- Email: [email protected]
The shell of Mytilus as an indicator of zonal variations of water quality within an estuary
Mytilus shell as a water quality indicator
265
of artificial spiked standardsprepared by addition of Specpure salts to calcite. The indicated reproducibilities were fO.005% for Si, &O. 25%for Ca, +O .03% for Fe, IfrO.002% for Cu and fO.Ol% for Sr (all reproducibilities at the 95% confidence level). Due to peak interference associated with the high concentrations of Ca it was not possible to determine the low levels of Mg present by XRFS. Ratios of Mg/Ca were determined by atomic absorption spectrophotometry, using solutions in dilute HCl, and the concentrations of Mg derived using the XRFS values for Ca. A reproducibility of *O-O001 wasobtained by the Mg/Ca ratio determination. For estimation of the aragonite proportion in the shell carbonate by X-ray diffraction, the samplepowders were back-packed against glassin aluminium sampleholders. A calibration curve of the principal peak intensity ratios for a seriesof known mixtures of calcite and aragonite was prepared following the method of Lowenstam (1954). The intensity ratios of the principal peaks of calcite, 3.03A (20 CuK,=29 *4”), and aragonite, 3 ‘40A (20 CuK,=26.2”), were used to determine the weight of aragonite (percent) in the shell carbonate mixtures. Chart peak heights were taken as a measure of intensity. A reproducibility of +O ‘05% aragonite was achieved. Results In Figure 1 the stretch of the estuary supporting colonies of Mytilus hasbeen divided into four geographic zones. These roughly correspond to the major musselbed zones mapped by Khayrallah and Jones(1975). Both Zone A, which adjoinsthe industrial/dock area, and Zone B, which borders the residential conurbation of Dundee/Broughty Ferry, show high population densities of Mytilus. The population density is least in Zone C, although the samesize range of individuals is found. The results of the individual analysesare summarized in terms of rangesand meansfor these four subareasof the estuary in Table 1. A full listing of the analytical data can be obtained from the authors. The mean concentration values for the chemical components show little variation between the zones. The rangesof variation within the zones, however, are relatively wide; considerably in excessof the reproducibility limits indicated for the analytical procedures. A strikingly different aragonite proportion is shown for Zone C, with a meanvalue some 12% below that for the whole system. The range of variation of aragonite is also rather restricted in Zone C whereas it is characteristically very wide in the other zones of the system. The range of compositionsfound for all parametersmeasuredreduces confidence in the use of the zonal mean values for comparisonand environmental interpretation. Complete shells, single valves and shell fragments were all used to provide values in the general sample. A number of experiments were undertaken to investigate the causesof variation, asessthe validity of the data and seek improvements in the methodology. Three live Myths specimens,from the samepopulation and showing no signsof shell damage, were collected and each individual valve analysed for Sr, Ca, Cu, Fe and Si. The results are shown in Table 2. Within the analytical precision, constant compositionswere obtained, both from valve to valve and shell to shell, for the population. Dodd (1965) and Chave (1962) reported that shell chemistry may vary with shell size. This was tested for Myths from the Tay estuary. The compositional ranges and means for four size ranges are presented in Table 3. No consistent pattern of chemical change with length is shown by this data.
M. A. M. Al-Dabbas,
266
TABLE 1. Summary
F. H. Hubbard
of analytical Percentage
Zone
Sr
Mg
Fe
data from weight
&J.
McManus
104 samples of Myzilus
(range
edulis
and mean)
cu
Si
ca
Organic matter
Aragonite
0~05-0~ 0.10
18
(@=A41)
0~07-0.10 0.08
0.03-0.26 0.15
O~CKM-0~014 0.007
0.02-0.09 0.05
36.8-40.0 38.8
1.4-5.6 2.3
38-83 60
(n :27,
0.05-O. 19 0.11
0~06-0.09 0.07
0.04-0.21 0.10
0.004-0.016 0.008
0.02-0’14 0.06
37.0-40.0 38.7
1.8-6.0 3.3
38-75 57
(&2)
0.05-0.22 0.12
0.06-0.09 0.07
0.04-0.24 0.13
0~004-0~015 0.008
0.03-0.17 0.06
37.2-39.8 38.6
1.8-5.7 3.2
32-57 45
(?I _D24)
0.04-0.17 0.09
0.06-0.26 0.08
0-06-0~26 0.10
0.006-0.015 0.010
0.02-O-07 0.04
36.3-39.6 38.2
2.0-6.0 3.9
36-79 56
3.4
57
Whole system (mean)
0.10
0.08
0.12
0,008
0.05
38.6
TABLE 2. Comparison of compositions of left (L) and (R) valves of specimens edtdis from the same population (percentage weight) Valve
