Shell characteristics, isotopic composition and trace-element contents of some euryhaline molluscs as indicators of salinity

Palaeogeography, Palaeoclimatology, Palaeoecology, 19(1976): 39--62 © Elsevier Scientific Publishing Company, Amsterdam -- Printed in The Netherlands

SHELL CHARACTERISTICS, ISOTOPIC COMPOSITION AND TRACEE L E M E N T C O N T E N T S O F SOME E U R Y H A L I N E M O L L U S C S AS I N D I C A T O R S OF S A L I N I T Y

D. EISMA, W. G. MOOK and H. A. DAS

Netherlands Institute for Sea Research, Texel (The Netherlands) Physics Laboratory, The University, Groningen (The Netherlands) Reactor Centre, Petten (The Netherlands) (Received November 25, 1974; revised and accepted July 7, 1975)

ABSTRACT Eisma, D., Mook, W. G. and Das, H. A., 1976. Shell characteristics, isotopic composition and trace-element contents of some euryhaline molluscs as indicators of salinity. Palaeogeogr,, Palaeoclimatol., Palaeoecol., 19: 39--62. The shell characteristics, 513C--5180 and trace-element contents of five euryhaline molluscs from the Dutch coastal waters are considered in relation to salinity. Shape and weight of the shells may be influenced by salinity but are too variable to show a significant correlation. Maximum size and maximum age decrease with salinity. Between 513C-150 and salinity there is a strong correlation allowing salinity to be determined within 0 . 5 ~ Cl'. Also the average number of ribs on Cardium edule shells is strongly related to salinity , which can be determined from the average rib number within + 1.5 ~ Cl'. The results on the relation between trace-element contents and salinity are contradictory. The various relationships with salinity are not clear and need further elucidation.

INTRODUCTION In o r d e r to d e t e r m i n e the c o n d i t i o n s of w a t e r t e m p e r a t u r e and salinity f r o m mollusc shells, t w o m e t h o d s can be followed. One is to s t u d y species assemblages, the ratio of n u m b e r of species to n u m b e r of specimens, etc., the m o s t useful species being t h o s e with the m o s t limited and sharply d e f i n e d t e m p e r a t u r e and salinity range. The o t h e r is to s t u d y the characteristics o f the mollusc shells themselves: it has been s h o w n t h a t the o x y g e n isotopic c o m p o s i t i o n and e.g. the c o n t e n t of m a g n e s i u m are related to the t e m p e r a t u r e of the s u r r o u n d i n g w a t e r (Urey, 1 9 4 8 ; Epstein et al., 1 9 5 3 ; Waskowiak, 1 9 6 2 ; D o d d , 1 9 6 5 ) but there is also a salinity e f f e c t w h i c h m a y be used to d e t e r m i n e the (average} salinity of the w a t e r (Mook, 1971). F o r this s e c o n d a p p r o a c h the m o r e e u r y h a l i n e species are the m o s t suitable. In this p a p e r the relation is discussed b e t w e e n salinity and the shell characteristics of five m a i n l y e u r y h a l i n e mollusc species c o m m o n in the

40 Dutch coastal waters: Cardium edule, Cardium glaucum, Macoma balthica, Mya arenaria and Mytilus edulis. They have a very broad salinity range: the shell material used for this work -- collected in the Wadden Sea, the former Zuiderzee (before 1932), the North Sea coast and the Rhine--Meuse--Scheldt delta area -- covers a range of 3--18 %o Cl' (only Cardium edule does not occur below 10~o Cl'). Attention was given to the length, width, height and weight of the shells, to their age and rate of growth, to the isotopic composition and trace-element contents, to the mineralogy and, for the Cardiurn shells, to the average number of ribs. Besides this shell material, Cardium edul~ shells from the Eemian were analysed; these were available from borings in the central Netherlands and obtained through the State Geological Survey at Haarlem. The Cardium samples had already been used in previous work (Eisma, 1965, 1966; Mook, 1968, 1971); some of the results obtained before are here discussed again in relation to more recent knowledge, such as the recognition of Cardium edule and Cardium glaucum as two different species. DESCRIPTION OF THE SAMPLES The Cardium samples have already been described by Eisma (1965) but the data have been partly rearranged because of the separation between Cardium edule and Cardium glaucum (formerly C. edule var. Lamarcki). Nearly all the other samples came from the museum collections and had either been collected alive or with parts of the dead animal still inside, or were collected at localities where it could reasonably be expected that they had not been moved very far from where they had been living. Additional samples of Mytilus edulis were collected in 1967/1968 along the Western Scheldt and in the western part of the Wadden Sea, where they grow in large banks on the tidal flats, and along the North Sea coast, where they live on the stony piers and dykes. Samples of Macorna balthica and of Mya arenaria were also at that time collected in the western Wadden Sea. One sample of Mya arenaria was collected in 1966 near Urk in fields which before 1932 had been part of the Zuiderzee. Since these shells had been lying exposed to fresh water and air since about 1934 they were not used for chemical and isotopic analysis. For reasons of space we do not include here a full list of all samples with their various characteristics and the analytical results, but the data are available at the Physics Laboratory, Groningen University (isotope data) and at the Netherlands Institute for Sea Research, Texel (all other data). ANALYTICAL METHODS Length, height and width of Cardium, Mya and Macorna shells were measured with a slide gauge that could be read with an accuracy of 0.1 mm, with in practice an error of about 0.2 mm. From visual inspection as well as from the literature (e.g. Coe and Fox, 1942; Seed, 1968) it was suspected that the

41 variability in length, width and height of Mytilus shells would be very large. Indeed the variability found at a few selected localities along the whole salinity range was so large that it virtually obscures any salinity influence that may exist. Therefore no other samples were measured. Weights were determined with an analytical balance that could be read with an accuracy of 0.01 g. Isotopic analysis was carried out at the Physics Laboratory of Groningen University. From each location radial cross-sections of several shells of living molluscs belonging to the same population were selected. The powdered sample was heated at 475°C in vacuo to remove disturbing organic impurities (Epstein et al., 1953; Mook, 1971). CO2 was prepared by treatment with 95% ortho-phosphoric acid at 25.0°C (McCrea, 1950). The isotopic analysis was performed with the Varian M.A.T. M86 mass spectrometer (Mook and Grootes, 1973). '3C contents are presented as 513(C) values in %0 relative to PDB, 1sO as 518 (O) relative to the PDB and SMOW standards for carbonates and water respectively. The precisions during this project were about 0.05%0. According to our calibration: 5 ~3(NBS20) = -1.0G%o(by def.); 513(NBS21) =-28.19°;o; 5~S(NBS20) = -4.14%0 (by def.); 518SMow(NBS1 ) = - 7.94% (by def.); 51SSMOW(NBS1A) = - 24.33~0 (Craig 1957, 1961). Trace elements (A1, Mn, Cu, Co, Zn, Sb, Na, Ba, Ce, Eu, La, Tb) were determined by activation analysis at the Reactor Centre at Petten (De Soete et al., 1972). At the Netherlands Institute for Sea Research, Texel, the contents of S, P, N, Sr and Mg were determined in a number of samples: S with barium chloride, P with a m m o n i u m m o l y b d a t e , N with a micro-Kjeldahl method and Sr and Mg with atomic absorption. Shell mineralogy was analysed with a Philips X-ray diffractometer, using the method of Turekian and Armstrong (1960) and Davies and Hooper (1963). The salinity data for the various sampling locations were taken from Eisma (1965). The Dutch coastal waters, besides containing broad areas of intermediate salinity (especially before the enclosure of the Zuiderzee) have the advantage of showing only small temperature differences between water of 5 %o Cl' and water of 16 %oCl' (Eisma, 1966), so that temperature influences are usually small or absent when shells formed at different salinities are compared. THE AVERAGE RIB-NUMBER OF CARDIUM SHELLS Eisma (1965) found a rather close relation between salinity and the average number of ribs on Cardium edule shells, which could be used to determine the average salinity of the water where the shell was formed. However, subsequent work by Koulman (1970) on chromosomes, by Jelnes et al., (1971) on enzymes and by Rygg (1970), Russell (1971, 1972 a, b), Boyden (1971, 1972), Boyden and Russell (1972) and Russell and H0pner Petersen

