiments include different levels of turbulence, nutrient availability, nutrient additions (varying from pulse-addition to constant supply) and different phytoplankton communities (flagellate- versus diatom-dominated systems). It therefore appears likely that the calanoid/cyclopoid ratio is of significance for determining the magnitude of the vertical flux of biogenic matter under a range of various conditions. This is in accordance with an increasing number of observations reported from different areas [e.g. (González and Smetacek, 994; González et al., 994; Taguchi and Saino, 998; Wassmann et al., 2000)], suggesting that the negative relationship between particulate carbon export and the presence of Oithona may be common. ACKNOWLEDGEMENTS We acknowledge O. Sergeeva for counting and measuring faecal pellets, S. Øygarden for POC analyses, and our co-workers at the Norwegian program Nutrients and Pelagic Production (NAPP) for making these experiments possible. The constructive comments by P. Wassmann, X. Irigoien, M. Reigstad and C. Wexels Riser improved this manuscript. We are also indebted to X. Irigoien for help with the calculation of ingestion rates. Financial support was provided from a Norwegian Research Council (NFR) grant to J. K. Egge and P. Wassmann. REFERENCES Atkinson, A. (996) Subarctic copepods in an oceanic, low chlorophyll environment: cilicate predation, food selectivity and impact on prey populations. Mar. Ecol. Prog. Ser., 30, Dagg, M. (993) Sinking particles as a possible source of nutrition for the large calanoid copepod Neocalanus cristatus in the subarctic Pacific Ocean. Deep-Sea Res., 40, Gamble, J. (978) Copepod grazing during a declining spring phytoplankton bloom in the North Sea. Mar. Biol., 49, González, H. E. and Smetacek, V. (994) The possible role of the cyclopoid copepod Oithona in retarding vertical flux of zooplankton faecal material. Mar. Ecol. Prog. Ser., 3, González, H. E., Gonzales, S. R. and Brummer, G.-J. A. (994) 925

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