Shellfish as Biosensors

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1		Alexander G. Dvoretsky	--	4728	2023-02-16 04:58:37

This entry is adapted from the peer-reviewed paper 10.3390/fishes8020102

The use of biological objects in monitoring the state of the environment and the changes caused by the impact of environmental pollution on marine and fresh waters is a promising tool due to a lower cost in comparison to traditional monitoring and the ability to receive immediate information about the ecosystem status. Since the mid-1980s, Russian specialists have developed online biomonitoring systems; as in the rest of world, there are two main approaches that are currently applied to study the physiological status of potential biosensor shellfish species and to monitor freshwater and marine systems: valvometry (registration of gaping activity in bivalve mollusks) and photoplethysmography (registration of cardiac activity in mollusks and crustaceans).

biomonitoring biosensors early warning systems photoplethysmography

1. Introduction

The assessment of harmful impacts on the aquatic environment and their effective control and minimization is a key factor in water quality management ^[1]^[2]^[3]. Monitoring efforts started mainly in the 1960s and focused on physical and chemical parameters ^[1]^[4]. Millions of tons of natural and synthetic chemicals have been produced, used, and released into the aquatic environment worldwide without knowledge of their possible environmental impact on recipient ecosystems ^[5]^[6]. Although most of these chemical substances did not have an immediate effect on the structure and functioning of the aquatic systems, the cumulative effects of the total load of pollutants have certainly contributed to environmental shifts ^[1]^[7]^[8].

The realization that anthropogenic chemicals can damage both wildlife and human health has led to the development and implementation of various procedures for testing threat-level concentrations of chemicals, including (a) laboratory toxicity tests that have been modified from conventional medical toxicology and (b) sensitive analytical methods for detecting specific chemicals in water and sediments ^[9]^[10]. Most of these studies have been conducted under controlled laboratory conditions ^[11]. These traditional approaches, however, have a number of serious limitations and cannot provide comprehensive real-time data relating to toxic events in aquatic systems ^[12]. For example, toxicity testing and environmental chemistry do not often provide insights into whether tested organisms are healthy, able to grow and reproduce, or perform their ecological roles ^[13]. The chemical approach cannot account for antagonistic, additive, or synergistic effects that might occur, and chemical data may be lacking for some constituents, particularly reaction products and trace metabolites, i.e., the chemical detection of a compound in water does not always imply that information is obtained about the biologically active form of this compound ^[9]. As the goal of aquatic biological monitoring is to provide reliable and proper information on the possible effects of chemicals present in the water due to human activities ^[14], in order to enable the protection of the aquatic ecosystems, and particularly to give scientific guidance for legislation and enforcement, new approaches using bioindicators or biomonitors (i.e., the biological objects used in monitoring the state of the environment and the changes caused by the impact of environmental pollution on marine and freshwater ecosystems ^[9]) have been developed in the past decades ^[11]^[15].

The in situ use of aquatic organisms as natural monitors provides additional and factual data concerning the present status of and past trends in the environment ^[9]. Instead of direct measurements, the development of biomonitoring methods has resulted in an increased focus on the use of biological effect measures, or biomarkers ^[12]^[16]. Biomarkers are defined as biological responses that signal exposure to anthropogenic chemicals and the adverse effects of these pollutants on health. Biomarkers encompass a huge variety of molecular, cellular, physiological, and behavioral endpoints such as measuring the function of subcellular organelles involved in the detoxification of contaminants, genetic damage, induction of metabolic enzymes, immune function and disease resistance, endocrine disruption, locomotor behavior, as well as circulatory and respiratory physiology ^[9]. The most important biochemical biomarkers include metallothioneins, stress proteins, glutathione transferases, lipid peroxidation, haem, and porphyrins ^[17], while the physiological biomarkers are heart rate, cardiac output, renal and hepatic blood flows, respiration rate, organ sizes, basal metabolism, and rate of cell turnover ^[9]. Behavioral biomarkers include movement, velocity, path changing, and space utilization. When affected, these functions may alter the life span, feeding habits, and even phylogenetic positions of aquatic organisms ^[9]. In most cases, biomarker analyses are less expensive and can be easier to perform than traditional chemical analyses ^[18]^[19]. Furthermore, biomarker responses may persist long after transient exposure to a pollutant that then degrades and is no longer detectable ^[9].

