Protozooplankton Community Research Articles

First phytoplankton community assessment of the Kong Håkon VII Hav, Southern Ocean, during austral autumn

Abstract. We studied phytoplankton and protozooplankton community composition based on light microscopy, flow cytometry, and photosynthetic pigment data in the Atlantic sector of the Southern Ocean during March 2019 (early austral autumn). Sampling was focused on the area east of the prime meridian in the Kong Håkon VII Hav, including Astrid Ridge, Maud Rise, and a south–north transect at 6∘ E. Phytoplankton community composition throughout the studied area was characterized by oceanic diatoms typical of the iron-depleted high-nutrient, low-chlorophyll (HNLC) Southern Ocean. Topography and wind-driven iron supply likely sustained blooms dominated by the centric diatom Chaetoceros dichaeta at Maud Rise and at a station north of the 6∘ E transect. For the remainder of the 6∘ E transect, diatom composition was similar to the previously mentioned bloom stations, but flagellates dominated in abundance, suggesting a post-bloom situation and likely top-down control by krill on the bloom-forming diatoms. Among flagellates, species with haptophyte-type pigments were the dominating group. At Astrid Ridge, overall abundances were lower and pennate diatoms were more numerous than centric diatoms, but the community composition was nevertheless typical of HNLC areas. The observations described here show that C. dichaeta can form blooms beyond the background biomass level and also fuels both carbon export and upper trophic levels within HNLC areas. This study is the first thorough assessment of phytoplankton communities in this region and can be compared to other seasons in future studies.

Novel high throughput sequencing - fluorometric approach demonstrates Microcystis blooms across western Lake Erie are promoted by grazing resistance and nutrient enhanced growth

Cyanobacterial harmful algal blooms (CHABs) are a global public health threat. While CHABs are often promoted by nutrients, an important and often overlooked influence on bloom dynamics is zooplankton grazing. In the present study, zooplankton grazing and nutrient enrichment experiments were combined with next generation sequencing and fluorometric analyses to quantify differential grazing and nutrient effects on specific cyanobacterial genera across the western basin of Lake Erie. Grazing by two different sized daphnids, Daphnia magna and Daphnia pulex, was compared to protozooplankton grazing effects assessed via a dilution approach at sites within the Maumee and Sandusky Bays where Planktothrix, Microcystis, Synechococcus, and Dolichospermum were the dominant genera. Daphnid grazing significantly reduced Synechococcus net growth rates at most sites as well as Planktothrix net growth in Sandusky Bay and Dolichospermum in Maumee Bay. Dilution resulted in significant growth increase of Synechococcus at half of the sites and Planktothrix at most sites evidencing substantial grazing pressure by the protozooplankton community on these genera. In contrast, Microcystis populations were largely unaffected by daphnids and protozooplankton grazing but benefitted from nutrient enrichment more than other CHAB genera. When diatoms were present in moderate abundance, grazing rates by daphnids on diatoms were significantly greater than grazing rates on cyanobacteria. The novel approach used in this study established differences in grazing pressure and nutrient effects on differing taxa and revealed that, while many taxa were grazed by multiple classes of zooplankton (e.g. Planktothrix, Synechococcus, Dolichospermum, diatoms), the lack of grazing pressure on Microcystis coupled with nutrient-enhanced growth in western Lake Erie promotes the occurrence of CHABs of this genus.

Broad-scale distribution of the winter protozooplankton community in the North Sea

Protozooplankton (PZP) (here size range: 12–200 μm) are rarely sampled over a broad scale, especially in ecosystem monitoring programs, despite their trophodynamic importance as grazers in the microbial loop and as prey for larger zooplankton and early life stages of fish. In this study we sampled PZP from Dutch, French, German and Norwegian research vessels taking part in the annual ICES coordinated International Bottom Trawl Survey (IBTS) which provides data on fish stock abundances and status for the entire North Sea. The abundance, biomass, composition and distribution of PZP were examined at 39 stations across the North Sea (from 3.2°W to 7.6°E and 50.5 to 59.8°N) in mid-winter (January–February 2014), a period of the year which is under-investigated so far. Twenty four taxa of dinoflagellates and ciliates were identified. Two groups comprised 89% of the total abundance of PZP: Gymnodinium spp. and other athecate dinoflagellates (68%) and Strombidium spp. and other naked ciliates (21%). The biomass of PZP at each station ranged between 0.08 and 2.4 μg C L−1, which is much lower than that reported for spring or summer (≥100 μg C L−1) in the North Sea. Relatively small-sized (<40 μm) PZP contributed 46% of the total biomass. No significant spatial pattern in the composition of the PZP community was found, although the total abundance of tintinnids was highest in the southern North Sea, an important over-wintering area for marine fish larvae. Using this fish survey (IBTS) as a sampling platform allowed us to obtain a synoptic view of the PZP community over a large area. The present collaborative effort provides an example of how existing monitoring platforms can be augmented in the future to collect relevant data and potential ecological indicators needed to advance the ecosystem-based approach to managing marine systems.