42 (1973) on the distribution, ecology and physiology of Cardiurn species d e m o n s tr ated that Cardium edule is not a single, very variable species but in fact consists of two genetically different species -- Cardium edule and Cardium glaucurn -- as had been pointed out previously by Mars (1951) and H~pner Petersen (1958) on the basis of differences in morphology. Koulman (1970), Russell (1972a) and Boyden (1973) found that the genetic component influences the n u m b e r of ribs on the shells (as is also evident when other Cardiurn species are compared) and Koulman (1970) dem onst rat ed that in the Western Scheldt, in salinities ranging f r om 12%o to 17%o Cl', the average rib-number of Cardium edule is closely related to salinity while for Cardium g l a u c u m there is no such relation. Boyden (1973), considering many data on pure C. edule and C. glaucurn populations, reached the same conclusion. Regrouping all data on samples from the Dutch coastal waters consisting only of Cardium edule (Eisma, 1965), gives a relation between the average rib-number and salinity (E2--E 2 in Fig.l) that is very similar to the relation f o u n d previously for all samples (C. edule + C. glaucurn) collected at average salinities between 12 and 18~oo Cl' ( E I - - E I in Fig.1 after Eisma, 1965). The relation f o u n d by Koulman for C. edule f r om the Western Scheldt ( K - - K in Fig.l) is also very similar but somewhat displaced towards lower salinities. F r o m the data o f Koulman (1970), which were collected only in the Western Scheldt, salinity between 12 and 17%o can be determined from the average rib-number with an accuracy of +- 0.9 %0 Cl' at the 5% level, from those of Eisma (1965), which cover also the ot her Dutch coastal waters, with an accuracy of +- 1.3%o Cl'. The relation between average rib-number and salinity becomes much less close when data f r om other areas are included ( B - - B in Averoge number of ribs 26-

B

25-

24-

22- B

~~

~

~

~

~

21-

Fig.1. Relation between average number of ribs on Cardium shells and chlorinity. E1--E 1, relation for Cardium edule + C. glaucum in the Dutch coastal waters (after Eisma, 1965); E2--E 2, relation for Cardium edule only; K--K, relation found by Koulman (1970) for Cardium edule in the Western Scheldt; B--B, relation found by Boyden (1973) for Cardium edule from Western Europe. Interrupted lines, confidence limits at 5% level with E1--E 1 as base (after Eisma, 1965).

43 Fig.1 after Boyden, 1972), as is also clear from.the data given by Eisma (1965, fig. 7). There may be several reasons for this increased range. First, the average salinity data for the other areas may be less reliable: for the Dutch coastal waters long series of salinity data are available, whereas for most other areas such data are far less complete. For the salinity distribution in the Delta-area, subsequent work by Peelen (1967) has shown that the salinity data given by Eisma (1965) for that area are correct except for the Eastern Scheldt where they tend to be 0.5%0 Cl' lower (at chlorinities of about 17 %0). The availability of good salinity data, therefore, may give the results for the Dutch coastal area more precision than those from elsewhere. Moreover Koulman's (1970) data are based on recent and carefully collected samples, whereas the data of Eisma (1965) are mainly based on older samples not specially collected for this purpose, which may have resulted in the better relationship found by Koulman (1970). Secondly, salinity may not be the only factor that influences average ribnumbers, also when only a single species is considered. Exposure to wave action as a possible factor is mentioned by Lauckner (in Kinne, 1971) and by Russell (1972a) and Boyden (1973): the influence of exposure would be obscured by the relation with salinity because the areas with lower salinities are generally also more sheltered. In the Dutch coastal area, however, the rate of exposure is difficult to determine as there is no simple relation between exposure and salinity: on the North Sea coast C. edule lives at water depths of 5--15 m (at salinities of 17--18%o Ct') whereas in the Wadden Sea, sheltered behind the Wadden islands, C. edule is mainly intertidal (at salinities of 10--16.5~oo Cl'). Also the substrate tends to be muddier at lower salinities but Boyden (1972) has shown that the nature of the substrate -- soft mud or m u d d y sand -- does not appear to influence directly the shell ribnumber. Russell (1972a) suggests that a low rib-number may be linked with a higher temperature threshold for spawning, which corresponds with the lower rib-number in C. glaucurn in populations mixed with C. edule. The samples from the Dutch Wadden Sea, however, do not suggest a temperature influence when only one species (C. edule) is considered; the relation between average rib-number and salinity is rather close, whereas temperature gradients in spring and early summer differ strongly from the salinity gradients. Thus, if temperature had more than a negligible influence on the average rib-number, there should be a far less good relation between ribnumber and salinity than is actually found. SHAPE AND WEIGHT Shape and weight of mollusc shells vary with environmental conditions and might be useful as indicators of salinity. However, for Macoma balthica and Mya arenaria in the Dutch coastal waters no correlation was found between average length, height and width of the shell. For Cardium edule the average height (at a standard length of 20 ram} of samples grown at 17%o Cl' tends

44 to be somewhat lower (in the order of 5--10%) than of samples from lower salinities (Eisma, 1965), indicating that in the coastal North Sea cockles are slightly more elongated than those living in more brackish water, but this may also be due to other environmental factors, since in the North Sea C. edule is subtidal but in the Wadden Sea is chiefly intertidal. For the length/width ratio no relation with salinity was found. A slight reduction in average height (also ca. 5--10%) towards very low salinities (6 %o Cl') exists for Cardium glaucum but this t oo may be due to less exposure because in the f o r mer Zuiderzee C. glaucurn was subtidal. The shape of Mytilus edulis shells is very variable, as has been observed by m a n y authors (e.g. Redeke, 1911; Seed, 1968). In our samples the height/ length ratio tends to be larger at higher salinities. This was also observed by Redeke (1911) who showed that this was related to exposure: shells of Mytilus living at 0--2 m below mean tidal level have a larger height/length ratio than those from 2--8 m below mean tidal level. Moreover the height/ length and width/length ratios change with the age (or the size) of the shell as was f o u n d by Coe and Fox (1942) for Mytilus californianus and by Basal (1972) and Everards (1973) for Mytilus edulis. Also the density of a mussel population influences the shell-form, a high density leading to an elongated form (Seed, 1968). It follows that differences in shell shape of the species considered here cannot be used as an indicator of salinity. The same is true for the average weight. For Cardium glaucum there is a general reduction in average weight (of 20 mm shells) at low salinities but the data show a considerable spread (Eisma, 1965). No such reduction was f o un d for Cardium edule, Mya arenaria, Mytilus edulis and Macoma balthica. Beukema (pers. comm., 1975) f o u n d in the Ems-estuary a strong reduction in weight of Macoma balthica shells, the average weight (at standard length) being reduced by ca. 30% in the Dollart at ca. 5%° Cl'. This weight reduction, however, may be due to the fine m u d d y substrate in this low-salinity area, since weight reductions of 10--25% were found in the Wadden Sea in finemud areas at much higher salinities. Shih (1937), who emphasized a reduction of weight and thickness at lower salinities, did not include b o t t o m conditions in his discussion. In Mytilus edulis shell weight is a function of immersiontime (Rao, 1953; Basal, 1972) and not primarily of salinity. MAXIMUM SIZE AND AGE Maximum size and age are clearly related to the salinity of the water: the reduction of the m a x i m u m size (length) of Cardium edule, Mya arenaria, Mytilus edulis and to a lesser e x t e n t t hat of Macoma balthica at lower salinities is well d o c u m e n t e d , especially in the Baltic (Remane, 1958; Hallam, 1965). A similar reduction is f ound in the Dutch coastal waters: for Cardium edule from 5.1 cm length to 3.7 cm, for Cardium glaucum from 4.8 cm to 2.3 cm, forMytilus edulis from 13 cm to 4 cm, forMya arenaria from 12 cm to 7 cm, and for Macoma balthica from 2.8 cm to 1.8 cm. In the Rappahan-

