Marcia M. Gowing

The “particle” flux: Origins and biological components

Abstract Sedimentation of organic matter from the oceans surface layers is intimately tied to biological events within the euphotic zone. Although the sedimentation rate is usually found to be positively correlated with primary production, the biological basis for the correlation is not well understood. In eutrophic environments, algal populations or large fecal pellets can account for high mass fluxes. The types of particles leaving oligotrophic systems, in contrast, are less clear. Similarly, various mechanisms have been invoked to explain the loss of particles with depth, but little direct evidence is available to distinguish among the possibilities. The fundamental causes of differences in export rates and of the rapid loss of particles at depth, however, will be reflected in the changing composition of particles across a productivity gradient and down through the water column. We have attempted to investigate the biological processes leading to the productivity-flux relationship and the depth-related losses, using Vertex samples from particle interceptor traps deployed in the Northeastern Pacific between 1980 and 1984. We found the previously reported correlation between production and flux in the Vertex data set ( Pace, Knauer, Karl and Martin , 1987) to result from related changes in intact and presumably living organisms in trap samples, not from non-living particles. The production-flux correlation depended, however, entirely on results from an upwelling station: when data from this station were excluded, no pattern was observed among the remaining 6 stations. Phytoplankton flux at the base of the euphotic zone was likewise significantly correlated with primary production, and the relationship persisted even after data from the upwelling station were removed. Important live contributors to traps also included sarcodine protozoans (foraminiferans and radiolarians), eggs of invertebrates, and invertebrate larvae too small to be removed as “swimmers”. (The present study focuses on smaller or unicellular organisms; another study considers also the role of larger, but also cryptic, “swimmers”: Michaels, Silver, Gowing and Knauer , in press). The flux of non-living materials, including fecal pellets and amorphous aggregates, was not related to primary production, nor was there a correlation between obvious parameters of fecal pellets (i.e. average size or numbers) and production. These results raise questions about the meaning of the term “particle flux”. An average of at least 35%, with a range of 11–80% (minimal values, because larger organisms were not included), of the carbon flux leaving the euphotic zone consisted of algae, protozoans, and small metazoans that may have been executing vertical movements as part of a life history strategy. Furthermore, these organisms continued to be important in the mesopelagic zone, where the sarcodines were sometimes substantive contributors (average of 12%, range up to 49%) to the carbon flux. The declining contribution of these living organisms within traps at depth can account for some of the decreases in carbon flux that have been interpreted as “regeneration”. Clearly, reasonable inferences from traps require a better understanding of the nature of the “particles”, and particularly, the contribution of living organisms to trap collections.

Cryptic zooplankton swimmers in upper ocean sediment traps

Abstract Sediment traps are the major oceanographic tool for collecting passively sinking particulate material (the “particle flux”) in the ocean. Sediment traps in the upper ocean also collect actively sinking zooplankton that are usually manually removed prior to analysis. Microscospic analysis of sediment trap samples collected over a 19-month period in the eastern North Pacific reveals that zooplankton “swimmers” are a larger problem than previously recognized. Zooplankton that are cryptic (i.e. difficult to see or distinguish from the detrital material) and difficult to remove (principally gelatinous zooplankton) may have contributed up to 20 mg C m −2 day −1 to the “particulate flux”, with the highest values in the upper 150 m. This swimmer problem is in addition to the previously recognized presence of crustaceans and other large metazoans in traps. Additionally, the detritus-laden, mucous-feeding structures (houses)of larvaceans probably enter the traps with the larvaceans and would be impossible to remove. We estimate that the contribution of the cryptic swimmers and larvacean houses could be as much as 96% of the measured carbon flux. The contribution is greatest in the euphotic zone and drops sharply below 200 m. Subtracting out this potential artifact at the VERTEX station results in vertical profiles of organic carbon flux that differ dramatically from the standard flux profile for carbon in the upper ocean: specifically, the implied “regeneration” rate is greatly reduced. Screened traps (300 μm screens below the baffles) contained numerous metazoans smaller than the screen mesh size. These traps also contained lower levels of other types of sinking particles, and it is unclear to what extent the screens reduced the relative contribution of swimmers to the trap-collected carbon. Although the expanded swimmer problem presented here is now documented at just the VERTEX site, we expect it exists elsewhere. The extent of this swimmer problem requires resolution before sediment traps, especially those deployed in the upper few 100 m, can be used to measure the “flux of particulate material.”