Trophic role and top-down control of a subarctic protozooplankton community

Plankton succession was investigated in the subarctic Godthabsfjord, Western Greenland, from March to August 2010. The trophic role of protozooplankton (ciliates and hetero- trophic dinoflagellates) was evaluated with emphasis on their seasonal succession and as prey for the copepod community. The integrated protozooplankton biomass ranged between 0.1 and 4.0 g C m �2 , and was dominated by ciliates. Over the 6 mo study period, maximum potential ingestion rates of the protozooplankton ranged from 0.02 to 1.2 g C m �2 d �1 , corresponding to 30 to 194% of primary production d �1 or 0.5 to 37% of phytoplankton biomass d �1 . The highest copepod biomass (24 g C m �2 ) occurred in spring, with Metridia longa alone contributing up to 92% of the biomass. A grazing experiment with M. longa feeding on a natural plankton assemblage confirmed that this species cleared cells in the size range 10 to 60 µm with an average clearance rate of 2.4 ml µg C �1 d �1 . The copepod community, dominated by the genera Calanus, Metridia, Pseudocalanus, Oithona, Microsetella and Triconia/Oncaea, accounted for 72 to 93% of the copepod biomass in the spring. After the large calanoid copepod species left the surface layer, the protozooplankton increased numerically and were the most important grazers for some weeks until a late summer copepod community, dominated by cyclopoids Oithona spp., controlled the protist community. Our study indicated that protozooplankton succession is regulated by copepod grazing during most of the season, and that these protists provide an essential source of nutrition for the copepod populations.

Grazing by the copepods Calanus helgolandicus and Acartia clausi on the protozooplankton community at station L4 in the Western English Channel

C. helgolandicus and A. clausi, respectively. Calanus helgolandicus obtained 2 – 27% of its daily ration as a percentage of body carbon from phytoplankton and 2 – 17% of its daily ration from PZP. Acartia clausi obtained 22– 161% of its daily ration from phytoplankton and 3 – 44% daily ration from PZP. Calanus helgolandicus and A. clausi populations together grazed up to 21% of the total PZP standing stock daily. Both C. helgolandicus and A. clausi demonstrated selective feeding on large choreotrich ciliates and heterotrophc dinoflagellates. Our results support the hypothesis that PZP comprise a significant proportion of the copepod diet after the spring bloom when the phytoplankton community is dominated by small cells.

Influence of Emergent and Submerged Macrophytes on the Structure of Planktonic Ciliate Communities in Shallow Freshwater Lakes (Eastern Poland)

AbstractData from two shallow macrophyte‐dominated lakes (Eastern Poland) sampled with standardized methods, were evaluated in order to examine the effects of various stands of macrophytes in predicting protozooplankton community structure. Differences in macrophyte structure led to two distinct groups of habitats having different patterns of ciliate distribution. The first group consists of two vegetated habitats of sparse stem density and of the open water zone, and the second of submerged macrophyte species, which were more dense and complex. The number of significant correlations was different in the studied habitats. In central zones of macrophyte habitats the number of ciliates had the strongest correlation with concentrations of total organic carbon and Ptot. On the other side in the border zone a significant correlation between the number of ciliates and the chlorophyll a concentration was found. (© 2008 WILEY‐VCH Verlag GmbH &amp; Co. KGaA, Weinheim)

Grazing by Calanus helgolandicus and Para-Pseudocalanus spp. on phytoplankton and protozooplankton during the spring bloom in the Celtic Sea

