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EFFECTS OF CHLORINATION ON MYTILUS EDULIS 77

SCI. MAR., 61 (Supl. 2): 77-85 SCIENTIA MARINA 1997

ECOLOGY OF MARINE MOLLUSCS. J.D. ROS and A. GUERRA (eds.)

Effects of low level chlorination on the recruitment,behaviour and shell growth of Mytilus edulis Linnaeus

in power station cooling water*

I.S. THOMPSON1, R. SEED1, C.A. RICHARDSON1, L. HUI2 and G. WALKER1

1 School of Ocean Sciences, University of Wales-Bangor, Menai Bridge, Gwynedd, LL59 5EY, UK. 2 South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China.

SUMMARY: Chlorination procedures are widely used to control biofouling in the cooling water systems of coastal powerstations. However, relatively little is known about the ways in which these procedures affect the ecology of major foulingorganisms such as the mussel, Mytilus edulis. High concentrations of chlorine (8 mg l-1), as sodium hypochlorite (NaOCl),lead to mortality of all planktonic larval stages, while lower concentrations (1 mg l-1), produce changes in the swimming andcrawling behaviour of larvae in experiments conducted in non-flow through systems. The age and growth history of indi-vidual mussels collected from power station culverts were determined from the growth lines present in acetate peels of pol-ished and etched shell sections. During periods of chlorination shell growth is severely reduced resulting in marked changesin shell structure and deposition. Consequently, growth rates of naturally occurring mussels were substantially greater thanthose occurring within the culverts. The information provided by this study, together with an ongoing monitoring pro-gramme of the natural periods of mussel settlement on artificial substrata, is currently being used to develop an appropriatechlorination protocol at Wylfa Nuclear Power Station, North Wales, UK. The use of mussels to evaluate the long-termeffects of low level chlorination is briefly discussed.

Key words: Mytilus edulis, chlorination, sodium hypochlorite, culverts, settlement, behaviour, growth.

RESUMEN: EFECTOS DE LA CLORACIÓN A BAJA CONCENTRACIÓN SOBRE EL RECLUTAMIENTO, COMPORTAMIENTO Y CRECIMIEN-TO DE LA CONCHA DE MYTILUS EDULIS LINNAEUS EN AGUA DE REFRIGERACIÓN DE UNA CENTRAL ENERGÉTICA. – En los sistemasde agua de refrigeración de las centrales energéticas costeras se utilizan por lo general procedimientos de cloración para con-trolar el concrecionamiento biológico. Sin embargo, no se sabe con exactitud la manera en que estos procedimientos afec-tan a la ecología de los principales organismos concrecionantes, como el mejillón, Mytilus edulis. Concentraciones eleva-das de cloro (8 mg l-1) en forma de hipoclorito sódico (NaOCl) producen la muerte de todos los estadios larvarios planctó-nicos, mientras que concentraciones menores (1 mg l-1) producen cambios en el comportamiento de natación y desplaza-miento de las larvas en experimentos realizados en sistemas sin flujo. Se determinó la edad y la historia del crecimiento demejillones recolectados en atarjeas de centrales energéticas a partir de las líneas de crecimiento presentes en réplicas de ace-tato de secciones de la concha pulidas y mordidas. Durante los períodos de cloración el crecimiento de la concha se reducedrásticamente, lo que conduce a cambios notables en la estructura y la deposición de la concha. En consecuencia, las tasasde crecimiento de mejillones que se encuentran en la naturaleza fueron sustancialmente mayores que las de los animales quese encuentran en las atarjeas. La información que este estudio proporciona, junto a un programa de seguimiento, actualmenteen marcha, de los períodos naturales de instalación de mejillones sobre sustratos artificiales, se están utilizando para desa-rrollar un protocolo de cloración adecuado en la Central Nuclear de Wylfa, en Gales del Norte, Reino Unido. Se comentabrevemente la utilización de mejillones para evaluar los efectos a largo plazo de la cloración a concentraciones bajas.

Palabras clave: Mytilus edulis, cloración, hipoclorito sódico, atarjeas, instalación, comportamiento, crecimiento.

*Received November 1995. Accepted October 1996.

