Effects of the toxic dinoflagellate Alexandrium catenella on the behaviour and physiology of the blue mussel Mytilus edulis.

The effects of harmful algae on bivalve physiology are complex and involve both physiological and behavioural responses. Studying those responses is essential to better describe and predict their impact on shellfish aquaculture and health risk for humans. In this study we recorded for two months the physiological response of the blue mussel Mytilus edulis from Eastern Canada to a one-week exposure to a paralytic shellfish poisoning producing dinoflagellate strain of Alexandrium catenella, isolated from the St Lawrence estuary, Canada. Mussels in a 'control' treatment were fed continuously with a non-toxic diet, while mussels in a 'starvation' treatment were fed the same non-toxic diet the first week and subsequently starved for seven weeks. Mussels in a 'toxic' treatment received A. catenella for one week before being starved until the end of the experiment. Over a two-month experiment we monitored shell and tissue growth, filtration capacity, respiration rate, byssal attachment strength, valve opening behaviour, and toxin content in tissues. Mussels fed normally on the toxic dinoflagellate and accumulated an average of 51.6 µg STXeq 100 g-1 after one week of exposure. After seven weeks of depuration, about half of the specimen showed levels around 18 µg STXeq 100 g-1. The condition index of exposed mussels ('toxic' treatment) decreased rapidly from the start as compared to mussels that received a one-week non-toxic diet ('starvation' treatment). Oxygen consumption rates increased in the 'toxic' treatment before leveling out with that of mussels from the 'starvation' treatment. Valve opening amplitude was lower in the 'toxic' treatment during and following the exposure. Average valve closure duration was higher right after the exposure, during the peak of mussel tissue intoxication. No significant change in byssal thread strength was observed through time in each treatment but less force was required to detach mussels from the 'toxic' and 'starvation' treatments. The number of byssus threads produced by mussels exposed to the toxic dinoflagellate was also lower than in the control group. These results represent advancements in our understanding of the impacts of harmful algae on bivalves and contribute to the development of mitigation measures necessary to both the safety of consumers and the sustainability of aquaculture operations.

Siltation negatively affects settlement and gaping behaviour in eastern oysters.

While high levels of siltation are known to be deleterious to eastern oysters (Crassostrea virginica), the collective effect of suspended and bedded sediment is understudied from the perspective of oyster farming and bed restoration. In this study, we used laboratory experiments to explore spat settlement rates on a wild bed proxy substrate (i.e., empty shells on the bottom of experimental tanks) in conditions simulating a siltation event and the presence of suspended spat collectors. Using high-frequency valvometry, we also described the behavioural effects of acute sediment burial on wild adult oysters in situ. The vast majority of larvae settled on bottom substrate as opposed to suspended collectors. Sediment negatively affected overall oyster spat settlement on bottom shell, as spat densities were ≈3 × lower when sediment was present. This negative effect was largely attributed to severely depressed spat densities on the upper side (top) of bottom shells. Settlement on the underside of bottom shell was less affected. Wild adult oyster behaviour was negatively affected by acute burial, which ultimately resulted in death. We suggest that the reduction in settlement in the presence of siltation is likely due to the combined effects of suspended sediment on cue detection and bedded sediment on substrate availability. Given that oysters are ecosystem engineers, the negative effects of siltation on both larval and adult oysters can ultimately result in cascading effects to the surrounding biological community.

Sensitivity to oil dispersants: Effects on the valve movements of the blue mussel Mytilus edulis and the giant scallop Placopecten magellanicus, in sub-arctic conditions.

In response to accidental oil spills at sea, chemical oil dispersants are utilized to limit negative impacts on nearby littoral zones. However, current evidence suggests that such dispersants may be toxic to aquatic organisms. Blue mussels (Mytilus edulis) and giant scallops (Placopecten magellanicus) were exposed to different environmentally relevant concentrations of oil dispersant and their behavioural responses were closely monitored using high frequency (10Hz) valvometry. Behavioural valve responses included rapid closures when oil dispersant was added to the experimental tanks. At higher concentrations, the mussels remained closed throughout the exposure period. The giant scallop displayed escape behaviours (clapping) prior to mortality, suggesting toxicity of the oil dispersant. Relationships between different behavioural indicators and oil dispersant concentrations were observed for both species, but with different trends. While scallops demonstrated positive correlations between gaping behaviours and dispersant concentration, mussels exhibited a concentration threshold beyond which the gaping behaviour was characteristic of longer closure periods. This study highlights behavioural response differences consistent with bivalve-specific biological traits: the continuous valve closure of an intertidal species, M. edulis, firmly attached to the substrate, and the escapement behaviours of a semi-mobile subtidal species, P. magellanicus. From these observations, it appears that valvometry could be used as a tool for environmental assessments.

The Mediterranean mussel Mytilus galloprovincialis: responses to climate change scenarios as a function of the original habitat.