Feeding rates and selectivity of the calanoid copepods Calanus helgolandicus and Para-Pseudocalanus spp. on natural assemblages of microplankton were evaluated in the English Channel and western Celtic Sea during non-bloom and bloom conditions in April 2002. Ingestion rates of total chlorophyll- a were low at non-bloom stations where the phytoplankton community was dominated by cells < 5 μm in length and higher during the bloom when the > 5 μm size fraction was dominant. Protozooplankton contributed to the copepod diet in all experiments, C. helgolandicus clearance and ingestion rates were highest for the ciliate Myrionecta rubra (626–1347 ml cop − 1 d − 1 ; 0.3–27 μg C cop − 1 d − 1 ). C. helgolandicus ingested between 1 and 18 μg C cop − 1 d − 1 (1–12% body C) from phytoplankton + protozooplankton food sources. The total carbon ingested by Para-Pseudocalanus spp. was lower (0.5–6 μg cop − 1 d − 1 ) but this was equivalent to between 6 and 78% of body carbon being ingested daily. Our data suggest that C. helgolandicus selected prey according to size; this was not the case for Para-Pseudocalanus spp. which became more selective as chlorophyll- a concentration increased. Grazing impact of the entire copepod community on protozooplankton was assessed. We found that at non-bloom stations between 12 and 17% of the protozooplankton community was being removed daily by the copepod community, whereas during the peak of the bloom the proportion being removed daily was only 2%. We conclude that during the spring bloom period copepods gained the majority of their carbon from phytoplankton ingestion but during non-bloom periods, protozooplankton and the ciliate M. rubra made a significant contribution to copepod diet.

Structure and function of the pelagic ecosystem in Young Sound, NE Greenland

An annual carbon budget of the pelagic food web is constructed for a 36 m deep station in Young Sound. Data were collected during a 2-week mid-summer sea-ice covered period in 1999, during the open-water period of 1996, 2003, 2004, 2005 and during winters of 1997 and 2003. The measurements revealed that during sea-ice cover the water column of outer Young Sound was strongly heterotrophic and sustained by organic material advected into the fjord from the open sea. The pelagic community thus originated from the marginal ice zone at the entrance to the fjord. No succession was observed in the plankton community during this period, and the grazing pressure of the dominating zooplankton groups (ciliates, heterotrophic dinoflagellates, meroplankton and copepods) was 10 times higher than primary production, while the bacterial carbon demand was three times higher than primary production.&#x0D; During the open-water period, the grazing community was completely dominated by copepods, which were capable of grazing down the entire primary production. This contrasts with several other investigated Arctic marine pelagic ecosystems further south, where the protozooplankton community is quantitatively more important than copepods. In Young Sound, both zooplankton groups are present simultaneously, and copepods thus act both as competitors for food and as predators in relation to the protozooplankton. On an annual basis, the carbon budget was unbalanced; the total carbon need of the grazers equaled primary production, leaving no room for the estimated bacterial carbon demand, which was of the same size as the carbon demand of the grazers. Thus, Young Sound is a net heterotrophic system relying on import of organic material from the open sea or possibly from land.

Protozooplankton community structure and grazing impact in the eastern Atlantic sector of the Southern Ocean in austral summer 1998

Abstract The protozooplankton community structure and grazing impact within the winter ice-edge zone (WIE), spring ice-edge zone (SIE) and in the vicinity of the Antarctic Polar Front (APF) in the eastern Atlantic sector of the Southern Ocean was investigated in austral summer (December 97—January 98). Total chlorophyll-a (Chl-a) concentrations in the vicinity of the SIZ and APF were always >0.5 μg l while at stations within the SIE total pigment concentrations were always 20 μm fraction was always dominated by ciliates comprising aloricates and tintinnids and dinoflagellates. The contribution of the larger components to the total was, however, always 60% of total pigment. These results suggest that the grazing impact of the protozooplankton was largely mediated by the contribution of the small phytoplankton cells to total pigment.