Pelagic and benthic ecology of the lower interface of the Eastern Tropical Pacific oxygen minimum zone

The distributions of pelagic and benthic fauna were examined in relation to the lower boundary of the oxygen minimum zone (OMZ) on and near Volcano 7, a seamount that penetrates this feature in the Eastern Tropical Pacific. Although the broad, pronounced OMZ in this region is an effective barrier for most zooplankton, zooplankton abundances, zooplankton feeding rates, and ambient suspended particulate organic carbon (POC) peaked sharply in the lower OMZ (about 740–800 m), in association with the minimum oxygen concentration and the increasing oxygen levels just below it. Zooplankton in the lower OMZ were also larger in size, and the pelagic community included some very abundant, possibly opportunistic, species. Elevated POC and scatter in the light transmission data suggested the existence of a thin, particle-rich, and carbon-rich pelagic layer at the base of the OMZ. Gut contents of planktonic detrifvores implied opportunistic ingestion of bacterial aggregates, possibly from this layer. Benthic megafaunal abundances on the seamount, which extended up to 730 m, peaked at about 800 m. There was a consistent vertical progression in the depth of first occurrence of different megafaunal taxa in this depth range, similar to intertidal zonation. Although the vertical gradients of temperature, salinity, and oxygen were gradual at the lower OMZ interface (in contrast to the upper OMZ interface at the thermocline), temporal variability in oxygen levels due to internal wave-induced vertical excursions of the OMZ may produce the distinct zonation in the benthic fauna. The characteristics of the lower OMZ interface result from biological interactions with the chemical and organic matter gradients of the OMZ. Most zooplankton are probably excluded physiologically from pronounced OMZs. The zooplankton abundance peak at the lower interface of the OMZ occurs where oxygen becomes sufficiently high to permit the zooplankton to utilize the high concentrations of organic particles that have descended through the OMZ relatively unaltered because of low metazoan abundance. A similar scenario applies to megabenthic distributions. Plankton layers and a potential short food chain (bacteria to zooplankton) at OMZ interfaces suggest intense utilization and modification of organic material, localized within a thin midwater depth zone. This could be a potentially significant filter for organic material sinking to the deep-sea floor.

Seasonal response of zooplankton to monsoonal reversals in the Arabian Sea

Abstract The US JGOFS Arabian Sea Process Study was designed to provide a seasonally and spatially resolved carbon budget for a basin exhibiting some of the highest and lowest concentrations of plant biomass in the world’s ocean. During the US JGOFS Process Study in the Arabian Sea (September 1994–January 1996), the absolute maximum in biomass of epipelagic zooplankton in the entire study was observed during the Southwest Monsoon season inshore of the Findlater Jet in the area of upwelling. The greatest contrast between high and low biomass in the study area also was observed during the Southwest Monsoon, as was the strongest onshore–offshore gradient in biomass. Lowest biomass throughout the study was observed at the most offshore station (S15), outside the direct influence of the monsoon forcing. The greatest day/night contrasts in biomass were observed nearshore in all seasons, with nighttime biomass exceeding daytime in the Northeast Monsoon season, but daytime exceeding nighttime in the Southwest Monsoon season. The diel vertical migration patterns in general reversed between the monsoons at all stations in the southern part of the study area. Virtually, no diel vertical migration of zooplankton took place in any season at the station with strong, persistent subsurface suboxic conditions (N7), suggesting that these conditions suppress migration. Based on the distribution of biomass, we hypothesize that inshore of the Findlater Jet, zooplankton grazing on phytoplankton is the dominant pathway of carbon transformation during both monsoon seasons, whereas offshore the zooplankton feed primarily on microplankton or are carnivorous, conditions that result in reduction of the carbon flux mediated by the zooplankton. Predation by mesopelagic fish, primarily myctophids, may equal daily growth of zooplankton inshore of the Findlater Jet during all seasons. This suggests that the food web inshore of the Findlater Jet is well integrated, may have evolved during past periods of intensified upwelling, and has a distinctly annual cycle.

Nano- and microplankton in the northern Arabian Sea during the Southwest Monsoon, August–September 1995 A US–JGOFS study

As part of the US Joint Global Ocean Flux Studies (JGOFS) Arabian Sea Program, we determined the abundance and biomass of autotrophic and heterotrophic nano- and microplankton in the upper 100 m at 10 stations in the northern Indian Ocean during the late Southwest Monsoon from 17 August through 15 September 1995. Autotrophic nano- and microplankton biomass ranged from 0.2 to 68.0 μg C l-1, with most of the biomass in the upper 20–60 m. Phytoplankton assemblages varied markedly in composition along a transect from onshore to about 1500 km offshore. Larger forms, such as diatoms and colonies of the prymnesiophyte Phaeocystis, dominated stations inshore of about 1000 km, whereas picoplankton dominated offshore. Heterotrophic nano- and microplankton biomass varied from ∼1 to 12 μg C l-1, and nanoflagellates, dinoflagellates, and ciliates reached maximum biomass at different locations and depths. Heterotrophs comprised 18–27% of the biomass over most of the transect. Biomass of all groups of organisms was strongly negatively correlated with depth and positively correlated with each other, suggesting a dynamic food web. Size structure of organisms among stations suggested that larger consumers occurred where phytoplankton cells were large. Sediment trap data indicate high organic carbon and biogenic silica flux at the time of our study. Our findings of abundant diatoms over much of the study area and their apparent transition from healthy-looking cells nearshore to senescent ones offshore suggest that populations could have sunk as a bloom terminated, in addition to being available for mesozooplankton grazers.