Co
Fe
Si
Sr
Ca
1L 1R 2L 2R 3L 3R
0,013 0,014 0,013 O-013 0.013 0.014
0.103 0.111 0.083 0.100 0.082 0.100
0.058 0,063 0,067 0.075 0.055 0,047
0,072 0.066 0.084 0.090 0,078 0,072
39.6 39.7 39.7 39.6 39.6 39.7
TABLE 3. Composition Tay estuary
ranges and means from four length ranges of Mpihs
Percentage Length range
&
Sr
4-5 cm (n=lO)
0.05-O. 14 0.08
0.06-0.09 0.07
5-6cm (n = 10)
0.04-0.14 0.08
6-7 cm (n=lO) 7-8 cm (n=5)
Fe
weight
(range and mean)
CU
Si
Ca
of Mph
edzdis from the
Organic matter
Aragonite
0.06-0.25 0.13
0~003-0.012 0.009
0.02Al.08 0.04
36.8-39.8 38.6
3.0-5.6 3.9
36-59 52.4
0.07-0.08 0.08
0.064.25 0.12
0~006-0~012 0,009
0.02-0.08 0.04
36.8-40.0 38.5
25.5-5.5 3.8
40-58 53.7
O.OM.15 0.09
0.06-0.08 0.07
0.06-0.24 0.08
0~006-0~012 0.009
0.024.12 0.05
36.8AO.O 38.8
2.5-5.8 3.8
43-72 53.7
0.05-0.12 0.08
0.06-0.07 0.06
0~05-0.15 0.08
0~006-0-008 0.008
0~03-0-11 0.05
37.2-39.6 38.3
2.5-5.3 3.7
45-59 50.4
-
Mytilus shell as a water quality indicator
TABLE 4. Population weight)
267
group analysis results from three zones of the Tay estuary
Percentage Zone
cu
Fe
(percentage
weight
Si
Sr
Ca
Mg
Aragonite
Zone B (Broughty Ferry)
1 2 3
0.006 0.006 0.006
o- 103 0.091 O-140
0,050 0,063 0.058
0.076 0,075 0,077
39.4 39.5 39.1
0.088 0,099 0.076
56.6 57.0 56.0
Zone C (Newport)
1 2 3
0.007 0.007 0.006
0.155 0.136 0.143
0.074 0.077 0.055
0,079 0.080 0.083
38.6 38.7 38.8
0.100 0.079 0.095
44.2 45.0 48.0
Zone D Pw4
1 2 3
0,010 0.012 0.010
0.070 0.068 0.076
0.033 0.034 0.033
0.084 0.085 0.087
38.1 38.1 38.4
0.086 0,077 0.081
54.8 54.3 51.0
It seemsprobable, therefore, that the main causeof the wide rangesof variation found within the zone samplesis to be found in the variable completenessof the polylayer shell system represented by the individual analytical samples.Investigations have shown selectivity of concentration of trace elements to specific carbonate shell layers controlled by the relative acceptability of the elementsinto the lattices (Lowenstam, 1954; Chave, 1954, 1962; Pilkey & Hower, 1960; Dodd, 1963). Analysis of detached aragonite from Tay Myzilus shellsshowed someconcentration of Sr relative to that in the calcite residues.For the other elements in the analysed suite, however, the variation was within the analytical error. The periostracum is frequently stripped to a variable degree, even in living individuals. Of the suite of elementsincluded in the survey, a qualitative SEM-microanalytical examination of the organic periostracal layer showed significant concentrations of Fe, Cu and Mg. The relatively high levels of P and S indicated are probably intrinsic to the organic matter. Low concentrations of Al and Si indicate only minor clay mineral contamination and/or incorporation. Some of the Na, Mg and K present may be associatedwith clay minerals but the repeated occurrence of Cl asa peak in the spectra suggeststhe presenceof chloride salts. Fe and Cu probably occur in metallo-organic complexes. A preferred associationof these trace metals with the outer periostracal layer is indicated. The results of these tests suggestthat shell damagelargely accounts for the grossvariations evident in the survey results. The effect of such irregular component loss on the composition obtained from individual shell sample analysis may be sufficient to obscure any compositional pattern determined by growth environment. Three groups of Mytilus shells (each containing 5-10 individuals) were collected from each of Newport (Zone C), Tayport (Zone D) and Broughty Ferry (Zone B) to represent populations living and growing in three relatively distinct environments. The shells from eachpopulation group sample were crushed, mixed and treated assingle samplesfor analysis. The analytical results are presented in Table 4, and showthat while essentiallyconstant compositions are maintained within the groups, there are some significant variations between the groups. Most striking is the maintenance of the low aragonite in Zone C suggestedby the general analysis programme. The relatively high Cu and low Fe and Si
268
M. A. M. Al-Dabbas,
F. H. Hubbard &J.
McManus
concentrations shown for the Zone D population were not evident from the general survey data. Population group analysis of this type seemspreferable to the procedure initially adopted in this survey. It hasthe effect of dampeningaccidental variations without obscuring zonal variations. The method, however, constrains the spread of sampling within the system. In grab sampling, only one or very few individuals may be obtained from a site.
