Phytoplankton blooms are strongly impacted by microzooplankton grazing in coastal North Pacific waters

Phytoplankton growth and microzooplankton grazing were measured in two productive coastal regions of the North Pacific: northern Puget Sound and the coastal Gulf of Alaska. Rates of phytoplankton growth (range: 0.09–2.69 day⁻¹) and microzooplankton grazing (range: 0.00–2.10 day⁻¹) varied seasonally, with lowest values in late fall and winter, and highest values in spring and summer. Chlorophyll concentrations also varied widely (0.19–13.65 μg l⁻¹). Large (>8 μm) phytoplankton cells consistently dominated phytoplankton communities under bloom conditions, contributing on average 65% of total chlorophyll biomass when chlorophyll exceeded 2 μg l⁻¹. Microzooplankton grazing was an important loss process affecting phytoplankton, with grazing rates equivalent to nearly two-thirds (64%) of growth rates on average. Both small and large phytoplankton cells were consumed, with the ratio of grazing to growth (g:μ) for the two size classes averaging 0.80 and 0.42, respectively. Perhaps surprisingly, the coupling between microzooplankton grazing and phytoplankton growth was tighter during phytoplankton blooms than during low biomass periods, with g:μ averaging 0.78 during blooms and 0.49 at other times. This tight coupling may be a result of the high potential growth and ingestion rates of protist grazers, some of which feed on bloom-forming diatoms and other large phytoplankton. Large ciliates and Gyrodinium-like dinoflagellates contributed substantially to microzooplankton biomass at diatom bloom stations in the Gulf of Alaska, and microzooplankton biomass overall was strongly correlated with >8 μm chlorophyll concentrations. Because grazing tended to be proportionally greater when phytoplankton biomass was high, the absolute amount of chlorophyll consumed by microzooplankton was often substantial. In nearly two-thirds of the experiments (14/23), more chlorophyll was ingested by microzooplankton than was available for all other biological and physical loss processes combined. Microzooplankton were important intermediaries in the transfer of primary production to higher trophic levels in these coastal marine food webs. Received: 12 November 1999 / Accepted: 4 October 2000     

Production of DMSP and DMS during a mesocosm study of an Emiliania huxleyi bloom: influence of bacteria and Calanus finmarchicus grazing

We investigated the influence of bacteria and metazooplankton on the production of dimethylsulfoniopropionate (DMSP) and dimethylsulfide (DMS) during blooms of Emiliania huxleyi (Lohmann) Hay and Mohler in seawater mesocosms. The phytoplankton succession was marked by the rapid collapse of an initial Skeletonema costatum (Greville) Cleve bloom followed by a small E. huxleyi bloom. The collapse of the diatom bloom was accompanied by an increase in concentrations of dissolved DMSP (DMSP_d) and bacterial abundance and activity (as determined by the thymidine incorporation technique). The increase in bacterial activity was followed by a rapid decrease in DMSP_d concentrations which remained low for the rest of the experiment, even during the subsequent collapse of the E. huxleyi blooms. The absence of DMSP_d and DMS peaks during the declining phase of the E. huxleyi blooms was attributed to the high bacterial activity prevailing at that time. The influence of metazooplankton grazing on DMSP and DMS production was investigated by adding moderate (24 mg dry weight m^-3) and high (520 mg dry weight m^-3) concentrations of Copepodite Stage V and adults of Calanus finmarchicus to two of four filtered (200 m mesh net) enclosures during the E. huxleyi blooms. The addition of C. finmarchicus, even in high concentrations, had no apparent effect on the dynamics of E. huxleyi, suggesting that the copepods were not grazing significantly on nanophytoplankton. The addition of copepods in high concentrations favored an accumulation of chlorophyll a and particulate DMSP. These results suggest that copepods were preying on the herbivorous microzooplankton which, in turn, was controlling the biomass of nanophytoplankton. DMS production was also enhanced in the enclosure with maximum metazooplankton biomass, suggesting that the grazing of C. finmarchicus on microzooplankton containing DMSP may contribute to DMS production. These results provide strong support to the emerging idea that bacteria and metazooplankton grazing play a dominant role in determining the timing and magnitude of DMS pulses following phytoplankton blooms.     