45 nock River estuary, however, Davies (1972) did not find a decrease in maximum size for Macoma balthica. A decrease of m a x i m u m age with salinity was found for Cardium edule and Cardium glaucurn (Eisma, 1965) and for Macorna balthica, which reaches 12--13 years along the North Sea coast and in the tidal inlets (Van der Bij, 1973), 6--8 years in the Wadden Sea and 6 years in the former Zuiderzee and the Dollart. Vogel (1959), however, only found a small difference in maximum age between Cardiurn edule/glaucurn from the North Sea (9 years) and from the inner Baltic (7 years) but he studied only a few samples. Segerstr~le (1960) found in the Gulf of Finland, at ca 6 ~o CI', maximum ages for Macoma balthica varying from 11 years in surface waters to 33 years at 35 m depth, but the validity of age determinations of more than 10 years for Macoma balthica has been questioned by Lammens (1967) because of the difficulty of measuring such ages correctly. The more or less simultaneous decrease of both maximum size and maximum age suggests a relationship, but all evidence points to a decrease in growth rate as being responsible for the size reduction. Segerstr~le (1960) gives examples of Macorna balthica from the Gulf of Finland where the greatest length (19 mm) is reached by the population with the lowest maxim u m age (11 years); the slowest growing populations reach a maximum length of 16 mm at a maximum age of 33 years. A decrease in growth rate (or calcification rate) with salinity has been found for Cardium edule and Cardium glaucum (Eisma, 1965), Macoma balthica (Vogel, 1959), Mytilus edulis (Malone and Dodd, 1967; Baird, 1966) and Mya arenaria (Matthiessen, 1960). Variations, however, are large, there being a considerable range of rates at intermediate and higher salinities, and growth rates may to a large extent be determined by the temperature (Gilbert, 1973). For Mya arenaria, Matthiessen (1960) found that at intermediate salinities the growth rate could be higher than in the adjacent sea depending on the abundance of flagellates in the water. Although maximum size and age in nearly all cases show a clear relation with salinity, this relation is useful only as a general indication since shells in a particular location may not yet have reached their maximum size or age. The relation between growth rate and salinity may offer some possibilities although the available data show a large variability: when considered over a large area maximum size, age and growth rate of shell populations may clearly show salinity trends. SHELL MINERALOGY As was mentioned already Cardium, and also Mya and Macoma shells, consist of aragonite, but Mytilus edulis shells have an outer calcitic and an inner aragonitic layer. The aragonite/caleite ratio of a My tilus edulis shell varies with temperature: the percentage of calcite is inversely related to the mean temperature of the water, higher temperatures favouring the formation

46

of aragonite (Lowenstam, 1954, 1964; Dodd, 1963, 1964). Lowenstam (1954) and Dodd (1963, 1966) also found indications for an inverse relation with salinity, b u t for Mytilus edulis from the Dutch coastal waters such a relation was not observed (Eisma, 1966). The data of Waskowiak (1962) for samples from Western Europe also do not indicate such a relation. In all cases, however, temperature differences may have influenced the results. Moreover, Dodd (1963, 1966) found different relations with salinity for Mytilus edulis edulis from Washington and Mytilus edulis diegensis from San Francisco, so that the contradictory results may also be explained by genetic differences -4 1

-2 I

=

0 I

~

÷2 I

+4 I

I~DB f i X . ) +4-

+2

. . . . . ter p d o /

-?// .:"

/

,~,y /

-2-

.f"

~,~ /

" CI

(%o)

....."I/L}... ..'x x

....,/./.

"

-'4%

-4-

/::}/ Western Scheldt

•:"11 ~ / "

/"//""

• Cardium edule

.."/// +

-6 ¸

o Mya arenaria x Mytilus edulis . ~ Cardium edule ~--.--~ Mytilus edulis

18 :: =-6.5%o

-8 ¸

/

... +~

-i 18

PDB ( % 0 )

Fig.2. Relation between 513 and 518 of shell carbonate in the Western Scheldt. The "carbonate lines" are drawn parallel to the "water line" (dotted line from Mook, 1970). The temperature scales indicate the isotopic composition of marine calcite and aragonite formed under isotopic equilibrium conditions at various temperatures in North Sea water (open square). The cockles are from Eisma (1965), the mussels were collected by Mook (cf. Mook, 1971).

47 between species and sub-species. As pointed out by Dodd (1966) as well as by others (Kennedy et al., 1969; Taylor et al., 1969), only experimental data may finally solve this problem. ISOTOPES In previous papers (Mook and Vogel, 1968; Mook, 1968, 1971) the relation between the carbon and oxygen isotopic composition of shell carbonate and respectively dissolved bicarbonate and water was demonstrated. Within certain limits a state of isotopic equilibrium for oxygen as well as for carbon between the carbonate and the surrounding water was observed for the species studied. Since in brackish waters the '3C and '80 content are largely determined by the mixing ratio of the fresh river and seawater (Mook, 1970), the isotopic composition of the carbonate also depends on the salinity. Fig.2, presenting a revised version of an earlier graph, shows the relation between 513 and 518 of shell carbonate in the Western Scheldt. According to our measurements on North Sea water, the average 5 ' 3 of total dissolved carbon is +1.3%o. In order to obtain the 5'3 of the dissolved bicarbonate fraction, corrections must be applied for the presence of dissolved carbon dioxide and carbonate; we have no information about the isotope fractionations involved in the occurrence of metal-carbonate complexes. With regard to the fractionations between the dissolved carbonate and bicarbonate, the experimental figures from the literature are believed to be uncertain, so that we prefer to use the theoretically calculated values by Thode et al. (1965). The figures for the fractionation between the dissolved CO2 and bicarbonate are taken from Mook et al., (1974): the resulting mean value of 5 '3 for the oceanic bicarbonate then is about +1.0~oo, while for 5 TM of the North Sea water an average of 0.0%0 was found. It follows that at decreasing salinities and thus decreasing '3C and J~O content, the isotopic composition of the water shifts towards the respective values of the fresh-water component. The condition of conservative mixing of the fresh and seawater (Mook, 1970) regarding 180 gives the 5'8--C1' relation: 51s = ( l - p ) 5 ' S ( f r e s h ) + pS'S(sea)

where p (= Cl'/Cl'marine) is the degree of brackishness; regarding ,3 C: (1-p)2C~esh. 5'3(fresh) + P~Cse a- 513(sea) 513

