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Growth of three bivalve molluscs transplanted along the axis of the Ems estuary
Netherlands Journal of Sea Research 19 (1): 45-51 (1985) GROWTH
OF THREE
BIVALVE MOLLUSCS TRANSPLANTED OF THE EMS ESTUARY
ALONG
THE AXIS
K. ESSINK and A. H. BOS Government Institute for Sewage and Waste Water Treatment (RIZA), Hereweg 99A, 9721 AA Groningen, The Netherlands
ABSTRACT Young specimens of Mya arenaria, Mytilus edulis and Cerastoderma edule were transplanted at the start of the growing season from the Wadden Sea to 5 sites in the Ems estuary. Changes in shell lengths and weights of the soft parts were determined by monthly sampling. Growth of all bivalves was relatively good in the outer part to decrease towards the inner parts of the estuary, reaching very low values in the innermost part in Cerastoderma and Mytilus. Along this traject strong gradients are present in salinity (decreasing), suspended matter (increasing) and TOC (increasing) to which factors growth was significantly correlated. Correlations were also found between growth and content of chlorophyll a and organic matter in the suspended matter, which factors did not show clear gradients in the estuary. The contribution of the individual environmental variables to total variability in growth could not be determined. It is supposed, however, that in the inner part of the estuary reduced salinity and enhanced suspended matter concentrations did affect Cerastoderma and Mytilus more than Mya.
ary at a number of places (VAN ES, 1977; DE WOLF, 1978). The macrobenthic fauna is relatively poor (VAN ARKEL & MULDER, 1979, 1982; DITTMER, 1981). Like many estuaries the Ems estuary has a high turbidity, especially in the inner part. As a consequence phytoplankton primary production is low (CADISE HEGEMAN, 1974; COLIJN, 1983). KOHL & MANN (1973) concluded that the turbidity in the estuary has increased from 1950 to 1970. Filter feeders like the mussel (Mytilus edulis), soft clam (Mya arenaria) and cockle (Cerastoderma edule) use their gills to obtain suspended particles from the water. The larger particles, are rejected as pseudofaeces. The remaining parti-
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1. INTRODUCTION The Ems estuary forms a part of the Wadden Sea at the Dutch-German border (Fig. 1). Its estuarine characteristics are established by the discharge of fresh water by the river Ems and Westerwoldse Aa (WWA). The latter discharges into the Dollard. The hydrography of the estuary is summarized by DE WOLF (1978) and HELDER& RUARDY (1982). Organic waste is discharged into the estu-
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~r~ ;,~ 53°1c.
Fig. 1.
o~ ~
7
Map of the Ems estuary with the location of the
experimental sites (11) and water sampling stations (o).
46
K. ESSINK & A.H. BOS
cles are transported to the mouth without any sorting according to quality (J@RGENSEN, 1966). The large amounts of suspended matter, as present in most estuaries, do not necessarily imply favourable feeding conditions. At a high density of suspended particles, a larger part of the material is rejected as pseudofaeces (J@RGENSEN, 1966; BAYNE et al., 1976). At still higher concentrations of suspended particles this may lead to low ingestion rates, which result in reduced growth. Mytilus and Cerastoderma occur in the outer and middle part of the estuary. Recordings from the brackish and turbid Dollard are rare. Mya occurs from the seaward end of the estuary to the central part of the Dollard (VAN ARKEL & MULDER, 1979, 1982). Results of transplantation experiments with cockles from the Ems estuary to the western Dutch Wadden Sea and vice-versa suggest growth limiting factors to be present in the Ems estuary (VRINS,1978). The quality of the suspended organic matter may be one of these factors (VAN ES & LAANE, 1982). One of the aims of RIZA is to increase knowledge on the functioning of the estuarine ecosystem under stress of human activities, such as dredging and discharging of waste. This knowledge may contribute to a more sound basis for the management of the estuary. The present study was undertaken to obtain information on the growth regulation of bivalves in the Ems estuary. Acknowledgements.--We are indebted to V.N. de Jonge, M.A. van Arkel and Dr. R.W.P.M. Laane for their comments on an early draft of the manuscript. Thanks are due to H.L. Kleef, P. Tydeman and the crew of the R.V. "Antares" for assistance in the field work. Mrs. H.E.J. BloemAbbingh typed the manuscript. Mr. R. Helsdingen prepared the figures. 2. MATERIAL AND METHODS 2.1. TRANSPLANTATION In the last week of April 1980, cockles, Cerastoderma edule, and soft clams, Mya arenaria, were collected in the eastern Dutch Wadden Sea 10 km west of Site 5. Mussels, Mytilus edulis, were collected 32 km west of Site 5 (Fig. 1). The day after collection 5 portions of 40 Cerastoderma and 40 Mytilus, and - 6 0 Mya of selected