Warming induces shifts in microzooplankton phenology and reduces time-lags between phytoplankton and protozoan production

Indoor mesocosm experiments were conducted to test for potential climate change effects on the spring succession of Baltic Sea plankton. Two different temperature (Δ0?°C and Δ6?°C) and three light scenarios (62, 57 and 49?% of the natural surface light intensity on sunny days), mimicking increasing cloudiness as predicted for warmer winters in the Baltic Sea region, were simulated. By combining experimental and modeling approaches, we were able to test for a potential dietary mismatch between phytoplankton and zooplankton. Two general predator–prey models, one representing the community as a tri-trophic food chain and one as a 5-guild food web were applied to test for the consequences of different temperature sensitivities of heterotrophic components of the plankton. During the experiments, we observed reduced time-lags between the peaks of phytoplankton and protozoan biomass in response to warming. Microzooplankton peak biomass was reached by 2.5 day °C^?1 earlier and occurred almost synchronously with biomass peaks of phytoplankton in the warm mesocosms (Δ6?°C). The peak magnitudes of microzooplankton biomass remained unaffected by temperature, and growth rates of microzooplankton were higher at Δ6?°C (μ_?0?°C?=?0.12 day^?1 and μ_?6?°C?=?0.25 day^?1). Furthermore, warming induced a shift in microzooplankton phenology leading to a faster species turnover and a shorter window of microzooplankton occurrence. Moderate differences in the light levels had no significant effect on the time-lags between autotrophic and heterotrophic biomass and on the timing, biomass maxima and growth rate of microzooplankton biomass. Both models predicted reduced time-lags between the biomass peaks of phytoplankton and its predators (both microzooplankton and copepods) with warming. The reduction of time-lags increased with increasing Q₁₀ values of copepods and protozoans in the tritrophic food chain. Indirect trophic effects modified this pattern in the 5-guild food web. Our study shows that instead of a mismatch, warming might lead to a stronger match between protist grazers and their prey altering in turn the transfer of matter and energy toward higher trophic levels.     

Microzooplankton herbivory on the Grand Bank (Newfoundland,Canada): A seasonal study

Grazing impact of microzooplankton on phytoplankton was investigated on the Grand Bank, Newfoundland, Canada, in April, July and October 1984, using a seawater dilution method. In April a large proportion of chlorophylla was in the microplankton size fraction (> 20µm) while in mid-summer and fall most was in the nanoplankton size fraction (< 20µm). Diatoms were the dominant phytoplankters in April, while undetermined flagellates and coccolithophores were abundant in other seasons. Major grazers were oligotrichous ciliates in all seasons. Instantaneous grazing rates on nanophytoplankton, as measured by changes in chlorophylla, varied from 0.12 to 0.43 d^–1 and those on microphytoplankton from 0.19 to 0.68 d^–1. Grazing rates did not change over 24 and 48 h intervals. This level of grazing corresponded to a daily loss of about 20 and 30% of standing stock of chlorophylla and about 50 and 70% loss of potential production in the two size fractions respectively. Taxon-specific grazing rates, calculated from microscopic enumeration, showed that small diatoms were grazed heavily, and their growth was controlled by grazing in late spring. In late summer and fall, undetermined flagellates and coccolithophores were also grazed at high rates but their growth rates were higher than the grazing rates, and therefore, were not controlled by microzooplankton. In general, microzooplankton grazed on whatever appropriate sized food was dominant in the experimental water. Their potential ability to control the growth of certain food species may be one of the causes determining the species composition of phytoplankton communities.     