--

(1-p)ECfres h + p~]Csea Eliminating p from these two relations gives the 513--518 equation presented by the (dotted) "water-line" in Fig.2. The latter relation implies the use of the total carbon content (~ C) instead of the bicarbonate fraction as is needed

48 in Fig. 2, which only means a small correction. Within a restricted chlorinity range this correction is irrelevant for the chlorinities (and temperature) deduced below. Assuming the formation of calcium carbonate by molluscs to be an isotopic equilibrium process, the isotopic composition of the carbonate can be calculated from that of the water. Thus, the oxygen isotope fractionation of calcite relative to ocean water (Epstein et al., 1953) as modified by Craig (1965), can be represented by: 18 2 18 0.13(6eDS) - 4.2 6eD B + (16.9 -- t) = 0

where t is the temperature in °C. An 0.6%0 enrichment of aragonite relative to calcite was found by Tarutani et al., (1969), whereas the carbon isotope fractionation at 25°C of calcite and aragonite with respect to dissolved bicarbonate were reported by Rubinson and Clayton (1969) as +0.9%0 and +2.7~oo respectively. The temperature dependence of this fractionation was taken from Emrich et al. (1970) as + 0 . 0 3 5 ~ per °C and assumed to be equal for calcite and aragonite. Starting from 613 and 6 ~s of the seawater (i.e. bicarbonate and water respectively) and using the above fractionation values, the resulting isotopic compositions of the marine carbonates were calculated and are present by the heavy lines in Figs.2--7. The temperature dependence of the fractionations is expressed in the temperature scale indicated. The state of isotopic equilibrium between the carbonate and the water also requires the isotopic results of the former to lie along the water-line. This "carbonate-line" is adjusted through the carbonate results parallel to the water-line. Extrapolation to marine conditions (heavy line) provides the average growth temperature of the molluscs. Moreover, the carbonate-line can be provided with a chlorinity scale. Since the laboratory experiments of Clayton's group result in two marine lines, one for calcite and one for aragonite, the problem arises which line should be taken for which molluscs. The species we have studied for the major part are Mytilus edulis (mussels) and Cardiurn edule (cockles). The latter consist of aragonite. Mussels form a thin inner layer of aragonite during each growing period and a rim of calcite along the edges. Since we took radial cross-sections of the shells, the samples consist of an u n k n o w n mixture of aragonite and calcite. In order to establish whether differences due to a calcitic or an aragonitic composition of the shell might occur, small samples were taken from the inner aragonite and the outer calcitic layer of a few specimens of Mytilus (it should be emphasized, however, that by this method no contemporaneously formed calcite and aragonite samples can be obtained in view of the way the layers are formed). The results are presented in Fig.6. The aragonite 613 values are consistently higher, in agreement with the measured fractionation values. The values for calcite, however, show a better agreement with the

49

average results presented in Fig.2. The fact is that, taking radial crosssections of the Mytilus shells, the carbonate samples (by X-ray analysis) consist of about 87% of calcite. This, however, does not solve the problem with regard to the Cardiurn species which consist of aragonite. This matter certainly deserves further study, primarily by growing molluscs in tanks under wellcontrolled isotopic conditions. In spite of the differences in the isotopic behaviour of calcite and aragonite we have two reasons to assume that they do not apply in our case: (1) The carbonate-lines from different estuaries in the same area (the Netherlands) should intersect where the estuaries meet, i.e. at the isotopic composition of carbonate in the North Sea. As can be seen from Fig.4 the -4

-2

0

~2

+4

6 13OSP( % o ) +4-

20

+2-

_ Ib

t (°c ) ..~.._

I0

CI (°/oo) .,~/

/, :'X, .'J

/

-2-

-4,

/'8"

#' ~f = - 8 % o

¢o

o7 /

o Cardium edule Zuiderzee ,, ,, Wodden Sea x Mocorna bolthico • Mya orenorio

-6-

•

-8 ~

-

-2

0

-*2

+4

18 o/, PDB oo;

Fig.3. Relation between 513 and 618 of shell carbonate in the former Zuiderzee--Wadden Sea estuary (cf. Fig.4). The samples are from Eisma (1965) (cf. Mook, 1971).

5O

-2

-4 L

I

I

,

0 I

A

+2 l

i

+4 I

o

13

6 PDB(~/oo) +4-

2~

+2

t (°c)

/ "fl/o, (O,oo) /..//

0

-2

•

'4////

J -4

/

/

~e~'~¢ ~ / /

• Cardium

-6

~ge ond

E0$tern Sch41tlo~ Grevalingqm

-8

i -4

i

-2

i

0

i

+2

i

+4

81:oe(%o)

Fig.4. Relations between ~ 13 and 818 of she[] carbonate in the former Eastern Seheldt estuary and Grevelingen. The samples are f r o m Eisma (1965) (ef. M o o k , 1971 ).

intersection agrees with the isotopic composition of marine calcite and n o t at all with that of aragonite. (2) From the C- and O-isotopic composition, the chlorinity is deduced using the chlorinity scales in the Figs.2, 3 and 4. The resulting Cl-values agree with the average chlorinities from the water as reported by Eisma (Fig.5). Using the aragonite line would result in chlorinities consistently more than 2 %ot o o low. In order to check also the representativeness of the chlorinity as deduced from the 5t3--5 is relation of single specimens, several shells of Mytilus from one population were analysed. The results are presented in Fig.8. It appears from the observed spread that, by taking the average of several specimens, the chlorinity value is defined to within 0.5~/oo.

51 CI (%o) 13_~18

from

÷ ~..*~*'+ +

14

o

o ~ M y x

+~+;4

V

I

+

.r

I0-

I oo ~

6-

/

/ "

+ • • o I

ilus edulis Western Cordium edule ,, ,, ,, ,, .

Scheldt ,, ,, Eastern Scheldt/Grevelingen ~ Wodden $eo glaucum Zuiderzee edule Eemian shells

CI (%0) from Eisma (1965)

Fig.5. Comparison between the chlorinities deduced from the ~ 13-h is relation (Figs.4, 5 and 6) and as given by Eisma (1965) (for the Eemian shells derived from the number of ribs, for others from the known chlorinity records). F r o m p o p u l a t i o n s o f Cardium, especially of fossil specimens, we have observed larger d i f f e r e n c e s b e t w e e n single shells. This is due to the presence of r e w o r k e d material. By taking averages o f m a n y (up to 20) specimens, the c h l o r i n i t y values d e d u c e d still a p p e a r to be meaningful. The spread in results, however, is larger t h a n for mussels (Fig.5). Finally, the same Cardium samples f r o m the marine Eemian (interglacial) deposits in the N e t h e r l a n d s as were used by Eisma ( 1 9 6 5 ) in his s t u d y on the relation b e t w e e n the n u m b e r of ribs and salinity were analysed for t3C and is O. Fig.7 presents a map o f the w e s t e r n p a r t of the Netherlands, indicating where the Cardium samples were c o l l e c t e d f r o m borings. The results are presented in the graph o f Fig.8. T h e carbonate-line d r a w n agrees with a 5 ,s value of the river Rhine of -10%o which is also the present average value. The actual E Cf~sh ( a d a p t e d 2.5 mmole/1) is of m i n o r i m p o r t a n c e for d e d u c i n g the chlorinities and t e m p e r a t u r e . The m e a n g r o w t h t e m p e r a t u r e of the cockles is s h o w n to be s o m e w h a t higher t h a n the present value, in a g r e e m e n t with estimates f r o m o t h e r sources ( | S O - p a l e o t e m p e r a t u r e s , pollen-analytical data). Based o n the resulting chlorinities, t e n t a t i v e isohalines are drawn as p r e s e n t e d in Fig.7. The same p a t t e r n is observed as was c o n c l u d e d earlier by Eisma ( 1 9 6 5 ) based on the n u m b e r of ribs. TRACE ELEMENTS Many a u t h o r s have f o u n d a relation b e t w e e n salinity and the t r a c e - e l e m e n t c o n c e n t r a t i o n of e u r y h a l i n e mollusc shells, but their results are c o n t r a d i c t o r y .

