1969_morton_studies on the biology of dreissena poltmorpha pall ii. correlation of the rhythms of...

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PTOC. malac. Soc. Land. (1969) 38, 401 .

STUDIES ON TH E BIOLOGY OFDREISSENA POLTMORPHA PALL

II . CORRELATION OF THE RHYTHMS OF ADDUCTORACTIVITY, FEEDING, DIGESTION AND EXCRETION

BRIAN MORTONDepartment of Zoology, Chelsea College of Science and Technology,

University of LondonI N T R O D U C T I O N

The concept of a continuous and simultaneous process of filtering, feeding anddigestion in filter-feeding bivalves is generally accepted, indeed, th e evolution ofthe crystalline style has been deemed to be a significant adaptation to this mode oflife, providing a continuous supply of extra-cellular enzymes in the lumen of thestomach. A growing mass of evidence, however, suggests that this view may notalways be true.

Marceau (1906, 1909) demonstrated that many bivalves have rhythms of adductoractivity and quiescence. Anodonta, Ostrea, Unio, Tapes, Venus and Cardium havingperiods of phasic adduction, followed by periods of time when th e shell valvesremained shut, whilst Lutraria, Mya and Solen had similar periods of activity followedby periods when the shell valves gape and remain quiescent. Loosanoff and Nomejko(1946) found that Crassostrea virginica kept its valves open for 90% of the timewhen living under natural conditions. Rhythmic variation in activity without inter-vening periods of complete rest has been described by Rao (1954) in Mytilus cali-fornianus and M. edulis. Hopkins (1937) reported that at naturally occurring tempera-tures Ostrea lurida was open for 20 hr/day and Crassostrea virginica for 10-14 hr.For several species of bivalves lengthy periods of interruption of water propulsionhave been reported in the literature, and to the list given by Verwey (1952) can beadded Venus mercenaria (Bennett, 1954) and Hyridella australis (Hiscock, 1950).Rhythmicity in oxygen uptake under laboratory conditions has been reported forMytilus californianus (Rao, 1953) and Ostrea virginica (Brown, 1954). RecentlySalanki (1966) has demonstrated a daily rhythm of adductor activity and quiescencein Pecten jacobaeus and Lithophaga lithophaga which can be regulated by changesin light and dark. Present records show that Dreissena polymorpha, Unio pictorum,Anodonta cygnea, Glycymeris glycymeris, Venus fascidta, Cyprina islandica, Ostreaedulis and Mya arenaria have alternate periods of phasic adductor activity and ofquiescence.

J. E. Morton (1956) showed that th e bivalve Lasaea rubra possessed a regularfiltering, feeding an d digestive rhythm, th e phases of which he related to the tidal

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4 0 2 P R O C E E D I N G S O F T H E M A L A C O L O G I C A L S O C I E T Yrhythm. Many workers consider Lasaea to be atypical in this respect, its habit ofliving high in the intertidal zone being unusual. The results of present work onDreissena polymorpha raises th e possibility that Lasaea may not be atypical inpossessing such a rhythm and that the alternate rhythms of phasic adduction andquiescence exhibited in other bivalves may be similarly related to a digestive rhythm.T H E R H Y T H M O F A D D U C T O R A C T I V I T Y A N D Q U I E S C E N C E

IN DREISSENA POLYMORPHAIndividual specimens of Dreissena were placed in the apparatus shown in Fig. 1.Usually Dreissena rapidly attached itself by means of new byssal threads to theshelf of the apparatus. The upper ends of the two arms were connected by a waxedthread (ABC). The mid point (B), of this thread was attached by another thread(BD) to a heart lever, writing on a smoked kymograph drum, rotating at a speed of

FIG. 1. Th e apparatus used to record the adductor activity of Dreissena polymorpha in aquaria.For exp lanation see text.