Conclusions and discussion The results of this preliminary investigation suggestthat, provided suitable samplingprocedures are adopted, the mineralogy and chemistry of the shellsof M. edtdis can provide a sensitive monitor of environmental variation within a restricted water system. The irregular distribution of components between the layers of the composite shells makes sampleshell damageimportant. The qualitative SEM microanalysis of the periostratum showed that this outer layer may be particularly significant where trace element compositions are of concern. Zonal trace element distinctions may be swamped by the irrational fluctuations due to irregular shell damage.Population group analysis improves the stability of the zonal trace element data and this approach seemspreferable to calculation of zonal meansfrom individual shell analyses. In the Tay estuary, the most useful parameter proved to be the proportion of aragonite with respect to calcite in the shell. This proportion, which is readily determined on a routine basis by X-ray powder diffraction, clearly defines a zone of low aragonite shell growth within the estuary. The differences in trace element chemistry proved too small to be well-defined by the single sampleregional survey method. The constancy of low aragonite in Zone C specimensin eachof the analysisprogrammes (i.e. individual shell, shell length group and population group) requires the existence of a distinctive environment of growth of Mytilus in the Newport reach of the Tay estuary. Crystallization of aragonite is believed to be favoured by high temperature (Lowenstam, 1954) and low salinity (Dodd, 1961). Watabe and Wilbur (1960) demonstrated a control on aragonite precipitation by the protein matrix composition, and Klug and Alexander (1974) suggestedthat smallamountsof organic and inorganic foreign material suchasalums and chlorates in the crystallizing solution can affect the habit of the crystals formed. Myths speciesliving in meanenvironmental temperatures above 22 “C lay down entirely aragonite shells, whereas at lower temperatures the composition of the shell is variable (Lowenstam, 1954). The meanwater temperature on the Newport bank of the Tay estuary does not differ markedly from those of the other reachesof the estuary. Nor is there any evidence for striking salinity differences within the estuary. Measurements of temperature and salinity over a spring and neap tidal cycle in June 1972 at stations 1 and 2 on Figure 1 (Buller et al., 1972) showed maximum temperature rangesof 11.O-13-3 “C (stn 1) and 10.8-13.7 “C (stn 2). The correspondingsalinity ranges observed were 32.2-l 1.O%O and 30.4-6 .O%O. West (1972) and Green (1974) showed a reduction in salinity in the main channel with increaseof mean river flow, i.e. westward. If any significant difference exists between the mean salinities at any point and Newport the latter should be less saline. According to Dodd (1961) therefore, aragonite would be favoured in Mjtihs at Newport vis-h-vis those at Tayport. The opposite trend is observed. A survey of data from zonesof similar temperate climate but varying salinities is instructive (Hubbard et al., 1981). The meanaragonite content in Mytilus shell from Trelleborg
Mytilus shell as a water quality indicator
269
and Kagghamra, Sweden is 56%where salinity is generally lower (<9%o) than in the Tay estuary (Lowenstam, 1954). Eisma (1966) has reported average aragonite proportions of 40% from the Netherlands with salinities of 5-17%0. Mytilus from the U.S. Atlantic coast where salinities are relatively high (32%.~)have similar or lower values of shell aragonite, e.g. Mount Desert, Maine 29.5%; Woods Hole, Massachussetts29.5% (Lowenstam, 1954). My&us from the Oslo Fjord, with a salinity range of 19-32X& has an average of 43% shell aragonite (Lowenstam, 1954). These data suggestthat salinity is not a sensitive control of aragonite secretion and that the predictable aragonite levels in the shells of My&us from temperate environments is of the order of 40%, i.e. similar to the ‘ low aragonite zone ’ of the Tay estuary. The cause of the shell carbonate variation in the Mytilus of the Tay estuary has not been precisely identified but it seemspossible that some effect of the effluent from the City of Dundee on the water chemistry and/or suspendedload is involved. The relatively high level of organic sewagepollution along the north shore of the middle and outer estuary (54 533cm3day-l, 80% untreated-Royal Commission, 1972) may influence the chemistry of the extrapallial fluid and the composition of the interplate organic matter of Mytilus in such a way asto promote aragonite development (Tanaka et al., 1960; Watabe & Wilbur, 1960; Hare, 1963; Wilbur & Watabe, 1963; Wilbur 1964). The ability of organic substances such asamino acidsto effect the precipitation of CaCO, polymorphs hasbeen demonstrated experimentally by Kitano and Hood (1965). Zone C of the estuary is largely protected from the influence of the Dundee effluent by its geographic location and the flow regime of the estuary. Although Zone D also lies on the south bank, it is downstream of the main sources of sewage outflow and is more subject to backwash contamination. In terms of aragonite proportion the musselsof Zone D occupy a position intermediate between those from the north bank and those of Zone C. The aragonite proportion of 45% in the shells of the Newport section of the estuary may therefore represent the temperature/salinity controlled ‘ norm ’ for M. edtdis in a temperate zone estuary with tidal and seasonalsalinity fluctuations while the increased aragonite secretion elsewherereflects environmental disturbance by pollution. Organic rather than inorganic pollutants seemmore significant in the determination of the shell crystallography. The effects of incorporation of inorganic componentsin MytiZus shell are poorly defined in the Tay estuary data. The shells of the Mytilus of Zone D (Tayport), where there are thriving populations of M. edtdis, contain the highest concentrations of Cu in the estuary and the lowest Fe. The shellsof Zone D alsohave the highest proportion of organic matter in their shell structure. It is not clear whether this implies that Cu stimulates development of the organic component or the higher proportion of secreted organic matter allowed the fixation of more Cu. Cation substitution in the shell carbonate showed no regular or significant trends. Reproducible element variation was restricted to Cu and Fe, both elements which can form organometallic complexes within the periostracum. This outer organic layer can act as a metallic pollutant sink, during and/or after growth. The resultant preconcentration allows a more ready detection of local pollution by shell analysis than by direct water analysis. Experiments are now in progress at stations throughout the lower and middle reaches of the Tay estuary with regular monitoring of water chemistry and suspendedload coupled with periodic shell analysis from implanted shell populations. The range of potential metallic pollutant elements analysed has been extended. In this way it is hoped to more fully determine the controls and operating limits of this natural sensor of water quality variation.