52

Rucker and Vallentyne (1961) established in Crassostrea virginica shells a significant correlation between salinity and the Mn- and Na-content and a multiple correlation between salinity and Mg-, (Mg + Sr)-, Mn- and Nacontent, which made it possible to determine salinity from one single shell with a a = 5.3%o S at a 5% confidence level. Berlin and Khabakov (1973) found a lower chlorine content in shells from more brackish waters. The data of Pilkey and Goodell (1963) are few but indicate in Crepidula fornicata shells only a general increase in trace-element content (Mn, Fe, Mg, Sr, Ba) at lower salinities. The extensive data of Leutwein and Waskowiak (1962), Waskowiak (1962) and Leutwein (1963) indicate a relation between salinity

13 J o

-4 I

-2 I

0 I

+2 I

+4 I

PDB ( % o )

+4-

25 15

IO

/ /

25

+2

Calcite ~

t .o

I0

-2-

V,,,,4"I

//~/"~

-4-

o ....

•

Pair a r a g o n i t e - c a l c i t e

x Single specimens

-6-

-8-

i

14

~

--2

i

0

i

i

+2

~'4

18 o ~; PDB (Yoo)

F i g . 6 . R e l a t i o n b e t w e e n ~ 13 a n d ~ Is o f shell c a r b o n a t e f r o m m u s s e l s c o l l e c t e d in t h e W e s t e r n S c h e l d t . F r o m single s p e c i m e n s t o t a l c r o s s - s e c t i o n s w e r e a n a l y s e d ( a b o u t 8 5 % c a l c i t e a n d 15% a r a g o n i t e ) f r o m o n e l o c a t i o n , w h e r e a s f r o m s p e c i m e n s f r o m d i f f e r e n t locations calcite and aragonite were analysed separately.

53

Fig.7. Sketch map of The Netherlands showing the Eemian coastline (heavily dashed line). The location numbers are given in Fig.8 and refer to Eisma (1965). The finely dashed lines represent the tentative isohalines. and magnesium c o n t e n t in Cardiidae, Veneridae, Myidae and Tellinaceae, and between b o r o n content, barium c ont e nt , and salinity in Cardiidae, Veneridae and Myidae, but no relations for other elements, whereas only the correlation with b o r o n c o n t e n t in shells of Cardium edule, Mya arenaria, Mytilus edulis and Littorina littorea was f ound to be significant: from the B-content of one single shell, salinity could be determined with a o varying between 6.6 and 8.8 %o S. Dodd (1965) found a relation between salinity and Mg-content of the prismatic (calcite) layer of Mytilus edulis, Mg-content being higher at lower salinities, whereas Jansen-Besemer (1974} found in Mytilus edulis and Cardiurn edule samples from the Dutch coastal waters no relation for magnesium c o n t e n t but only for St-content and salinity, the Sr-content increasing at lower salinities. Hallam and Price (1968), however, had found no such correlation for strontium in Cardiurn edule shells from Western Europe, while Dodd's (1965) results for the strontium c o n t e n t in the aragonitic layer of My tilus edulis shells from Washington were inconclusive. Following the results of Jansen-Besemer (1974), we determined magnesium and strontium c o n t e n t in Macorna balthica and Mya arenaria for the same Dutch coastal

54

areas and found that for these species too there appears to be no relation for magnesium content but only for strontium content and salinity (Fig.9). Finally Davies (1972) found a lower Mg-content and a higher St-content at lower salinities in Brachydontes recurvus shells. His results, however, are not directly comparable to those of Dodd (1965), Hallam and Price (1968), Jansen-Besemer (1974) and ourselves because he used whole shells instead of only the aragonitic layer (thus including the thin calcitic outer layer) and calculated the average Mg- and Sr-content at a standard shell length of 30 mm. The results of most authors are based on shell material of different areas grouped together so that environmental differences between these areas may play a large role. Therefore we determined the content of a number of trace elements (Al, Na, Ba, Mn, Cu, Co, Zn, Sb, Ce, Eu, La, Tb, S, P and N) in Cardium edule and Cardium glaucum shells from one area (the Dutch coastal waters). The relations between trace-element concentrations and salinity are given in Fig.10 and do not indicate a significant correlation between salinity -; 13

-,2

o

..,2

+;

' •

Poe (Yoo) +4.

+2 ¸

[5

Calcite

I0

5

,f"/

./,°

-2,

//" 4

-4,

6-10 -6 ¸

/

~ 11-13 4 14-J6 4 17-18

~

-21

'a 22 ~ 23-25 6 26

Eemion Rhine

+

Cordiurn edule

27

~18= - 1 0 % o -8

: ~ C f = 2.5 mmole/I

POB

oo

Fig.8. Relation between 513 and 5 Is of shell carbonate from Eemian cockles. The results given refer to the different groups of samples reported by Eisma (1965, p. 535). The locations are indicated in Fig.7.

55 )rn S r 5000

p p m Sr

-

Mya

3OOo ~

orenorio

2000"

Mocomo

boJthico

2000•

i

x

x

x

=

}000

- J6

18 % o C t

pprn Mg

,oo%L~%-ppm M 9 500-

Myo

orenorio

x

Mocomo

bolthicc]

Ii

4OO

400-

5OO-

x

x x

x

2OO

x

1 x

4

6

8

IO

J2

14

16

!8 ° / ~ C I ~-

I00

~

~

~o

12

~

b6

18

%o cr

Fig.9. Relation between chlorinity and strontium and magnesium content of Macoma balthica and Mya arenaria shells. and trace-element content. The concentration of some elements has a tendency to increase or decrease at lower salinity, while the concentration of most trace elements is independent of salinity. The concentrations of Ce and N were found to be very low (Ce < 0.1 ppm in most cases, N < 0.2 ppm} and could not be used for correlation with salinity. The results, together with those of the other authors, are summarized in Table I. For most trace elements it is not clear in what form they are present in mollusc shells: they may occur in the mineral phase of the shell, in the organic matter, in inclusions or on exchange positions. Strontium and magnesium predominantly substitute for calcium in the carbonate lattice, strontium in aragonite and magnesium in calcite. Amiel et al. ( 1 9 7 3 ) f o u n d that in aragonite corals strontium is for more than 90% present in the crystal lattice and for less than 7% in the organic matter. Magnesium in aragonite, or strontium in calcite, may be present for up to 70--80% in the mineral part of the shell, either as ion substituting for calcium or in the form of a finely divided mineral. The same applies to sodium which in aragonite corals was found to be present in the mineral part for more than 90%, probably replacing calcium, but with a necessary compensation for excess valences. Potassium

56 % A[ Co

3001 ppb

0"12 t

O

00/

w

I

ppm

O

,iil

0

Mn

240-

pprT

200 -

80-

F60 -

60-

[20 -

40-

80-

•

$• r

•

!