The impact of simulated seawater acidification and warming conditions on specimens of the mussel Mytilus galloprovincialis locally adapted to very distinct, widely separated sites in the Mediterranean Sea (Tunisia) and Atlantic Sea (Galicia, NW Spain) was evaluated in relation to key behavioural and eco-physiological parameters. Over the 2-month exposure to the experimental conditions, mussels were fed optimally to ensure that there are no synergistic interactions between climate change drivers and energetic status of the individuals. In general, regardless of origin (Atlantic or Mediterranean), the mussels were rather resilient to acidification for most of the parameters considered and they were able to grow in strongly acidified seawater through an increased feeding activity. However, shell strength decreased (40%) consistently in both mussel populations held in moderately and highly acidified seawater. The observed reduction in shell strength was not explained by slight alterations in organic matter, shell thickness or aragonite:calcite ratio. The combined effects of high acidification and warming on the key response of byssus strength caused a strong decline in mussel performance, although only in Galician mussels, in which the valve opening time decreased sharply as well as condition index (soft tissue state) and shell growth. By contrast, the observed negative effect of highly acidified scenario on the strength of Tunisian mussel shells was (partly but not totally) counterbalanced by the higher seawater temperature. Eco-physiological and behavioural interactions in mussels in relation to climate change are complex, and future scenarios for the ecology of the species and also the feasibility of cultivating them in Atlantic and Mediterranean zones are discussed.

Behavioural responses to predators in Mediterranean mussels (Mytilus galloprovincialis) are unaffected by elevated pCO2.

Ocean acidification is expected to affect marine organisms in the near future. Furthermore, abrupt short-term fluctuations in seawater pCO2 characteristic of near-shore coastal regions and high-density aquaculture sites currently have the potential to influence organismal and community functioning by altering animal behaviour. While anti-predator responses in fishes exposed to elevated pCO2 are well documented, such responses in benthic marine invertebrates are poorly studied. We used high frequency, non-invasive biosensors to test whether or not short term (3-week) exposure to elevated pCO2 could impact behavioural responses to the threat of predation in adult Mediterranean mussels from Galicia on the northwestern coast of Spain. Predator alarm cues (crushed conspecifics) resulted in a prolonged (1 h) reduction in the degree of valve opening (-20%) but had no clear effect on overall valve movement activity, while elevated pCO2 did not affect either response. Our results add to the increasing body of evidence suggesting that the effects of end-of-century pCO2 levels on marine animal behaviour are likely weak. Nonetheless, longer-term exposures spanning multiple generations are needed to better understand how ocean acidification might impact behavioural responses to predation in marine bivalves.

Modelling bivalve culture - Eutrophication interactions in shallow coastal ecosystems.

Assessing the carrying capacity of ecosystems is crucial to the selection of suitable and sustainable locations for aquaculture farms. In Malpeque Bay (PEI, Canada), the potential expansion of mussel farms has driven a series of numerical modelling studies. We coupled sub-models for sea lettuce, wild and cultured oysters and wild softshell clams to an existing ecosystem model to better understand nutrient dynamics and the carrying capacity of Malpeque Bay. Simulations suggested that competition for nutrients between phytoplankton and sea lettuce and filtration by cultured bivalves predominantly mitigate eutrophication effects. The addition of sea lettuce reduced mussel growth by 2% on average and up to 9% near eutrophic estuaries favouring macroalgae growth. Projected new mussel farms reduced current mussel growth by 2% also, suggesting that the carrying capacity of the bay may not be reached yet. Both current and projected aquaculture activities seemed to have limited effects on natural bivalve growth.

Elevated seawater temperature, not pCO2, negatively affects post-spawning adult mussels (Mytilus edulis) under food limitation.

Pre-spawning blue mussels (Mytilus edulis) appear sensitive to elevated temperature and robust to elevated pCO2; however, the effects of these stressors soon after investing energy into spawning remain unknown. Furthermore, while studies suggest that elevated pCO2 affects the byssal attachment strength of Mytilus trossulus from southern latitudes, pCO2 and temperature impacts on the byssus strength of other species at higher latitudes remain undocumented. In a 90 day laboratory experiment, we exposed post-spawning adult blue mussels (M. edulis) from Atlantic Canada to three pCO2 levels (pCO2 ~625, 1295 and 2440 µatm) at two different temperatures (16°C and 22°C) and assessed energetic reserves on Day 90, byssal attachment strength on Days 30 and 60, and condition index and mortality on Days 30, 60 and 90. Results indicated that glycogen content was negatively affected under elevated temperature, but protein, lipid, and overall energy content were unaffected. Reduced glycogen content under elevated temperature was associated with reduced condition index, reduced byssal thread attachment strength, and increased mortality; elevated pCO2 had no effects. Overall, these results suggest that the glycogen reserves of post-spawning adult M. edulis are sensitive to elevated temperature, and can result in reduced health and byssal attachment strength, leading to increased mortality. These results are similar to those reported for pre-spawning mussels and suggest that post-spawning blue mussels are tolerant to elevated pCO2 and sensitive to elevated temperature. In contrast to previous studies, however, elevated pCO2 did not affect byssus strength, suggesting that negative effects of elevated pCO2 on byssus strength are not universal.

Response of Two Mytilids to a Heatwave: The Complex Interplay of Physiology, Behaviour and Ecological Interactions.

