Pierre Ciret

Evidence for a Plastic Dual Circadian Rhythm in the Oyster Crassostrea gigas

Although a significant body of literature has been devoted to the chronobiology of aquatic animals, how biological rhythms function in molluscan bivalves has been poorly studied. The first objective of this study was to determine whether an endogenous circadian rhythm does exist in the oyster, Crassostrea gigas. The second objective was to characterize it in terms of robustness. To answer these questions, the valve activity of 15 oysters was continuously recorded for 2 mo in the laboratory under different entrainment and free-running regimes using a high-frequency noninvasive valvometer. The present work demonstrates the presence of a circadian rhythm in the oyster Crassostrea gigas. First, oysters were entrained by 12 L:12 D conditions. Then, free-running conditions (D:D and L:L) indicated that the most frequently observed period ranged from 20 to 28 h, the circadian range. That endogenous circadian rhythm was characterized as weak. Indeed, the period (τ) of the individual animals exhibited high plasticity in D:D and L:L, and the animals immediately followed a 4-h phase advance or delay. Additionally, C. gigas appeared as a dual organism: all oysters were nocturnal at the beginning of the laboratory experiment (January), whereas they were diurnal at the end (March). That shift was progressive. Comparison with a full-year in situ record showed the same behavioral duality as observed in the laboratory: the animals were nocturnal in autumn–winter and diurnal in spring–summer. The significant advantage of a plastic and dual circadian rhythm in terms of adaptability in a highly changing environment is discussed. (Author correspondence: d.tran@epoc.u-bordeaux1.fr)

In the darkness of the polar night, scallops keep on a steady rhythm

Although the prevailing paradigm has held that the polar night is a period of biological quiescence, recent studies have detected noticeable activity levels in marine organisms. In this study, we investigated the circadian rhythm of the scallop Chlamys islandica by continuously recording the animal’s behaviour over 3 years in the Arctic (Svalbard). Our results showed that a circadian rhythm persists throughout the polar night and lasts for at least 4 months. Based on observations across three polar nights, we showed that the robustness and synchronicity of the rhythm depends on the angle of the sun below the horizon. The weakest rhythm occurred at the onset of the polar night during the nautical twilight. Surprisingly, the circadian behaviour began to recover during the darkest part of the polar night. Because active rhythms optimize the fitness of an organism, our study brings out that the scallops C. islandica remain active even during the polar night.

High Frequency Non-invasive (HFNI) Bio-Sensors As a Potential Tool for Marine Monitoring and Assessments

Marine ecosystems all over the globe are facing multiple simultaneous stressors including rapid climatic change and increased resource exploitation, such as fishing, petroleum exploration and shipping. The EU-funded DEVOTES project (DEVelopment Of innovative Tools for understanding marine biodiversity and assessing good Environmental Status) aims to better understand the relationships between pressures from human activities and climatic influences and their effects on marine ecosystems. To achieve these goals, it is necessary among others, to test and validate innovative monitoring tools to improve our understanding of ecosystem and biodiversity changes. This paper outlines the application of a high frequency non-invasive (HFNI) valvometer as a potential tool for long-term marine monitoring and assessments. The principle of the method is based on the regular gaping behaviour (closing and opening of the valves) of bivalve molluscs and the fact that physical or chemical stressors disrupt that gaping reference pattern. Bivalve gaping behaviour is monitored in the natural environment, remotely, continuously over a time period of years, requirements that must be fulfilled if bivalve behaviour is to be a useful biomonitoring tool. Here, we review the literature and highlight potential uses of the HFNI valvometry as a biosensor, to monitor and provide early-warning alerts of changes in water quality, such as global temperature increase, releases of contaminants and toxic algal blooms. Finally, potential relevant applications for monitoring and assessing environmental status of marine waters in the context of the Marine Strategy Framework Directive are identified. Relevant descriptors, Criteria and Indicators of Good Environmental Status that might be monitored using the HFNI valvometer are discussed for monitoring bathing beaches and harbours, petroleum installations and aquaculture sites.