Trophic implications of cross-shelf copepod distributions in the Southeastern Bering Sea

Spring distributions of some numerically dominant copepods reflect associations with two distinct water masses separated along the 80- to 100-m isobaths. Seaward of this middle shelf front, the oceanic Bering Sea hosts populations of Calanus cristatus, C. plumchrus, and Eucalanus bungii bungii; Metridia pacifica, Oithona similis, and Pseudocalanus spp. are also present. The large oceanic species are much less abundant in waters shallower than 80 m where the community is seasonally dominated by smaller copepods, O. similis, Acartia longiremis, and Pseudocalanus spp. Experimental and field-derived estimates of carbon ingestion indicate that the oceanic/outer shelf copepods can occasionally graze the equivalent of the daily plant production and probably routinely remove 20–30% of the primary productivity. Conversely, stocks of middle shelf copepods rarely ingest more than 5% of the plant carbon productivity. During 45 d between mid April to late May, 1979, approximately three times more organic matter was ingested m^-2 by the outer shelf/oceanic copepod community than by middle shelf species. This imbalance in cross-shelf grazing permits middle shelf phytoplankton stocks to grow rapidly to bloom proportions, and to sink ungrazed to the seabed. Over the outer shelf and particularly along the shelf break, a much closer coupling to phytoplankton supports a large biomass of oceanic grazers. Here, copepod stocks approaching 45 g dry wt m^-2 occur in late spring as a narrow band at the shelf break.Supported by National Science Foundation Grant DPP 76-23340Contribution no. 485, Institute of Marine Science, University of Alaska, Fairbanks     

Phytoplankton growth and microzooplankton grazing rates in a restricted Mediterranean lagoon (Bizerte Lagoon,Tunisia)

Phytoplankton growth and microzooplankton grazing were investigated in the restricted Bizerte Lagoon in 2002 and 2004. The 2002 study, carried out at one station from January to October, showed significant seasonal variations in phytoplankton dynamics. High growth rates (0.9–1.04 day⁻¹), chlorophyll a (Chl a) concentrations (6.6–6.8 μg l⁻¹) and carbon biomass (392–398 μg C l⁻¹) were recorded in summer (July), when several chain-forming diatoms had intensively proliferated and dominated the carbon biomass (74%). In 2004, four stations were studied during July, a period also characterized by the high proliferation of several diatoms that made up 70% of the algal carbon biomass. In 2004, growth rates (0.34–0.45 day⁻¹) and biomass of algae (2.9–5.4 μg Chl a l⁻¹ and 209–260 μg C l⁻¹) were low, which may be related to the lower nutrient concentrations recorded in 2004. Microzooplankton >5 μm were mainly composed of heterotrophic dinoflagellates and ciliates. Microzooplankton biomass peaked during summer (2002 320–329, 2004 246–361 μg C l⁻¹), in response to the enhanced phytoplankton biomass and production. The grazer biomass was dominated by ciliates (71–76%) in July 2002 and by heterotrophic dinoflagellates (52–67%) in July 2004. Throughout the year and at different stations, microzooplankton grazed actively on phytoplankton, removing 26–58% of the Chl a and 57-84% of the primary production. In 2002, the highest grazing impact was observed on the large algae (>10 μm) during the period of diatom dominance. These results have a significant implication for carbon export to depth. Indeed, the recycling of most of the diatom production by the microbial food web in the upper water column would reduce the flux of material to the seafloor. This should be considered when modeling the carbon cycling in coastal environments and under conditions of diatom dominance. During both studies, ciliates had higher growth rates (0.5–1.5 day⁻¹) and a higher carbon demand (165–470 μg C l⁻¹ day⁻¹) than dinoflagellates (0.1–0.5 day⁻¹, 33–290 μg C l⁻¹ day⁻¹). Moreover, when grazer biomass was dominated by ciliates (in July 2002), herbivory accounted for 71–80% of the C ingested by microzooplankton while it accounted only for 14–23% when dinoflagellates dominated the grazer biomass (in July 2004). These results suggest that, in contrast to findings from open coastal waters, ciliate species of the restricted Bizerte Lagoon were more vigorous grazers of the large algae (diatoms) than were dinoflagellates.     