sizes were transplanted to each of 5 experimental sites on the tidal flats of the Ems estuary (Fig. 1). The size range of the animals was 21.0 to 23.0 mm in Mytilus, 9.0 to 11.0 mm in Cerastoderma, and 6 to 15 mm in Mya. Galvanised wire netting was used to reduce loss by washing out or predation. The shells were color-marked to prevent mixing up with animals already present at the sites. All experimental sites were choosen in such a way that the time of submergence was about 7 hours per tide. With intervals of 4 weeks the portions were collected again and brought to the laboratory. Shell length was measured to the 0.1 mm below. Ash-free dry weight (ADW) of the soft parts was determined as described earlier (ESSlNK, 1978). In this transplant experiment animals with equal environmental history and equal genetic constitution are compared with respect to their growth under different environmental conditions. 2.2. ENVIRONMENTAL VARIABLES Information on environmental variables was derived from the Institutes weekly water quality monitoring programme (ANON., 1980). Only data from stations close to the experimental sites were used (Fig. 1). For each growth period, i.e. interval between successive collections of the molluscs, mean concentrations were calculated for salinity (measured as chlorosity), suspended matter, chlorophyll a, total organic carbon (TOC). The percentage of organic matter (POM) in the suspended matter, and the chlorophyll a content of the suspended matter were calculated to serve as an indication of the quality or utility of the suspended matter. 3. RESULTS Gales in spring and summer caused the loss of most of the transplanted animals at Site 4. Also at Site 1 and 3 some portions vanished. At Site 2 all cockles died between July 16 and August 15. Therefore, the planned monthly collection scheme was not completely realised. Part of the environmental variables, such as salinity, suspended matter and TOC, showed clear gradients in the estuary whereas others did not (Fig. 2). Salinity, chlorophyll a, chlorophyll a in suspended matter and TOC showed some seasonal variation; other variables varied both in time and space without much consistency. In Mytilus edulis the increase in mean ADW
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Regression analyses were done, using only data from collection days on which samples from 3 or more sites were available (Table 1). Both shell length and ADW of the soft parts were positively correlated with the salinity in the preceding period of 4 weeks. The slope of the regression for cockles became steeper as time proceded. The few data for Mya suggest a similar trend. The growth of Cerastoderma was negatively correlated with the amount of suspended matter, as was the growth of Mytilus. In both species the data from July also showed a steeper regression than in previous months. For Mya no significant correlation was found in May and June. In July and August, however, when only data from 2 sites were available, the higher length and ADW, respectively, were found at the site with the lower suspended matter content. Shell growth and ADW showed negative relationships with the concentrations of both TOC and chlorophyll a. TOC in the Ems estuary consists mainly of DOC, which behaves conservatively (LAANE, 1980), and is inversely correlated with salinity. Positive correlations were present
5 she
Fig. 2. Some environmental parameters measured in the Ems estuary in the periods 24 April to 21 May (A), 22 May to 18 June (L~), 19 June to 15 July (O) and July 16 to August 15 (©) 1980. a. Mean salinity, b. Suspended matter (g-m-3), c.TOC (g-m-3), d. Chlorophyll a (mg-m-3), e. POM in suspended matter (%), f. Chlorophyll a in suspended matter (#g.g-1).
/
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/
20 5 28
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w a s h i g h e s t in the outer half of the e s t u a r y (Sites
conditions did deteriorate during summer (Fig. 3). Site 5, at which Mytilus showed the highest increase in ADW, the growth of the shell was not significantly different from growth at Sites 3 and 4. In Cerastoderma edule the growth of soft parts and shell was far less in the inner part than in the outer part of the estuary (Fig. 4). These results show the same pattern as found in Mytilus. The distribution of growth rates of Mya arenaria (Fig. 5) differed somewhat from those observed in Cerastoderma and Mytilus. As far as data are available, growth of Mya at Site 1 was similar to that at Site 3 and 5 during the first 2 months of the experiments. Reduced growth was most clear at Site 2.
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Fig. 3. Mean shell length (mm) and mean ADW of the soft parts (mg) with standard deviations of Mytilus edulis at the experimental sites 1 to 5 in 1980.
48
K. ESSINK & A.H. BOS
25 rnm
5
mg 15C
3
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I A
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Fig. 4. Mean shell length (mm) and mean ADW of the soft parts (mg) with standard deviations of Cerastoderma edule at the experimental sites 1 to 5 in 1980.
between growth of shell and soft parts and the qualitative aspects of suspended matter (chlorophyll a and POM content). These correlations became s i g n i f i c a n t in June-July, and were present most clearly in Cerastoderma and Mytilus (Table 1).