Spatial distribution pattern of living polycystine radiolarian taxa — baseline study for paleoenvironmental reconstructions in the Southern Ocean (Atlantic sector)

The horizontal and vertical distribution of living polycystine radiolarian taxa was investigated at seven locations on a N-S transect between the Antarctic Zone (54 °S) in the Southern Ocean and the Subtropical zone (30 °S) in the southeastern South Atlantic during austral autumn. Four to five depth intervals from 0 to 1000 m depth were sampled with 55 μm mesh opening/closing nets in combination with a hydrographic CTD survey. A factor analysis for the delineation of specific assemblages and the relation between different taxa and taxa groups resulted in eight factors, of which five represent surface and subsurface factors and three deep water factors. The spatial distribution pattern of the factors shows that distinct radiolarian assemblages are closely related to water depth, distribution of water masses, hydrographic boundaries such as frontal systems, and nutrients. This documents that the distribution of individual radiolarian assemblages is controlled by specific hydrographic conditions and water depth, and allows the definition and consolidation of the autecological demands. These data are crucial for the paleoenvironmental interpretation of fossil polycystine radiolarian assemblages. The comparison of living polycystine radiolarian taxa with those preserved in surface sediments shows general similarities. This study includes the first documentation on the distribution of living Cycladophora davisiana in Circumpolar Deep Water and supports previous studies stating that C. davisiana also lives in deep-water masses.

CARBON PARTITIONING WITHIN PHAEOCYSTIS ANTARCTICA (PRYMNESIOPHYCEAE) COLONIES IN THE ROSS SEA, ANTARCTICA

The haptophyte Phaeocystis antarctica Karsten is a dominant species within the seasonal bloom in the Ross Sea. One of the unique characteristics of this form is that carbon is partitioned between the cells and the colonial matrix, a relationship that is poorly documented for this region. We combined particulate organic carbon measurements and microscopic analysis of P. antarctica‐dominated samples to assess the contribution of single cells, colony‐associated cells, and mucilage to the carbon concentrations of waters with P. antarctica. Two cruises to the Ross Sea were completed, one in austral spring 1994 and one in summer 1995–1996. In 1994 the bloom was dominated by colonial P. antarctica that contributed up to 96% of the total autotrophic carbon, whereas in 1995–1996 a mixture of P. antarctica and diatoms occurred. P. antarctica colony volume (V ) was related to colonial cell number (NC) by the relationship V = 417 ×NC1.67. Total colony carbon (CCOL) was calculated as the sum of cell carbon (CCC) and mucus‐related carbon (CM). We found the contribution of mucus carbon to be 213 ng C mm−3 of colony volume. For P. antarctica‐dominated assemblages sampled at the peak of the bloom, CM represented a minor fraction (14 ± 4%) of colony carbon, and during early summer conditions CM was at most 33% of CCOL. This organism plays a cardinal role in the carbon cycle of many regions. These results constrain the partitioning of carbon between cellular material and the colony matrix, information that is necessary to accurately describe the biogeochemical cycles influenced by this species.

Winter plankton assemblage in the ice edge zone of the Weddell and scotia seas: composition, biomass and spatial distributions