Contribution of salps to carbon flux of marginal ice zone of the Lazarev Sea, southern ocean

In order to estimate the in situ grazing rates of Salpa thompsoni and their implications for the development of phytoplankton blooms and for the sequestration of biogenic carbon in the high Antarctic, a repeat-grid survey and drogue study were carried out in the Lazarev Sea during austral summer of 1994/1995 (December/January). Exceptionally high grazing rates were measured for S. thompsoni at the onset of a phytoplankton bloom (0.2 to 0.8 μg chlorophyll a l⁻¹) in December 1994, with up to ≃160 μg of plant pigments consumed by an individual salp of 7 to 10 cm length per day. Dense salp swarms extended throughout the marginal ice zone, consuming up to 108% of daily phytoplankton production and 21% of the total chlorophyll a stock. Due to the much faster sinking rates and higher carbon content of salp faecal pellets, the efficiency of downward carbon flux through salps is much higher than through the other major grazers, krill and copepods. S. thompsoni can thus export large amounts of biogenic carbon from the euphotic zone to the deep ocean. With the observed ingestion rates during December 1994, this flux could have attained levels of up to 88 mg C m⁻² d⁻¹, accounting for the bulk of the vertical transport of carbon in the Lazarev Sea. However, in January 1995, when phytoplankton concentrations exceeded a threshold level of 1.0 to 1.5 μg chlorophyll a l⁻¹, salps experienced a drastic reduction in their feeding efficiency, possibly as a result of clogging of their filtering apparatus. This triggered a dramatic reversal in the relationship, during which a dense phytoplankton bloom developed in conjunction with the collapse of the salp population. Increases in the biomass and geographic range of the tunicate S. thompsoni have occurred in several areas of the southern ocean, often in parallel with a rise in sea-surface temperature during sub-decadal periods of warming anomalies. Received: 10 August 1997 / Accepted: 21 October 1997     

Trophodynamic function of copepods,appendicularians and protozooplankton in the late summer zooplankton community in the Skagerrak

The study was carried out in the Skagerrak during late summer when population development in the pelagic cycle culminated in the yearly maximum in zooplankton biomass. The cyclonic circulation of surface water masses created the characteristic dome-shaped pycnocline across the Skagerrak. The large dinoflagellate Ceratium furca dominated the phytoplankton biomass. Ciliates and heterotrophic dinoflagellates were the major grazers and, potentially, consumed 43–166% of daily primary production. The grazing impact of copepods was estimated from specific egg production rates and grazing experiments. The degree of herbivory differed between species (14–85%), but coprophagy (e.g. feeding on fecal pellets) and ingestion of microzooplankton were also important. The appendicularian Oikopleura dioica was present in lower numbers than copepods, but cleared a large volume of water. The grazing impact of copepods and O. dioica was estimated to 57±24% and 12±12% of daily primary production, respectively. Sedimentation of organic material (30 m) varied between 169 and 708 mg C m^–2 day^–1, and the contribution from the mesozooplankton (copepod fecal pellets and mucus houses with attached phytodetritus of O. dioica) was 5–33% of this sedimentation. Recycling of fecal pellets and mucus houses in the euphotic zone was 59% and 36%, respectively. However, there was a high respiration of organic material by microorganisms in the mid-water column, and 34% of the sedimenting material actually reached the benthic community in the deep, central part of the Skagerrak.     

The impact of grazing by microzooplankton in northern Hiroshima Bay,the Seto Inland Seam,Japan

The abundance of microzooplankton and their grazing impact on phytoplankton were studied using the dilution technique from May 1990 to November 1991 in northern Hiroshima Bay, a typical eutrophic area in the Seto Inland Sea. Microzooplankton, dominated in number by tintinnid ciliates, were abundant from June to September when chlorophyll-a concentrations were high. Maximum density of microzooplankton ranged from 3.8×10³ to 25.4×10³ ind l^-1. During the period of investigation, mean microzooplankton density and mean chlorophyll-a concentration of the <20-m fraction increased toward the inner region of the bay. The microzooplankton grazing on phytoplankton increased from summer to early autumn, and decreased from late autumn to winter. At an offshore station, the annual means of the daily grazing loss for total chlorophyll-a and the chlorophyll-a of the <20-m fraction were 12 and 15% of the initial standing stock, respectively. At an estuarine station, the microzooplankton grazed 19 and 29% of the total and <20-m initial standing stock, respectively. The quantity of grazed chlorophyll-a correlated positively and linearly with the potential production of chlorophyll-a at both stations. The quantity of chlorophyll-a grazed by microzooplankton and the potential production of chlorophyll-a were nearly equivalent in the <20-m fraction at the estuarine station. This suggests that the microzooplankton assemblage was able to consume almost all the nanoplankton newly produced in the eutrophic estuary.     