Taking into account an increase in the global pollution load, there is a need for the development of early warning systems ^[11]^[15]^[20]^[21]. The latter (also referred to as online biomonitors, continuous biotests, or biotest automates) use the reactions of selected organisms, especially physiological and behavioral reactions to physical or chemical stress as a sensitive alarm system to detect exposure to contaminants within short exposure times and provide information about possible permit violations and the need for secondary treatment ^[9]^[11]^[20].

In recent decades, many attempts have been made to develop bioassay models that will enable more or less continuous surveillance of water quality with respect to the possible presence of contaminants ^[22]^[23]^[24]^[25]. Most of the model systems consist of flow-through tanks in which aquatic organisms are exposed on a frequent or continuous basis to the water or wastewater being tested ^[26]^[27]^[28]^[29]^[30]. A behavioral or physiological parameter of the organism is monitored by a recording device with the capability of responding to abnormal conditions indicated by the test organism ^[21]^[31].

Continuous biological monitoring systems for river and ocean monitoring have been developed since the 1990s, including novel online sensors ranging from conventional sensors to non-invasive sensor techniques using laser technology and optical sensors ^[32]^[33]^[34]. Russian specialists have also been involved in this process, and there has been significant progress in this field in the past decades.

2. Mollusks as Biomonitors

2.1. Blue Mussels

The first observations of valve movement activity were conducted in 1986 and 1987 in Dalnezelenetskaya Bay and Yarnyshnaya Bay, i.e., in typical coastal areas of the Barents Sea with no pollution ^[35]^[36]. Blue mussels (size 40–50 mm) were collected by hand in the upper and lower littoral and were placed into 4–5 L containers supplied with running seawater (rate 700–1200 mL min⁻¹). These conditions were very close to those in the field ^[37]^[38]. Valve opening levels (VOLs) of the blue mussels tested demonstrated high sensitivity to environmental factors; significant effects were detected for the following changes: 0.1–0.05 °C for water temperature, 0.2 psu for salinity, 0.1 mg L⁻¹ for suspended matter, and 300 cells L⁻¹ for phytoplankton. There was a seasonal pattern in the mussel behavior: in spring and summer, an increase in temperature led to a smooth but expressed decrease in VOL. This result was associated with decreased salinity, which was the main limiting factor for blue mussels. In autumn, the seston concentration was found to be the driving factor of VOL. The detection limit for suspended matter, i.e., the lowest concentration causing changes in VOL, was 0.5–0.6 mg L⁻¹. In winter, there was a direct positive relationship between water temperature and VOL ^[37]^[38].

This pattern was associated with a decrease in concentrations of phytoplankton and organic matter, i.e., less favorable conditions for blue mussels. Resting periods in this species followed vertical gradients in the concentrations of biogenic matter appearing first at 1.5 m depth in August and then registering in the surface layer in September ^[39].

Recordings of gaping and cardiac activity were made simultaneously over a 10 d period from December 2006 to January 2007 under laboratory conditions to reveal possible relationships between VOL and HR using both valvometry and photoplethysmography. Daily HR varied from 0 to 20 beats min⁻¹, averaging 12.6 beats min⁻¹ at 10 °C ^[40]. This level was higher than that of blue mussels from the White Sea at −0.1 °C (5.3 beats min⁻¹) ^[41]. Correlations between VOL and HR were unstable, changing from 0.7 to −0.5 ^[40]. In the first days, when the mussels were not acclimated to rearing conditions, this correlation was positive, while after acclimation, when the duration of resting phases increased, this correlation became negative. The most expressed correlation was found between VOL and variability in HR in the periods when VOL demonstrated substantial fluctuations ^[42]. The author concluded that the feeding conditions were the most important factors driving the cardiac activity in blue mussels under natural conditions. The same conclusion was made for the White Sea blue mussels monitored for their cardiac activity with a photoplethysmograph ^[43]^[44].