Abstract As part of the Antarctic Marine Ecosystem Research in the Ice Edge Zone (AMERIEZ) program, we examined the biomass and distribution of phytoplankton and protozooplankton at an advancing ice edge in the Weddell and Scotia Seas during the early austral winter. The advance of ice cover, local melting of sea ice and advection of water masses, possibly from lower latitude regions, were the main sources of variability in the physical regime of the ice-edge zone. Analysis of the plankton assemblage showed phytoplankton biomass (PPC) in the upper 100 m ranging from 100 to 272 mg C m −2 and protozooplankton biomass (PZC) ranging from 177 to 410 mg C m −2 . Autotrophic dinoflagellates dominated phytoplankton stocks, followed by other autotrophic nanoflagellates and diatoms in decreasing biomass. Heterotrophic flagellates dominated protozooplankton biomass followed by ciliates and sarcodines. The biomass of major groups comprising the planktonic assemblage was similar at most stations with the exception of one station where diatoms predominated. Integrated PPC and PZC showed no relationship to water column stability. Integrated autotrophic flagellate biomass was higher at open water stations than at ice-covered stations, but none of the other integrated group biomasses showed variations that could be related to ice cover or water mass characteristics. Analysis of discrete-depth samples indicated that all groups (except the sarcodines) showed near surface maxima, that total PPC, diatoms and autotrophic flagellates showed higher biomasses at ice-edge and open water stations than at ice-covered stations and that none of the heterotrophs showed variations related to ice cover. Some groups, however, showed differences that could be related to water mass characteristics, but this was less evident than was the effect of depth or ice cover. Comparison of species assemblages of diatoms and choanoflagellates among water column stations indicated variations that could be related to the differing cruise legs and water mass characteristics. Similar diatom assemblages were found in both ice and water, but higher concentrations occured in the ice assemblages. A few diatom species were found to be indicator species for ice versus water assemblages and to distinguish among the varying hydrographic regimes. Although phytoplankton stocks were higher at non ice-covered than at ice-covered stations, we were not able to see distinct differences between ice-edge stations and those north of the furthest ice extent. We hypothesize that advection of sea ice into water above the freezing point and subsequent melting of ice probably affected much of our study area, so that any effects of “enhanced production” in the ice-edge zone would have been difficult to resolve. Moreover, absolute primary production was very low, and based on the trophic composition of the planktonic assemblage and production estimates from our AMERIEZ colleagues, we concluded that neither algal nor bacterial production was sufficient to produce an enrichment of protozooplankton stocks in the ice-edge zone. Calculations of a carbon budget suggested bacterial production was a significant proportion of total production and that the nano- and microheterotrophs must predominate in the utilization of both phyto- and bacterioplankton production at the winter ice edge. An analysis of species assemblages suggested little advection of populations from lower latitude regions and supports the contention that material was apparently released from sea ice during localized melting events. This input of carbon biomass and detritus from ice may supply the carbon needed to support the high concentrations of heterotrophs observed in our study, but this interpretation is confounded because ice-edge heterotrophic plankton populations also may be enriched by seeding from sea ice.

Trophic biology of phaeodarian radiolarians and flux of living radiolarians in the upper 2000 m of the North Pacific central gyre

Fluxes of living radiolarians collected in particle traps in the North Pacific central gyre ranged from 5.4 × 104 m−2 at 50 m (of which 52% resulted from individuals of colonial radiolarians) to 103 m−2 day−1 at 2000 m. The fluxex of total radiolarians (living plus skeletons) were as high as or higher than fluxes reported for oceanographic regions where radiolarians are more abundant. Living radiolarians contributed 1.3% (at 150 m) to 26% (at 900 m) of the organic carbon flux. Reproductive individuals of the nassellarian Lithopera bacca were found to 700 m. Examination of the feeding vacuoles and wastes of phaeodarian radiolarians with transmission electron microscopy shows that the organisms feed on detritus and microorganisms commonly associated with detritus, and that the majority of phaeodarians are trophic generalists. Phaeodarian radilarians may play a role in regulation of decomposition of detritus and complete with ciliates for food. The presence of abundant living radiolarians to skeletons to determined to refine models 2000 m requires that ratios of living radiolarians to skeletons to determined to refine models relating standing stocks to flux, and to assess the contribution of radiolarian skeletons to biogenic opal flux.

Abundance and feeding ecology of larger protozooplankton in the ice edge zone of the Weddell and Scotia Seas during the austral winter

Abstract Biomasses, abundances and feeding ecology of larger (> 50 μm diameter) protozooplankton were studied in the upper 210 m in the ice edge zone of the Weddell/Scotia Sea area in the austral winter of 1988. Sixty-liter water samples were taken at five depths at 17 stations, and organisms were concentrated by reverse-flow filtration. Mean abundances of the total assemblage of larger protozooplankton (radiolarians, formaminiferans, acantharians, the heliozoan Sticholonche, tintinnid and aloricate ciliates, and thecate and athecate dinoflagellates) ranged from 2040 to 3745 M−3 in the upper 210 m. Biomass ranged from 33 to 48 μg C m−3 in the upper 85 m, and from 32 to 54 μg C m−3 from 115 to 210 m. Phaeodarian radiolarians larger than 1.6 mm (sampled with plummet nets) contributed an additional 3 μg C m−3 in the upper 100 m and an additional 7 μg C m−3 from 100 to 200 m. These abundances and biomasses are lower than for other seasons in the Antarctic, but are comparable to abundances reported for several of these groups in lower latitude waters. We attribute the low winter abundances to slower growth and reduced food, rather than to increased mortality. The large protozooplankton are trophically diverse; in addition to heterotrophy on a variety of organisms, we found apparent evidence of mixotrophy and symbiosis in some of the groups. The large protozooplankton fed on both autotrophic and heterotrophic organisms in winter, although the biomass of smaller forms is dominated by heterotrophs. Feeding on detrital particles also was indicated by the presence of siliceous fragments in vacuoles. The larger protozooplankton in the winter ice edge zone may be important in reducing particle flux to the deep sea and as a food source for larger zooplankton, especially from the base of the euphotic zone to 210 m.