Trophic role of small cyclopoid copepod nauplii in the microbial food web: a case study in the coastal upwelling system off central Chile

Copepod grazing impact on planktonic communities has commonly been underestimated due to the lack of information on naupliar feeding behaviour and ingestion rates. That is particularly true for small cyclopoid copepods, whose nauplii are mainly in the microzooplankton size range (<200 μm). The trophic role of Oithona spp. nauplii was investigated off Concepción (central Chile, ~36°S) during the highly productive upwelling season, when maximum abundances of these nauplii were expected. Diet composition, ingestion rates, and food-type preferences were assessed through grazing experiments with different size fractions of natural planktonic assemblages (<3, <20, <100, and <125 μm) and cultures of the nanoflagellate Isochrysis galbana. When the Oithona spp. nauplii were offered a wide range of size fractions as food (pico- to microplankton), they mostly ingested small (2–5 μm) nanoflagellates (5–63 × 10³ cells nauplius⁻¹ day⁻¹). No ingestion on microplankton was detected, and picoplankton was mainly ingested when it was the only food available. Daily carbon (C) uptake by the nauplii ranged between 28 and 775 ng C nauplius⁻¹, representing an overall mean of 378% of their body C. Our relatively high ingestion rate estimates can be explained by methodological constraints in previous studies on naupliar feeding, including those dealing with “over-crowding” and “edge” effects. Overall, the grazing impact of the Oithona spp. nauplii on the prey C standing stocks amounts up to 21% (average = 13%) for picoplankton and 54% (average = 28%) for nanoplankton. These estimates imply that the nauplii of the most dominant cyclopoid copepods exert a significant control on the abundances of nanoplankton assemblages and, thereby, represent an important trophic link between the classical and microbial food webs in this coastal upwelling system.     

Differences in photosynthetic pigment signatures between phytoneuston and phytoplankton communities in a coastal lagoon of Baja California

In order to understand the relationships between the dynamics of phytoplankton populations in the surface microlayer (MIL) and in the water column below (SSW), this study used high-performance liquid chromatography-derived pigment markers in samples from a coastal lagoon of Baja California (Estero de Punta Banda, EPB) under summer (October 2003) and winter (December 2003) conditions. Photosynthetic pigment signatures of phytoplankton at the air–sea interface (phytoneuston) and subsurface measurements were related to bottom-up (temperature, salinity, nutrient concentrations) and top-down factors (zooplankton abundance). Slicks and scum layers were observed in the inner part of the lagoon and coincided with greater stratification of layers just below the sea surface and lower wind intensities. In general, spatial variability in pigment markers and ancillary data was very high and resulted in non-significant differences between MIL and subsurface samples when different regions of EPB or sampling dates were compared. However, different patterns were found between pigments and environmental factors of MIL and SSW samples when the relative numbers of stations with positive and negative differences (ΔX = X _MIL−X _SSW) were computed. For each survey, pigment markers of phytoneuston and phytoplankton samples were not necessarily correlated. Further analysis revealed that those markers (19′-butanoyloxyfucoxanthin, prasinoxanthin, divinil-chlorophyll a) corresponded to picophytoplankton groups (haptophyte, prasinophyte, and prochlorophyte). On both dates, the MIL was enriched in 19′-hexanoyloxyfucoxanthin (a marker for a type 4 haptophyte) and fucoxanthin (marker for bacillariophytes, haptophytes, and crysophytes) and depleted in peridinin (marker for dinophytes). Different zooplankton grazers accumulated in the MIL (loricate tintinnids) and in SSW (copepod nauplii).     