Zn

20Q Q

40-

•

0

J

ppm

u

n

;°:

0 ppm

T

i

Sb

8-

Cu 64-

O

"8 |

i

2

•

•

2-

i

4

6

~4

|

p~

18 °/oo CI"

Fig.10. Relation b e t w e e n chlorinity and trace-element content of shells of Cardium edule and, at less than llYoo Cl', Cardium glaucum. (Continued on next page. )

is, more than sodium, present in the organic matter and on exchange positions (together about 2 0 - 2 5 % } . It is not clear in what form the other trace elements occur in the shells. The Mn-, Fe- and probably also Cu-, Co-, Pb-, Sn-, Ni- and Ag-contents are more or less correlated with lattice structure, all being predominantly present in calcite (Leutwein and Waskowiak, 1962; Harriss, 1965}. These elements presumably replace calcium to some extent. They may also be partly present in or on clay or silt particles that are present as inclusions in the shells. Bertine and Goldberg (1972} mention some other possibilities such as inclusion of iron-oxide floccules with adsorbed heavy metals, adsorption on the shell surface, and adsorption by microorganisms on the shell surface. Boron probably occurs as borate: the B-content of My tilus edulis shells is positively correlated with aragonite content (Leutwein and Waskowiak, 1962), which suggests a substitution of CO3 by BO3. Since BO3 is trivalent, this must be compensated for by the presence of other cations (such as sodium}. Some metals may be present as carbonate, or as sulphate or phosphate, since the Cardium edule shells from the Dutch coastal area were found to contain 0.01--0.41% SO4 and 5--700 ppm P2Os (but less than 0.2 ppm N).

57

%No i.

...

..:~...

:

01°1 pDm O0

/

ppm

Tb

0"31

200

0.2 o.tJ |'•

0.0 ppm ~-u

Bo

l

300-

• T

'

'

° :

,

'°ii

•

f

r

r

°

°

• !

r

ppm P2 05 600 t

0.2 0"3t 03 0.0

Lo 1.5~

4001

•"

I 0

,i

~

°,

•

°i1

,

ppm

%i 04 0.40.5 LO1 0.0 2

; Fig.10. (contd.)

•

I0

12

.°

•

:

t"

!

0.2-

", ,

•

!

, • ?

14

• ,. " " '

16

.

18%o01" 2 '~ !

O0

The amount of trace elements in mollusc shells, according to various authors (summarized in Wolf et al., 1967), is determined by: (a) the availability of trace elements in the water; (b) salinity; (c) genetic factors; (d) temperature; (e) shell mineralogy; (f) animal physiology; (g) individual difference; and (h) possible other and as yet poorly understood influences. Some indication of h o w these factors may be interrelated can be obtained from the results of Davies (1972) which show that the inclusion of strontium and magnesium in Brachydontes shells is not related to the water chemistry directly, so that it is difficult to define a direct salinity influence. Calcification however occurs at lower salinities at progressively higher temperatures: low-salinity shells, therefore, should have a higher strontium content, as indeed has been found by Davies (1972), Jansen-Besemer (1974), in this study and to some degree by Pilkey and Goodell (1963). Thus the strontium content in the shells is probably more related to the combined effects of temperature and salinity on calcification processes in the animal than to the strontium and magnesium concentrations in the water. The number of factors that determine the trace-element content of mollusc shells, leading to the contradictory results discussed above, mean that trace-element content cannot be used as a safe means to determine salinity from mollusc

58

shells -- except perhaps in the case of boron and sodium. However, as Odum (1957) has pointed out for strontium, trace elements can be helpful if used together with other salinity indicators. CONCLUSIONS

(1) From the average rib number of Cardium edule, salinity can be determined, within one area and with adequate sampling, with an accuracy of less than +- 1%o Cl'. When a larger area is considered, the accuracy becomes somewhat lower, in the order of + 1.5%o Cl'. For Cardium glaucum there is no relation between average rib number and salinity. (2) Shape and weight of Cardium edule, Cardium glaucum, Mytilus edulis, Mya arenaria and Macoma balthica may be influenced by salinity, b u t they are t o o variable to show a significant correlation with salinity. Maximum size, m a x i m u m age and growth rate decrease with salinity for all five species considered here, but there is a large variability, especially at intermediate and higher salinities. (3) A clear relation between 513--5 TM and salinity was found for Cardium TABLE I Summary of the relations between trace-element content and salinity as found by various authors (see text) Species

Significant correlation with salinity

Concentration generally higher at lower salinities

Concentration generally lower at lower salinities

No relation with salinity

Cardium edule

B, Na, Sr

Sr, Ba, Cu, Ni

Ba, Co, Mg

Mytilus edulis Macoma balthica

B Sr

St, Fe, Mg Mg

Cu --

Mya arenaria

B, Sr

Pb, Ba

Ba, Mg

Littorina littorea

B

Pb, Cu, Mn, Fe, Ni, Mg, Sr Mg

--

Sr, Mg, Ni*, Pb*, Cu, Fe*, Mn, Sb, Zn, A1 Mg*, Ni*, Pb, Mn Sr, Mg, Ni*, Pb*, Cu*, Fe*, Mn, B Sr, Ni, Mg, Cu*, Fe*, Mn* --

--

B, Cu, Sr

Ba

Mg --

Crassostrea virginica Na, Mn,

(Na + Mn + Mg + (St + Mg)) Venus gallina Crepidula fornicata Brachydontes recurvus

--

Mn, Fe, Mg, Sr, Ba Sr

*Highest concentrations at 1 4 - - 2 8 ~ S.