Abundância de tecamebas no plâncton de reservatórios do Estado do Paraná

This study aimed to investigate patterns of spatial and temporal distribution of testate amoebae (Rhizopoda) abundance in plankton of different reservoirs of Parana State and the importance of hydrodinamical and morphometrical factors on determining these patterns. Thirty reservoirs studied are located in six different watersheds, including environments with variable area, morphometry and age. Sampling were carried out in July and November 2001, dry and rainy seasons, respectively. Samples were obtained at the surface of reservoirs, in the lacustrine region, using a motorized pump (600 liters per sample) and a plankton net with a mesh size of 68µm. Testate amoebae were registered in 23 of 30 reservoirs.Higher density were observed in JMF, Salto do Meio, Melissa, Mourao and Salto do Vau reservoirs, during dry season, and JMF, Salto Osorio, Salto do Meio and Melissa reservoirs, during wet season These reservoirs present similar characteristics, as reduced depth and morphometric dimensions Besides that, most of them have hydrodynamical features similar to lotic environments, due to presenting high current velocity. On the other hand, testate amoebae were absent or presented low density, in general, in reservoirs with higher dimensions and depth. Instead of expected, seasonally, higher densities values were observed during dry season, for the most of studied reservoirs. These results can be related to the fact that the reservoirs during dry season have a remarkable reduction of their dimentions (area and depth), determining a greater influence of the benthonic organisms to the composition and abundance of the protozooplankton community

Structure of the protozooplankton community in a tropical shallow and eutrophic lake in Brazil

Monte Alegre Lake is a shallow, eutrophic and polymictic reservoir situated in Southeastern Brazil. Seasonal distributions of planktonic protozoans (HgCl2 fixed samples) and bacteria (AODC) were sampled at the surface and bottom, fortnightly from April 1988 to March 1989. Species composition and biomass (wet weight) of protozooplankton were analysed. Protozoan densities ranged from 3.60 × 103 to 3.89 × 105 ind l–1 at the surface and from 7.11 × 103 to 9.75 × 104 ind l–1 at the bottom, and the biomass ranged from 37 to 1170 μg l–1 and from 63 to 4958 μg l–1. The highest densities and biomass of both protozoans and bacteria were detected during the water column stratification period with anoxia at the bottom (warm-wet season). The smallest protozoan species prevailed at the surface and the largest at the bottom. Chlamydophrys sp., Arcella hemisphaerica, Mesodinium pulex and Halteria grandinella were numerically more important. On the other hand, Holophrya cf. discolor, Arcella hemisphaerica, Paramecium spp. and Spirostomum teres were dominant in biomass. Coccoid bacterial cells were abundant, except during the wet season when a phototrophic elongated ovoid bacterium, Thiopedia rosea, accounted for 61% of the total bacterial biomass at the bottom. The controlling factor of the protozooplankton is probably the food availability (bacteria) associated with dissolved oxygen and high temperatures.

Food web interactions in a Calanus finmarchicus dominated pelagic ecosystem--a mesocosm study

The significance of nauplii versus copepodite stage V of Calanus finmarchicus grazing and their effects on the structure of the food web were investigated during two sampling periods of 7–8 days in March and April in experimental mesocosms held in a Norwegian fjord over a 2 month period. The mesocosms were manipulated by the addition of two different levels of inorganic nutrients (control versus enriched). During the ‘naupliar’ period in March, the phytoplankton was characterized by a diatom bloom while during the ‘copepodite’ period in April, it was in a post-bloom phase characterized by small-celled species, mainly Phaeocystis pouchetii. Phytoplankton, bacterial and protozooan biomass and production rates were measured in addition to copepod biomass. Copepod grazing was estimated by three different methods: (i) gut fluorescence; (ii) chlorophyll clearance from the water; and (iii) growth method measured as body carbon increase. The two latter methods gave similar results for nauplii, but all three gave different results for the copepodites. Independent somatic growth, based on changes in abundance and individual carbon content, and grazing estimates revealed an overall growth efficiency of 0.66 ± 0.20 (mean ± S.E.) for copepodites. Empirical carbon flow models were constructed, which indicated that the nauplii could not control either phytoplankton or protozoan growth in either the control or in the enriched system. Ignoring recycling and sedimentation, the fate of the primary production for the nauplii-dominated community was to be grazed by a diverse and abundant protozooplankton community. In the copepodite-dominated community, the copepods grazed >100% of the daily primary production, and also grazed heavily on a protozooplankton community of low biomass and diversity and presumably on detritus. The fate of the primary production in the two different copepod scenarios followed predicted routes for ‘low meso-zooplankton’ and for ‘high meso-zooplankton’ biomass systems, as suggested by Wassmann (Wassmann, 1998).