Diel feeding behavior of neritic copepods during spring and fall blooms in Akkeshi Bay,eastern coast of Hokkaido,Japan

In situ diel feeding behavior of neritic copepods was investigated using the gut fluorescence method, during spring and fall bloom periods in Akkeshi Bay, on the eastern coast of Hokkaido, Japan. Acartia omorii and Paracalanus sp. were the dominant species during the fall, and Pseudocalanus spp. and A. longiremis during the spring. During both bloom periods, diel rhythms were always observed for the gut pigment contents of these dominant copepods, although there were interspecific differences in the pattern. The maximum gut pigment content was always observed during the night and the minimum during the day. For all species, except Paracalanus sp., the average gut pigment content during the night was significantly higher (p<0.05) than during daytime by factors of between 1.5 and 2.7. There were no significant differences between the gut evacuation rate constants determined during the day and the night, and initial gut pigment content had no effect on the value of gut evacuation rate constants. The instantaneous ingestion rates of individual copepods calculated from gut pigment and the mean value of gut evacuation rate constants followed the same diel rhythms as gut pigment contents. Copepod daily ingestion rates were higher than the daily requirements for respiration during both bloom periods. Estimated daily ration was 40 to 91% of body carbon during the fall bloom, and 17 to 28% during the spring bloom. The higher daily rations during fall were probably due to the difference in in situ temperature (ca. 14°C).     

In situ grazing rate of the copepod population in the western subarctic North Pacific during spring

Time series sampling with a multi-layer plankton sampler was carried out in the western subarctic North Pacific during spring 1991. Neocalanus cristatus, N. flemingeri and Eucalanus bungii dominated and accounted for 88.5% of the copepod population in volume. Neocalanus spp. were distributed in the upper mixed layer, while E. bungii was mainly distributed between 120 and 300 m throughout the day and night. In contrast, Metridia pacifica, Pleuromamma scutullata and Gaetanus simplex showed clear diel vertical migration. Grazing activities were estimated simultaneously by gut fluorescence. Nocturnal grazing was observed for diel migrating species. Neocalanus spp. did not have a diel feeding rhythm and had relatively low gut fluorescence. E. bungii was considered to be dormant during the observation period. The estimated grazing rate of the copepod population on phytoplankton was 1.4 to 2.0% of the primary production while the metabolic requirement was 8.3 to 12.4% of the primary production. These facts suggest that the copepod population was unimportant as primary consumers and that microzooplankton plays a much more important role in sustaining low standing stock of phytoplankton and a high nutrient concentration in the western subarctic Pacific Ocean.     

Feeding and predation impact of two chaetognath species, Eukrohnia hamata and Sagitta gazellae, in the vicinity of Marion Island (southern ocean)

The predation impact of the two chaetognaths Eukrohnia hamata and Sagitta gazellae on mesozooplankton standing stock were investigated in three depth layers during two 24 h stations occupied in the vicinity of Marion Island in late austral summer (April/May) 1986. The zooplankton community at both stations was dominated by small copepods (Oithona spp., Microcalanus spp.), which accounted for >95% of total zooplankton abundance. Chaetognaths comprised <2% of total zooplankton abundance. E. hamata constituted >95% of the total chaetognath stock. The general trend in both species was decreasing abundance with increasing depth, which appeared to be correlated to the distribution of copepods (r ² = 0.45; P <0.05). Gut-content analysis showed that copepods (mainly Oithona spp., Calanus spp. and Rhincalanus gigas) and ostracods were the main prey of both species, accounting for 87 and 61% of the total number of prey in E. hamata and S.␣gazellae stomachs, respectively. In the guts of S.␣gazellae, pteropods (Limacina spp.) and chaetognaths were also well represented. The mean number of prey items (NPC) for E. hamata ranged from 0.02 to 0.06 prey individual⁻¹ which corresponds to an individual feeding rate (Fr) of between 0.05 and 0.12 prey d⁻¹. For S.␣gazellae, the NPC values were higher, varying between 0.04␣and 0.20 prey individual⁻¹, or between 0.15 and 0.76 prey d⁻¹. The daily predation impact of the two chaetognaths was estimated at between 0.3 and 1.2% of the copepod standing stock or between 7 and 16% of the daily copepod production. Predation by S. gazellae on chaetognaths accounted for up to 1.6% of the chaetognath standing stock per day. Received: 26 November 1996 / Accepted: 31 October 1997     