INTRODUCTION

Many coastal power stations use seawater intheir cooling systems and consequently both micro-and macrofouling can be a potentially serious prob-lem leading to reduced heat exchange efficiency(Challinor, 1991), reduced water flow (Davis andWhite, 1966; Lynch and Edyvean, 1988) and block-age of the small bore condenser tubes (Whitehouseet al., 1985). In order to counteract this problem,various antifouling procedures have been imple-mented; these include chlorination in the form ofchlorine gas injection, hypochlorite dosing and theproduction of chlorine through electrolytic sources(Whitehouse et al., 1985). The common mussel,Mytilus edulis Linnaeus, is often a major source offouling in temperate coastal power stations and sodi-um hypochlorite is commonly used to minimise lar-val settlement and/or reduce adult shell growth. Inthe British nuclear electric generating industry thestandard practice is to dose continuously at a levelthat achieves a concentration of 0.2 mg NaOCl l-1 atthe entrance to the condensers (Whitehouse et al.,1985). When sodium hypochlorite is added to sea-water there is an immediate demand as chlorinereacts with the organic matter present in the seawa-ter (Khalanski and Bordet, 1980; Grove, 1983); thisis followed by further decay due to mixing, resultingin a lower concentration than that produced by sim-ple dilution (Taylor, C. J. L., pers. comm.). At WylfaNuclear Power Station on the wave-exposed northcoast of Anglesey in North Wales chlorination is ini-tiated when the seawater temperature reaches 12°Cin the summer and stopped when the temperaturefalls below 12°C in the autumn. This protocol hasproved effective in preventing mussel settlement(Pool and Rogers, 1989). However, chlorination isexpensive and by-products of this procedure aretoxic to both marine and freshwater organisms. It isclearly desirable therefore, on both economic andenvironmental grounds, to optimise the use of sodi-um hypochlorite and minimise its impact on thecoastal ecosystem.

The cooling water at Wylfa is abstracted at a rateof 48 m3 s-1 at full load, pumped via an intake cul-vert running under the seabed and wells up into thescreen forebays which house the drum screens(Bamber, 1991). These rotating metal mesh drumsact as filters to remove larger debris and animalsfrom the cooling water. However, the mesh size ofthe drums is too large (10 mm) to remove smallernektonic organisms and plankton (Whitehouse et al.,

1985). From the drum screens the cooling water ispumped through the culverts at a velocity of 1.5-3.0m s-1 to a series of small bore tubes (10 mm diame-ter), the condensers (Bamber, 1991). These con-densers are particularly vulnerable to fouling andonly a few individual mussels are necessary to causecomplete blockage, which could potentially result inthe temporary closure of the whole culvert in orderto allow cleaning. After leaving the condensers thewater is pumped via outflow culverts and dischargedsome 10°C higher into the surrounding coastalwaters (Bamber, 1991).

This paper presents some preliminary data on theeffects of chlorination on the settlement, behaviourand shell growth of Mytilus edulis.

MATERIALS AND METHODS

A monitoring programme was established withinthe power station using KEMA mussel settlementmonitors (Jenner, 1985) to determine the timing ofsettlement of mussel spat at the drum screens and atthe entrance to the condensers. These monitors sim-ulate conditions found within the power station cul-verts in terms of laminar flow and water velocity(Whitehouse et al., 1985). Each monitor holds eightpreviously roughened PVC (polyvinyl chloride)plates (Whitehouse et al., 1985; Pool and Rogers,1989) onto which nylon scouring pads (15.0 × 11.5× 0.8 cm) were attached. These pads (ViledaIndustrial Super Scourer) provide a suitable fibroussurface for the settlement of post-larval mussels(King et al., 1990).

Scouring pads were collected and replaced withnew pads every 2-4 weeks over the period June 1994to August 1995. In the laboratory the pads were jetwashed with freshwater until all the mussel spat hadbeen removed. The washings were sieved through a190 µm sieve and made up to a constant volume.Each sample was then divided into eight subsamplesusing a sample splitter (Jensen, 1982) and the numberof mussels in one of these subsamples counted. Thedata obtained were presented as numbers of musselsper m2. Zooplankton samples were also collected atthe drum screens every 1-2 weeks over the same peri-od of time using an 80 µm mesh plankton net, and thenumber of planktonic mussels counted using themethod described by Newell and Newell (1963).