Under a Joint project of Murmansk Marine Biological Institute, French Nationals Center of Marine Research, and TOTAL Exploration and Production, a long-term monitoring study based on high-frequency non-invasive (HFNI) valvometery was undertaken for 1 year in Dalnezelenetskaya Bay ^[45]. The HFNI valvometer is a high frequency (10 Hertz), non-invasive biosensor employed to monitor the gaping behavior of bivalves. This device is equipped with a pair of electrodes with 1–1.5 m flexible cables glued onto each half of the mussel shell. The electrodes, designed to minimize disturbance to the bivalve’s behavior, are made up of two resin-coated electromagnets (56 mg each) ^[46]. The use of this technique provided new insights into the biological rhythms and shell opening status of the Barents Sea blue mussels. The authors reported that valve-closing activity was dependent on the tide and light regimes, with largely open valves and few valve movements during high tides and more frequent crossing during daytime ^[45].

Cardiac activity in blue mussels from the White Sea was first studied by Bahmet et al. ^[47]. The authors reported that in sub-littoral individuals, HR was higher than in littoral ones (range 0–0.32 Hz, mean 0.239 ± 0.026 Hz vs. 0–0.25 Hz, and 0.179 ± 0.029 Hz). A decrease in salinity from 25 to 15 psu and an increase from 25 to 35 psu caused a decrease in HR by 80% ^[47]^[48]. Later studies confirmed these findings: HR levels in sub-littoral and littoral mussels were 18.6 ± 1.1 and 13.1 ± 0.5 beats min⁻¹, respectively ^[49]. In contrast, recovery times (T_rec) after salinity stress were 31 ± 2 and 38 ± 1.3 min, respectively ^[49]. However, in some individuals, this parameter reached 2 h ^[50]

Biotesting experiments performed to reveal the effects of 0.001% drilling fluid (0.01 g L⁻¹) on VOL of blue mussels indicated that the duration of the resting phase demonstrated a 400% increase (from 2 to 8 h per day) when the mollusks were exposed to these pollutants for 14 days ^[37]^[51]. An extract of drilling mud at a 10% concentration caused a higher VOL (99%) and higher VOA ^[52]. These results were the first to demonstrate that the Barents Sea blue mussels have promising potential as biosensors to pollutants ^[37]. Similar findings were reported by Hamilton et al. ^[53], who studied the effects of whole drilling mud (concentrations 50–600 mg L⁻¹) on the shell movements of the bay scallop, Argopecten irradians, and found more intensive gaping activity after the exposure.

In terms of early warning detection of pollutants, behavior is a more relevant tool for bioindication, because shifts in VOL and VLC are registered earlier (immediately after exposure) than significant changes in HR (30–60 min after exposure) ^[54]^[55]. For example, under laboratory conditions, the first significant changes in VOL were registered when concentrations of Cu and Cd were 5–10 times higher than their maximum allowable concentrations (MAC, Cu = 1 mg L⁻¹, Cd = 0.001 mg L⁻¹), whereas HR demonstrated significant changes when the MACs were oversubscribed by more than 50–100 times ^[55].

2.2. Black Sea Mussels

A submersible complex on the basis of Hall sensors was used to study typical behavior patterns in Mytilus galloprovicialis. Valve gaping activity was registered in a group of 16 mollusks in an aquatic area of Kazachia Bay, Black Sea, under laboratory conditions ^[56]^[57]^[58]. The authors found a clear 24 h rhythm in valve activity, with the maximal valve opening (6–8 mm, 6.38 ± 0.61 mm or 90–100%) at nighttime and minimal (4–6 mm, 4.67 ± 0.64 mm, 60–70%) during daytime ^[57]^[58]^[59]^[60]. The highest VOL was 10–12 mm. This feature seems to be species-specific because the same rhythm was noted for Mytilus galloprovicialis from other geographical locations as well ^[61]. Trusevich et al. ^[57] detected two movement patterns in the daily rhythm of Mytilus galloprovicialis: (a) short rapid valve closures (amplitude 4–8 mm or 1–2 mm) maintaining excretion and metabolism and (b) slow, very short valve movements maintaining filtration and respiration. Ultradian rhythms in cardiac activity of Mytilus galloprovicialis lasted for 10–30 min were registered using analysis of their plethysmograms ^[62].