1 rev/week. The apparatus, in a 500 ml beaker was then placed in an aquariumthrough which water circulated. As the shell 'valves gaped or closed so the armsof the apparatus were pushed ap art or came together, thereby causing a correspondingrise or fall of the writing lever. Fig. 2 shows a typical kymograph record. Activityof over 50 specimen weeks was recorded in this way. Animals generally took 2-3 daysto settle down in the apparatus, probably due to movements involved in byssal



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MORTON: DAEISSEJVA POLTMORPHA. II 403attachment. Thereafter they exhibited regular alternate periods of activity andquiescence. D uring the period of quiescence the valves were almost fully adducted,whilst during the period of activity, the valves gaped most of the time, bu t under-went phasic adductions from time to time. O n average a period of activity lastedfor approximately 12 hr, and a period of quiescence also lasted for 12 hr. Th e periodof adductor activity invariably occurred at night; Salanki (1966) has reported asimilar behaviour pattern in Lithophaga.

FIG. 2. Part of a typical kymograph record of the activity of Dreissena polymorpha obtained byuse of the apparatus shown in Fig. 1. The time scale at the bottom of the record is in hours.Anodonta possesses a rhythm of adduction that is maintained by impulses fromthe cerebral ganglia, and shows a highly variable number of phases of activity inthe course of a week (Barnes, 1955, 1962). This suggests that Anodonta possesses arhythm of addu ctor activity tha t is not attributable to rhythms of the external environ-ment . Dreissena on the other hand possesses a loosely based circadian rhythm.

FILTER FEEDING IN DREISSENA POLYMORPHAThe process by which particulate material reaches the mouth of Dreissena has beenpreviously described (B. S. Morton, 1969). On to this process must be superimposedthe consequences of the rhythmical pattern of adductor activity.During th e period of activity contraction of the addu ctor muscles, particularly th eposterior, expels water from the infra-branchial and supra-branchial chambers viathe inhalant and exhalant siphons respectively. This action also expels faeces andpseudofaeces. With the relaxation of the adductor muscles the elastic ligament forcesthe shell valves apart causing more water, rich in oxygen and food material, toenter the mantle cavity via the inhalan t siphon. Durin g the period of adductor activitythe anima l is also filtering p articles of food material, suspended in the inhalant stream.



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404 PROCE EDING S OF THE MALACOLOGICAL SOCIE TYIt follows that the pumping action described above, may augment the rate of collectionof. food particles.

During the quiescent phase, the shell valves are seen on close inspection to be about1 mm apart, with both siphons retracted, so that no water can enter the mantlecavity. It seems logical to assume that during the quiescent phase little or nofiltration of particulate material from the water is taking place, and that filtrationis the function of the active phase of the rhythm. It may be that during the quiescentphase the mouth closes (as has been observed in Dreissena) or that the cilia aroundthe mouth become inactive as reported for some pholads by Purchon (1955), so thatno food material is passing to the stomach in the quiescent phase of the rhythm.

T H E D I G E S T I V E D I V E R T I G U L AStarved and unstarved specimens of Dreissena polymorpha were fed with titaniumdioxide and colloidal graphite (dag 554*) for various periods of time, and the digestivediverticula then fixed and sectioned.

The cytological appearance of the digestive diverticula as seen in these preparationswas found to be more or less constant in any one animal, but to differ in differentspecimens. The structure of the primary and secondary ducts was essentially asdescribed for many other bivalves (Owen, 1955) and bears a very close resemblanceto those of Mytilus edulis. The primary ducts possess a well-defined ciliated gutter.The secondary ducts connect the primary ducts and tubules; they are non-ciliatedbut possess a brush border and do not branch. Th e tubules themselves were occasion-ally observed to possess a structure that corresponded closely with diagrams of digestivetubules of other species of bivalves (Owen, 1955; Dinamani, 1957). In other specimensthe tubules differed considerably in appearance, as indicated diagrammatically inFig. 3, and the various conditions observed are interpreted as successive stages in acyclical rhythm.