Ciliates and heterotrophic dinoflagellates in the marginal ice zone of the central Barents Sea during spring

Diversity and biomass of ciliates and heterotrophic dinoflagellates were analysed at six stations on a south–north transect (mimicking a time span of months in the biological succession during the Arctic spring–summer) from open water through drift ice and into fast ice (72°30′N 76°32′N) during spring 1993 in the open Barents Sea. A pycnocline was observed beneath the sea ice at 40–50 m. A diatom spring bloom beneath the ice with chlorophyll-a maximum &gt;10 μg l−1 and a diverse protozoan community with a peak biomass of 34 μg C l−1 was associated with this bloom. Maximum biomass of tintinnids (1 μg C l−1), athecate dinoflagellates (8 μg C l−1) and thecate dinoflagellates (26 μg C l−1) were found associated with the chlorophyll-a maximum in the upper 10 m of the water column beneath the sea ice at the northern stations. In contrast, the protozooplankton community was dominated by naked ciliates at the southern open water stations. Here chlorophyll-a was low (&lt;1 μg l−1) and the maximum biomass of protozooplankton was 10 μg C l−1 of which naked ciliates accounted for &gt;50%.Cell sizes and estimated carbon content of cells &gt;11 μm, as well as depth by depth biomass of 12 species/types of naked ciliates, 12 tintinnids, 12 athecate dinoflagellates and 24 thecate dinoflagellates, are presented. The community of naked ciliates was dominated by Strombidium spp. and Strobilidium spp., the tintinnids were dominated by Parafavella spp., Ptychocylis, Leprotintinnus, Acanthostomella and Tintinnopsis. The very small gyro-/gymnodinoid cells and Gyrodinium cf. spirale dominated the athecate dinoflagellates and the thecate dinoflagellates by the heterotroph Protoperidinium spp. generally accounted for the major part of the protozooplankton biomass along the transect. The Margalef diversity index revealed lowest diversity of ciliates and heterotrophic dinoflagellates in the open water and higher at ice-associated stations. The overall diversity was coupled with prey availability in terms of food concentration, but already saturated at 0.1 μg chlorophyll-a l−1.

Structure and grazing impact of the protozooplankton community in the waters surrounding the Prince Edward Islands (Southern Ocean)

The structure and grazing dynamics of the protozooplankton community at ten stations in the upstream and downstream region of the Prince Edward Islands (46°38′S, 37°57′E) were investigated during early austral autumn (April/May) 1997. Total chlorophyll-a (chl-a) concentrations throughout the investigation were 20 μm) generally contributed 20 μm fraction was dominated by dinoflagellates. Instantaneous growth rates of phytoplankton at upstream stations ranged from 0.01 to 0.18 day−1 and between 0.01 and 0.19 day−1 at downstream stations. Instantaneous grazing rates of protists on phytoplankton upstream of the islands ranged from 0.03 to 0.07 day−1, which corresponds to a loss of up to 8% (mean = 5%) of the initial phytoplankton standing stock or up to 71% (mean = 37%) of the potential primary production per day. Downstream of the islands, although the grazing rates of the protists were within the same range (0.01–0.07 day−1), the grazing impact was lower, corresponding to up to 7% (mean = 3%) of the initial standing stock or up to 47% (mean = 25%) of the potential primary production per day. The spatial difference in the grazing impact of protozooplankton appears to reflect a shift in the size structure of the phytoplankton community resulting from the “island mass effect”.

Factors controlling pelagic populations of ciliates and heliozoans— late summer investigations in an acidic lake before and after liming

Ciliates and heliozoans were studied in a small oligotrophic Swedish lake with the objective of investigating what controlled the community structure and population dynamics. Enclosure experi- ments were performed with five levels of inorganic nutrient concentrations and the presence or absence of crustacean zooplankton. The experiments were performed during the summers immedi- ately preceding and following liming of the lake. The responses of protozooplankton to these manipu- lations were investigated and compared with the responses of bacterioplankton, phytoplankton and metazooplankton. In contrast to most studies on protozoan zooplankton, ciliates were determined to the lowest taxon possible, and biomasses and abundances were calculated for the different taxa. The protozooplankton biomass of the lake, expressed as summer average, did not change between the years. However, the community composition changed from smaller to larger species as the small pro- stomatid ciliates Urotricha and Balanion were largely replaced by oligotrichs of the genera Strom- bidium and Strobilidium. The experiments suggested that the protozooplankton community in the lake was controlled by metazooplankton in the acidic environment, while food limitation was the most important controlling factor after liming. Before liming, Urotricha and Balanion were unaffected by nutrient additions as well as by metazooplankton, while other ciliates and Heliozoa showed a signifi- cantly negative response to metazooplankton. After liming, Urotricha and Balanion showed a signifi- cant positive response to nutrient addition as well as to bacterioplankton biomass. A possible explanation for this response in these algivore genera is that the response was indirect and mediated through small chrysoflagellates.