Usually, VFL of Black Sea mussels fluctuate from 4–5 to 10 and more closures per min. The mollusks demonstrate immediate valve closure (2–3 s) as a typical response to various stimuli, including tapping the surface of the lab aquarium, sharp sounds, vibration, turning off lights, touching the shell, and changes in water current. The valves remain closed for a few seconds or a few minutes. Frequent repetition of these stimuli leads to less expressed reactions ^[56]^[57]^[58]. Long-term observations detected no seasonal changes in the valve activity despite a smooth drop in water temperature from 22–23 °C in summer to 7–9 °C in winter, suggesting the appearance of feeding activity in this species during the colder season. Furthermore, rapid summer increases in water temperature to 26–28 °C or decreases to 9–17 °C (due to upwelling) led to stress reactions (a decrease in VOA) ^[57]. T_rec, however, was as short as 3–5 h ^[60]. Feeding conditions can also affect the gaping activity. Observations indicated that the period of full valve closure in mussels reared in aerated seawater over a 13 d period increased from 13 to 32% ^[63] and coupled with peaks in gaping activity when the water was renewed and food availability was improved ^[64].

In 2007, cardiac activity of the Black Sea mussels was studied using the photoplethysmography method ^[65]. Daily HR varied from 0 to 20, averaging 15.6 beats min⁻¹. This parameter varied from 8–18 (mean 14.8) beats min⁻¹ at night to 6–19 (mean 13.7) beats min⁻¹ in the morning hours, and to 9–20 (mean 16.2) beats min⁻¹ in the afternoon hours. There were fluctuations in correlations between VOL and HR from 0.5 to −0.7. Slow heartbeat events (3 beats min⁻¹) coincided with the minimum VOL ^[65]. Further studies revealed that mussels exposed to seawater with lower salinity (a decrease from 18 to 12 psu for 20 min) showed increased gaping activity 3 h after the exposure and were completely closed 15 after the exposure. This process was accompanied by an increase in HR from 20 to 28 beats min⁻¹. The initial tachycardia occurred for 30 min after the end of this experiment ^[62].

Chronic stress caused rapid degradation of normal daily rhythm and an increase in the period when the mollusks were fully closed, from 4–6 h per day to 12–18 per day ^[56]. Hydroquinone was found to cause an increase in HR from 16.5 to 21 beats min⁻¹ for 20 min followed by a sharp drop to 4.8–6 beats min⁻¹. T_rec for the cardiac activity and valve-opening activity in this experiment were 3 h 15 min and 12 h, respectively ^[62].

According to valve movement responses, Trusevich et al. ^[66] established that Black Sea mussels are sensitive to the following concentrations of ammonia NH₄OH, copper CuSO₄ * 5H₂O, and sodium lauryl sulfate: 5, 0.1, and 3 mg L⁻¹, respectively. For the latter detergent, this level was corrected to 1.7 mg L⁻¹ thanks to research on cardiac activity ^[66]. Cooper ions were found to decrease HR by 50% in the mussels with T_rec = 3 h ^[67]. According to Ait Fdil et al. ^[68], a 1 h exposure of Mytilus galloprovincialis sampled on the Atlantic coast of Morocco to heavy metals induced a decrease in the time of normal opening and the appearance of sequences of stress behavior, including enhanced valve adductions and complete closure at high concentrations. They concluded that Hg was the most toxic to the valve activity, with a threshold effective concentration of 10 μg L⁻¹, followed by Cu (20 μg L⁻¹), Zn (100 μg L⁻¹), and Cd (2000 μg L⁻¹).

