[Advances in Marine Biology] Advances in Marine Biology Volume 22 Volume 22 || Effects of Environmental Stress on Marine Bivalve Molluscs

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  • Effects of Environmental Stress on Marine Bivalve Molluscs

    He Be Akberali

    Departments of Zoology and Botany, University of Manchester, England

    and

    E. R. Trueman

    Department of Zoology, University of Manchester, England

    I. Introduction . . . . . . . . . . . . . . . . . . A. Definition of stress . . . . . . . . . . . . . . B. Occurrence of natural and man-made stresses . . . . . . C. Threshold levels of pollutant stress . . . . . . . . . . D. Development of experimental techniques . . . . . . . .

    11. Behavioural Responses to Stress . . . . . . . . . . . . A. Valve closure as a protective mechanism . . . . . . . . B. Relationship between heart rate, valve movement, and pumping

    activity . . . , . . . . . . . . . . . . .. C. Behavioural response to some pollutant stressors . . . . D. Relevance of valve closure in epifaunal and infaunal species . . E. Effect of subthreshold levels on behaviour . . .. .. F. Effect of temperature on heart rate . . . . . . . . . .

    111. Detection of Stress . . . . . . . . . . . . . . . . A. The significance of registering changes in the environment . . B. Sites of reception . . . . . . . . . . . . . . C. Detection and response to environmental changes . . . .

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    102 102 104 104 105 108 108

    I l l 1 I7 121 128 130 132 132 134 136

    ADVANCES IN MARINE BIOLOGY, VOL. 22 Copyright Q 1985. by Academic Press Inc. (London1 Ltd. All righlr o f reproduction in any form reserved.

    ISBN 0- 12-026122-7

  • 102 H . B . AKBERALI AND E. R . TRUEMAN

    IV. Respiratory Physiology during Stress . . . . . . . . . . Valve closure and cessation of aerobic processes. . . . . . Relationship between heart rate, valve movements, PO>. and pC02

    A. B. C. Anaerobic respiration during valve closure.. . . . . . . D. Valve activity and pH changes . . . . . . . . . .

    V. The Role of the Shell . . . . . . . . . . . . . . A. Physical protection and isolation from environmental stress . . B. Shell closure and calcium reabsorption . . . . . . . . C. Effect of prolonged stress on shell strength . . . . . .

    VI. Action of Heavy Metal Stressors . . . . . . . . . . . . A. Accumulation of heavy metals . . . . . . . . .. B. Effects of heavy metals on tissues . . . . . . . . . .

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    . . 163 C . Effects of heavy metals on released gametes and embryonic and juvenile

    stages . . . . . . . . . . . . . . . . . . . . 168 D. Effects of heavy metals on cellular organelles . . . . . . . . 175

    VII. Conclusions . . . . . . . . . . . . . . . . . . . . 182 References . . . . . . . . . . . . . . . . . . . . 183

    I. Introduction

    A. Definition of Stress

    Concern about changes in the environment and their effect on animals has recently evoked extensive research on Bivalvia based on behavioural, physiological, and biochemical responses at organismal, tissue, or cellular levels. Bayne (1975) offered the following working definition of stress as applied to marine bivalve molluscs: Stress is a measurable alteration of a physiological (behavioural, biochemical, or cytological) steady-state which is induced by an environmental change, and which renders the individuals (or the population) more vulnerable to further environmental change.

    Most adult bivalves are relatively immobile, and any change in the environment of transient, recurrent, or permanent occurrence has to be accommodated by the animal. In the aquatic environment, many low levels of natural or man-made changes are within their normal adaptive range and are tolerated without serious consequences. More extreme changes may be temporarily resisted but can ultimately result in the death of organisms. Between these limits of tolerance and resistance to environ- mental stressors, a region of sublethal response occurs whereby the capa- bility for survival may be reduced as a consequence of the stressor.

    The species used in this article are listed in Table I with their authori- ties.

  • EFFECTS OF STRESS ON MARINE BIVALVE MOLLUSCS 103

    TABLE I. THE LIST OF SPECIES WITH THEIR AUTHORITIES USED IN THIS ARTICLE

    Species Authority

    Anadara s e n i h Anodonta anatina Anodonta cygnea Arctica islandica Cardium (Cerastoderma) edule Cardium (Cerastoderma) gluucum Chlamys opercularis Choromytilus meridionalis Crassostrea commercialis Crassostrea gigas Crassostrea margaritacea Crassostrea uirginica Donax denticulatus Donax juliane = Donax trunculus Donax serra Donax trunculus Helix uspersa Isognomon alatus Ligumia subrostrata Lima scabra Loligo pealii Lolliquneula breuis Macoma batthica Mercenaria (Venus) mercenaria Modiolus demissus Modiolus modiolus Mya arenaria Mytilus californianus Mytilus edulis Mytilus edulis planulatus Mytilus galloprovincialis Mytilus uiridis Neotrigonia margaritacea Ostrea edulis Pecten irradians Pecten maximus Perna perna Pimpehales promelas Pleurobema coccineum Scrobicularia plana Spisula solidissima Tellina fabula Unio tumidus Venerupis decussuta Venus striatula