The behaviour of mussel larvae at two develop-mental stages was observed at selected intervals dur-ing 6 h exposure to various concentrations of sodi-

78 I.S. THOMPSON et al.

um hypochlorite in a non-flow through system. Werecorded the responses of D-shaped larvae and pedi-veligers to two concentrations of sodium hypochlo-rite, 0.98 ± 0.05 SD mg l-1 and 7.71 ± 0.33 SD mg l-

1 (subsequently referred to as 1 and 8 mg l-1 respec-tively). In each treatment 100 larvae were added to3 ml of seawater and the appropriate volume of sodi-um hypochlorite was then added to achieve therequired concentration; these data were not replicat-ed. Three categories of response were used todescribe the behaviour of the mussel larvae: 1) lar-vae actively swimming in the water column; 2) lar-vae lying on the bottom of the experimental con-tainer, but still showing activity, including shellvalve and foot movements; 3) larvae lying motion-less on the bottom of the experimental container. Inorder to study how the dissociation of sodiumhypochlorite in the static system might vary the con-centration during the experimental period of 6 h,readings were taken from two concentrations, 0.98 ±0.05 SD mg l-1 and 2.01 ± 0.06 SD mg l-1 (subse-quently referred to as 1 and 2 mg NaOCl l-1 respec-tively) using a “Nanocolor® PT2”, filterphotometer(Macherey-Nagel, Düren, Germany).

Natural mussel populations are scarce on thewave-exposed north coast of Anglesey, though atWylfa large numbers can be found on the legs of thepower station jetty around low water of spring tides.Random clumps of mussels, each containing 100-400 individuals, were collected opportunisticallyfrom this population either by boat or by SCUBAdivers. Forty to sixty of the biggest individuals fromthis population and from a population growinginside the culverts were aged and their growth ratesdetermined from the seasonal patterns of widely-spaced microgrowth bands which alternate withgroups of narrow bands within the prismatic layer ofthe shell. In order to study these banding patterns,acetate peel replicas were made of polished andetched embedded shell valve sections using themethod previously described by Richardson et al.(1979) and subsequently modified by Plaza andRichardson (unpubl. data). Rather than using 0.01MHCl, the polished shell surfaces were etched in 1%“Decal” (trade name for a histological decalcifyingagent: National Diagnostics, New Jersey, USA). Thegroups of narrow bands in the shells of mussels fromthe legs of the jetty are deposited annually duringthe winter, whilst those formed in the shells of mus-sels from inside the culverts result from the annualperiod of chlorination during the summer. The dis-tance between the umbo and each annually produced

group of narrowly spaced bands was measured fromthe peels using vernier callipers and growth curvesfitted to the data using the von Bertalanffy growthequation.

RESULTS

The occurrence of mussels within the power sta-tion shows a peak of settlement between June andAugust in both 1994 and 1995, though the actualnumbers settling during this period exhibit markedinterannual variation (Fig. 1A). Thus, in July 1994approximately 18,000 mussels m-2 settled comparedto only 3,000 mussels m-2 in July 1995. Minor peaksare also evident, indicating that some settlementactivity can occur more or less throughout the year.These peaks in settlement can be directly related toperiods when mussel larvae are most abundant in thecooling waters of the power station, though once


FIG. 1. – A, Abundance (mean +1 SD) of recently settled mussels atthe drum screens within Wylfa Power Station. B, Occurrence ofplanktonic mussels within the cooling water at the drum screens.Full dots, Drum screen 2; Triangles, Drum screen 3. C, Temperature

of the cooling water.

again both seasonal and annual variations are clear-ly evident (Fig. 1B). Variation in the number ofplanktonic mussel stages also occurred between thetwo intake culverts of the power station (Fig. 1B).Chlorination was initiated either during or immedi-ately following the peak in abundance of planktonicmussels, but before the onset of the major period ofmussel settlement. In 1994 and 1995, chlorinationcommenced when the seawater temperature exceed-ed 12°C (Fig. 1C).