270
M. A. M.
Al-Dabbas,
F. H. Hubbard
& 3. McManus
References Al-Dabbas, M. A. M. 1980 An examination of shell fragment distribution and geochemical features of Myn’1u.s edulis in the Tay estuary. Ph.D. Thesis, University of Dundee. Bayne, B. L. 1976 Marine mussels: their ecology and physiology. Inrernational Biological Programme 10. Cambridge University Press, Cambridge. Buller, A. T., Charlton, J. A. & McManus, J. 1972 Data from physical and chemical measurements in the Tay estuary for neap and spring tides, June 1972. Research Report 2, Tay Estuary Research Centre, University of Dundee. Chave, K. E. 1954 Aspects of the biogeochemistry of magnesium in calcareous marine organisms. Journal of Geologv 62, 266-283. Chave K. E. 1962 Factors influencing the mineralogy of carbonate sediments. Limnology and Oceanography 7, 218-223. Dodd, J. R. 1961 Palaeoecological implications of shell mineralogy in two west coast pelecypod species. Abstract Geological Society of America Special Papers 68, 163 Dodd, J. R. 1963 Palaeoecological implications of shell mineralogy in two pelecypod species. 3ourmzl of Geology 71, I-11. Dodd, J. R. 1965 Environmental control of strontium and magnesium in Mytilus. Geochimica Cosmochimica Acta 29,7354X98. Eisma, D. 1966 The influence of salinity on mollusc shell mineralogy: a discussion. 3ournul of Geology 74, 89-94. Green, C. D. 1974 Sedimentary and morphological dynamics between St Andrews Bay and Tayport, Tay estuary, Scotland. Ph.D. Thesis, University of Dundee. Hare, P. E. 1963 Amino acids in the proteins from aragonite and calcite in the shells of Myttlus califarnianus. Science 139, 216217. Hepper, B. T. 1957 Notes on Mytilus galloprovincaalis Lamarck in Great Britain. Journal of the Marine Biological Association 36. Hubbard, F. H., Al-Dabbas, M. A. M. & McManus, J. 1981 Environmental influences on the shell mineralogy of Mytilus edtdis. Geomarine Letters 1, 267-269. Khayrallah, N. & Jones, A. M. 1975 A survey of the benthos of the Tay estuary. Proceedings of the Royal Society of Edinburgh B75, 113-135. Kitano, Y. & Hood, D. W. 1965 The influence of organic material on the polymorphic crystallisation of calcium carbonate. Geochimica Cosmochimica Acta 29, 29-42. Klug, H. P. & Alexander, L. E. 1974 X-ray Dtflraction Procedures for Polycrystalline and Amorphous Materials. Wiley Interscience Publications, New York. Lewis, J. R. i? Powell, H. T. 1961 The occurrence of curved and ungulate forms of the mussel Myrilus edulis L. in the British Isles and their relationship to M. Galloprovincialis Lamarck. Proceedings of the Zoological Society of London 137, 535-593. Lowenstam, H. A. 1954 Factors affecting the aragonite: calcite ratios in carbonate secreting mineral organisms, Journal of Geology 62, 284-322. Pilkey, 0. H. & Hower, J. 1960 The effect of environment on the concentration of skeletal magnesium and strontium in Dendrasfar. Journal of Geology 68, 216. Royal Commission 1972 Royal Commrssion on Environmental Pollutton 3rd Report (Cmnd. 5054). HMSO, London. Tanaka, S., Hatano, H. & Itasaka, 0. 1960 Biochemical studies on pearl: IX. Amino acid composition of conchiolin in pearl and shell. Bulletin of the Chemical Society of Japan 33, 543-545. Watabe, N. & Wilbur, K. M. 1960 Influence of organic matrix on crystal type in molluscs. Nature 188, 334. West J. R. 1972 Water movements in the Tay estuary. Proceedings of the Royal Society of Edinburgh B71, 115-129. Wilbur, K. M. 1964 Shell formation and regeneration. In Physiology of Mollusca (Wilbur, K. M. & Yonge, C. M. eds). 1, 243-282. Academic Press, New York. Wilbur, K. M. & Watabe, N. 1963 Experimental studies on calcification in molluscs and the alga Coccoltthus hexleyi. Annals of the New York Academy of Science 109, 82-l 12.