lead to the mortality of C e r a s t o d e r m a and to the reduced growth of Mya at Site 2 after July 15 (Fig. 5). These phenomena show a parallel to the decreasing tolerance of low salinities by Cera s t o d e r m a , Mytilus and Mya (WOLFF, 1973). In the regression analyses Mya showed less strong correlations between growth and environmental variables than Mytilus and Cerastoderma. This may at least partly be caused by the larger variation in initial lengths and weights in the transplanted Mya specimens as compared with Mytilus and Cerastoderma. In the last 3 months of the experiment all three bivalve species showed significant correlations between growth and 2 or more of the environmental variables measured. The question w h i c h of these variables are responsible for the major part of the variation in the growth recorded cannot be easily answered as some environmental variables are mutually strongly correlated (Fig. 2), e.g. salinity and suspended matter. Furthermore, the question can be raised whether the environmental variables measured at the water sampling stations are representative. It is likely
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4. DISCUSSION
~2
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All 3 species showed relatively fast growth rates in the outer part of the estuary, and reduced growth in the inner part. In the outer part of the estuary, however, growth did not appear to be optimal. Data from mussels held in cages suspended from buoys show that in the summer of 1980 growth of the soft parts of Mytilus edulis in the outer part of the Ems estuary was less than in the western most part of the Dutch Wadden Sea (DE KOCK & MARQUENIE, 1981). The decrease in weight in Cerastoderma and Mytilus observed at Site 2 between June 18 and July 15 may have been the effects of surplus fresh water pumped into the estuary 1 km west of this site during an extremely wet spell that lasted from June 23 till July 27. This fresh water reached Site 2 during flood tide relatively unmixed with estuarine waters (H.L. KLEEF, personal communication). These local c o n d i t i o n s may also have
3z / ///i 5 //
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Fig. 5. Mean shell length (mm) and mean ADW of the soft parts (mg) with standard deviations of Mya arenaria at the experimental sites 1 to 5 in 1980.
GROWTH OF TRANSPLANTED BIVALVES
49
TABLE 1 Regression equations (y -- ax + b) and linear correlation coefficients (r) for the relation between shell length and ADW (y) of the 3 bivalves (Mytilus edulis, Mya arenaria, Cerastoderma edule) and the environmental variables (x) salinity, suspended matter (g.m-1), POM (% in suspended matter)and chlorophyll in suspended matter (/zg.g-1) (no regression data are given in case of correlation coefficients with p >0.05). Species
Environmental variable
Date
N
Mytilus
Salinity Suspended matter POM in susp. matter Chlor. in susp. matter
Aug. Aug. Aug. Aug.
15 15 15 15
117 117 117 117
Mya
Salinity
May 21 June 18 May 21 June 18 June 18 June 18
102 110 102 110 110 110
May 21 June 18 July 15 May 21 June 18 July 15 May 21 June 18 July 15 May 21 June 18 July 15
124 110 31 124 110 31 124 110 31 124 110 31
Susp. matter POM in susp. matter Chlor. in susp. matter Cerastoderma
Salinity Susp. matter POM in susp. matter Chlor. in susp. matter
that the samples taken in the tidal channels do not represent the c o n d i t i o n s of the water pumped through by the transplanted bivalves at the sites on the flats. Therefore, the results should be interpreted with caution. The role of salinity as important factor governing the growth of Cerastoderma edule can be well understood. Of the 3 species in this experiment it is least tolerant to low salinities (THEEDE & LASSIG, 1967; WOLFF, 1973). Recordings of Cera s t o d e r m a edule from the brackish Dollard are rare (VAN ARKEL & MULDER, 1979, 1982). The observed mortality at Site 2 during a period of fresh water discharge fits in this picture. A positive relation between salinity and shell growth was reported by VOGEL (1959) and EISMA (1965). VRINS (1978) transplanted cockles from the Eros estuary (close to our Site 4) to more saline waters in the western Dutch Wadden Sea near Texel and vice versa. She concluded that growth limiting factors were present in the Ems estuary, She also found increasing mean lengths of 2 year old cockles from Delfzijl to Borkum, i.e. with increas-
Shell length (ram) r
a
0.66 -0.77 0.29 0.81
0.46 -0.03 0.35 0.02
b
20.21 28.65 20.79 21.31
ADW (mg) r
0.19 0.49 0.78 - 0,02 -0.02 -0.05 0.11 0.67 1.13 0.01 0.03
9.08 9.90 8.13 12.96 17.61 23.01 9.97 6.97 2.74 12.76 9.80
b
0.84 1 7 . 2 -75.2 -0.80 -0.9 218.2 0.59 2 0 . 6 -159.2 0.76 0,5 6.6 0.15 0.26 -0.14 -0.11 0.40 0.13
0.55 0.80 0.91 - 0.56 -0.64 -0.92 0.20 0.72 0.92 0.16 0.48 0.94
a
2.0
33.5
4.8
-6.3
0.55 1.6 2.6 0.89 7.1 -34.2 0.91 1 2 . 5 -92.4 - 0.57 - 0.2 34.8 -0.74 -0.3 78.0 -0.92 -0.8 145.2 0.09 0.75 9.0 -68.0 0.92 17.9 - 175.7 0.01 0.53 0.1 7.9 0.89 0.4 - 56.7
ing salinity. These data cannot be explained unequivocally as the locations where the animals were found and those where they were transplanted to will have differed in duration of tidal submergence. Mytilus edulis is a non-selective suspension feeder; its gills retain all particles larger than 2 to 5 ~m with 100% efficiency (DAVIDS, 1964; DRAL, 1967; VAHL, 1972; J@RGENSEN, 1975; BAYNE et al., 1977). The filtration rate is adapted to the concentration of suspended particles (LOOSANOFF & TOMMERS, 1948; J@RGENSEN, 1966; EORSTERSMITH, 1975). The clearance rate, i.e. the volume of water cleared of particles per unit of time, in Mytilus edulis is negatively correlated with the particle concentration in the water as shown by WIDDOWS et al. (1979). Their results show minimum feeding and pumping activity at suspended matter concentrations of - 2 2 0 , 260 and 330 g-m - 3 for mussels of 3, 5 and 7 cm in length. For the mussels used in the present study (mean lengths 21 to 28 mm) this critical value may be - 2 0 0 g.m -3. In the Dollard suspended matter
