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The nocturnal life of the great scallops (Pecten maximus, L.): First description of their natural daily valve opening cycle [1]

['Elie Retailleau', 'Société D Observation Multi-Modale De L Environnement', 'Brest', 'Arthur Chauvaud', 'Gaetan Richard', 'Delphine Mathias', 'Laurent Chauvaud', 'Laboratoire Des Sciences De L Environnement Marin', 'Lemar', 'Umr Cnrs']

Date: 2023-03 

Valvometry techniques used to monitor bivalve gaping activity have elucidated numerous relationships with environmental fluctuations, along with biological rhythms ranging from sub-daily to seasonal. Thus, a precise understanding of the natural activity of bivalves (i.e., not exposed to stressful environmental variations) is necessary as a baseline for detecting abnormal behaviors (deviations). This knowledge is also needed to reliably interpret observations of bivalve gaping behavior and associated biological processes (e.g., respiration, nutrition) acquired over time-limited periods. With this in mind, we investigated the natural daily gaping activity of the great scallop (Pecten maximus) by continuously monitoring 35 individuals in several individual tanks and in situ (Bay of Saint-Brieuc, Brittany, France) using fully autonomous Hall effect sensors. Our results revealed a circadian cycle (τ = 24.0h) in scallop gaping activity. Despite significant inter-individual variability in mean opening and cycle amplitude, almost all individuals (87.5%) exhibited nocturnal activity, with valves more open at night than during the day. A shift in light regime in the tanks triggered an instantaneous change in opening pattern, indicating that light levels strongly determine scallop activity. Based on the opening status of scallops, we also identified several gaping behaviors deviating from the regular daily pattern (lack of rhythmicity, high daytime opening), potentially reflecting physiological weakness. While further long-term studies are required to fully understand the natural activity of scallops, these findings pave the way for studies focused on the scallop response to external factors and introduce further research into the detection of abnormal behaviors. Coupling observations of diel valve gaping cycles with other daily variations in organismal and environmental parameters could help explain mechanisms driving the growth patterns of scallops observed in their shell striations. From a technical perspective, our field-based monitoring demonstrates the suitability of autonomous valvometry sensors for studying mobile subtidal bivalve activity in remote offshore environments.

Introduction

Bivalves are a class of marine and freshwater mollusks characterized by a shell with two hinged parts (left and right valves) enclosing a soft body [1]. In keeping with a largely sedentary and filter-feeding lifestyle, most species move their valves to perform various vital functions such as respiration and nutrition by ventilating their paleal cavity, expelling feces, and releasing gametes into surrounding waters [2]. For most species, the closure of their valves isolates the soft body from the external environment and confers protection from predators and other threats [1]. Some species, such as pectinids, can perform complex valve movements to bury themselves in sediments, jump, or even swim [3]. Thus, by reflecting routine and discrete behaviors, bivalve gaping activity can potentially be used as a proxy of their biological processes (e.g., respiration, nutrition, reproduction, interaction between organisms) and responses to environmental variations.

The main valvometry methods for measuring valve opening include imaging [4], accelerometry [5, 6], and electromagnetic-based sensors using the Hall effect principle [7, 8] or electromagnetic induction between two electric coils (High-Frequency NonInvasive) [9, 10]. These technologies allow monitoring of the opening state of valves (with a low sampling rate for low-frequency movements) and discrete (i.e., punctual) behaviors such as jumps and closing events (with a high sampling frequency to detect fine-scale movements).

Studies using valvometry sensors have highlighted direct behavioral responses to environmental fluctuations in temperature [11], salinity [12], pH [10, 13] and oxygen conditions [14, 15]. Comeau et al. [11] found that the oyster Crassostrea virginica wakes up (opens valves) when temperatures exceed a certain threshold (0.2 to 4.0°C) and is completely closed below this threshold. A decrease in the seawater salinity leads to a decrease in the valve opening and number of movements in the blue mussels (Mytilus edulis), up to a threshold triggering a complete closure, protecting them from osmotic stress [12]. Bamber [12] explained that the salinity threshold value varies among populations and depends on the mussel’s natural environment and their adaptive evolutionary development. A drastic decrease in pH (6.2) triggers an increase in valve movements in the black clam (Arctica islandica), a subtidal species, likely because of a respiratory response to hypercapnia (buildup of carbon dioxide) [13]. This reaction seems to differ among species since Clement et al. [16] found that pH decreases down to 6.8 did not affect valve gaping of the eastern oysters (Crassostrea virginica). Lab and field studies have shown that eastern oysters respond to severe hypoxia by closing their valves [14, 15]. Behavioral responses (valve movements) also have been reported with exposure to toxic microalgae [8, 17], increased concentrations of suspended particle matter [18] and sedimentation [19], and exposure to low-frequency sounds (<1 kHz) [20, 21].