265
of artificial spiked standardsprepared by addition of Specpure salts to calcite. The indicated reproducibilities were fO.005% for Si, &O. 25%for Ca, +O .03% for Fe, IfrO.002% for Cu and fO.Ol% for Sr (all reproducibilities at the 95% confidence level). Due to peak interference associated with the high concentrations of Ca it was not possible to determine the low levels of Mg present by XRFS. Ratios of Mg/Ca were determined by atomic absorption spectrophotometry, using solutions in dilute HCl, and the concentrations of Mg derived using the XRFS values for Ca. A reproducibility of *O-O001 wasobtained by the Mg/Ca ratio determination. For estimation of the aragonite proportion in the shell carbonate by X-ray diffraction, the samplepowders were back-packed against glassin aluminium sampleholders. A calibration curve of the principal peak intensity ratios for a seriesof known mixtures of calcite and aragonite was prepared following the method of Lowenstam (1954). The intensity ratios of the principal peaks of calcite, 3.03A (20 CuK,=29 *4”), and aragonite, 3 ‘40A (20 CuK,=26.2”), were used to determine the weight of aragonite (percent) in the shell carbonate mixtures. Chart peak heights were taken as a measure of intensity. A reproducibility of +O ‘05% aragonite was achieved. Results In Figure 1 the stretch of the estuary supporting colonies of Mytilus hasbeen divided into four geographic zones. These roughly correspond to the major musselbed zones mapped by Khayrallah and Jones(1975). Both Zone A, which adjoinsthe industrial/dock area, and Zone B, which borders the residential conurbation of Dundee/Broughty Ferry, show high population densities of Mytilus. The population density is least in Zone C, although the samesize range of individuals is found. The results of the individual analysesare summarized in terms of rangesand meansfor these four subareasof the estuary in Table 1. A full listing of the analytical data can be obtained from the authors. The mean concentration values for the chemical components show little variation between the zones. The rangesof variation within the zones, however, are relatively wide; considerably in excessof the reproducibility limits indicated for the analytical procedures. A strikingly different aragonite proportion is shown for Zone C, with a meanvalue some 12% below that for the whole system. The range of variation of aragonite is also rather restricted in Zone C whereas it is characteristically very wide in the other zones of the system. The range of compositionsfound for all parametersmeasuredreduces confidence in the use of the zonal mean values for comparisonand environmental interpretation. Complete shells, single valves and shell fragments were all used to provide values in the general sample. A number of experiments were undertaken to investigate the causesof variation, asessthe validity of the data and seek improvements in the methodology. Three live Myths specimens,from the samepopulation and showing no signsof shell damage, were collected and each individual valve analysed for Sr, Ca, Cu, Fe and Si. The results are shown in Table 2. Within the analytical precision, constant compositionswere obtained, both from valve to valve and shell to shell, for the population. Dodd (1965) and Chave (1962) reported that shell chemistry may vary with shell size. This was tested for Myths from the Tay estuary. The compositional ranges and means for four size ranges are presented in Table 3. No consistent pattern of chemical change with length is shown by this data.
M. A. M. Al-Dabbas,
266
TABLE 1. Summary
F. H. Hubbard
of analytical Percentage
Zone
Sr
Mg
Fe
data from weight
&J.
McManus
104 samples of Myzilus
(range
edulis
and mean)
cu
Si
ca
Organic matter
Aragonite
0~05-0~ 0.10
18
(@=A41)
0~07-0.10 0.08
0.03-0.26 0.15
O~CKM-0~014 0.007
0.02-0.09 0.05
36.8-40.0 38.8
1.4-5.6 2.3
38-83 60
(n :27,
0.05-O. 19 0.11
0~06-0.09 0.07
0.04-0.21 0.10
0.004-0.016 0.008
0.02-0’14 0.06
37.0-40.0 38.7
1.8-6.0 3.3
38-75 57
(&2)
0.05-0.22 0.12
0.06-0.09 0.07
0.04-0.24 0.13
0~004-0~015 0.008
0.03-0.17 0.06
37.2-39.8 38.6
1.8-5.7 3.2
32-57 45
(?I _D24)
0.04-0.17 0.09
0.06-0.26 0.08
0-06-0~26 0.10
0.006-0.015 0.010
0.02-O-07 0.04
36.3-39.6 38.2
2.0-6.0 3.9
36-79 56
3.4
57
Whole system (mean)
0.10
0.08
0.12
0,008
0.05
38.6
TABLE 2. Comparison of compositions of left (L) and (R) valves of specimens edtdis from the same population (percentage weight) Valve
Co
Fe
Si
Sr
Ca
1L 1R 2L 2R 3L 3R