50
K. ESSINK & A.H. BOS
concentrations frequently surpass this value. The same may be the case at Site 2 due to resuspension of relatively muddy sediment. In laboratory experiments with mussels fed with algal cells WINTER (1976) found the filter feeding activity stimulated by low quantities of suspended silt. These findings, however, were obtained at low total suspended matter contents (less than 13 g.m-3). In Mya arenaria the organic matter content of the suspended matter seems to play a part in growth. This species tolerates low salinities and is relatively abundant in the central part of the Dollard (VAN ARKEL & MULDER, 1979, 1982), but the animals are relatively small here. MATTHIESEN (1960) found growth of Mya to be dependent on salinity. Highest densities, especially of young specimens, are normally found in fine sediments (KOHL, 1952; JEPSEN, 1965; WOLFF, 1973; ESSINK, 1978). Therefore, this species may be well adapted to high suspended matter concentrations. But, as Mya is reported to be a slow suspension feeder (THAMDRUP, 1935; MANN, 1952), the quality of the suspended matter is likely to be more important for growth than the quantity. As a matter of fact all 3 mollusc species showed significant correlations between growth and the organic matter content of the suspended matter during the last 3 months of the experiment (Table 1). However, the loss-of-weight-onignition method used for determining the organic matter content of the suspended matter is a rather crude one (DANKERS & LAANE, 1983). VAN ES & LAANE (1983) are of the opinion that the labile fraction of POC gives a better indication of food availability for filter feeders than total POC. They found that during the growing season of filter feeders the labile POC concentration as well as the ratio of labile POC to total POC increased from low values in the Dollard to high values in the outer part of the estuary. The work by VRINS (1978) on Cerastoderma edule also indicates that differences in quality of food play a part in the growth of this filter feeder. 6. REFERENCES
ANON., 1980. Kwaliteitsonderzoek in de rijkswateren. Verslag van de resultaten over 1980. Rijkswaterstaat, Rijksinstituut voor de Volksgezondheid, Rijksinstituut voor Drinkwatervoorziening, Lelystad. ARKEL, M.A. VAN & M. MULDER, 1979. Inventarisatie van de macrobenthische fauna van het Eems-Dollard estuarium. Publikaties en Verslagen Biologisch Onderzoek Eems-Dollard Estuarium, 1979-2.
, 1982. Macrobenthische fauna van het EemsDollard estuarium: een qualitatieve survey (1978); een quantitatieve survey (1979) veranderingen in een periode van vijf jaar. Publikaties en Verslagen Biologisch Onderzoek Eems-Dollard Estuarium, 1982-7. BAYNE, B.L., R.J. THOMPSON& J. WIDDOWS, 1976. Physiology I. In: B.L. BAYNE. Marine mussels: their ecology and physiology. Cambridge: 121-206. BAYNE, B.L., J. WIDDOWS & R.I.E. NEWELL, 1977. Physiological measurements on estuarine bivalve molluses in the field. In: B.F. KEEGAN, P.O'CEIDIGH & P.J.S. BOADEN. Biology of benthic organisms. Pergamon Press, Oxford: 57-68. CADEE, G.C. & J. HFGEMAN, 1974. Primary production of phytoplankton in the Dutch Wadden Sea.--Neth. J. Sea Res. 8: 240-259. COLIJN, F., 1983. Primary production in the EemsDollard estuary. Publikaties en Verslagen Biologisch Onderzoek Eems-Dollard estuarium, 1983-2 (Ph.D. thesis). DANKERS, N. & R.W.P.M. LAANE, 1983. A comparison of wet oxidation and loss on ignition of organic material in suspended matter.--Environm. Technol. Letters 4: 283-290. DAVIDS, C., 1964. The influence of suspensions of micro-organisms of different concentrations on the pumping and retention of food by the mussel (Mytilus edulis L.).--Neth. J. Sea Res. 2: 233-249. DITTMER, J.D., 1981, The distribution of subtidal macrobenthos in the estuaries of the rivers Ems and Weser. In: N. DANKERS,H. K(JHL & W.J. WOLFF. Invertebrates of the Wadden Sea. Balkema, Rotterdam: 189-206. DRAL, A.D.G., 1967. The movements of the laterofrontal cilia and the mechanism of particle retention in the mussel (Mytilus edulis L.).--Neth. J. Sea Res. 3." 391-422. EISMA, D., 1965. Shell characteristics of Cardium edule as indicators of salinity.--Neth. J. Sea Res. 2: 492-540. ES, F.B. VAN, 1977. A preliminary carbon budget for a part of the Ems estuary: the Dollard.-Helgol,~nder wiss. Meeresunters. 30: 283-294. Es, F.B. VAN & R.W.P.M. LAANE, 1982. The utility of organic matter in the Ems-Dollard estuary.--Neth. J. Sea Res. 16: 300-314. ESSINK, K., 1978. The effects of pollution by organic waste on macrofauna in the eastern Dutch Wadden Sea. Publication Series Netherlands Institute for Sea Research 1: 1-135. FOSTER-SMITH, R.L., 1975. The effect of concentration of suspension on the filtration rates and pseudofaecal production for Mytilus edulis L., Cerastoderma edule (L.) and Venerupis pullastra (Montagu).--J. exp. mar. Biol. Ecol. 17: 1-22. HELDER, W. & P. RUARDY,1982. A one-dimensional mixing and flushing model of the Ems-Dollard estuary: calculation of time scales at different river discharges.--Neth. J. Sea Res. 15: 293-312. JEPSEN, U., 1965. Die Struktur der WattenbiozSnosen im VormQndungsgebiet der Elbe.--Arch. Hydrobiol. 29: 252-370.