A young growing tubule (Fig. 3, A) has a very wide lumen. Th e cells of thetubules are extremely short, with their nuclei occupying a central position. In alater condition (Fig..3, B) two types of epithelial cells can be distinguished, of whichthe two or three groups of cells with darkly staining cytoplasm can be equated withthe 'nests of young cells' of Yonge (1926a). These darkly staining cells have noflagella. In a later condition (Fig. 3, G) the second type of cell, the digestive cell,has elongated, and has taken in food material to form numerous food vacuoles, witha corresponding diminution of the lumen of the tubule. The young cells have nowproduced long flagella, which presumably assist in the circulation of the fluid contentsof the tubules, thus bringing food material into contact with the digestive cells.The digestive cells can phagocytose suspended particles (Fig. 3, Gl) . Globular massesof yellowish particles were occasionally observed within some of- the digestive cells(Fig. 3, C2) alongside the nucleus. Similar masses of yellowish particles also occurredin the haemocoel surrounding the digestive diverticula (Fig. 3, D) and also in thecells of the pericardial gland (Fig. 3, X and Y). Yonge (1926a) observed similar

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MORTON: DREISSEXA POLTMORPHA. IIA B

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FIG. 3. Diagrammatic representations of the different cytological conditions of the digestivetubules (A-E ) and pericardial tubules (X and Y) observed in Dreissena polymorpha. A, Newlyformed tubule; B, developing tubule; C, absorbing (digesting) tubule; CI, a group of absorbingcells, one of which has phagocytosed p articles of titanium dioxide; C2, a group of absorbingcells, one of which has com pacted a mass of naturally occurring yellowish p articles; D, tubulebreakdown under normal feeding conditions with the production of fragmentation spherules,fragmentation amoebocytes and clusters of young cells from which new tubules will develop;Dl, tubule breakdown under conditions of starvation with the production of fragmentationspherules only; E, a cluster of young cells lying free in th e haemoco el; X, an empty pericardial" gland tubule; Y, a pericardial tubule the cells of which are full of dag . Not all to same scale.



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406 PROC EEDING S OF THE MALA COLOG ICAL SOCIETYconcretions in the digestive gland of Pecten opercularis. In Dreissena particles ofdag and titanium dioxide were also observed basally in the digestive cells. In someanimals the condition of the tubules suggested breakdown (Fig. 3, D). Particles ofdag were observed apparently passing out of the bases of the digestive cells in frag-mentation amoebocytes. It is suggested that these particular fragmentation amoebo-cytes were formed by breakdown of the digestive cell into two parts. The distalportion of the cell may form an excretory spherule, which passes down the secondaryand primary ducts into the stomach, whilst the basal nucleated portion passes withexcretory material (dag and titanium dioxide under experimental conditions) intothe haemocoel. At the same time (Fig. 3, D) the 'nests of young cells' have seeminglylost their flagella, and formed large bulges on the sides of the tubules. Each clusterof cells eventually dissociates itself from the old tubule, to lie free in the haemocoel,and eventually to organize itself into a new tubule, with a central lumen (Fig. 3, E).Such new tubules can be distinguished in fixed sections by the absence of a peripheralmeshwork of muscle fibres, whereas old tubules possess such muscles. Another con-dition, encountered only when the animal had been starved, was of tubule break-down w ith the production of many fragmentation spherules (Fig. 3, D l) b ut w ithoutformation of new tubules or of fragmentation amoebocytes. Dag and titanium dioxidewere observed in amoebocytes in the haemocoel, but not in fragmentation spherules,whereas the reverse was shown for Cardium (Owen, 1955) and Lasaea (J . E. Morton,1956). In Dreisscna, und er experimental conditions, dag was found in large quantitiesin the cells of the pericardial gland (Fig. 3, Y) 3-4 hr after feeding; the swollen cellsoccupied much of the lumen of the tubule. Where an animal had not been fed on dagthe cells of the pericardial gland were much contracted and largely devoid ofparticulate excretory material (Fig. 3, X).