The behavioural responses exhibited by mussellarvae were significantly similar for both D-shapedlarvae and pediveligers (Fig. 2A,B) following expo-sure to the two concentrations of sodium hypochlo-rite (Pearson’s Correlation: r=0.832 and 0.989 for 1mg l-1 and 8 mg l-1 respectively; both at p<0.01,n=10). Correlations were made between the per-centage activity displayed by both sets of larvae ateach concentration, where activity was classed aslarvae swimming and larvae showing movementwhile on the bottom of the experimental container.At the higher concentration of 8 mg NaOCl l-1, nosigns of activity were observed after approximately1 h exposure and no recovery was evident after 6 h.At the lower concentration (1 mg NaOCl l-1) the

number of larvae that were either swimming ormoving on the bottom fell to a minimum afterapproximately 1 h of exposure, following whichthere was a period of recovery so that after 6 h theactivity of D-shaped larvae had returned to a levelsimilar to that at time zero; the pattern of recoveryof pediveligers, however, was less marked. Both theD-shaped larvae and the pediveligers showed a sig-nificant difference in behavioural response to 1 mgl-1 as compared to 8 mg l-1 of sodium hypochlorite(Sign test p<0.01 for both D-shaped larvae, n=10and pediveligers, n=11).

The dissociation of sodium hypochlorite in fil-tered seawater over a period of 6h is illustrated inFigure 2C. At 1 mg l-1, there is a reduction in con-centration of 77.2%, whilst at 2 mg l-1, dissocia-tion results in a reduction of 84.9%. These figurescan only be taken as an approximation for the rateof dissociation, due to the slight variability of thestock solution of sodium hypochlorite used andthe conditions under which the chemical had beenstored.

Acetate peel replicas of shell sections of musselscollected from the power station culverts (Fig. 3B),unlike those from the naturally occurring population(Fig. 3A), show only a very faint banding patternand in areas all that is visible is the crystalline struc-ture of the shell. However, during the periods ofchlorination, prominent dark bands alternating withclearer bands were deposited as a result of reducedgrowth when the shell valves remain tightly closed(Fig. 3C,D). Thus, shell growth of culvert mussels isseverely reduced during the summer months at atime when growth in naturally occurring temperatewater mussel populations should be at its highest.Using these chlorination growth checks, the age ofindividual mussels from the culverts can be deter-mined and the period of the year when they settledestimated, thus allowing growth over time to be cal-culated. The marked reduction in the rate of shellgrowth during periods of chlorination, as comparedto that during non-chlorination periods, is clearlyevident in Figure 4.

Figure 5 compares the growth of mussels fromthe culvert population (B) with those of the naturalpopulation from the jetty legs (A). Growth rates ofmussels from the natural population were muchfaster than those from the culvert population; thusafter four years, mussels from the natural populationmeasured approximately 47 mm in shell lengthwhereas those from the culverts only measuredaround 30 mm. However, it is somewhat unusual to


FIG. 2. – Behavioural responses (% activity), of: A, D-shaped lar-vae, and B, pediveligers, on exposure to two concentrations of sodi-um hypochlorite. In all treatments n = 100. C, Dissociation of two

concentrations of sodium hypochlorite.


FIG. 3. – Photomicrographs of acetate peel replicas of radial shell sections of M. edulis showing microgrowth banding patterns in the pris-matic layer (PL) of the shell. All scale bars = 100µm. A, Shell section of a mussel from the Menai Strait to show the clear pattern of semi-diurnal tidal bands; Gb, growth band. B, Shell section of a mussel from the power station culverts during a period of non-chlorination; P,periostracum on the external surface of the shell. C,D, Shell sections of mussels from the power station culverts during a period of

chlorination; Gi, growth increment; C, cleft in shell.

FIG. 4. – Growth in shell length of mussels in the power station culverts. Values are means +1 SD.

find mussels over two years old in the culverts asthese are drained for cleaning and inspection everytwo years. Nevertheless, some residual seawater isinevitably left in the bottom of the culverts allowinga few mussels to survive this period when the cool-ing water system is temporarily closed.

DISCUSSION

On the Welsh coast spawning in Mytilus edulishas been reported between March and Augustalthough maximum spawning activity typicallyoccurs during April and May (Seed, 1975).Although we have not monitored the reproductivecycle of mussels in the vicinity of Wylfa, the appear-ance of large numbers of mussel larvae in the plank-ton during June (Fig. 1B) is wholly consistent witha predominantly spring spawning. Mussel larvaeusually remain in the plankton for 2-4 weeks but thiscan vary according to temperature, food supply andthe availability of a suitable settlement surface and

in some cases ten weeks or more can elapse betweenfertilisation and the settlement of post-larval mus-sels (Seed and Suchanek, 1992).