Mg

59 edule a n d Mytilus edulis. F r o m Mytilus edulis shells, c a r e f u l l y s a m p l e d in the Western Scheldt, average salinity c o u l d be d e t e r m i n e d w i t h i n 0.5~oo Cl'. (4) On t h e r e l a t i o n b e t w e e n t r a c e - e l e m e n t c o n t e n t a n d salinity (as well as on t h e r e l a t i o n b e t w e e n a r a g o n i t e c o n t e n t and salinity in Mytilus edulis) t h e results of various a u t h o r s are c o n t r a d i c t o r y . ,(5) The v a r i o u s relationships with salinity are n o t clear. Thus, it is n o t k n o w n w h y the average rib n u m b e r o f Cardium edule decreases w i t h salinity and to w h a t e x t e n t salinity d e t e r m i n e s the a r a g o n i t e / c a l c i t e r a t i o in M y tilus edulis. T h e 513--518 relation o f shell c a r b o n a t e is c o r r e l a t e d w i t h t h e isotopic c o m p o s i t i o n of the water, as w o u l d f o l l o w f r o m t h e r m o d y n a m i c e q u i l i b r i u m c o n d i t i o n s . This in spite of the f a c t t h a t t h e m e c h a n i s m o f f o r m a t i o n o f c a l c i u m c a r b o n a t e is u n k n o w n . Also it is i m p e r f e c t l y k n o w n w h a t d e t e r m i n e s the a m o u n t of trace e l e m e n t s in m o l l u s c shells or in w h a t f o r m t h e y are present. C o n t r o l l e d t a n k e x p e r i m e n t s are necessary to elucidate these questions. ACKNOWLEDGEMENTS In the c o u r s e of this w o r k the a u t h o r s received m u c h h e l p f r o m Mr. Sj. van der Gaast, Mr. J. K a l f and Mr. B. M o o r e n , w h o carried o u t c h e m i c a l and mineralogical analyses, Mrs. C van der Molen-Sijbolts, w h o did the i s o t o p i c analyses, Mrs. N. C. J a n s e n - B e s e m e r , w h o studied c a l c i t e / a r a g o n i t e relations d u r i n g a s h o r t s t a y in G r o n i n g e n , and Mr. J. Z o n d e r h u i s , w h o assisted in the a c t i v a t i o n analyses; we all w a n t to t h a n k t h e m for t h e i r c o o p e r a t i o n and advice. We are also i n d e b t e d to the R i j k s m u s e u m van N a t u u r l i j k e H i s t o r i e at Leiden and the Zoological M u s e u m at A m s t e r d a m for the use of shell s a m p l e s f r o m the m u s e u m collections. REFERENCES Amiel, A. J., Friedman, G. and Miller, D. S., 1973. Distribution and nature of incorporation of trace elements in modern aragonitic corals. Sedimentology, 20: 47--64. Baird, R. H., 1966. Factors affecting the growth variation of mussels. Fish. Invest., Ministr. Agric. Fish. Food (G.B.), Ser. II, Salmon Freshwater Fish., 25(2): 1--33. Basal, M., 1972. Measurements on the influence of the length of the daily submergence time on the condition and appearance of mussels. Unpublished report N.I.O.Z. 1972--2. Berlin, T. S. and Khabakov, A. V., 1973. Ca--Mg ratios, Cl' contents and mineral compositions in shells of recent Pelecypod molluscs. Geokhimiya, 8:1253--1260 (transl. in Geochem. Int., 10(4): 939--946). Bertine, K. K. and Goldberg, E. D., 1972. Trace elements in clams, mussels and shrimp. Limnol. Oceanogr., 17(6): 877--884. Boyden, C. R., 1971. A comparative study of the reproductive cycles of the cockles Cerastoderma edule and C. glaucum. J. Mar. Biol. Assoc. U.K., 51: 605--622. Boyden, C. R., 1972. The behaviour, survival and respiration of the cockles Cerastoderma edule and C. glaucum in air. J. Mar. Biol. Assoc. U.K., 52: 661--680. Boyden, C. R., 1973. Observations on the shell morphology of two species of cockle Cerastoderma edule and C. glaucum. Zool. J. Linn. Soc., 52: 269--292.

60 Boyden, C. R. and Russell, P. J. C., 1972. The distribution and habitat of the brackish water cockle Cardium (Cerastoderma) glaucum in the British Isles. J. Anita. Ecol., 41: 719--734. Coe, W. R, and Fox, D. L., 1942. Biology of the California sea mussel (Mytilus cal.); influence of temperature, food supply, sex and age on the rate of growth. J. Explor. Zool., 90: 1--30. Craig, H., 1957. Isotopic standards for carbon and oxygen and correction factors for mass spectrometric analysis of carbon dioxide. Geochim. Cosmochim. Acta, 12: 133--149. Craig, H., 1961. Standard for reporting concentrations of deuterium and oxygen 18 in natural waters. Science, 133: 1833--1834. Craig, H., 1965. The measurement of oxygen isotope paleotemperatures. Proc. Spoleto Conf. Stable Isotopes in Oceanogr. Studies Paleotemperatures, Pisa, 1965, pp.3--24. Davies, T. T., 1972. Effect of environmental gradients in the Rappahannock river estuary on the molluscan fauna. In: B. W. Nelson (Editor), Environmental Framework of Coastal Plain Estuaries. Geol. Soc. Am. Mem., 133: 263--290. Davies, T. T. and Hooper, P. R., 1963. The determination of the calcite: aragonite ratio in mollusc shells by X-ray diffraction. Mineral. Mag., 33: 608--612. De Soete, D., Gijbels, R. and Hoste, J., 1972. Neutron Activation Analysis. WileyInterscience, New York, N.Y., 836pp. Dodd, J. R., 1963. Paleoecological implications of shell mineralogy in two pelecypod species. J. Geol., 71: 1--11. Dodd, J. R., 1964. Environmentally controlled variation in the shell structure of a pelecypod species. J. Palaeontol., 38: 1065--1071. Dodd, J. R., 1965. Environmental control of strontium and magnesium in Mytilus. Geochim. Cosmochim. Acta, 29: 385--398. Dodd, J. R., 1966. The influence of salinity on mollusc shell mineralogy: a discussion. J. Geol., 74: 85--89. Eisma, D., 1965. Shell characteristics of Cardium edule L. as indicators of salinity. Neth. J. Sea Res., 2: 493--540. Eisma, D., 1966. The influence of salinity on mollusc shell mineralogy: a discussion. J. Geol., 74: 89--94. Emrich, K., Ehhalt, D. and Vogel, J. C., 1970. Carbon isotope fractionation during the precipitation of Calcium carbonate. Earth Planet. Sci. Lett., 8 : 3 6 3 - - 3 7 1 . Epstein, S., Buchsbaum, R., Lowenstam, H. A. and Urey, H. C., 1953. Revised carbonatewater isotopic temperature scale. Bull. Geol. Soc. Am., 64: 1315--1325. Everards, K., 1973. De groei van Mytilus edulis L. als functie van de onderdompelingstijd. Unpublished report N.I.O.Z. 1973--2. Gilbert, M. A., 1973. Growth rate, longevity and maximum size of Macoma balthica (L.). Biol. Bull., 145: 119--126. Hallam, A., 1965. Environmental causes of stunting in living and fossil marine benthonic invertebrates. Palaeontology, 8(1): 132--155. Hallam, A. and Price, N. B., 1968. Environmental and biochemical control of strontium in shells of Cardium edule. Geochim. Cosmochim. Acta., 32: 319--328. Harriss, R. C., 1965. Trace element distribution in molluscan skeletal material. I. Magnesium, iron, manganese and strontium. Bull. Mar. Sci., 15: 265--273. H~bpner Petersen, G., 1958. Notes on the growth and biology of the different Cardium species in Danish brackish water areas. Medd. Komm. Danm. Fisk. Havunders. N.S.II, 22: 1--31. Jansen-Besemer, N. C., 1974. Sr/Ca, Ca/Mg en Ca/Zn verhoudingen in het skelet van een aantal recente Pelecypoden species als mogelijke milieu-indikatoren. Unpublished report Vening Meinesz Laboratory, Utrecht State University. Jelnes, J. E., H~bpner Petersen G. and Russell, P. J. C., 1971. Isoenzyme taxonomy applied on four species of Cardium from Danish and British waters with a short description of the distribution of the species (Bivalvia). Ophelia, 9:15--20.

