Mary W. Silver

Characteristics, dynamics and significance of marine snow

Abstract Macroscopic aggregates of detritus, living organisms and inorganic matter known as marine snow, have significance in the ocean both as unique, partially isolated microenvironments and as transport agents: much of surface-derived matter in the ocean fluxes to the ocean interior and the sea floor as marine snow. As microhabitats, marine snow aggregates contain enriched microbial communities and chemical gradients within which processes of photosynthesis, decomposition, and nutrient regeneration occur at highly elevated levels. Microbial communities associated with marine snow undergo complex successional changes on time scales of hours to days which significantly alter the chemical and biological properties of the particles. Marine snow can be produced either de novo by living plants and animals especially as mucus feeding webs of zooplankton, or by the biologically-enhanced physical aggregation of smaller particles. By the latter pathway, microaggregates, phytoplankton, fecal pellets, organic debris and clay-mineral particles collide by differential settlement or physical shear and adhere by the action of various, biologically-generated, organic compounds. Diatom flocculation is a poorly understood source of marine snow of potential global significance. Rates of snow production and breakdown are not known but are critical to predicting flux and to understanding biological community structure and transformations of matter and energy in the water column. The greatest challenge to the study of marine snow at present is the development of appropriate technology to measure abundances and characteristics of aggregates in situ .

Mortality of sea lions along the central California coast linked to a toxic diatom bloom.

Over 400 California sea lions (Zalophus californianus) died and many others displayed signs of neurological dysfunction along the central California coast during May and June 1998. A bloom of Pseudo-nitzschia australis (diatom) was observed in the Monterey Bay region during the same period. This bloom was associated with production of domoic acid (DA), a neurotoxin that was also detected in planktivorous fish, including the northern anchovy (Engraulis mordax), and in sea lion body fluids. These and other concurrent observations demonstrate the trophic transfer of DA resulting in marine mammal mortality. In contrast to fish, blue mussels (Mytilus edulus) collected during the DA outbreak contained no DA or only trace amounts. Such findings reveal that monitoring of mussel toxicity alone does not necessarily provide adequate warning of DA entering the food web at levels sufficient to harm marine wildlife and perhaps humans.

Primary production, sinking fluxes and the microbial food web

Abstract The size distribution of pelagic producers and the size and trophic position of consumers determine the composition and magnitude of sinking fluxes from the surface communities in a simple model of oceanic food webs. Picoplankton, the dominant producers in the model, contribute little to the sinking material, due primarily to the large number of trophic steps between picoplankton and the consumers that produce the sinking particles. Net phytoplankton are important contributors to the sinking materials, despite accounting for a small fraction of the total primary production. These net phytoplankton, especially those capable of nitrogen fixation, also dominate the fraction of the new production that is exported on its first pass through the food chain. The sinking flux is strongly determined by the community structure of the consumers and varies by an order of magnitude for different food webs. The model indicates that generalist grazers, zooplankton that consume a broad size spectrum of prey (including pico-and nanoplankton), play a critical role in exporting particles. The role of generalists that occasionally form swarms, such as thaliaceans (salps and doliolids), can be particularly difficult to assess. Short-term studies probably miss the relatively infrequent population blooms of these grazers, events that could control the average, long-term exports from surface oceanic communities.

Detection of domoic acid in northern anchovies and california sea lions associated with an unusual mortality event

The occurrence of an unusual mortality event involving California sea lions (Zalophus californianus) along the central California coast in May 1998 was recently reported. The potent neurotoxin domoic acid (DA), produced naturally by the diatom Pseudo-nitzschia australis and transmitted to the sea lions via planktivorous northern anchovies (Engraulis mordax), was identified as the probable causative agent. Details of DA analyses for anchovy tissues and sea lion feces are described. Domoic acid levels were estimated in anchovy samples by HPLC-UV, and in sea lion feces using the same method as well as a microplate receptor binding assay, with absolute confirmation by tandem mass spectrometry. The highest DA concentrations in anchovies occurred in the viscera (223 +/- 5 microg DA g(-1)), exceeding values in the body tissues by seven-fold and suggesting minimal bioaccumulation of DA in anchovy tissue. HPLC values for DA in sea lion fecal material (ranging from 152 to 136.5 microg DA g(-1)) required correction for interference from an unidentified compound. Inter-laboratory comparisons of HPLC data showed close quantitative agreement. Fecal DA activity determined using the receptor binding assay corresponded with HPLC values to within a factor of two. Finally, our detection of P. australis frustules, via scanning electron microscopy, in both anchovy viscera and fecal material from sea lions exhibiting seizures provides corroborating evidence that this toxic algal species was involved in this unusual sea lion mortality event.