GROWTH OF TRANSPLANTED BIVALVES
JONGE, V.N. DE, 1983. Relation between annual dredging activities, suspended matter concentrations, and the development of tidal regime in the Ems estuary.--Can. J. Fish. Aq. Sci. 40 (Suppl. 1): 289-300. J@RGENSEN, C.B., 1966. Biology of suspension feeding. Pergamon Press, New York. - - - - , 1975. On gill function in the mussel Mytilus edulis L - - O p h e l i a 13: 187-232. KOCK, W.C. DE & J.M. MARQUENIE, 1981. De experimenteie toepassing van de mossel, Mytilus edulis L., bij het meten van zware metalen en organische microverontreinigingen in Nederlandse kustwateren. TNO, Delft, Rapport MD-N & E 81/2. KUHL, H., 1952. 0ber die Siedlungsweise yon Mya arenaria.--Verh, dt. zool. Ges. 1951: 385-391. KOHL, H, & H. MANN, 1973. Untersuchungen zur Hydrobiologie der unteren Ems.--Arch. FischWiss. 23: 243-268. LAANE, R,W.P.M., 1980. Conservative behaviour of dissolved organic carbon in the Ems estuary and the western Wadden Sea.--Neth. J. Sea Res. 14: 192-199. LOOSANOFF, M.L. & F.D. TOMMERS, 1948. Effect of suspended silt and other substances on the rate of feeding of oysters.--Science, N.Y. 107: 69-70. MANN, H., 1952. Vergleichende Unterschungen an einigen Muscheln des Watts.--Zool. Anz. (Suppl.) 16: 374-378, MATTHIESSEN, G.C., 1960. Observations on the ecology
51
of the soft clam, Mya arenaria, in a salt pond.-Limnol. Oceanogr. 5: 291-300. THAMDRUP, H., 1935. Beitr&ge zur Okologie der Wattenfauna auf experimentelle Grundlage.--Meddr Kommn Danm. Fisk.-og Havunders. (Ser. Fisk.) 10: 1-125. THEEDE, H. & J. LASSIG, 1967. Comparative studies on cellular resistance of bivalves from marine and brackish waters.--Helgol&nder wiss. Meeresunters. 16: 119-129. VAHL, O., 1972. Efficiency of particle retention of Mytilus edulis L. of different sizes.--Ophelia 12: 45-52. VOGEL, K., 1959. Wachstumunterbrechungen bei Lamellibranchiaten und Brachiopoden.--Neues Jb. Geol. Pal&ont. Abh. 109: 109-129. VRINS, A., 1978. De groei van populatiedichtheid van kokkels op enkele plaatsen in de Eems-Dollard. Publikaties en Verslagen Biologisch Onderzoek Eems-Dollard Estuarium, 1978-6. WINTER, J.E., 1976. Feeding experiments with Mytilus edulis L. at small laboratory scale. II. The influence of suspended silt in addition to algal suspensions on growth. In: G. PERSOONE & E. JASPERS. Proceedings of the 10th European Symposium on Marine Biology 1: 583-600. WOLFF, W.J., 1973. The estuary as a habitat.--Zo61. Verh., Leiden: 1-242. WOLFF, P. DE, 1978. Effects of organic waste on primary and secondary production in the Ems-Dollard estuary.--Hydrobiol. Bull. 12: 260-272.
OF THREE
BIVALVE MOLLUSCS TRANSPLANTED OF THE EMS ESTUARY
ALONG
THE AXIS
K. ESSINK and A. H. BOS Government Institute for Sewage and Waste Water Treatment (RIZA), Hereweg 99A, 9721 AA Groningen, The Netherlands
ABSTRACT Young specimens of Mya arenaria, Mytilus edulis and Cerastoderma edule were transplanted at the start of the growing season from the Wadden Sea to 5 sites in the Ems estuary. Changes in shell lengths and weights of the soft parts were determined by monthly sampling. Growth of all bivalves was relatively good in the outer part to decrease towards the inner parts of the estuary, reaching very low values in the innermost part in Cerastoderma and Mytilus. Along this traject strong gradients are present in salinity (decreasing), suspended matter (increasing) and TOC (increasing) to which factors growth was significantly correlated. Correlations were also found between growth and content of chlorophyll a and organic matter in the suspended matter, which factors did not show clear gradients in the estuary. The contribution of the individual environmental variables to total variability in growth could not be determined. It is supposed, however, that in the inner part of the estuary reduced salinity and enhanced suspended matter concentrations did affect Cerastoderma and Mytilus more than Mya.