0,013 0,014 0,013 O-013 0.013 0.014
0.103 0.111 0.083 0.100 0.082 0.100
0.058 0,063 0,067 0.075 0.055 0,047
0,072 0.066 0.084 0.090 0,078 0,072
39.6 39.7 39.7 39.6 39.6 39.7
TABLE 3. Composition Tay estuary
ranges and means from four length ranges of Mpihs
Percentage Length range
&
Sr
4-5 cm (n=lO)
0.05-O. 14 0.08
0.06-0.09 0.07
5-6cm (n = 10)
0.04-0.14 0.08
6-7 cm (n=lO) 7-8 cm (n=5)
Fe
weight
(range and mean)
CU
Si
Ca
of Mph
edzdis from the
Organic matter
Aragonite
0.06-0.25 0.13
0~003-0.012 0.009
0.02Al.08 0.04
36.8-39.8 38.6
3.0-5.6 3.9
36-59 52.4
0.07-0.08 0.08
0.064.25 0.12
0~006-0~012 0,009
0.02-0.08 0.04
36.8-40.0 38.5
25.5-5.5 3.8
40-58 53.7
O.OM.15 0.09
0.06-0.08 0.07
0.06-0.24 0.08
0~006-0~012 0.009
0.024.12 0.05
36.8AO.O 38.8
2.5-5.8 3.8
43-72 53.7
0.05-0.12 0.08
0.06-0.07 0.06
0~05-0.15 0.08
0~006-0-008 0.008
0~03-0-11 0.05
37.2-39.6 38.3
2.5-5.3 3.7
45-59 50.4
-
Mytilus shell as a water quality indicator
TABLE 4. Population weight)
267
group analysis results from three zones of the Tay estuary
Percentage Zone
cu
Fe
(percentage
weight
Si
Sr
Ca
Mg
Aragonite
Zone B (Broughty Ferry)
1 2 3
0.006 0.006 0.006
o- 103 0.091 O-140
0,050 0,063 0.058
0.076 0,075 0,077
39.4 39.5 39.1
0.088 0,099 0.076
56.6 57.0 56.0
Zone C (Newport)
1 2 3
0.007 0.007 0.006
0.155 0.136 0.143
0.074 0.077 0.055
0,079 0.080 0.083
38.6 38.7 38.8
0.100 0.079 0.095
44.2 45.0 48.0
Zone D Pw4
1 2 3
0,010 0.012 0.010
0.070 0.068 0.076
0.033 0.034 0.033
0.084 0.085 0.087
38.1 38.1 38.4
0.086 0,077 0.081
54.8 54.3 51.0
It seemsprobable, therefore, that the main causeof the wide rangesof variation found within the zone samplesis to be found in the variable completenessof the polylayer shell system represented by the individual analytical samples.Investigations have shown selectivity of concentration of trace elements to specific carbonate shell layers controlled by the relative acceptability of the elementsinto the lattices (Lowenstam, 1954; Chave, 1954, 1962; Pilkey & Hower, 1960; Dodd, 1963). Analysis of detached aragonite from Tay Myzilus shellsshowed someconcentration of Sr relative to that in the calcite residues.For the other elements in the analysed suite, however, the variation was within the analytical error. The periostracum is frequently stripped to a variable degree, even in living individuals. Of the suite of elementsincluded in the survey, a qualitative SEM-microanalytical examination of the organic periostracal layer showed significant concentrations of Fe, Cu and Mg. The relatively high levels of P and S indicated are probably intrinsic to the organic matter. Low concentrations of Al and Si indicate only minor clay mineral contamination and/or incorporation. Some of the Na, Mg and K present may be associatedwith clay minerals but the repeated occurrence of Cl asa peak in the spectra suggeststhe presenceof chloride salts. Fe and Cu probably occur in metallo-organic complexes. A preferred associationof these trace metals with the outer periostracal layer is indicated. The results of these tests suggestthat shell damagelargely accounts for the grossvariations evident in the survey results. The effect of such irregular component loss on the composition obtained from individual shell sample analysis may be sufficient to obscure any compositional pattern determined by growth environment. Three groups of Mytilus shells (each containing 5-10 individuals) were collected from each of Newport (Zone C), Tayport (Zone D) and Broughty Ferry (Zone B) to represent populations living and growing in three relatively distinct environments. The shells from eachpopulation group sample were crushed, mixed and treated assingle samplesfor analysis. The analytical results are presented in Table 4, and showthat while essentiallyconstant compositions are maintained within the groups, there are some significant variations between the groups. Most striking is the maintenance of the low aragonite in Zone C suggestedby the general analysis programme. The relatively high Cu and low Fe and Si
268
M. A. M. Al-Dabbas,
F. H. Hubbard &J.
McManus
concentrations shown for the Zone D population were not evident from the general survey data. Population group analysis of this type seemspreferable to the procedure initially adopted in this survey. It hasthe effect of dampeningaccidental variations without obscuring zonal variations. The method, however, constrains the spread of sampling within the system. In grab sampling, only one or very few individuals may be obtained from a site.
