Sandra E. Shumway

Paralytic Shellfish Toxins in Bivalve Molluscs: Occurrence, Transfer Kinetics, and Biotransformation

This is a critical review of the global distribution, sources of variation in toxicity, anatomical partitioning, metabolism, and detoxification kinetics of paralytic shellfish poisoning (PSP) toxins (carbamate, TV-sulfocarbamoyl, and decarbamoyl saxitoxin derivatives) in bivalve molluscs. Marked interspecific differences in toxin accumulation are related to differences in toxin sensitivity, determined from neurological, physiological, and behavioral responses. Toxicity also varies considerably with body size, immersion time, off-bottom position, and over distances ≤1 km. Bivalve species can be broadly classified as rapid (e.g., Mytilus eduJis) or slow detoxifiers (e.g., Placopecten mageJJanicus). The former takes weeks to detoxify to the regulatory level (up to 15% toxin loss day−1); the latter takes months to years to detoxify (≤3% loss day−1). Toxin biotransformation, which may lead to changes in net toxicity, varies greatly among species. A few clam species, such as Protothaca staminea and Spisula soli...

Particle selection, ingestion, and absorption in filter-feeding bivalves

Abstract Measurements were made of the clearance rate of six bivalve species each in the presence of mixed cell suspensions of the dinoflagellate Prorocentrum minimum (Pavillard) Schiller (clone Exuv), the diatom Phaeodactylum tricornutum Bohlin (clone Phaeo), and the cryptomonad flagellate Chroomonas salina (Wislouch) Butcher (clone 3C). Use of flow cytometry allowed estimation not only of the clearance rate of individual cell types, but also of their proportional occurrence in the pseudofaeces and faeces. It has been recognized that at least three mechanisms of selecting suspended particles may be present in isolation or in combination. These are: (a) preferential clearance on the ctenidia: Ostrea edulis L., for example, preferentially clears the dinoflagellate Exuv compared with similar sized cells of the diatom Phaeo and the cryptomonad flagellate 3C; (b) preingestive selection on the labial palps: the diatom Phaeo was consistently and preferentially rejected in the pseudofaeces of Ensis directus Conrad, Placopecten magellanicus (Gmelin) and Arctica islandica (L.), (c) differential absorption in the gut i.e., post-ingestive selection: of the mixed diet which was ingested, there is clear evidence of a preferential absorption of the cryptomonad flagellate 3C in the majority of the bivalves from which we obtained faecal material. The possibility of selective removal of particular components of the available food resource, especially in the case of our experiments with the cryptomonad flagellate 3C, suggests that such organisms may be quantitatively more important in the diet of bivalves than their relative abundance under natural conditions might lead us to suppose. The ability of the oyster Ostrea edulis to selectively clear the dinoflagellate Exuv from mixed cell suspensions also may have important implications in our understanding of how toxic dinoflagellates may be concentrated on the ctenidia of commercially significant bivalves.

The effects of the toxic dinoflagellate Protogonyaulax tamarensis on the feeding and behaviour of bivalve molluscs

A series of experiments was carried out to assess the effects of the toxic dinoflagellate Protogonyaulax tamarensis on shell-valve activity, rates of particle clearance, preingestive, and postingestive particle selection in seven species of bivalve molluscs from three geographic localities: Maine, Rhode Island, and Spain. The responses observed were species-specific and varied with collection locality. Responses included shell-valve closure and/or siphon retraction (Mya arenaria, Mytilus edulis, Geukensia demissa), reduced rates of particle clearance (M. arenaria, G. demissa), increased rates of particle clearance (Ostrea edulis), production of mucus (M. edulis from Spain and Rhode Island, Placopecten magellanicus, G. dernissa). Mortalities were noted in M. edulis from both Spain and Rhode Island. Two species (Modiolus modiolus and Spisula solidissma) exhibited no effects of the toxic dinoflagellates. Data are also presented for particle selection, clearance and filtration rates for the seven species. It is suggested that species which are periodically exposed to dinoflagellate blooms may have evolved mechanisms permitting them to exploit the toxic organisms as food with no ill effects.