In Great Britain Dreissena grows only when the water temperature exceeds 11 G,during which time the animal may increase in length by as much as 1 cm. To dothis new tubules must be produced, to meet the increasing demands of the growinganimal. It is postulated that at this time the 'nests of young cells' produce newtubules (Fig. 3, D) as originally suggested by Yonge (1926a), and as demonstratedby J. E. Morton (1956) for Lasaea. During the summer months, the digestive tubulesof Dreissena pass very few fragmentation spherules into the stomach, but pass wastematerial, contained in the basal nucleated fragmentation amoebocytes into thehaemocoel. This may be an important source of blood amoebocytes. Millott (1937)described a similar process in the nudibranch Jorunna where wandering phagocytesare derived by nuclear division from the epithelium of the digestive gland. Potts(1923) too, speaking of the digestive diverticula of Teredo stated that : ' I thinkthat the epithelium passes through phases and that ciliar retraction is followed bythe putting out of pseudopodia and ingestion of wood. In such places there is alsomultiplication of the nuclei accompanying assimilation and separation of nucleatephagocytic cells'.

Under conditions of artificial starvation in aquaria the digestive tubules behavedifferently. The digestive cells absorb fluid with little nutritive content. After absorp-tion has ceased, breakdown ensues but due to the absence of particulate waste few



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MORTON: DREISSEJYA POLTMORPHA. II 407fragmentation amoebocytes are produced. There is in consequence no need for the'nests of young cells' to produce new tubules, or for replacement of digestive cells(Fig. 3, Dl). Many spherules are produced, perhaps as a means of voiding excessfluid. These conditions may hold good for specimens living under natural conditionsduring the winter months.

THE DIGES TIVE RH YTHMMany specimens of Dreissena were fixed at different stages in the 24 hr of the adductorrhythm and the histology of the digestive diverticula examined in detail. From theresults of these investigations it was established that the rhythm of cytological changesin the digestive diverticula (as described earlier) is closely correlated with the rhythmof movement of the shell valves (Fig. 4).

A thorough understanding of the whole process of feeding and digestion in D.polymoTpha depends upon establishing the close co-ordination of various activitiesincluding adduction, filtration, cytological phases of the digestive diverticula, forma-tion and dissolution of the crystalline style, the physical and chemical conditionsin the stomach and the sequence of extra-cellular and intra-cellular digestion. Tothis end we must specify the timing of the cytological changes of the digestivediverticula with respect to the ryhthm of adduction, as follows:

During the active phase of the rhythm of adductor activity and quiescence theanimal is filtering food from the water, and ingesting particles of suitable size, andin suitable quantities. In the early stages of this active phase, the tubules are newlyformed (Fig. 4, A and B) while later flagella become evident (G). During this phasethere is grading of particles within the lumen of the stomach. Towards the end ofthe phase of adductor activity, the cells of the tubules are taking in food material,and eventually become swollen (D). When the shell valves are closed at the beginningof .the quiescent phase, the tubules undergo the process of breakdown (E), resultingfinally in the production of fragmentation spherules and fragmentation amoebocytes;new tubules are formed towards the end of the quiescent phase. This process isthen repeated with the start of the next phase of adductor activity. It can be seenthat the various cytological states of the digestive diverticula are arranged in a timesequence which is related to the rhythm of adductor activity and quiescence.

Coincident with these investigations, the pH of the stomach contents was measuredat regular intervals throughout the periods of adductor activity and quiescence.Most records in the literature give only one value, or a narrow range of values forthe stomach pH of any one species, e.g. Mya arenaria pH 5-8 (Yonge, 1925) andOstrea edulis pH 5'4-5-6 (Yonge, 1926b). A large number of readings of the pHof the stomach contents of Dreissena reveals that the pH of the stomach in thisgenus is very variable (6-6-8-2). It was further established that these readings variedsystematically in co-ordination with the rhythm of movements of the shell valvesand with the cytological rhythm of the digestive diverticula. It was found thatduring the active adduction phase, the pH rose from 7-2 to 8-2, presumably throughthe influx of food and water into the stomach while the animal was actively feeding.



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