ary at a number of places (VAN ES, 1977; DE WOLF, 1978). The macrobenthic fauna is relatively poor (VAN ARKEL & MULDER, 1979, 1982; DITTMER, 1981). Like many estuaries the Ems estuary has a high turbidity, especially in the inner part. As a consequence phytoplankton primary production is low (CADISE HEGEMAN, 1974; COLIJN, 1983). KOHL & MANN (1973) concluded that the turbidity in the estuary has increased from 1950 to 1970. Filter feeders like the mussel (Mytilus edulis), soft clam (Mya arenaria) and cockle (Cerastoderma edule) use their gills to obtain suspended particles from the water. The larger particles, are rejected as pseudofaeces. The remaining parti-
&
~s
40
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1. INTRODUCTION The Ems estuary forms a part of the Wadden Sea at the Dutch-German border (Fig. 1). Its estuarine characteristics are established by the discharge of fresh water by the river Ems and Westerwoldse Aa (WWA). The latter discharges into the Dollard. The hydrography of the estuary is summarized by DE WOLF (1978) and HELDER& RUARDY (1982). Organic waste is discharged into the estu-
!
N
~r~ ;,~ 53°1c.
Fig. 1.
o~ ~
7
Map of the Ems estuary with the location of the
experimental sites (11) and water sampling stations (o).
46
K. ESSINK & A.H. BOS
cles are transported to the mouth without any sorting according to quality (J@RGENSEN, 1966). The large amounts of suspended matter, as present in most estuaries, do not necessarily imply favourable feeding conditions. At a high density of suspended particles, a larger part of the material is rejected as pseudofaeces (J@RGENSEN, 1966; BAYNE et al., 1976). At still higher concentrations of suspended particles this may lead to low ingestion rates, which result in reduced growth. Mytilus and Cerastoderma occur in the outer and middle part of the estuary. Recordings from the brackish and turbid Dollard are rare. Mya occurs from the seaward end of the estuary to the central part of the Dollard (VAN ARKEL & MULDER, 1979, 1982). Results of transplantation experiments with cockles from the Ems estuary to the western Dutch Wadden Sea and vice-versa suggest growth limiting factors to be present in the Ems estuary (VRINS,1978). The quality of the suspended organic matter may be one of these factors (VAN ES & LAANE, 1982). One of the aims of RIZA is to increase knowledge on the functioning of the estuarine ecosystem under stress of human activities, such as dredging and discharging of waste. This knowledge may contribute to a more sound basis for the management of the estuary. The present study was undertaken to obtain information on the growth regulation of bivalves in the Ems estuary. Acknowledgements.--We are indebted to V.N. de Jonge, M.A. van Arkel and Dr. R.W.P.M. Laane for their comments on an early draft of the manuscript. Thanks are due to H.L. Kleef, P. Tydeman and the crew of the R.V. "Antares" for assistance in the field work. Mrs. H.E.J. BloemAbbingh typed the manuscript. Mr. R. Helsdingen prepared the figures. 2. MATERIAL AND METHODS 2.1. TRANSPLANTATION In the last week of April 1980, cockles, Cerastoderma edule, and soft clams, Mya arenaria, were collected in the eastern Dutch Wadden Sea 10 km west of Site 5. Mussels, Mytilus edulis, were collected 32 km west of Site 5 (Fig. 1). The day after collection 5 portions of 40 Cerastoderma and 40 Mytilus, and - 6 0 Mya of selected
sizes were transplanted to each of 5 experimental sites on the tidal flats of the Ems estuary (Fig. 1). The size range of the animals was 21.0 to 23.0 mm in Mytilus, 9.0 to 11.0 mm in Cerastoderma, and 6 to 15 mm in Mya. Galvanised wire netting was used to reduce loss by washing out or predation. The shells were color-marked to prevent mixing up with animals already present at the sites. All experimental sites were choosen in such a way that the time of submergence was about 7 hours per tide. With intervals of 4 weeks the portions were collected again and brought to the laboratory. Shell length was measured to the 0.1 mm below. Ash-free dry weight (ADW) of the soft parts was determined as described earlier (ESSlNK, 1978). In this transplant experiment animals with equal environmental history and equal genetic constitution are compared with respect to their growth under different environmental conditions. 2.2. ENVIRONMENTAL VARIABLES Information on environmental variables was derived from the Institutes weekly water quality monitoring programme (ANON., 1980). Only data from stations close to the experimental sites were used (Fig. 1). For each growth period, i.e. interval between successive collections of the molluscs, mean concentrations were calculated for salinity (measured as chlorosity), suspended matter, chlorophyll a, total organic carbon (TOC). The percentage of organic matter (POM) in the suspended matter, and the chlorophyll a content of the suspended matter were calculated to serve as an indication of the quality or utility of the suspended matter. 3. RESULTS Gales in spring and summer caused the loss of most of the transplanted animals at Site 4. Also at Site 1 and 3 some portions vanished. At Site 2 all cockles died between July 16 and August 15. Therefore, the planned monthly collection scheme was not completely realised. Part of the environmental variables, such as salinity, suspended matter and TOC, showed clear gradients in the estuary whereas others did not (Fig. 2). Salinity, chlorophyll a, chlorophyll a in suspended matter and TOC showed some seasonal variation; other variables varied both in time and space without much consistency. In Mytilus edulis the increase in mean ADW
