Anoxic survival potential of bivalves: (arte)facts (2023)

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Volume 131, Issue 3,

March 2002

, Pages 615-624

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The anoxic survival time of the bivalves Chamelea gallina, Cerastoderma edule and Scapharca inaequivalvis from two different ecosystems and differing anoxia tolerances was studied in static (closed) and flow-through systems. The antibiotics chloramphenicol, penicillin and polymyxin were added, and molybdate (specific inhibitor of the process of sulfate reduction). Survival in (near) anoxic seawater of Chamelea was studied in a static system by comparing untreated seawater with autoclaved seawater and untreated clams with clams incubated in well-aerated seawater, containing the broad-spectrum antibiotic chloramphenicol, prior to the anoxic survival test. With untreated clams and natural seawater (median mortality time 2.4 days) a decrease in pH and exponential accumulation of sulfide and ammonium was observed in the anoxic medium, indicating excessive growth of (sulfate reducing) bacteria. In sterilized seawater LT50 (2.1 days) was not significantly different and again considerable amounts of ammonium and sulfide accumulated. However, pre-treatment of clams with chloramphenicol resulted in an increase of LT50 (11.0 days) by approximately fivefold. Accumulation of ammonium and sulfide was retarded, but was finally even stronger than in the medium containing untreated clams. Median mortality times were 2.5 and 2.4 days for Chamelea and 2.7 and 2.9 days for Cerastoderma for static and flow-through incubations, respectively. Addition of chloramphenicol increased strongly survival time in both systems with corresponding values of 11.0 and 16.3 days for Chamelea, and 6.4 and 6.5 days for Cerastoderma. LT50 of Scapharca in anoxic seawater was 14.4 days. Chloramphenicol and penicillin increased median survival time to 28.5 and 28.7 days, respectively, whereas polymyxin displayed no effect (LT50=13.6 days). Molybdate added to artificial sulfate free seawater blocked biotic sulfide formation, but did not improve survival time (LT50=13.7 days). Overall the results indicate that proliferation of anaerobic pathogenic bacteria, firmly associated with the bivalves, is a main cause of death besides lack of oxygen. Bacterial damage is probably caused by injury of the tissues of the clams and not by the release of noxious compounds to the medium.


Knowledge of anoxia tolerance of organisms is important for modeling the impact of poor water quality. Therefore, a large number of studies deal with anoxia tolerance of aquatic invertebrates (von Brand, 1943; Theede et al., 1969; Theede, 1973; Dries and Theede, 1974; Rosenberg et al., 1991; Diaz and Rosenberg, 1995; de Zwaan and Eertman, 1996; Modig and Ólafsson, 1998; de Zwaan et al., 2001a). Theede (1973) observed large differences in anoxia tolerance between lower invertebrate phyla on one hand and arthropods and echinoderms on the other. In general the former groups are very tolerant compared to the latter. Nevertheless, organisms within taxonomic closely related groups might show very distinct capabilities to survive anoxia.

From comparative studies it appears that the cockle Cerastoderma edule (Theede et al., 1969; Hammen, 1976) and the ‘vongole’ Chamelea (Venus) gallina (Brooks et al., 1991) are relatively intolerant bivalves. In physiological and biochemical studies these species have therefore been selected and compared with very tolerant ones. This comparative approach revealed that the following biochemical adaptations contribute to anaerobiosis: (1) maintenance of high reserves of fermentable fuel; (2) mechanisms for minimising metabolic acidosis; (3) alternative end products linked to enhanced anaerobic ATP yield; and (4) metabolic rate depression (Storey and Storey, 1990).

In a closed system without water renewal, proliferation of anaerobic bacteria in the incubation medium may occur with adverse effects on anoxic survival (Felder, 1979; Groenendaal, 1980; Llansó and Diaz, 1994). Sulfide production in static systems is indicated by shell valve blackening (Oeschger and Theede, 1988) and the creation of a distasteful odour (Groenendaal, 1980). Since most (cited) studies about anoxia tolerance have been carried out in (semi-) static incubations, we therefore should doubt whether such literature data represent maximum survival times. For this reason we decided to carry out anoxic experiments with the aim to study possible effects on survival times of bivalves by proliferation of anaerobic bacteria.

First we checked the hypothesis that bacterial interference is caused by the release of noxious compounds, with a main role for sulfide. Sulfide formation depends on sulfate-reducing bacteria (SRB) or decomposition of sulfur containing amino acids of tissue proteins by heterotrophic bacteria. Sulfate is a major ion of seawater, and molybdate is a specific inhibitor of the process of sulfate-reduction. We exposed bivalves species to anoxia and sulfide stress concurrently, in order to establish toxicity of this compound. We subsequently suppressed formation of biotic sulfide by exposing bivalves in artificial sulfate free seawater containing molybdate.