Based on the current literature, factors that are often associated with discrete events (phytoplankton bloom, storm, maritime anthropogenic activities) appear to induce an increase in discrete movements, particularly closure events. Such responses have been observed for Akoya pearl oysters (Pinctada fucata) exposed to a harmful dinoflagellate (Heterocapsa circularisquama) [8] and for Mediterranean mussels (Mytilus galloprovincialis) [17] and great scallops (P. maximus) [6] exposed to toxic Alexandrium minutum. An increased number of closure events also has been reported for P. maximus in response to high concentrations of suspended particles [18]. Recently, Charifi et al. [20] and Hubert et al. [21] reported that the Pacific oyster (Crassostrea gigas) and the blue mussel (M. edulis) react to low-frequency sound emissions by partially closing their valves.

Besides the direct response to natural or anthropogenic stressors, several studies monitoring gaping behaviors over time, have shown cyclical patterns at different time scales, linked to extrinsic factors [22–24]. Circadian rhythms (periodicity cycle “τ” = 24.0h) in valve gaping, with a clear opening difference between day and night, have been reported for many bivalves, including freshwater and marine species, in various environments from temperate to tropical to Arctic waters. Nocturnal activity (i.e., valves more open at night) has been observed for fresh water mussels (Anodonta anatina and Unio tumidus) [25], Mediterranean mussels (M. galloprovincialis) [26, 27], blue mussels (M. edulis) [7, 28, 29], zebra mussels (Dreissena polymorpha) [30], green-lipped mussels (Perna canaliculus) [31], and Arctic scallops (Chlamys islandica) [32]. Conversely, Schwartzmann et al. [33] showed that the giant clam (Hippopus hippopus) exhibits a circadian cycle with diurnal activity, closing its valves at night. These observed rhythms are mainly driven by the light cycle and result from strategies associated with predation or symbiotic relationships [26, 28, 33]. Nocturnal activity is often considered as a strategy for feeding while minimizing the likelihood of predation [26–28, 34], although the diurnal activity of the giant clam is probably associated with physiological oxidative stress triggered by symbiotic zooxanthellae [33]. Gaping rhythms with annual shifts have been reported for at least two species, the fan mussel (Pinna nibilis) and the oyster C. gigas [22, 23]. Both apparent circadian and circalunar cycles were first observed in the gaping activity of the fan mussel [35]. In a more recent study, Garcia-March [23] found seasonal activity patterns: from mid-July to early November, fan mussels opened their valves based on the position and illumination of the sun and moon, whereas during the rest of the time, gaping activity was directly influenced by current intensity and direction. These findings were supplemented by Hernandis Caballero et al. [24] showing that temperature regulates the switch between these seasonal trends. Oyster gaping activity seems driven by a complex association of solar and lunar cycles, exhibiting circadian and seasonal rhythms with nocturnal activity in autumn–winter and diurnal activity in spring–summer [22, 36]. Mat et al. [22] suggested links among the seasonal observed pattern in C. gigas, food availability, gametogenesis, and metabolic demand.

Thus, numerous relationships between bivalve gaping activity and environmental fluctuations have been elucidated and, as with a wide range of marine organisms, biological rhythms (circadian and others ranging from sub-daily to monthly or seasonal) appear to be common for many species [37, 38].

An accurate baseline knowledge of their natural activity (i.e., activity observed without any stressful environmental variations, generated by natural or anthropogenic factors) [25, 39] is therefore necessary to detect abnormal behaviors (deviation from routine behavior), which is of particular interest to study their behavioral response to external factors or to develop biomonitoring systems (i.e., monitoring bivalve health and detection of abnormal behaviors linked to potential perturbations of its surrounding environment [30, 40–43]). This knowledge is also needed to reliably interpret observations of bivalve gaping behavior and associated biological processes (e.g., respiration, nutrition) acquired over time periods of limited length (study duration shorter than the period of a biological cycle performed by an organism, e.g., less than 24h for an organism performing a circadian cycle).

The present study focuses on the great scallop (P. maximus), a subtidal bivalve (Pectinidae) of great economic importance with a large distribution in the Atlantic NE ocean, from temperate waters (Spain/Morocco) to sub-Arctic waters (North of Norway, Lofoten Island). This bivalve is known to be particularly alert with a developed sensitive system including in particular a remarkable visual acuity thanks to numerous eyes distributed all around the margin of the mantle fold [44–46]. Scallops are also able to realize complex behaviors such as swimming to avoid predators [3]. Although a myriad of aspects of its biology have been studied, including its punctual behaviors (e.g., swimming event, jumps), its gaping activity across periods of several days remains largely unknown. Technological advances have enabled transformation of valvometry sensors into non-invasive, autonomous, and field-deployable monitoring devices. These new tools appear to be particularly suitable for studying the activity of these swimming bivalves in experimental tanks and even in their natural habitat at 40m depth on sandy bottoms.

The aim of this study was to acquire a baseline understanding of the natural valve opening behavior of the great scallop. As a first approach and considering previous studies reporting daily rhythms in the activity of various bivalves, we focused on the gaping state (i.e., valve opening without discrete behaviors) of the scallop on a day-to-day scale. To monitor the daily activity of the scallops, we used recently developed valvometers (Valve-Trek; Technosmart Europe srl, www.technosmart.eu), which are fully autonomous and operate based on the Hall effect principle. A total of 35 scallops were monitored through tank and field experiments. This work is a necessary step for future studies focusing on the effect of environmental disturbances on the behavior of this species.

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[1] Url: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0279690

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