Using valvometry, Russian scientists studied how the Black Sea mussels respond to diesel oil. The mollusks with 55–65 mm shell lengths were reared in aquariums with running seawater ^[69]^[70]. The mussels were exposed for 2 h to a water emulsion of diesel oil at different concentrations. After 2–3 min, there were synchronous 30, 40, and 50% decreases in VOF at diesel oil concentrations of 25, 50, and 500 mg L⁻¹, respectively. At the end of the experiment, VOL decreased to 20–25% at 25 mg L⁻¹ and to 10% at 50 mg L⁻¹, whereas VOL immediately decreased to 10% at 500 mg L⁻¹. After a rapid decrease in VOA, lasting for a few minutes, this parameter was unstable, with periodical valve closures to 2–3% for 3–5 min. Mussels showed rapid recovery in VOA when the exposure was completed, and full recovery to normal rhythm was observed 2–4 h after the end of the experiment ^[69]^[70]. For comparison, the influence of 10 µL L⁻¹ of diesel oil dispersed by the same concentration of the oil slick dispersant SD-25 caused a 50% decrease in HR of Mytilus galloprovicialis from the Adriatic Sea (from 18.7 to 9.1 beats min⁻¹), with a T_rec of 3 h 12 min ^[71]. Similar responses (decreased VCF and VOA) were reported for the brown mussel Perna perna exposed to 5 and 20% diesel water-accommodated fractions ^[72]^[73], and for the Asiatic clam Corbicula fluminea exposed to 28.2% crude oil from the North Sea ^[74]. In contrast, the clam Venus verrucosa collected on the north-eastern coast of Malta demonstrated a higher degree of valve activity after exposure to water-accommodated fractions of crude oil at a concentration of 610 µL L⁻¹ ^[75]. Impaired valve activity in Mytilus galloprovicialis can be induced by other toxicants. For example, Cypermethrin, a widely used pyrethroid pesticide, caused a reduction in the time of normal valve opening in a concentration-dependent manner, with the lowest effect concentration at 100 µL L⁻¹ ^[76].

Analysis of cardiac activity and responses of Black Sea mussels to a drop in salinity from 18 to 9 psu was conducted for individuals collected at coastal sites with different levels of pollution using the photoplethysmographic technique. HR and T_rec varied from 24.4 ± 12.3 to 33.3 ± 7.5 beats min⁻¹ and from 31.7 ± 4.2 to 76.8 ± 9.1 min, respectively, being significantly higher at the site where higher levels of Cu and Pb were registered in the hepatopancreas and gills of the mussels tested ^[77]. At sites with higher levels of nitrates, nitrites, and silicates, T_rec in Mytilus galloprovicialis after a salinity test was significantly higher than that at reference sites ^[78]. Similar results were found for the same species from Boka Kotorska Bay (South Adriatic Sea) ^[79].

2.3. Iceland Scallops

Recording of gaping activity in Iceland scallops was first conducted during June–August 1987. Scallops were collected on Goose Bank at 70–80 m depth and then transferred to the laboratory in Dalnezelenetskaya Bay, where their behavior patterns were registered using valvometry. There were stable fluctuations in VOL (range 50–80%, mean 65%) with periodical attenuation of short rhythms. VCL varied from 18 to 26 closures per day, averaging 23 closures per day ^[80]. During a coastal MMBI expedition in June 2011 in Grøn-fjord (a glacier fjord of West Svalbard ^[81]), Iceland scallops were collected by divers and then placed in aquariums with aerated seawater (temperature 2 °C, salinity 34 psu) ^[82]^[83]. Under constant conditions and without feeding, the scallops demonstrated stable VOL (60 ± 23%) and VCF (12 ± 3 closures per day). The former parameter was close to that of Tridonta borealis (62 ± 10%) but lower than in Mya truncata (75 ± 18%), while there were zero VCL in Tridonta borealis and Mya truncata. The latter two species were concluded to be inappropriate biosensors due to their less expressed reactions to stimuli ^[82]. The same conclusion was made for the horse mussel Modiolus modiolus, which demonstrated a low-level VOA and less expressed fluctuations in VOL (10–40%, mean 25%) ^[80]. The lower VOL and VCF in Iceland scallops from Svalbard waters in comparison to their conspecifics reared in the coastal zone of the Barents Sea are associated with more favorable and less stable conditions in terms of higher food availability and water temperature ^[81]^[82].