Bacterial growth can be suppressed by antibacterial agents. We added different antibiotics to the anoxic seawater. The antibiotics applied were selected on their mode of action. Penicillin is active against gram-positive bacteria and interferes with the synthesis of the bacterial cell wall. Polymyxin binds to and interferes with the permeability of the bacterial cytoplasmic membrane and acts on gram negative bacteria. Chloramphenicol is a so-called broad-spectrum antibiotic, because it acts both on gram-positive and gram-negative bacteria by interference with bacterial protein synthesis.

Secondly, we checked the hypothesis that bacteria may act directly by injury of tissues of the (weakened) bivalve after prolonged anoxia. We compared different incubation systems (no exchange, regular medium exchange and continuous flow of incubation medium) and studied the effect of chloramphenicol. A continuous flow-through of incubation medium prevents changes in the chemical environment. In case tissue damage by bacteria is a main cause of death the type of incubation will not matter, whereas addition of the antibiotics always should have a positive effect on anoxic survival.

We used a comparative approach in our studies by selecting from very different ecosystems three bivalve species each with differing anoxia tolerances. From the Adriatic Sea (Mediterranean zone) we studied the blue mussel Mytilus galloprovincialis, C. gallina and the blood clam Scapharca inaequivalvis. The first two species are commercially important. The latter, a native of the Indo-Pacific region, is rapidly growing and out-competing native species (Ghisotti and Rinaldi, 1996). In the recent past we selected the same species to carry out an extensive analysis of the physiological and biochemical responses to low oxygen exposure (Brooks et al., 1991; de Zwaan et al., 1991; Thillart et al., 1992). From the Dutch Scheldt estuary (Temperate zone) we selected the Baltic clam Macoma balthica, C. edule and the sea mussel Mytilus edulis. These species serve as prey for fish and shorebirds, are dominant and (except for M. balthica) are commercially important (Bachelet, 1980; Beukema and Meehan, 1985; Ducrotoy et al., 1991).

Here we add new data on C. gallina, S. inaequivalvis and C. edule and discuss the results in context with already published data on these and the other species of our comparative study (Babarro and de Zwaan, 2001; de Zwaan and Babarro 2001; de Zwaan et al., 2001a, de Zwaan et al., 2001b).

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Section snippets


Infaunal C. gallina and S. inaequivalvis were dredged from approximately 10 m depth a few miles offshore near Cesenatico in the Adriatic Sea, Italy. The animals were held in unfiltered natural seawater placed in open baskets suspended in 3000-l polyester tanks at the institute of Cesenatico. The water was well aerated and maintained at ambient seawater temperature by equilibration with the air-conditioned aquarium room. The seawater was pumped in from an inlet approximately 300 m offshore.

C. gallina: sterile seawater and chloramphenicol pre-treatment

Fig. 1a shows that the median survival time (LT50) of C. gallina in natural untreated anoxic seawater was 2.4 days. There was a fast increase of ammonium and sulfide in the incubation water. At day 6, there was 783 μmol/l ammonium and 270 μmol sulfide/l in the water (Fig. 1b). During the incubation period, the pH dropped by 1.2 units (Fig. 1c). When the seawater was sterilized LT50 (2.1 days) was not significantly different (P>0.05), whereas again comparable amounts of ammonium (≤611 μmol/l)


For all three species used in the current studies blackening of the shells was observed when incubated in anoxic seawater under static conditions. In accordance sulfide accumulation could be detected in the incubation medium. In the case of C. edule discoloration did not occur in the presence of chloramphenicol and indeed biotic sulfide formation appeared to be blocked. Similar results were obtained for M. balthica (de Zwaan and Babarro, 2001). In S. inaequivalvis shell blackening was also

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      The Thau lagoon is a Mediterranean coastal lagoon used for shellfish farming. It is periodically affected by anoxia events that trigger oyster mortality. To investigate the effects of an anoxia event focussed on nutrient dynamics and the responses of the microbial planktonic communities a 13-day in situ experiment was performed in September 2020. Transparent mesocosms (270L) were placed at a depth of 4m, inserted in the sediment, and kept closed throughout the experiment. The experiment comprised three treatments: i) Natural environment (N), i.e. in the natural water outside the mesocosms containing a rope of 30 oysters (Crassostrea gigas), ii) Control mesocosm (C) filled with natural water with no oysters, and iii) Oyster mesocosm (O) filled with natural water containing a rope of 30 oysters. Oyster respiration in the oyster mesocosm depleted oxygen after 54h. All the oysters from O mesocosm were dead after nine days and decomposition of their flesh combined with releases from the water-sediment interface increased dissolved inorganic nitrogen (dominated by ammonium), phosphates, and ∑H2S up to 390, 17 and 295μmol·L−1, respectively. Phytoplankton biomass consequently increased by 20 (11.8μg chlal −1) and abundance by 4.5 (186×106 cells·L1) dominated largely by green algae <5μm. During the oyster mortality period (day 6 to day 9) high abundances of heterotrophic flagellates and large ciliate specimens were observed. This shift in the community towards small phytoplankton favours the microbial loop and is detrimental to shellfish farming. In a context of global warming in which the risk of anoxia is higher, the results of the present investigation demonstrate that anoxia triggers shellfish mortality and that the change in the plankton community disrupts the normal functioning of the ecosystem, causing serious financial losses. In this context, it is crucial to predict possible hypoxia and anoxia events using high frequency measurements of dissolved oxygen, by avoiding using shallow zones for oyster production and by reducing shellfish stocks, or by mechanically lifting the oysters out of the water during the night to reduce oxygen respiration in the ecosystem.