f2s
S
GROWTH OF TRANSPLANTED BIVALVES
mgm
20
3
\
15
f
81 5 13 ,
,
,
|
,
1
2
2
4
5
d
0
% 20
rm-2 ]50
-
200
-
\
%~,
15
150 100 1o
50
e
b
m-3 5oo 'x
20O
C
1
2
3
4
47
Regression analyses were done, using only data from collection days on which samples from 3 or more sites were available (Table 1). Both shell length and ADW of the soft parts were positively correlated with the salinity in the preceding period of 4 weeks. The slope of the regression for cockles became steeper as time proceded. The few data for Mya suggest a similar trend. The growth of Cerastoderma was negatively correlated with the amount of suspended matter, as was the growth of Mytilus. In both species the data from July also showed a steeper regression than in previous months. For Mya no significant correlation was found in May and June. In July and August, however, when only data from 2 sites were available, the higher length and ADW, respectively, were found at the site with the lower suspended matter content. Shell growth and ADW showed negative relationships with the concentrations of both TOC and chlorophyll a. TOC in the Ems estuary consists mainly of DOC, which behaves conservatively (LAANE, 1980), and is inversely correlated with salinity. Positive correlations were present
5 she
Fig. 2. Some environmental parameters measured in the Ems estuary in the periods 24 April to 21 May (A), 22 May to 18 June (L~), 19 June to 15 July (O) and July 16 to August 15 (©) 1980. a. Mean salinity, b. Suspended matter (g-m-3), c.TOC (g-m-3), d. Chlorophyll a (mg-m-3), e. POM in suspended matter (%), f. Chlorophyll a in suspended matter (#g.g-1).
/
~mg 01
mm
30
/
20 5 28
I3 ~ 4
J I
w a s h i g h e s t in the outer half of the e s t u a r y (Sites
conditions did deteriorate during summer (Fig. 3). Site 5, at which Mytilus showed the highest increase in ADW, the growth of the shell was not significantly different from growth at Sites 3 and 4. In Cerastoderma edule the growth of soft parts and shell was far less in the inner part than in the outer part of the estuary (Fig. 4). These results show the same pattern as found in Mytilus. The distribution of growth rates of Mya arenaria (Fig. 5) differed somewhat from those observed in Cerastoderma and Mytilus. As far as data are available, growth of Mya at Site 1 was similar to that at Site 3 and 5 during the first 2 months of the experiments. Reduced growth was most clear at Site 2.
/i
~5o
26 /'
3 ,
100 '//
24
,,~,
~--------~---/'"~ 12
/" 22
501
IA
I M I J
I
J
I
A
]
1A
I
M
I
j
I j
I
A
I
Fig. 3. Mean shell length (mm) and mean ADW of the soft parts (mg) with standard deviations of Mytilus edulis at the experimental sites 1 to 5 in 1980.
48
K. ESSINK & A.H. BOS
25 rnm
5
mg 15C
3
5
20 100
15
10•
I A
7 I M
1J
50
2
i J
I A
I
0
A IM IJ
I J I A I
Fig. 4. Mean shell length (mm) and mean ADW of the soft parts (mg) with standard deviations of Cerastoderma edule at the experimental sites 1 to 5 in 1980.
between growth of shell and soft parts and the qualitative aspects of suspended matter (chlorophyll a and POM content). These correlations became s i g n i f i c a n t in June-July, and were present most clearly in Cerastoderma and Mytilus (Table 1).
lead to the mortality of C e r a s t o d e r m a and to the reduced growth of Mya at Site 2 after July 15 (Fig. 5). These phenomena show a parallel to the decreasing tolerance of low salinities by Cera s t o d e r m a , Mytilus and Mya (WOLFF, 1973). In the regression analyses Mya showed less strong correlations between growth and environmental variables than Mytilus and Cerastoderma. This may at least partly be caused by the larger variation in initial lengths and weights in the transplanted Mya specimens as compared with Mytilus and Cerastoderma. In the last 3 months of the experiment all three bivalve species showed significant correlations between growth and 2 or more of the environmental variables measured. The question w h i c h of these variables are responsible for the major part of the variation in the growth recorded cannot be easily answered as some environmental variables are mutually strongly correlated (Fig. 2), e.g. salinity and suspended matter. Furthermore, the question can be raised whether the environmental variables measured at the water sampling stations are representative. It is likely
30- mm
mg
25 -
4. DISCUSSION
~2
1
100 i
All 3 species showed relatively fast growth rates in the outer part of the estuary, and reduced growth in the inner part. In the outer part of the estuary, however, growth did not appear to be optimal. Data from mussels held in cages suspended from buoys show that in the summer of 1980 growth of the soft parts of Mytilus edulis in the outer part of the Ems estuary was less than in the western most part of the Dutch Wadden Sea (DE KOCK & MARQUENIE, 1981). The decrease in weight in Cerastoderma and Mytilus observed at Site 2 between June 18 and July 15 may have been the effects of surplus fresh water pumped into the estuary 1 km west of this site during an extremely wet spell that lasted from June 23 till July 27. This fresh water reached Site 2 during flood tide relatively unmixed with estuarine waters (H.L. KLEEF, personal communication). These local c o n d i t i o n s may also have
3z / ///i 5 //
20-
50 15-
10-
IA
IMIJ
IJ
IA
I
A I M I J I J I A 1
Fig. 5. Mean shell length (mm) and mean ADW of the soft parts (mg) with standard deviations of Mya arenaria at the experimental sites 1 to 5 in 1980.