Different combinations of behavioural and physiological responses may play a crucial role in the ecological success of species, notably in the context of biological invasions. The invasive mussel Xenostrobus securis has successfully colonised the inner part of the Galician Rias Baixas (NW Spain), where it co-occurs with the commercially-important mussel Mytilus galloprovincialis. This study investigated the effect of a heatwave on the physiological and behavioural responses in monospecific or mixed aggregations of these species. In a mesocosm experiment, mussels were exposed to simulated tidal cycles and similar temperature conditions to those experienced in the field during a heat-wave that occurred in the summer of 2013, when field robo-mussels registered temperatures up to 44.5°C at low tide. The overall responses to stress differed markedly between the two species. In monospecific aggregations M. galloprovincialis was more vulnerable than X. securis to heat exposure during emersion. However, in mixed aggregations, the presence of the invader was associated with lower mortality in M. galloprovincialis. The greater sensitivity of M. galloprovincialis to heat exposure was reflected in a higher mortality level, greater induction of Hsp70 protein and higher rates of respiration and gaping activity, which were accompanied by a lower heart rate (bradycardia). The findings show that the invader enhanced the physiological performance of M. galloprovincialis, highlighting the importance of species interactions in regulating responses to environmental stress. Understanding the complex interactions between ecological factors and physiological and behavioural responses of closely-related species is essential for predicting the impacts of invasions in the context of future climate change.

Bivalve aquaculture-environment interactions in the context of climate change.

Coastal embayments are at risk of impacts by climate change drivers such as ocean warming, sea level rise and alteration in precipitation regimes. The response of the ecosystem to these drivers is highly dependent on their magnitude of change, but also on physical characteristics such as bay morphology and river discharge, which play key roles in water residence time and hence estuarine functioning. These considerations are especially relevant for bivalve aquaculture sites, where the cultured biomass can alter ecosystem dynamics. The combination of climate change, physical and aquaculture drivers can result in synergistic/antagonistic and nonlinear processes. A spatially explicit model was constructed to explore effects of the physical environment (bay geomorphic type, freshwater inputs), climate change drivers (sea level, temperature, precipitation) and aquaculture (bivalve species, stock) on ecosystem functioning. A factorial design led to 336 scenarios (48 hydrodynamic × 7 management). Model outcomes suggest that the physical environment controls estuarine functioning given its influence on primary productivity (bottom-up control dominated by riverine nutrients) and horizontal advection with the open ocean (dominated by bay geomorphic type). The intensity of bivalve aquaculture ultimately determines the bivalve-phytoplankton trophic interaction, which can range from a bottom-up control triggered by ammonia excretion to a top-down control via feeding. Results also suggest that temperature is the strongest climate change driver due to its influence on the metabolism of poikilothermic organisms (e.g. zooplankton and bivalves), which ultimately causes a concomitant increase of top-down pressure on phytoplankton. Given the different thermal tolerance of cultured species, temperature is also critical to sort winners from losers, benefiting Crassostrea virginica over Mytilus edulis under the specific conditions tested in this numerical exercise. In general, it is predicted that bays with large rivers and high exchange with the open ocean will be more resilient under climate change when bivalve aquaculture is present.

Informing Marine Spatial Planning (MSP) with numerical modelling: A case-study on shellfish aquaculture in Malpeque Bay (Eastern Canada).

A moratorium on further bivalve leasing was established in 1999-2000 in Prince Edward Island (Canada). Recently, a marine spatial planning process was initiated explore potential mussel culture expansion in Malpeque Bay. This study focuses on the effects of a projected expansion scenario on productivity of existing leases and available suspended food resources. The aim is to provide a robust scientific assessment using available datasets and three modelling approaches ranging in complexity: (1) a connectivity analysis among culture areas; (2) a scenario analysis of organic seston dynamics based on a simplified biogeochemical model; and (3) a scenario analysis of phytoplankton dynamics based on an ecosystem model. These complementary approaches suggest (1) new leases can affect existing culture both through direct connectivity and through bay-scale effects driven by the overall increase in mussel biomass, and (2) a net reduction of phytoplankton within the bounds of its natural variation in the area.

Byssus attachment strength of two mytilids in mono-specific and mixed-species mussel beds.

The mussel Xenostrobus securis is endemic to the brackish waters of New Zealand and Australia, but has successfully invaded the inner Galician Rías of NW Spain, where it coexists with the indigenous mussel Mytilus galloprovincialis. In this laboratory study, the plasticity of the byssus attachment strength of two mytilids was compared by manipulating substratum, salinity, and bed assembly. M. galloprovincialis showed stronger byssus detachment strength than X. securis, despite lower byssus coverage. Both species responded similarly to the substratum, with substantially lower byssus strength on methacrylate, which offered the lowest surface free energy. Byssus detachment values for M. galloprovincialis were lower at lower salinity. In mixed beds, a number of mussels moved upwards, eventually colonising the upper layers of the assemblage. This behaviour increased byssus strength but only for X. securis. X. securis is adapted to a wide spectrum of abiotic conditions, a trait that may promote its dissemination within estuarine environments.