Conclusions and discussion The results of this preliminary investigation suggestthat, provided suitable samplingprocedures are adopted, the mineralogy and chemistry of the shellsof M. edtdis can provide a sensitive monitor of environmental variation within a restricted water system. The irregular distribution of components between the layers of the composite shells makes sampleshell damageimportant. The qualitative SEM microanalysis of the periostratum showed that this outer layer may be particularly significant where trace element compositions are of concern. Zonal trace element distinctions may be swamped by the irrational fluctuations due to irregular shell damage.Population group analysis improves the stability of the zonal trace element data and this approach seemspreferable to calculation of zonal meansfrom individual shell analyses. In the Tay estuary, the most useful parameter proved to be the proportion of aragonite with respect to calcite in the shell. This proportion, which is readily determined on a routine basis by X-ray powder diffraction, clearly defines a zone of low aragonite shell growth within the estuary. The differences in trace element chemistry proved too small to be well-defined by the single sampleregional survey method. The constancy of low aragonite in Zone C specimensin eachof the analysisprogrammes (i.e. individual shell, shell length group and population group) requires the existence of a distinctive environment of growth of Mytilus in the Newport reach of the Tay estuary. Crystallization of aragonite is believed to be favoured by high temperature (Lowenstam, 1954) and low salinity (Dodd, 1961). Watabe and Wilbur (1960) demonstrated a control on aragonite precipitation by the protein matrix composition, and Klug and Alexander (1974) suggestedthat smallamountsof organic and inorganic foreign material suchasalums and chlorates in the crystallizing solution can affect the habit of the crystals formed. Myths speciesliving in meanenvironmental temperatures above 22 “C lay down entirely aragonite shells, whereas at lower temperatures the composition of the shell is variable (Lowenstam, 1954). The meanwater temperature on the Newport bank of the Tay estuary does not differ markedly from those of the other reachesof the estuary. Nor is there any evidence for striking salinity differences within the estuary. Measurements of temperature and salinity over a spring and neap tidal cycle in June 1972 at stations 1 and 2 on Figure 1 (Buller et al., 1972) showed maximum temperature rangesof 11.O-13-3 “C (stn 1) and 10.8-13.7 “C (stn 2). The correspondingsalinity ranges observed were 32.2-l 1.O%O and 30.4-6 .O%O. West (1972) and Green (1974) showed a reduction in salinity in the main channel with increaseof mean river flow, i.e. westward. If any significant difference exists between the mean salinities at any point and Newport the latter should be less saline. According to Dodd (1961) therefore, aragonite would be favoured in Mjtihs at Newport vis-h-vis those at Tayport. The opposite trend is observed. A survey of data from zonesof similar temperate climate but varying salinities is instructive (Hubbard et al., 1981). The meanaragonite content in Mytilus shell from Trelleborg
Mytilus shell as a water quality indicator
269
and Kagghamra, Sweden is 56%where salinity is generally lower (<9%o) than in the Tay estuary (Lowenstam, 1954). Eisma (1966) has reported average aragonite proportions of 40% from the Netherlands with salinities of 5-17%0. Mytilus from the U.S. Atlantic coast where salinities are relatively high (32%.~)have similar or lower values of shell aragonite, e.g. Mount Desert, Maine 29.5%; Woods Hole, Massachussetts29.5% (Lowenstam, 1954). My&us from the Oslo Fjord, with a salinity range of 19-32X& has an average of 43% shell aragonite (Lowenstam, 1954). These data suggestthat salinity is not a sensitive control of aragonite secretion and that the predictable aragonite levels in the shells of My&us from temperate environments is of the order of 40%, i.e. similar to the ‘ low aragonite zone ’ of the Tay estuary. The cause of the shell carbonate variation in the Mytilus of the Tay estuary has not been precisely identified but it seemspossible that some effect of the effluent from the City of Dundee on the water chemistry and/or suspendedload is involved. The relatively high level of organic sewagepollution along the north shore of the middle and outer estuary (54 533cm3day-l, 80% untreated-Royal Commission, 1972) may influence the chemistry of the extrapallial fluid and the composition of the interplate organic matter of Mytilus in such a way asto promote aragonite development (Tanaka et al., 1960; Watabe & Wilbur, 1960; Hare, 1963; Wilbur & Watabe, 1963; Wilbur 1964). The ability of organic substances such asamino acidsto effect the precipitation of CaCO, polymorphs hasbeen demonstrated experimentally by Kitano and Hood (1965). Zone C of the estuary is largely protected from the influence of the Dundee effluent by its geographic location and the flow regime of the estuary. Although Zone D also lies on the south bank, it is downstream of the main sources of sewage outflow and is more subject to backwash contamination. In terms of aragonite proportion the musselsof Zone D occupy a position intermediate between those from the north bank and those of Zone C. The aragonite proportion of 45% in the shells of the Newport section of the estuary may therefore represent the temperature/salinity controlled ‘ norm ’ for M. edtdis in a temperate zone estuary with tidal and seasonalsalinity fluctuations while the increased aragonite secretion elsewherereflects environmental disturbance by pollution. Organic rather than inorganic pollutants seemmore significant in the determination of the shell crystallography. The effects of incorporation of inorganic componentsin MytiZus shell are poorly defined in the Tay estuary data. The shells of the Mytilus of Zone D (Tayport), where there are thriving populations of M. edtdis, contain the highest concentrations of Cu in the estuary and the lowest Fe. The shellsof Zone D alsohave the highest proportion of organic matter in their shell structure. It is not clear whether this implies that Cu stimulates development of the organic component or the higher proportion of secreted organic matter allowed the fixation of more Cu. Cation substitution in the shell carbonate showed no regular or significant trends. Reproducible element variation was restricted to Cu and Fe, both elements which can form organometallic complexes within the periostracum. This outer organic layer can act as a metallic pollutant sink, during and/or after growth. The resultant preconcentration allows a more ready detection of local pollution by shell analysis than by direct water analysis. Experiments are now in progress at stations throughout the lower and middle reaches of the Tay estuary with regular monitoring of water chemistry and suspendedload coupled with periodic shell analysis from implanted shell populations. The range of potential metallic pollutant elements analysed has been extended. In this way it is hoped to more fully determine the controls and operating limits of this natural sensor of water quality variation.