The sense of hearing in the Pacific oyster, Magallana gigas

There is an increasing concern that anthropogenic noise could have a significant impact on the marine environment, but there is still insufficient data for most invertebrates. What do they perceive? We investigated this question in oysters Magallana gigas (Crassostrea gigas) using pure tone exposures, accelerometer fixed on the oyster shell and hydrophone in the water column. Groups of 16 oysters were exposed to quantifiable waterborne sinusoidal sounds in the range of 10 Hz to 20 kHz at various acoustic energies. The experiment was conducted in running seawater using an experimental flume equipped with suspended loudspeakers. The sensitivity of the oysters was measured by recording their valve movements by high-frequency noninvasive valvometry. The tests were 3 min tone exposures including a 70 sec fade-in period. Three endpoints were analysed: the ratio of responding individuals in the group, the resulting changes of valve opening amplitude and the response latency. At high enough acoustic energy, oysters transiently closed their valves in response to frequencies in the range of 10 to <1000 Hz, with maximum sensitivity from 10 to 200 Hz. The minimum acoustic energy required to elicit a response was 0.02 m∙s-2 at 122 dBrms re 1 μPa for frequencies ranging from 10 to 80 Hz. As a partial valve closure cannot be differentiated from a nociceptive response, it is very likely that oysters detect sounds at lower acoustic energy. The mechanism involved in sound detection and the ecological consequences are discussed.

How annual course of photoperiod shapes seasonal behavior of diploid and triploid oysters, Crassostrea gigas

In this work, we study if ploidy (i.e. number of copies of chromosomes) in the oyster Crassostrea gigas may introduce differences in behavior and in its synchronization by the annual photoperiod. To answer to the question about the effect of the seasonal course of the photoperiod on the behavior of C. gigas according to its ploidy, we quantified valve activity by HFNI valvometry in situ for 1 year in both diploid and triploid oysters. Chronobiological analyses of daily, tidal and lunar rhythms were performed according the annual change of the photoperiod. In parallel, growth and gametogenesis status were measured and spawning events were detected by valvometry. The results showed that triploids had reduced gametogenesis, without spawning events, and approximately three times more growth than diploids. These differences in physiological efforts could explain the result that photoperiod (daylength and/or direction of daylength) differentially drives and modulates seasonal behavior of diploid and triploid oysters. Most differences were observed during long days (spring and summer), where triploids showed longer valve opening duration but lower opening amplitude, stronger daily rhythm and weaker tidal rhythm. During this period, diploids did major gametogenesis and spawning whereas triploids did maximal growth. Differences were also observed in terms of moonlight rhythmicity and neap-spring tidal cycle rhythmicity. We suggest that the seasonal change of photoperiod differentially synchronizes oyster behavior and biological rhythms according to physiological needs based on ploidy.

Noise pollution limits metal bioaccumulation and growth rate in a filter feeder, the Pacific oyster Magallana gigas

Shipping has increased dramatically in recent decades and oysters can hear them. We studied the interaction between noise pollution and trace metal contamination in the oyster Magallana gigas. Four oyster-groups were studied during a 14-day exposure period. Two were exposed to cadmium in the presence of cargo ship-noise ([Cd++]w ≈ 0.5 μg∙L-1; maximum sound pressure level 150 dBrms re 1 μPa), and 2 were exposed only to cadmium. The Cd concentration in the gills ([Cd]g) and the digestive gland ([Cd]dg), the valve closure duration, number of valve closures and circadian distribution of opening and closure, the daily shell growth-rate and the expression of 19 genes in the gills were studied. Oysters exposed to Cd in the presence of cargo ship-noise accumulated 2.5 times less Cd in their gills than did the controls without ship noise and their growth rate was 2.6 times slower. In the presence of ship noise, oysters were closed more during the daytime, and their daily valve activity was reduced. Changes in gene activity in the gills were observed in 7 genes when the Cd was associated with the ship noise. In the absence of ship noise, a change in expression was measured in 4 genes. We conclude that chronic exposure to cargo ship noise has a depressant effect on the activity in oysters, including on the volume of the water flowing over their gills (Vw). In turn, a decrease in the Vw and valve-opening duration limited metal exposure and uptake by the gills but also limited food uptake. This latter conclusion would explain the slowing observed in the fat metabolism and growth rate. Thus, we propose that cargo ship noise exposure could protect against metal bioaccumulation and affect the growth rate. This latter conclusion points towards a potential risk in terms of ecosystem productivity.

Monitoring Biological Rhythms Through the Dynamic Model Identification of an Oyster Population

The measurements of valve activity in a population of bivalves under natural environmental conditions (16 oysters in the Bay of Arcachon, France) are used for a physiological model identification. A nonlinear autoregressive exogenous (NARX) model is designed and tested. The method to design the model has two parts: 1) structure of the model: the model takes into account the influence of environmental conditions using the measurements of sunlight intensity, the moonlight, tide levels, precipitation, and water salinity levels. A possible influence of the internal circadian/circatidal clocks is also analyzed and 2) least square calculation of the model parameters. Through this paper, it is demonstrated that the developed dynamical model of the oyster valve movement can be used for estimating normal physiological rhythms of permanently immersed oysters and can be considered for detecting perturbations of these rhythms due to changes in the water quality, i.e., for ecological monitoring.