Experimental evidence for internal predation in microzooplankton communities

The fate of microzooplankton production, whether it is channeled to mesozooplankton or recycled within the microbial food web, has major implications for the oceanic carbon cycle. The aim of this study was to estimate internal predation within naturally occurring microzooplankton communities. A dilution series based on the Landry and Hasset technique was created by mixing 200-μm-screened water (used as whole water) with 5-μm-screened seawater due to the dominance of pico- and small nanoplankton at our study site. This modification of the original technique allows for gradual reduction in microzooplankton abundance and thus internal predation while maintaining sufficient phytoplankton prey levels for microzooplankton growth in diluted treatments. Microzooplankton growth and mortality rates were calculated based on the changes in abundance during 24-h incubation. In the diluted treatments, microzooplankton growth rates were significantly higher (1.21 ± 0.20 day^?1 for ciliates and 0.88 ± 0.05 day^?1 for heterotrophic dinoflagellates) compared to those in whole seawater where microzooplankton abundance remained unchanged or even declined over time. Approximately 79 % of microzooplankton production was consumed within the microzooplankton, with aloricate ciliates being the most vulnerable to predation. These findings support the assumption that trophic interactions between microzooplankton can be an important factor controlling their production and, thus, energy transfer in picoplankton-dominated pelagic ecosystems.     

Microzooplankton grazing and selectivity of phytoplankton in coastal waters

Microzooplankton grazing activity in the Celtic Sea and Carmarthen Bay in summer 1983 and autumn 1984 was investigated by applying a dilution technique to high-performance liquid chromatographic (HPLC) analysis of photosynthetic pigments in phytoplankton present within natural microplankton communities. Specific grazing rates on phytoplankton, as measured by the utilisation of chlorophyll a, were high and varied seasonally. In surface waters during the autumn, grazing varied between 0.4 d^-1 in the bay and 1.0 d^-1 in the Celtic Sea, indicating that 30 and 65% of the algal standing stocks, respectively, were grazed daily. Grazing rates by microzooplankton within the thermocline in summer suggest that 13 to 42% of the crop was grazed each day. Microzooplankton showed selection for algae containing chlorophyll b, in spite of a predominance of chlorophyll c within the phytoplankton community. Changes in taxon-specific carotenoids indicated strong selection for peridinin, lutein and alloxanthin and selection against fucoxanthin and diadinoxanthin. This indicates a trophic preference by microzooplankton for dinoflagellates, cryptophytes, chlorophytes and prasinophytes and selection against diatoms, even when the latter group forms the largest crop within the phytoplankton. Interestingly, those algal taxa preferentially grazed also showed the highest specific growth-rates, suggesting a dynamic feed-back between microzooplankton and phytoplankton. Conversion of grazing rates on each pigment into chlorophyll a equivalents suggests firstly, that in only one experiment could all the grazed chlorophyll a be accounted for by the attrition of other chlorophylls and carotenoids, and secondly that in spite of negative selection, a greater mass of diatoms could be grazed by microzooplankton than any other algal taxon. The former may be due either to a fundamental difference in the break-down rates of chlorophyll a compared to other pigments, or to cyanobacteria forming a significant food source for microzooplankton. In either case, chlorophyll a is considered to be a good measure of grazing activity by microzooplankton.     

Patterns of microzooplankton growth in dilution experiments across a trophic gradient: Implications for herbivory studies

To investigate the growth and grazing patterns of microzooplankton (MZP) in environments of differing productivity, dilution experiments measuring phytoplankton growth (μ) and grazing mortality (m) rates were performed using samples from contrasting locations along the Texas coast. Samples were collected from estuaries, coastal lagoons and offshore Gulf of Mexico locations in the spring and summer of 2001. MZP growth rates were determined in each dilution treatment. Although MZP biomass changed over time in most dilution treatments, adjusting μ and m for the actual grazer gradient (represented by geometric mean MZP biomass) did not cause a significant deviation from the nominal dilution gradient. Likewise, these adjustments did not yield significant regressions where none existed before adjustment. The dynamics of MZP taxonomic groups (ciliates, dinoflagellates) and size categories differed suggesting that in some cases internal predation may lead to trophic cascades. MZP biomass was higher in productive coastal waters and included a larger proportion of dinoflagellates than in the oligotrophic, ciliate-dominated waters of the Gulf of Mexico. The MZP biomass-to-chlorophyll a ratio was lowest in the hypereutrophic Nueces River, where MZP biomass significantly increased in all dilution treatments (net growth rates up to 2 day⁻¹) suggesting a strong top–down control. In the brown-tide dominated Upper Laguna Madre and the oligotrophic seagrass-dominated Lower Laguna Madre MZP growth was decoupled from that of phytoplankton. At these sites, MZP were likely fueled by bacterial carbon and mixotrophy, respectively. Observing the growth response of MZP in dilution experiments can provide insight into trophic structure and efficiency of the microbial food web.     