Impact of fouling organisms on mussel rope culture: interspecific competition for food among suspension-feeding invertebrates☆

The clearance rate of natural planktonic assemblages was measured for the blue mussel Mytilus edulis (L.) and a co-occurring fouling community from mussel rope cultures using flow cytometry. Blue mussels had significantly higher clearance rates for all particle types and size classes. In addition, blue mussels showed selective feeding in favor of small phytoplankton (3–5 μm), whereas the solitary ascidian Ciona intestinalis (L.) and the suspension-feeding gastropod Crepidula fornicata (L.) showed preferential selection for large phytoplankton (> 16 μm). Clearance rates for large phytoplankton by these members of the fouling community were, however, always lower than blue mussels. Under conditions where food is not a limiting factor, interspecific competition for food by the associated fouling community should not significantly limit the yield of mussels.

Phycotoxin‐related shellfish poisoning: Bivalve molluscs are not the only vectors

Abstract The continuing increase in numbers of toxic algal species coupled with increased incidences of blooms of these species presents a constant threat to public health worldwide. Traditionally, only filter‐feeding molluscs that concentrate these toxic algae are considered in monitoring programs for paralytic (PSP), diarrhetic (DSP), neurotoxic (NSP), and amnesic (ASP) shellfish poisons; however, increasing attention is being paid to higher‐order consumers such as carnivorous gastropods and crustaceans. This review summarizes data on accumulation of phycotoxins by “non‐target”; species frequently consumed by humans, and stresses the importance of including such species in routine monitoring programs, especially in regions where nontraditional spedes are being harvested.

Site of particle selection in a bivalve mollusc

Bivalve molluscs form dense populations that exert profound effects on the particle loads and phytoplankton composition of coastal waters. It has long been known that bivalves can select among different particle types, including selecting against those of poor nutritional value, but because of difficulties in observing particle transport processes in the pallial cavity in vivo, the mechanism of selection was not known. We now use a combination of video endoscopy and flow cytometry to show that oysters can select living particles from non-living detritus on the gills. Our methods could aid the study of suspension feeding in many animal groups.

Sequestering and putative biotransformation of paralytic shellfish toxins by the sea scallop Placopecten magellanicus: seasonal and spatial scales in natural populations

The seasonal sequestering and elimination of paralytic shellfish poisoning (PSP) toxins in various tissue compartments of wild stocks of the sea scallop Placopecten magellanicus Gmelin were compared for inshore ( mantle > gill > gonad > adductor muscle), although mantles were briefly more toxic than digestive glands in the fall. Differences in toxin composition between scallop populations were not as significant as the intra-population seasonal variation. However, the profile of residual toxin in different tissues of individual scallops revealed differential toxin accumulation. Relatively high toxin levels were found in the early spring, particularly in digestive gland tissue ( > 200 μg STX eq · 100 g−1), suggesting that substantial toxin may have been sequestered through the winter. An increase in the N-sulfocarbamoyl:carbamate toxin ratio between early spring and the previous fall provided circumstantial evidence of new toxin accumulation, although this occurred before major blooms of the toxigenic dinoflagellate Alexandrium typically occur in the Gulf of Maine. The toxin profiles in scallop tissues were found to differ substantially from that of a representative PSP toxin-producing dinoflagellate, Alexandrium tamarense (GT429) isolated from the Gulf of Maine. The major PSP toxins found in scallop tissues were low toxicity N-sulfocarbamoyl (C1C2) derivatives, and highly potent carbamate toxins, including gonyautoxins (GTX1-GTX4), neosaxitoxin (NEO) and saxitoxin (STX). The α-epimers of the C-11 sulfated gonyautoxins and N-sulfocarbamoyl derivatives generally predominated in the scallops, in contrast to the dinoflagellate, where the β-epimers were in higher proportion. The clearest evidence of toxin biotransformation was in the gonads of offshore scallops, where a decrease in the relative amount of toxins C1–C4 and NEO in the spring was followed by a major increase in GTX2GTX3 and de novo appearance of STX. The use of toxin ratios in scallops as indices of toxin transfer and for retrospective analysis of dinoflagellate bloom events were confounded by apparent rapid epimerization and by equilibration of the N-sulfocarbamoyl:carbamate toxin ratio on a shorter time-scale than the sampling frequency.