    Linnaeus Linnaeus Linnaeus Linnaeus Linnaeus Poiret Linnaeus Krauss Iredale and Roughley Thunberg Lamarck Grnelin Linnt Linnaeus Roding Linnaeus Linnaeus Gmelin

    Born Lesueur Blainville Linnaeus Linnaeus Dillwyn Linnaeus Linnaeus Conrad Linnaeus Lamarck Lamarck LinnC Lamarck Linnaeus Lamarck Linnaeus Linnaeus Rafinesque Conrad da Costa Dillwyn Gmelin Philipsson Linnaeus da Costa

    Say

  • 104 H. B. AKBERALI A N D E. R. TRUEMAN

    B. Occurrence of Nuturul and Man-made Stresses

    Bivalve molluscs are found in aquatic habitats ranging from oceanic wa- ters to fresh water. The open marine environment is relatively stable with respect to its physicochemical composition, but in coastal and estuarine habitats significant fluctuations may occur in salinity, temperature, oxy- gen levels, and turbidity. Bivalves may also be subjected to further stresses arising from mans activities, such as off-shore drilling, dredging, or the release of pollutants.

    C. Threshold Levels of Pollutant Stress

    Bivalve molluscs may be either suspension or deposit feeders, and these feeding strategies pose different problems with respect to threshold levels of environmental stress. Suspension-feeding bivalves, e.g., Mytilus edu- lis, Cerastoderma edule, or Anodonta cygnea, filter suspended particles from the water current entering the mantle cavity, whereas deposit-feed- ing bivalves, e.g., Scrobiculuria plana, feed on the sediment surface with long extensible siphons but are also capable of suspension feeding (Hughes, 1969; Earll, 1975b). The principal source of pollutant stress in suspension feeders is from pollutants in solution and associated with sus- pended particles, whereas in deposit-feeding animals the most important source will be the sediment. In Scrobicularia, which is both a deposit and suspension feeder, the uptake of pollutants will be related to both modes of feeding. Different feeding strategies may determine the stressors likely to affect different bivalves; for example, several heavy metals, such as zinc, manganese, cadmium, or selenium, are largely taken up with partic- ulate matter either in suspension or from the sediment, whereas the more acutely toxic metals, such as mercury, copper, and silver, are absorbed most rapidly from solution (Bryan, 1976, 1979). Evidence of significant differential absorption of metals from solution by various tissues has been reported; for example, copper is absorbed from solution about three times more rapidly by the gills and mantle/siphons than by the digestive gland and other tissues (Bryan and Uysal, 1978). The uptake of heavy metals bound to suspended food or inorganic particulate matter is less harmful than direct availability from solution since bound heavy metals have first to be isolated by digestive processes. They may thus be dealt with by metal scavenging systems, such as metallothionein proteins, which have been shown to exist in bivalve molluscs (see Section VI,A). It is also possible that the low toxicity threshold level for mercury and copper is partly related to their direct uptake from the solution. Metals such as zinc and cadmium have a higher toxicity threshold level (Bryan, 1976, 1979)

  • EFFECTS OF STRESS ON MARINE BlVALVE MOLLUSCS 105

    because they are less readily taken up in the free form from the solution. The sensitivity of bivalve molluscs to zinc in, for example, Mya arenaria (Eider, 1977), Mytilus viridis (DSilva and Kureishy, 1978), Mytilus edulis planulatus and Neotrigonia margaritacea (Ahsanullah, 1976), and S. plana (Akberali et al., 1981), in terms of both the threshold for any behav- ioral response and acute toxicity is one order of magnitude lower than the corresponding values for copper in S . plana (Akberali and Black, 1980), M. edulis (Davenport and Manley, 1978), and other bivalve molluscs (DSilva and Kureishy, 1978; Manley and Davenport, 1979). Differences in the threshold levels of response to salinity decline have also been reported in terms of siphonal closure and shell valve adduction, which occur at about 25 and 20%0, respectively, in M . edulis (Davenport, 1979) and S. plana (Akberali and Davenport, 1981).