Sinking rates of fecal pellets from gelatinous zooplankton (Salps, Pteropods, Doliolids)

Sinking rates were determined for fecal pellets produced by gelatinous zooplankton (salps, Salpa fusiformis and Pegea socia; pteropods, Corolla spectabilis; and doliolids, Dolioletta gegenbaurii) feeding in surface waters of the California Current. Pellets from the salps and pteropods sank at rates up to 2 700 and 1 800 m d-1, respectively; such speeds exceed any yet recorded for zooplankton fecal pellets. Fecal pellets of salps were rich in organic material, with C:N ratios from 5.4 to 6.2, close to values for living plankton. The relation between volume and sinking rate indicates that salp and pteropod pellets are slightly less dense than those of pelagic Crustacea; moreover, pellet density varied between different collection dates, probably because of differences in composition. In contrast, doliolid pellets sank at rates up to 208 m d-1, a rate much lower than would be expected from pellet size. Thus, density and sinking rates of pellets are much more variable in zooplankton than would be expected from studies of crustaceans alone. Moreover, the extraordinarily high sinking rates of fecal pellets of salps indicates that these tunicates may be disproportionately important in the flux of biogenic materials during periods when they form dense population blooms.

From sanddabs to blue whales: the pervasiveness of domoic acid

Domoic acid (DA) is a potent food web transferred algal toxin that has caused dramatic mortality events involving sea birds and sea lions. Although no confirmed DA toxicity events have been reported in whales, here we present data demonstrating that humpback and blue whales are exposed to the toxin and consume DA contaminated prey. Whale fecal samples were found to contain DA at levels ranging from 10 to 207microg DA g(-1) feces via HPLC-UV methods. SEM analysis of whale feces containing DA, collected from krill-feeding whales, revealed the presence of diatom frustules identified as Pseudo-nitzschia australis, a known DA producer. Humpback whales were observed feeding on anchovies and sardines that contained DA at levels ranging from 75 to 444microg DA g(-1) viscera. DA contamination of whale feces and fish occurred only during blooms of toxic Pseudo-nitzschia. Additionally, several novel fish species collected during a toxic diatom bloom were tested for DA. Fish as diverse as benthic sanddabs and pelagic albacore were found to contain the neurotoxin, suggesting that DA permeates benthic as well as pelagic communities.

Novel symptomatology and changing epidemiology of domoic acid toxicosis in California sea lions (Zalophus californianus): an increasing risk to marine mammal health

Harmful algal blooms are increasing worldwide, including those of Pseudo-nitzschia spp. producing domoic acid off the California coast. This neurotoxin was first shown to cause mortality of marine mammals in 1998. A decade of monitoring California sea lion (Zalophus californianus) health since then has indicated that changes in the symptomatology and epidemiology of domoic acid toxicosis in this species are associated with the increase in toxigenic blooms. Two separate clinical syndromes now exist: acute domoic acid toxicosis as has been previously documented, and a second novel neurological syndrome characterized by epilepsy described here associated with chronic consequences of previous sub-lethal exposure to the toxin. This study indicates that domoic acid causes chronic damage to California sea lions and that these health effects are increasing.

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.”

Obligate mixotrophy inLaboea strobila, a ciliate which retains chloroplasts

The planktonic ciliateLaboea strobila Lohmann sequesters photosynthetically functional chloroplasts derived from ingested algae. The chloroplasts lie free in the cytoplasm and are most abundant just under the pellicle of the ciliate. The maximum rate of photosynthesis (Pmax) was 925 pg C ciliate-1h-1 (3.7 pg C pg chl.a-1h-1). At saturating irradiance, the amount of carbon fixed h-1 equaled 12.6% of the body carbon of the ciliate. To grow,L. strobila requires both light and algal food. In the absence of food, survival ofL. strobila is significantly longer in the light than in the dark. Based on ingestion rate and photosynthetic rate, we calculate that photosynthesis can make an important contribution to this ciliates carbon budget even when algal food is plentiful.