Using the HFNI method described above, the joint Russian–French team studied growth patterns in Iceland scallops reared in a monitoring system installed at 16 m depth in Dalnezelenetskaya Bay. As the HFNI valvometry requires gluing of electrodes to each valve and measures the distance between the valves, this technique allows measuring growth increments in mollusks over time. The authors found a continuous growth from March to September, with a 0.4–0.5 μm daily increase in the valve distance. A dramatic decrease was found after the third week of May, indicating a shift in the physiological status of scallops associated with spawning events or changes in water quality ^[45].

There was a complete recovery in respiratory and gaping activity 6 h after the treatment. The study demonstrated that concentrations of diesel oil higher than 5 mg L⁻¹ are detectable by this method ^[40].

2.4. Freshwater Mussels Anodonta

Laboratory research conducted by Sharov and Kholodkevich ^[84] showed that HR in Anodonta anatina from the coastal zone of the Gulf of Finland at rest fluctuated from 8 ± 2 beats min⁻¹ at 16 °C to 22 ± 5 beats min⁻¹ at 26 °C. Ultradian and circadian rhythms were not expressed in this species. After a 24 d rearing period in aquariums, the freshwater mussels demonstrated a decrease in HR by 24%, reflecting adaptation to artificial conditions. Air exposure for 1 h caused a decrease in HR, but T_rec was as low as 1–5 min. Interestingly, the mollusks did not completely close their valves during this test. There was a decrease in HR when the shell length (SL) increased (HR = −0.23SL + 39, R² = 0.84 at 23 °C), and in large individuals (SL > 10 cm) at rest, bradycardia was registered for a few minutes in contrast to smaller mollusks ^[84]. A rapid (during 1–2 min) salinity increase (from 0 to 3 psu) led to increased HR, whereas a decrease in HR was always registered at salinity of 5–8 psu. Lower water temperatures (<7°) compensated for physiological reactions to salt stress, and HR was stable at 0 and 3–8 psu ^[84]. Mollusks at ages 3–6 had the same adaptive potential to unfavorable salinity conditions ^[85]. According to salinity test results (exposure to 6 mg L⁻¹ NaCl for 1 h), T_rec for Anodonta anatina collected at different sites varied from 35 ± 11 to 357 ± 33 following the level of pollution ^[86]^[87]^[88].

The physiological status of Anodonta cygnea from locations with different pollution loads (Rybinsk Reservoir, Borok and the Yagorba River, Cherepovets, Russia) was studied by Kholodkevich et al. ^[89]^[90] using photoplethysmography. After a short-term salinity increase from 0 to 6 psu, HR increased from 12 to 14–16 beats min⁻¹, and T_rec for the specimens from a polluted location (320 ± 17 min) was significantly higher than that for the mollusks from a site with good ecological health (38 ± 6 min). A 1 h exposure of Anodonta cygnea to salinity of 3 psu caused an increase in HR from 12.3 to 18.2 beats min⁻¹. T_rec was 90 ± 18 min ^[91].