The marked seasonal abundance of small mus-sels on filamentous algae reported by Bayne (1964)was not observed by Seed (1969) on wave-exposedrocky shores in north-east England where high den-sities of mussels persisted throughout much of theyear. In the latter study, filamentous algae, togetherwith other algal species, seemed to provide anextensive reservoir of young mussels, many ofwhich could be migrating onto the adult beds moreor less throughout the year, thus accounting for thesporadic and often unpredictable pulses of recruit-ment that characterise many natural populations ofMytilus. In some populations, however, post-larvalmussels do appear to settle directly onto adult bedswithout an initial phase on filamentous substrata(McGrath et al., 1988; Lasiak and Barnard, 1995).At Wylfa, mussels settled on the artificial filamen-tous surfaces mainly during July, albeit with smallerintermittent pulses throughout the summer andautumn (Fig. 1A). Chlorination was initiated duringor shortly after the appearance of the first peak ofmussel larvae in the plankton; in 1994 and 1995,chlorination commenced when the seawater temper-ature exceeded 12°C, and continued whilst the tem-perature remained above this level (Fig. 1C).

Both D-shaped larvae and pediveligers respond tosodium hypochlorite by shell valve closure, thuseffectively isolating their body tissues from theexternal environment. At high concentrations ofsodium hypochlorite, (≈8 mg l-1) all larvae were deadafter six hours and had probably died within one hourof exposure, but at lower concentrations (≈1 mg l-1)larvae began to recover after being exposed for aperiod of 40-70 minutes. This recovery started earli-er, and was more sustained amongst the D-shapedlarvae (Fig. 2A) than amongst the pediveligers (Fig.2B) suggesting that the different developmentalstages of Mytilus are differentially susceptible tohypochlorite. Roberts et al. (1975) showed that juve-nile stages of oysters, Crassostrea virginica, andclams, Mercenaria mercenaria, were typically moreresistant to hypochlorite than the larval stages, whilstRoosenburg et al. (1980) found that pediveligers ofC. virginica, were generally more resistant tohypochlorite than straight-hinged larvae, especiallywith increasing exposure time. Recovery of musselsis presumably possible because sodium hypochloritein seawater dissociates over time, and at lower initialdosages the concentration soon falls to a level that is


FIG. 5. –. Length at age data for: A, the mussel population on thelegs of the power station jetty (adapted from Plaza and Richardson,unpubl. data.), and B, the population from within the power stationculverts. Curves fitted using the von Bertalanffy growth equation.

less toxic to the larvae. Thompson and Richardson(1993) found that cockles, Cerastoderma edule,exposed to approximately 25 mg l-1 sodiumhypochlorite for 8 h in a non-flow through system,exhibited increased shell valve activity during theperiod of exposure and attributed this to hypochloritedissociation. However, Khalanski and Bordet (1980)showed that mussels (M. edulis and M. galloprovin-cialis) continuously exposed to hypochlorite at aconstant level (0.2-1.0 mg l-1), a situation whichmore closely simulates the conditions within thepower station cooling waters, led to 100% mortalityover a period of 15 to 135 days.

Internal growth patterns present in polished andetched sections of bivalve shells have been usedextensively to investigate their age and growth rate(Richardson, 1993). Semi-diurnal microgrowthbands are clearly observed in the prismatic layer ofthe shells of mussels collected at the extreme lowwater mark of spring tides from the jetty legs of thepower station. Dark bands formed each time themussel is emersed during low tide provide a recordof the daily (tidal) and seasonal pattern of musselshell growth (see also Richardson, 1989). Shell sec-tions revealed a clearly marked annual pattern in thedeposition of the tidally-induced bands, with groupsof these narrowly spaced bands representing periodsof reduced linear growth, produced each year as aresult of lower seawater temperatures and decliningfood supplies in the autumn and winter. During thesummer, however, when feeding conditions arefavourable, these tidal bands are widely spaced. Thedistinct groupings of narrowly spaced bands can belocated along the length of the shell and used todetermine the age of the mussel, and hence rates ofshell growth (Richardson et al., 1990). In theabsence of emersion, a weak pattern of banding isobserved in mussel shells which has been shown tobe related to an endogenous rhythm of shell deposi-tion (Richardson, 1989). Mussels collected fromwithin the culverts experienced continuous submer-sion and were subjected to a consistent high veloci-ty current flow providing a constant nutrient supplythroughout their life, favourable conditions for rapidshell growth (Rajagopal et al., 1991).