A paradox of the ciliates? High ciliate diversity in a resource-poor environment

Ecological theory predicts that low productivity systems should have low biodiversity. However, despite the oligotrophic status of the Gulf of Aqaba (Northern Red Sea) ciliate species richness was unexpectedly high. In addition, phytoplankton, as main ciliate prey, was made up by only few genera, indicating a significant niche overlap among the grazers. Up to 97% of the ciliates were from the same taxonomic group and of the same size range, implying very similar food niches. Ciliate diversity was highest at times of lowest chlorophyll concentrations, during the period of stable abiotic conditions, but relatively high genetic diversity within the ciliate prey, notably among the cyanobacteria Synechococcus and Prochlorococcus. In the absence of disturbance and with little predation pressure, the alternate explanations for the observed ciliate diversity are either very fine niche partitioning by the ciliates, or their competitive equivalence resulting in a random assortment of species immigrating from a larger metacommunity, in accordance with Hubbell’s, (The unified neutral theory of biodiversity and biogeography. Princeton University Press, Princeton, 2001) neutral model. While the use of species abundance distributions (SAD’s) is far from definitive, the theoretical SAD’s that best fit the Gulf of Aqaba ciliate data was most often not that expected by neutral theory.     

Species-specific grazing rates of heterotrophic dinoflagellates in oceanic waters,measured with a dual-label radioisotope technique

A dual-isotope method was developed to measure grazing rates and food preferences of individual species of heterotrophic dinoflagellates from natural populations, collected from the Slope, Gulf Stream, and Sargasso Sea and from a transect from Iceland to New England, in 1983. The isotope method measures the grazing rates of microzooplankton which cannot be separated in natural populations on the basis of size. Tritiated-thymidine and ¹⁴C-bicarbonate were used to label natural heterotrophic and autotrophic food, respectively. Nine oceanic dinoflagellate species in the genera Protoperidinium, Podolampas, and Diplopsalis fed on both heterotrophic and autotrophic food particles with clearance rates of 0.4 to 8.0 l cell^-1 h^-1, based on ³H incorporation, and 0.0 to 28.3 l cell^-1 h^-1, based on ¹⁴C incorporation. Two dinoflagellate species, Protoperidinium ovatum and Podolampas palmipes, fed only on ³H-labelled food particles. Several species of dinoflagellates fed on bacteria (<1 m) which had been prelabelled with ³H-thymidine. The clearance rates of heterotrophic dinoflagellates and ciliates were similar and within the range of tintinnid ciliate clearance rates reported in the literature. As heterotrophic dinoflagellates and ciliates can have comparable abundances in oceanic waters, we conclude that heterotrophic dinoflagellates may have an equally important impact as microheterotrophic grazers of phytoplankton and bacteria in oceanic waters.Partially supported by a grant from the National Science Foundation, OCE-81-17744     

Identification of calanoid copepod prey species via molecular detection of carbon fixation genes

Zooplankton and their phytoplankton prey form the basis of the marine food web, yet historically it has been difficult to discern species-specific trophic interactions. Molecular techniques provide opportunities to obtain taxonomic data where the traditional methodologies for gut content analysis lack resolution. The large subunit gene of RubisC/O, rbcL, was utilized as a molecular marker for the identification of prey species in calanoid copepods. Clone libraries were generated from DNA extracted from seawater and whole copepods during a transect cruise on the northern Gulf of Mexico shelf. Sequence data analysis provided evidence of diatoms, nanoplankton-sized chlorophytes, and cyanobacteria in DNA extracted from whole copepods. These data demonstrate that rbcL can be a useful marker for the identification of copepod phytoplankton prey. Combining the described approach with quantitative techniques such as quantitative PCR will provide opportunities for the assessment of species-specific predator–prey interactions.