2.5. Painter’s Mussels

According to laboratory observations, HR in Unio pictorum at rest varied from 12 ± 3 beats min⁻¹ at 16 °C to 31 ± 7 beats min⁻¹ at 26 °C. There was a positive relationship between log-transformed water temperature and HR ^[90]. For comparison, in the zebra mussel Dreissena polymorpha, HR without stress factors was 15 ± 1 beats min⁻¹ at 20 °C. Like other freshwater mussels, Unio pictorum demonstrated no circadian or ultradian rhythms in cardiac activity ^[49]. Air exposure for 1 h led to a drop in HR and to closure of the valves, but this stress was not critical, and T_rec was 1–5 min. Further laboratory research indicated that, according to HR responses, the critical thermal maximum for Unio pictorum is 35 °C ^[92]. Kuznetsova et al. ^[93]^[94] studied cardiac activity in Unio pictorum and found that mean HR was 18.6 ± 2.8 beats min⁻¹ and variability in the cardiac rhythm was as low as 10%. T_rec after salinity stress (exposure to 6–8 mg L⁻¹ NaCl) was 45 ± 15 min.

The most expressed changes in the gaping behavior of mussels were found for Cu. The negative effects of pollutants intensified substantially in non-flowing water ^[95] but decreased in polluted natural freshwater rich in humic acids ^[96]. For example, toxic effects for Painter’s mussels exposed for 2 h to Pb, Ni, Cd, and Cr were registered at concentrations of 0.6, 2, 0.02, and 1 mg L⁻¹, respectively ^[96], thus indicating that the presence of humic acids in water should be considered when calculating the sensitivity of this biomonitoring system. A decrease in valve gaping activity was reported by Jou et al. ^[97] for the freshwater clam Corbicula fluminea exposed to 19.5 μg L⁻¹ Cu based on a response time of 30 min. Further laboratory studies established that Unio pictorum demonstrates high sensitivity to seawater, acetic acid, and liquid washing powders ^[98].

Another study examined the effects of diesel oil on the behavior of Painter’s mussels reared in 120 L aquariums supplied with running fresh water from the Black River, Sevastopol, at a flow rate of 4 L min⁻¹ ^[99]. The bivalves demonstrated high sensitivity to this pollutant, and detectable reactions occurred at 0.005 mL L⁻¹. The most expressed responses were found for the highest tested level (0.5 mL L⁻¹): the mollusks rapidly increased VOF to 10–20 closures per h and decreased VOA by 40%. Some specimens remained completely closed for the whole exposure period and 8−10 h after the pollutant removal ^[99].

Diclofenac at a concentration of 0.1 µg L⁻¹ caused an increase in HR of Unio pictorum from 17.9 to 20.1 beats min⁻¹ at 25 °C and from 24.9 to 29.5 beats min⁻¹ at 30 °C. This toxicant, at a concentration of 1 µg L⁻¹, increased HR to 19.15 and 27.6 beats min⁻¹, respectively. For the lower concentration, T_rec was 39.5 and 119 min at 25 °C and 30 °C, respectively, while the higher dose resulted in T_rec of 207.8 and 95 min, respectively ^[100]. HR in Unio pictorum was also found to be affected by cyanobacteria: a decrease from 14.3 to 12.9 beats min⁻¹ was registered as a response to exposure to 3.5 ± 0.5 mL L⁻¹. Correspondingly, T_rec increased from 82 to 193 min ^[101]. The effects of toxic microalgae at a concentration of 3500 cells mL⁻¹ were also evident for the oyster Crassostrea gigas. This mollusk demonstrated an increased daily valve-opening duration and micro-closure activity but decreased VOA ^[102].

According to long-term observations, the following criteria were developed to assess the quality status of an ecosystem based on T_rec of Unio pictorum (northern populations) after a salinity test: (a) high (T_rec < 50 min), (b) good (T_rec = 50–70 min), (c) satisfactory (T_rec = 70–100 min), (d) bad (T_rec = 100–200 min), and (e) very bad (T_rec > 200 min) ^[103]^[104].