Banding patterns in the shells of the culvert mus-sels were poorly defined, whilst in some areas of theshell they appeared to be totally absent.Nevertheless, at several locations along the length ofthe shell, groups of clearly defined bands weredeposited. These bands are the result of exposure tothe annual summer chlorination dosing period and

are thought to be formed when the shell valves closetightly in response to this exposure. During periodsof prolonged shell valve closure, it is known thatbivalves respire anaerobically leading to decalcifi-cation of the newly deposited shell (Crenshaw,1980; Lutz and Rhoads, 1980) or an alteration in therate of shell mineralisation (Deith, 1985). The for-mation of clearly marked banding patterns is thus arecord of how securely the shell valves remainedclosed, effectively isolating the body tissues fromthe external environment. At Wylfa Power Station,the practice of chlorination is a regime of continuouslow level dosing at approximately 0.2 mg l-1; how-ever, under normal operating conditions, chlorina-tion must occasionally be interrupted to meet certainlegal requirements for discharges. Consequently,mussels probably experience hypochlorite-free peri-ods during chlorination dosing allowing them toopen their shell valves for short periods to respireaerobically, feed and recommence shell deposition.These breaks in chlorination may account for thetolerance and survival of mussels to periods ofhypochlorite exposure in excess of four months. Thesequence of growth bands deposited in the musselshells during chlorination, dark prominent growthbands alternating with clearer growth increments,presumably reflects a sequence of hypochloriteexposure and interruption to the supply.

The overall effect of chlorination is to deter set-tlement of the post-larval mussels and slow thegrowth rate of any mussels which do settle.Exposure to these non-lethal levels of sodiumhypochlorite, resulting in closure of the valves, leadsto a marked reduction in shell growth (Khalanskiand Bordet, 1980). Valve closure results in reducedfeeding time, and hence reduced formation of shellmaterial; consequently, any prolonged interruptionto normal feeding activity will lead to reducedgrowth rate (Seed and Suchanek, 1992). In the cul-vert mussels this reduced rate is particularly obviousduring the summer months when chlorination coin-cides with increased seawater temperatures and thusoccurs at a time when growth is at a maximum fornatural temperate water populations of mussels andother bivalves (Richardson, 1989; Richardson et al.,1980). Growth rate of adult mussels is reduced onexposure to various concentrations of sodiumhypochlorite, though the concentrations producingreduced growth and/or mortality vary greatly in theliterature (Blogoslawski, 1980; Khalanski andBordet, 1980; Lewis, 1983). Larval and juvenilestages appear to be even more sensitive to exposures


to hypochlorite than adult stages (Blogoslawski,1980; Lewis, 1983). Analysis of the banding pat-terns from the shells of culvert and jetty-leg musselpopulations has allowed their growth to be assessed.It appears that chlorination reduces the growth of themussels within the culverts by approximately onethird, thus indicating that even under ideal growthconditions, low level continuous chlorination isachieving its objective of reducing mussel growth.The ability of mussels to incorporate within theirshells an historical record of their growth thus hasuseful applications in assessing the efficiency ofchlorination procedures within power station cool-ing water culverts.

In this study we have demonstrated that musselssurvive and grow, albeit more slowly, when exposedto low levels of hypochlorite (0.1-0.2 mg l-1), andthat there are periods during the dosing regime whenthe mussels can apparently recover and deposit shellmaterial. Banding patterns in mussel shells fromboth the cooling water culverts and natural popula-tions in close proximity to power stations can there-fore be analysed to determine the impact of chlori-nation procedures.

ACKNOWLEDGEMENTS

We are grateful to Wylfa Power Station, NuclearElectric plc., for the provision of a research grant(WYE/14165) to C.A.R., R.S. and G.W.. We arealso indebted to Roger Lunt (Station Chemist, WylfaPower Station) for his commitment, enthusiasm andencouragement during the course of this research.L.H. is grateful for support provided through a tri-partite educational link between University ofWales, Bangor, Hong Kong University and SouthChina Sea Institute of Oceanology.

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