Microzooplankton grazing and protozooplankton community structure in the South Atlantic and in the Atlantic sector of the Southern Ocean

Microzooplankton grazing and protozooplankton community structure in the South Atlantic and Atlantic sector of the Southern Ocean were investigated during late austral summer (January/February) 1993. Grazing rates and numerical abundances of protozooplankton were estimated in the surface waters and at the subsurface chlorophyll maximum (SCM) by employing the dilution technique and epifluorescent microscopy. Protozooplankton abundance co-varied with chlorophyll concentrations at both depths. Nanoheteroflagellates (< 20 μm) dominated numerically at all stations while the > 20 μm component was dominated by ciliates, comprising aloricate ciliates and tintinnids. Instantaneous growth rates of alga along the transect ranged between 0.24 and 1.86 ay −1 in surface waters and between 0.06 and l.87 day −1 at the SCM. Instantaneous grazing rates of microzooplankton on phytoplankton varied from 0 to 0.33 day −1 in the surface waters and between 0 and 0.58 day −1 at the SCM. This level of grazing corresponds to a daily loss of 0–23% of the initial standing stock (0–46% of potential production) in the surface waters and between 0 and 44% (0–60% of potential production) of the initial standing stock at the SCM. Analysis of variance and multiple range tests indicate that both the initial standing stock and potential production removed were not significantly different between depths ( F=0.84; F=0.29: P<0.05). Indirect evidence presented, suggests that microzooplankton are preferentially grazing on the nano- and picophytoplankton size fractions. The spatial distribution of phytoplankton size classes in the different zones of the Southern Ocean has important ecological implications for the oceanic carbon flux. South of the Antarctic Polar Front (APF), where larger netphytoplankton dominates chlorophyll concentration, the bulk of the photosynthetically fixed carbon appears to be channelled into the meso/macrozooplankton component or is lost by sedimentation. However, north of the APF, the contribution of the smaller fractions to total chlorophyll increases, suggesting a relative increase in the amount of carbon channelled into the smaller grazing fractions.

Microzooplankton Grazing in the Southern Ocean: Implications for the Carbon Cycle

Abstract. Microzooplankton grazing and protozooplankton community structure was investigated in austral summer (Jan./Feb.) and winter (June/July) 1993 in the Atlantic sector of the Southern Ocean during the SAAMES (South African Antarctic Marine Ecosystem Study) Il and III cruises. Grazing was estimated at 22 stations in summer and at 15 stations in winter by employing the sequential dilution technique. Nano‐heterotrophic flagellates (&lt; 20 μm) and ciliates (aloricate ciliates and tintinnids) dominated the protozooplankton assemblages along both transects. Densities in winter were, however, nearly an order of magnitude lower than in summer. Microzooplankton grazing removed between 0 and 28% (mean = 13.2%) of the initial phytoplankton stock in summer and, between 24 and 51 % of the initial stock (mean = 37.6%) in winter. The potential primary production removed during summer ranged between 0 and 46% (mean = 22.0%) compared with the winter range of 56–83% (mean = 67.2%). Size selectivity grazing experiments conducted during both studies suggest that microzooplankton preferentially graze on the nano‐ (20–2.0μm) and picophytoplankton (2.0–0.2μm) size fractions. These results have important implications for the efficiency of the carbon pump in the Southern Ocean. During summer when the larger cells dominate phytoplankton biomass, the bulk of the photosynthetically fixed carbon appears to be channelled to the meso‐ and macrozooplankton fractions. This results in a rapid transfer of organic carbon out of the zone of regeneration to the deep ocean via vertical migration and large faecal pellet production. During winter, however, an increase in the contribution of the smaller size fractions to total phytoplankton biomass results in a greater proportion of the photosynthetically fixed carbon being channelled to the microzooplankton fraction. The efficiency of the carbon pump is, therefore, reduced in that the transfer of carbon below the zone of regeneration is reduced as carbon is recycled mostly within the microbial loop in the upper mixed layer.