3. Crustaceans as Biomonitors

3.1. Crayfish

Narrow-clawed crayfish were used as biosensor organisms in the early warning system at St. Petersburg drinking Water Supply Stations based on the photoplethysmograhy method ^[105]. The circadian rhythms of this species represent periodic alterations in HR, with an increase from 35–38 beats min⁻¹ at daytime to 85–87 bats min⁻¹ at nighttime, reflecting the life-history traits of this species associated with nocturnal feeding activity ^[106]. A similar trend in cardiac activity was found for the red claw crayfish Cherax quadricarinatus: during daytime, its HR varied from 50 to 56 beats min⁻¹, while at nighttime, it varied from 121 to 127 beats min⁻¹. The light switch caused an increase in HR of Pontastacus leptodactylus to 126–148 beats min⁻¹ ^[107]^[108].

Pontastacus leptodactylus demonstrated a rapid (1–2 min) two-fold increase in HR from 55 to 120 beats min⁻¹ for 4–5 min as a response to handling. A 2 h air exposure caused an increase in the duration of heart rhythm from 0.80 to 0.99 s and an increase in the mean amplitude from 14.4 to 15.0% ^[109]. Salt stress reactions in narrow-clawed crayfish were studied by Kozák et al. ^[110]. They found that at 100, 400, 800, and 1600 mg L⁻¹ NaCl, only a few specimens demonstrated changes in HR. More expressed responses (an increase in HR from 42–75 to 54–94 beats min⁻¹ and an increase in stress index, SI, from 21–297 to 92–2257 units) were registered for 3200, 6400, 12,800, and 25,600 mg L⁻¹ NaCl. Both HR and SI returned to normal parameters within a few minutes or hours after NaCl addition ^[110]. Although an increase in SI after the salt exposure occurred somewhat later (after 2–4 min) than the immediate increase in HR, SI was concluded to be a more appropriate indicator of the physiological status, due to its much higher variation ^[111].

Kozák et al. ^[112] studied the effects of nitrites on the cardiac activity of narrow-clawed crayfish and found that significant changes in SI and HR occurred at concentrations of 7.5 and 30 mg L⁻¹, respectively. Fluctuations in pH significantly affected HR in narrow-clawed crayfish. Exposure to a low pH (3.4) resulted in an increased HR (115.7 ± 43.8 beats min⁻¹) in comparison to conditions at a normal pH of 6.8 (39.1 ± 3.2 beats min⁻¹) ^[113].

In an early warning system, a rapid salinity increase from 0 to 6.5 psu led to a 30% decrease in HR, and such a response is considered an “alarm” signal ^[114]. In the case of low toxicant concentrations, when a short-term (1–5 min) “sensory response” occurs, the alarm signal is detected if the difference between actual HR and HR at rest exceeds three standard deviations at rest ^[115].

3.2. Red King Crabs

Photoplethysmography was used to study the physiological responses of commercial male red king crabs (carapace width > 150 mm) captured in their non-native area, the Barents Sea. The crabs were transferred to the laboratory of the Russian Federal Research Institute of Fisheries and Oceanography, Moscow, and reared in individual 200 L aquariums supplied with artificial seawater at a salinity of 32 psu and temperature of 5 °C ^[116]^[117].

HR of red king crabs at rest (18–25 bets min⁻¹ at 5 °C) was lower than those in the green crab Carcinus maenas (30–90 beats min⁻¹ at 16 °C) ^[118] and in the pebble crab Gaetice depressus (75–189 beats min⁻¹ at 27 °C) ^[119], probably due to species-specific adaptations ^[117].

Air exposure led to an increase in HR of red king crabs from 30 to 40 beats min⁻¹. Three hours later, HR decreased to 20–25 beats min⁻¹. During the following 20 h, HR smoothly decreased to 15 beats min⁻¹. When the crab was placed into seawater after the end of this 24 h experiment, its HR remained low for 30 min but then increased to 40 beats min⁻¹. SI was 3500 units. During the next day, these parameters varied from 42 to 47 beats min⁻¹ and from 200 to 2000 units, respectively ^[117]. A longer experiment indicated that some red king crabs can endure a 47 h aerial exposure period, but this period was fatal for other crabs ^[117].

As the red king crab is a cold-water species, its cardiac activity can be used as an indicator of stress conditions at high latitudes.

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