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      Deoxygenated water temperatures within both reservoirs was maintained at 22°C using heaters (Eheim Thermocontrol 300 W), a fine-tuned thermostat and a water pump (Hailea HX6530). A flow through system from the reservoirs to experimental tanks was developed to mitigate the effects of excretion, sulphide accumulation, bacterial production and large shifts in tank pH (de Zwaan et al., 2002; Coffin et al., 2021). Daily measurements of water temperature and DO saturation (%) (YSI™ ProODO Optical Dissolved Oxygen meter; resolution 0.1% air saturation (Yellow Springs, Ohio, USA; YSI (2020)) were taken from the top 3 cm of the tank.

      Eutrophication-induced hypoxia is among the most widespread anthropogenically deleterious environmental issues occurring globally in coastal marine environments, contributing to a suite of major stressors on marine organisms. Changes to biogeochemical processes and loss of biodiversity and ecosystem function are symptoms of stressors on aerobic organisms, particularly in estuaries. The response of a species to a single stressor is often very different when compared to exposure in a multiple stressor environment. Using an experimental approach, we tested the sub-lethal and lethal effects of hypoxia and chronic nutrient enrichment on the critical estuarine bivalve Austrovenus stutchburyi. Findings of the present study highlight the cumulative mortality of A. stutchburyi nearly doubled when exposed to elevated ammonia when it was combined with elevated hypoxic stress. A positive feedback loop is hypothesized to explain the result, whereby A. stutchburyi stressed by low oxygen produce and excrete more ammonia waste, increasing their risk of mortality and subsequent lethal ammonia concentrations. Water samples taken across the 45-day experiment support the hypothesis, with ammonia concentrations differing between treatments with bivalves in hypoxic treatments producing more ammonia than normoxic treatments. Siphon activity and respiration rate responses to hypoxic stress also demonstrated the importance of hypoxia as a primary driver of stress responses by A. stutchburyi. These findings highlight the threats to estuarine ecosystems with bivalve populations, whereby, extensive degradation of algal mats results in increased oxygen consumption from microbial respiration, which leads to hypoxia and shallowing of the oxygenated layer. Consequently, chemical reduction in sediments can be associated with an efflux of ammonium into the water column. The experimental results presented here on interactions between stressors highlights the substantial detrimental implications for bivalve populations and subsequent ecosystem functions given increased prevalence of warming and eutrophication in estuaries and coastal environments.

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      These organisms often have a high tolerance to eutrophic conditions compared to other taxonomic groups and have the potential to be used in sediment bioremediation (Vadillo-Gonzalez et al., 2019). Tolerance to eutrophic conditions arises from their unique mechanisms to cope with low oxygen concentrations in sediments (i.e., siphon stretching, anaerobic metabolic pathways or burial depth reduction; De Zwaan et al., 2002; Vaquer-Sunyer and Duarte 2008 and Wright et al., 2010). Eutrophication has also been linked to bivalve mortality and sublethal effects on individual body growth in many coastal environments (Carmichael et al., 2012).

      Eutrophication is an increasing problem worldwide and can disrupt ecosystem processes in which macrobenthic bioturbators play an essential role. This study explores how intraspecific variation in body size affects the survival, mobility and impact on sediment organic matter breakdown in enriched sediments of an infaunal bivalve. A mesocosm experiment was conducted in which monocultures and all size combinations of three body sizes (small, medium and large) of the Sydney cockle, Anadara trapezia, were exposed to natural or organically enriched sediments. Results demonstrate that larger body sizes have higher tolerance to enriched conditions and can reduce survival of smaller cockles when grown together. Also, large A. trapezia influenced sediment organic matter breakdown although a direct link to bioturbation activity was not clear. Overall, this study found that intraspecific variation in body size influences survival and performance of bioturbators in eutrophic scenarios.

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