    D. Development of Experimental Techniques

    The development of electronic and other analytical techniques has led to significant advances in our knowledge of bivalve behaviour. These tech- niques allow continuous monitoring of heart activity and valve move- ments both in the laboratory and under field conditions (Hoggarth and Trueman, 1967; Trueman, 1967; Vero and Salanki, 1969; Trueman et al., 1973; Coleman, 1974; Earl1 and Evans, 1974; Brand, 1976) and have stim- ulated interest in the physiological and biochemical adaptations associ- ated with behavioural changes. Electronic techniques are a considerable advance over previous studies, which involved cutting holes in the shell to observe the heart or the use of a cumbersome system of threads and levers to record valve movements (Koch, 1917; Brown, 1954; Barnes, 1955; Schleiper, 1955; Segal, 1956; Pickens, 1965). To minimize distur- bance to the animals, attempts have been made to observe heart activity without cutting the shell, e.g., in A. cygnea (Koch, 1917) and in M. edulis (Schleiper, 1957), observation of heart activity being made through the almost transparent shell of young individuals. Hers (1943) etched away the outer shell layers of older Anodonta with acid and viewed the heart through the thin, transparent, inner nacreous sheet. Although these modi- fications of the shell hole technique might reduce interference with the animal, the use of direct observation is time consuming and impractical in the field.

    Monitoring of heart activity using the impedance technique developed by Trueman (1967) requires the positioning of electrodes through the shell on either side of the heart. Once the electrodes are properly positioned, the animal need not be disturbed further and recordings can be made remotely, hence facilitating laboratory and field studies. Recordings of

  • 106 H . B. AKBERALI A N D E. R. TRUEMAN

    hydrostatic pressure in the pericardium and electrocardiographs have confirmed that the heart rate is satisfactorily recorded by the impedance technique (Helm and Trueman, 1967; Brand, 1976).

    The impedance technique has been used, both in the laboratory and in the field, to record heart and valve activity of bivalve molluscs and other marine invertebrates in relation to a variety of environmental changes such as tidal exposure (Trueman, 1967; Helm and Trueman, 1967; Col- eman and Trueman, 1971; Coleman, 1972, 1974; Earll, 1975a), feeding (Thompson and Bayne, 1972; Widdows, 1973), temperature fluctuations (Segal, 1962; Trueman and Lowe, 1971; Lowe, 1974; Coleman, 1973, 1974; Parker, 1978; De Fur and Mangum, 1979; Dietz and Tomkins, 1980; Stone, 1980; Davenport and Carrion-Cotrina, 1981), environmental oxy- gen levels (Bayne, 1971; Lowe and Trueman, 1972; Badman, 1974; Brand and Roberts, 1973), salinity (Davenport, 1976, 1979; Akberali, 1978; Akberali and Davenport, 1981), pollution studies (Davenport, 1977; Man- ley and Davenport, 1979; Akberali and Black, 1980; Akberali et al., 1981, 1982b; Manley, 1983), and mantle cavity ventilation (Walne, 1972; Akberali and Trueman, 1979; Davenport, 1979). The relative size of the animals has also been shown to affect heart rate; in general, the heart beat in small specimens is faster than that of larger individuals in similar condi- tions (Pickens, 1965; Earll, 1975a).

    Monitoring of the water-pumping activity of bivalves has also been improved with the development of thermistor flow meters (Heusner and Enright, 1966; Brand and Taylor, 1974; Earll, 1975a,b; Brand, 1976; Fos- ter-Smith, 1976; Akberali, 1978; Parker, 1978; Stone, 1980), although these have yet to be adapted for field recordings. This technique was, however, a great improvement on previous attempts at measuring the water flow through the mantle cavity involving the direct determination of water volumes by the insertion of tubes into the mantle cavity (Galtsoff, 1926, 1928) or the attachment of rubber aprons (Loosanoff and Engle, 1947) which considerably disturbed the animal being monitored. An alter- native approach is the use of indirect particle filtration techniques which have posed a number of problems in the interpretation of the results, for these depend on several assumptions, any of which may not be met during the course of an experiment (Coughlan, 1969). In Pecten irradians after initial clearance on the gills, phytoplankton such as Nitzschia and Chlarny- dornonas may be returned to the suspension (Chipman and Hopkins, 1954). Further doubt on the accuracy of plankton filtration studies has been cast by Hildreth (1980), who observed that considerable amounts of particulate material were produced from the faeces of M . edulis, which may be added to the suspension, resulting in an underestimate of filtration rate on the order of 35%. Furthermore, the flow rate of water across the

  • EFFECTS OF STRESS ON MARINE BIVALVE MOLLUSCS I07

    gills can vary enormously, depending upon experimental procedure (Jergensen, 1966).

    A laser diffraction technique has recently been employed to measure the shell growth of Mytilus when subjected to fluctuating salinity regimes (Gruffydd et al., 1984) or the presence of copper or zinc in the sea water (Manley et al., 1984). This technique appears to be particularly suitable for future laboratory studies of the effect of stressors on shell growth.

    The use of electronic techniques has given further insight as to what constitutes activity in bivalve molluscs. The isolated observation of valve movements or indirect filtration methods led to a widely held inter- pretation of bivalve behaviour as a steady state of continuous feeding and activity (Loosanoff, 1939; Jgrgensen, 1966; Purchon, 1968). Recently, with the development of electronic techniqu...

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