61 Kennedy, W. J., Taylor, J. D. and Hail, A., 1969. Environmental and biological controls on bivalve shell mineralogy. Biol. Rev., 44: 499--530. Kinne, O., 1971. Marine Ecology, vol. I, part 2. Wiley-Interscience, New York, N.Y., 1244 pp. Koulman, J. G., 1970. Onderzoek naar Cardium edule and Cardium glaucum in het Deltagebied. Unpublished report Delta-Instituut Yerseke. Lammens, J. J., 1967. Growth and reproduction in a tidal flat population of Macoma balthica (L.). Neth. J. Sea Res., 3: 315--382. Leutwein, F., 1963. Spurenelemente in rezenten Cardien verschiedener Fundorte. In: Unterscheidungsmoglichkeiten mariner und nicht mariner Sedimente. Fortschr. Geol. Rheinl. Westfalen, 10: 283--292. Leutwein, F. and Waskowiak, R., 1962. Geochemische Untersuchungen an rezenten marinen Molluskenschalen. Neues Jahrb. Mineral. Abh., 99: 45--78. Lowenstam, H. A., 1954. Factors affecting the aragonite--calcite ratios in carbonate secreting marine organisms. J. Geol., 62: 284--322. Lowenstam, H. A., 1964. Coexisting calcites and aragonites from skeletal carbonates of marine organisms and their strontium and magnesium contents. In: Recent Researches in the Fields of Hydrosphere, Atmosphere and Nuclear Geochemistry. Tokyo, pp. 373--4O4. Malone, Ph. G. and Dodd, R. J., 1967. Temperature and salinity effects on calcification rate in My tilus edulis and its paleoecological implications. Limnol. Oceanogr., 12: 432--436. Manuels, M. W. and Rommets, J. W., 1973. Metingen van zoutgehalte, temperatuur en zwevend materiaal in de Waddenzee, april 1970--oktober 1972. Unpublished report N.I.O.Z. 1973--6. Mars, P., 1951. Essai d'interpretation des formes gdndralement groupSs sous le nom de Cardium edule Linnd. Bull. Mus. Hist. Nat. Marseille, 11: 1--31. Matthiessen, G. C., 1960. Observations on the ecology of the soft clam, Mya arenaria, in a salt pond. Limnol. Oceanogr., 5: 291--300. McCrea, J. M., 1950. On the isotopic chemistry of carbonates and a paleotemperature scale. J. Chem. Phys., 18: 849--857. Mook, W. G., 1968. Geochemistry of the Stable Carbon and Oxygen Isotopes of Natural Waters in The Netherlands. Thesis, Groningen University, 157 pp. Mook, W. G., 1970. Stable carbon and oxygen isotopes of natural waters in the Netherlands. Proc. I.A.E.A. Conference Use of Isotopes in Hydrology, Vienna, 1970, pp. 163--190. Mook, W. G., 1971. Paleotemperatures and chlorinities from stable carbon and oxygen isotopes in shell carbonate. Palaeogeogr., Palaeoclimatol., Palaeoecol., 9: 245--263. Mook, W. G. and Grootes, P. M., 1973. The measuring procedure and corrections for the high-precision mass-spectrometric analysis of isotopic abundance ratios, especially referring to carbon, oxygen and nitrogen. Int. J. Mass Spectrom. Ion Phys., 12: 273--298. Mook, W. G. and Vogel, J. C., 1968. Isotopic equilibrium between shells and their environment. Science, 159: 874--875. Mook, W. G., Bommerson, J. C. and Staverman, W. H., 1974. Carbon isotope fractionation between dissolved bicarbonate and gaseous carbon dioxide. Earth Planet. Sci. Lett. 22: 169--176. Odum, H. T., 1957. Biochemical deposition of strontium. Inst. Mar. Sei., 4: 38--114. Peelen, R., 1967. Isohalines in the Delta area of the rivers Rhine, Meuse and Scheldt. Neth. J. Sea Res., 3: 575--597. Pilkey, O. H. and Goodell, H., 1963. Trace elements in Recent mollusc shells. Limnol. Oceangr., 8: 137--148. Rao, K. P., 1953. Shell weight as a function of intertidal height in a littoral population of Pelecypods. Experientia, IX: 465--466.

62 Redeke, H. C., 1911. Over den groei der Zuiderzee-mosselen. In: Verslag van den Staat der Nederlandsche Zeevisscherijen over 1910. Bijlage IV: Rapport over schelpdierenvisscherij en schelpdierenteelt in de noordelijke Zuiderzee. Den Haag. Remane, A., 1958. Oekologie des Brackwassers. In: Die Biologie des Brackwassers. Die Binnengew~ser, 22: 1--216. Rubinson, M. and Clayton, R. N., 1969. Carbon-13 fractionation between aragonite and calcite. Geochim. Cosmochim. Acta., 33: 997--1002. Rucker, J. B. and Valentine, J. W., 1961. Salinity response of trace element concentration in Crassostrea virginica. Nature, 190: 1099--1100. Russell, P. J. C., 1971. A reappraisal of the geographical distributions of the cockles Cardium edule L. and C. glaucum Bruguiere. J. Conchol., 27: 225--234. Russell, P. J. C., 1972a. A significance in the number of ribs on the shells of two closely related Cardium species. J. Conchol., 27: 401--409. Russell, P. J. C., 1972b. Biological studies on Cardium glaucum, based on some baltic and mediterranean populations. Mar. Biol., 16: 290--296. Russell, P. J. C. and H6pner Petersen, G., 1973. The use of ecological data in the elucidation of some shallow water European Cardium species. Malacologia, 14: 223--232. Rygg, B., 1970. Studies on Cerastoderrna edule (L.) and Cerastoderma glaucum (Poiret). Sarsia, 43: 65--80. Seed, R., 1968. The ecology of Mytilus edulis L. (Lamellibranchiata) on exposed shores. II. Growth and mortality, Ecologia 3: 317--350. Segerstr~le, S. G., 1960. Investigations on Baltic populations of the bivalve Macoma balthica (L.). Soc. Sci. Fenn. Comm. Biol., XXIII 2: 1--72. Shih, Chen-Ya-, 1937. Die Abh~ngigkeit der Gr~Jsse und Schalendicke mariner Mollusken yon der Temperatur und dem Salzgehalt des Wassers. Sitzungsber. Ges. Naturf. Freunde Berlin, pp. 238--287. Stephen, A. C., 1931. Notes on the biology of certain lamellibranchs on the Scottish coast. J. Mar. Biol. Assoc. U.K., 17: 277--300. Tarutani, T., Clayton, R. N. and Mayeda, T. K., 1969. The effect of polymorphism and magnesium substitution on oxygen isotope fractionation between calcium carbonate and water. Geochim. Cosmochim. Acta, 33: 987--996. Taylor, J. D., Kennedy, W. J. and Hall, A., 1969. The shell structure and mineralogy of the Bivalvia. Introduction. Nuculacea--Trigonacea. Bull. Br. Mus. (Nat. Hist.), Zool., Suppl. 3. Thode, H. G., Shima, M., Rees, C. F. and Krishnamurty, K. V., 1965. Carbon-13 isotope effects in systems containing carbon dioxide, bicarbonate, carbonate and metal ions. Can. J. Chem., 43: p.582. Turekian, K. K. and Armstrong, R. L., 1960. Magnesium, strontium and barium concentrations and calcite--aragonite ratios of some recent molluscan shells. J. Mar. Res., 18: 133--151. Urey, H. C., 1948. Oxygen isotopes in nature and in the laboratory. Science, 108: 489--496. Van der Bij, R. J., 1973. Leeftijdssamenstelling van enkele Macoma-populaties in Noord- en Waddenzee. Verband tussen zeewatertemperatuur en ]aarklassesterkte. Unpublished report N.I.O.Z. 1973--10. Vogel, K., 1959. Wachstumunterbrechungen bei Lamellibranchiaten und Brachiopoden. Neues Jahrb. Geol. Pal~ontol. Abh., 109: 109--129. Waskowiak, R., 1962. Geochemische Untersuchungen an rezenten Molluskenschalen mariner Herkunft. Freib. Forschungsh. C., 136. Wolf, K. H., Chilingar, G. V. and Beales, F. W., 1967. Elemental composition of carbonate skeletons, minerals and sediments. In: G. V. Chilingar, H. J. Bissell and R. W. Fairbridge (Editors), Carbonate Rocks. Elsevier, Amsterdam, pp. 23--149.