270
M. A. M.
Al-Dabbas,
F. H. Hubbard
& 3. McManus
References Al-Dabbas, M. A. M. 1980 An examination of shell fragment distribution and geochemical features of Myn’1u.s edulis in the Tay estuary. Ph.D. Thesis, University of Dundee. Bayne, B. L. 1976 Marine mussels: their ecology and physiology. Inrernational Biological Programme 10. Cambridge University Press, Cambridge. Buller, A. T., Charlton, J. A. & McManus, J. 1972 Data from physical and chemical measurements in the Tay estuary for neap and spring tides, June 1972. Research Report 2, Tay Estuary Research Centre, University of Dundee. Chave, K. E. 1954 Aspects of the biogeochemistry of magnesium in calcareous marine organisms. Journal of Geologv 62, 266-283. Chave K. E. 1962 Factors influencing the mineralogy of carbonate sediments. Limnology and Oceanography 7, 218-223. Dodd, J. R. 1961 Palaeoecological implications of shell mineralogy in two west coast pelecypod species. Abstract Geological Society of America Special Papers 68, 163 Dodd, J. R. 1963 Palaeoecological implications of shell mineralogy in two pelecypod species. 3ourmzl of Geology 71, I-11. Dodd, J. R. 1965 Environmental control of strontium and magnesium in Mytilus. Geochimica Cosmochimica Acta 29,7354X98. Eisma, D. 1966 The influence of salinity on mollusc shell mineralogy: a discussion. 3ournul of Geology 74, 89-94. Green, C. D. 1974 Sedimentary and morphological dynamics between St Andrews Bay and Tayport, Tay estuary, Scotland. Ph.D. Thesis, University of Dundee. Hare, P. E. 1963 Amino acids in the proteins from aragonite and calcite in the shells of Myttlus califarnianus. Science 139, 216217. Hepper, B. T. 1957 Notes on Mytilus galloprovincaalis Lamarck in Great Britain. Journal of the Marine Biological Association 36. Hubbard, F. H., Al-Dabbas, M. A. M. & McManus, J. 1981 Environmental influences on the shell mineralogy of Mytilus edtdis. Geomarine Letters 1, 267-269. Khayrallah, N. & Jones, A. M. 1975 A survey of the benthos of the Tay estuary. Proceedings of the Royal Society of Edinburgh B75, 113-135. Kitano, Y. & Hood, D. W. 1965 The influence of organic material on the polymorphic crystallisation of calcium carbonate. Geochimica Cosmochimica Acta 29, 29-42. Klug, H. P. & Alexander, L. E. 1974 X-ray Dtflraction Procedures for Polycrystalline and Amorphous Materials. Wiley Interscience Publications, New York. Lewis, J. R. i? Powell, H. T. 1961 The occurrence of curved and ungulate forms of the mussel Myrilus edulis L. in the British Isles and their relationship to M. Galloprovincialis Lamarck. Proceedings of the Zoological Society of London 137, 535-593. Lowenstam, H. A. 1954 Factors affecting the aragonite: calcite ratios in carbonate secreting mineral organisms, Journal of Geology 62, 284-322. Pilkey, 0. H. & Hower, J. 1960 The effect of environment on the concentration of skeletal magnesium and strontium in Dendrasfar. Journal of Geology 68, 216. Royal Commission 1972 Royal Commrssion on Environmental Pollutton 3rd Report (Cmnd. 5054). HMSO, London. Tanaka, S., Hatano, H. & Itasaka, 0. 1960 Biochemical studies on pearl: IX. Amino acid composition of conchiolin in pearl and shell. Bulletin of the Chemical Society of Japan 33, 543-545. Watabe, N. & Wilbur, K. M. 1960 Influence of organic matrix on crystal type in molluscs. Nature 188, 334. West J. R. 1972 Water movements in the Tay estuary. Proceedings of the Royal Society of Edinburgh B71, 115-129. Wilbur, K. M. 1964 Shell formation and regeneration. In Physiology of Mollusca (Wilbur, K. M. & Yonge, C. M. eds). 1, 243-282. Academic Press, New York. Wilbur, K. M. & Watabe, N. 1963 Experimental studies on calcification in molluscs and the alga Coccoltthus hexleyi. Annals of the New York Academy of Science 109, 82-l 12.