The effects of anoxia and hydrogen sulphide on survival, activity and metabolic rate in the coot clam, Mulinia lateralis (Say)

Abstract The mactrid clam Mulinia lateralis (Say) shows ephemeral success in colonizing a variety of marine substrata, most commonly “soupy”, reducing muds. Depending on temperature and body size, LT50 values during exposure to anoxia and hydrogen sulphide range from 2 to 11 days, at the lower end of the range reported for infaunal bivalve molluscs. Unlike most bivalves, M. lateralis maintains high levels of feeding, shell valve, and locomotory activities under anoxia, which may be an adaptation to escape periodic burial in unstable, oxygen-deficient sediment. The rate of metabolic heat dissipation under anoxia is the same as under normoxic conditions, which implies a greatly elevated rate of anaerobic glycolysis (Pasteur effect) during anoxic exposure. This may explain the rather short anoxic survival times in this species, and emphasizes its adaptation to short-term as opposed to chronic oxygen deficiency, which may occur in dense deposit-feeding communities from which M. lateralis is excluded.

The effect of fluctuating salinity on the concentrations of free amino acids and ninhydrin-positive substances in the adductor muscles of eight species of bivalve molluscs

Abstract Eight species of bivalve molluscs were exposed both to gradual and abrupt salinity fluctuations and the changes in free amino acids and ninhydrin-positive substances in their adductor muscles measured. In all the species there was an initial rise in the concentration of ninhydrin positive substances when exposed to decreasing salinities. After acclimation for one week (14 cycles) to a 30 % sea-water minimum sinusoidal salinity regime there was no difference in the concentration of ninhydrin positive substances at high and low salinities in the adductor muscles of Mytilus edulis L. Together, the changes in taurine and non-essential amino acids alanine, aspartic acid, glutamic acid, and glycine largely accounted for the changes in the free amino-acid pool. It was found that ‘shell-closing’ mechanisms may result in changes in the free amino-acid pool brought about by reductive amination of Krebs cycle and other keto-acids under anaerobic conditions. It is suggested that ninhydrin-positive substances and free amino acids are used as osmotic effectors in marine bivalves exposed to constantly lowered salinities, but are not used for the same purpose in animals exposed to cyclic salinity changes.

DIVERSE FEEDING RESPONSES OF FIVE SPECIES OF BIVALVE MOLLUSC WHEN EXPOSED TO THREE SPECIES OF HARMFUL ALGAE

Abstract Shell closure and restriction of filtration are behavioral responses by which bivalve molluscs can limit exposure of soft tissues to noxious or toxic agents, including harmful microalgae. In this study, we assessed the clearance rates of five species of bivalve mollusc—the northern bay scallop Argopecten irradians irradians, the eastern oyster Crassostrea virginica, the northern quahog Mercenaria mercenaria, the softshell clam Mya arenaria, and the blue mussel Mytilus edulis—exposed for one hour to each of three harmful-algal strains: Prorocentrum minimum, Alexandrium fundyense, and Heterosigma akashiwo. Clearance rates of harmful-algal cells were compared with clearance rates of a benign microalga, Rhodomonas sp., and to a Mix of each harmful alga with Rhodomonas sp. Qualitative observations of valve closure and production of biodeposits were also assessed during the exposure experiments. Feces and pseudofeces were collected and observed with light and fluorescence microscopy for the presence or absence of intact, potentially-viable algal cells or temporary cysts. Results increase our understanding of the high variation between the different bivalve/harmful alga pairs. Responses of bivalve species to the different harmful algae were species-specific, but in most cases indicated a preferential retention of harmful algal cells, probably based upon different characteristics of the algae. Each shellfish species also reacted differently to the harmful-algal exposures; several remained open; whereas, others, such as oysters exposed to the toxic raphidophyte Heterosigma akashiwo, closed shells partially or totally. Similarly, production of feces and pseudofeces varied appreciably between the different bivalve/alga pairs; with the exception of softshell clams Mya arenaria, intact cells of most harmful-algal species tested were seen in biodeposits of the other four bivalve species. These results extend our understanding of the high species specificity in the interactions between harmful algae and bivalve molluscs and confirm that generalizations about feeding responses of bivalves to harmful algae cannot easily be made. In most cases, however, there was at least some ingestion of the harmful algae leading to exposure of soft tissues to the algal cells.