GROWTH OF TRANSPLANTED BIVALVES
49
TABLE 1 Regression equations (y -- ax + b) and linear correlation coefficients (r) for the relation between shell length and ADW (y) of the 3 bivalves (Mytilus edulis, Mya arenaria, Cerastoderma edule) and the environmental variables (x) salinity, suspended matter (g.m-1), POM (% in suspended matter)and chlorophyll in suspended matter (/zg.g-1) (no regression data are given in case of correlation coefficients with p >0.05). Species
Environmental variable
Date
N
Mytilus
Salinity Suspended matter POM in susp. matter Chlor. in susp. matter
Aug. Aug. Aug. Aug.
15 15 15 15
117 117 117 117
Mya
Salinity
May 21 June 18 May 21 June 18 June 18 June 18
102 110 102 110 110 110
May 21 June 18 July 15 May 21 June 18 July 15 May 21 June 18 July 15 May 21 June 18 July 15
124 110 31 124 110 31 124 110 31 124 110 31
Susp. matter POM in susp. matter Chlor. in susp. matter Cerastoderma
Salinity Susp. matter POM in susp. matter Chlor. in susp. matter
that the samples taken in the tidal channels do not represent the c o n d i t i o n s of the water pumped through by the transplanted bivalves at the sites on the flats. Therefore, the results should be interpreted with caution. The role of salinity as important factor governing the growth of Cerastoderma edule can be well understood. Of the 3 species in this experiment it is least tolerant to low salinities (THEEDE & LASSIG, 1967; WOLFF, 1973). Recordings of Cera s t o d e r m a edule from the brackish Dollard are rare (VAN ARKEL & MULDER, 1979, 1982). The observed mortality at Site 2 during a period of fresh water discharge fits in this picture. A positive relation between salinity and shell growth was reported by VOGEL (1959) and EISMA (1965). VRINS (1978) transplanted cockles from the Eros estuary (close to our Site 4) to more saline waters in the western Dutch Wadden Sea near Texel and vice versa. She concluded that growth limiting factors were present in the Ems estuary, She also found increasing mean lengths of 2 year old cockles from Delfzijl to Borkum, i.e. with increas-
Shell length (ram) r
a
0.66 -0.77 0.29 0.81
0.46 -0.03 0.35 0.02
b
20.21 28.65 20.79 21.31
ADW (mg) r
0.19 0.49 0.78 - 0,02 -0.02 -0.05 0.11 0.67 1.13 0.01 0.03
9.08 9.90 8.13 12.96 17.61 23.01 9.97 6.97 2.74 12.76 9.80
b
0.84 1 7 . 2 -75.2 -0.80 -0.9 218.2 0.59 2 0 . 6 -159.2 0.76 0,5 6.6 0.15 0.26 -0.14 -0.11 0.40 0.13
0.55 0.80 0.91 - 0.56 -0.64 -0.92 0.20 0.72 0.92 0.16 0.48 0.94
a
2.0
33.5
4.8
-6.3
0.55 1.6 2.6 0.89 7.1 -34.2 0.91 1 2 . 5 -92.4 - 0.57 - 0.2 34.8 -0.74 -0.3 78.0 -0.92 -0.8 145.2 0.09 0.75 9.0 -68.0 0.92 17.9 - 175.7 0.01 0.53 0.1 7.9 0.89 0.4 - 56.7
ing salinity. These data cannot be explained unequivocally as the locations where the animals were found and those where they were transplanted to will have differed in duration of tidal submergence. Mytilus edulis is a non-selective suspension feeder; its gills retain all particles larger than 2 to 5 ~m with 100% efficiency (DAVIDS, 1964; DRAL, 1967; VAHL, 1972; J@RGENSEN, 1975; BAYNE et al., 1977). The filtration rate is adapted to the concentration of suspended particles (LOOSANOFF & TOMMERS, 1948; J@RGENSEN, 1966; EORSTERSMITH, 1975). The clearance rate, i.e. the volume of water cleared of particles per unit of time, in Mytilus edulis is negatively correlated with the particle concentration in the water as shown by WIDDOWS et al. (1979). Their results show minimum feeding and pumping activity at suspended matter concentrations of - 2 2 0 , 260 and 330 g-m - 3 for mussels of 3, 5 and 7 cm in length. For the mussels used in the present study (mean lengths 21 to 28 mm) this critical value may be - 2 0 0 g.m -3. In the Dollard suspended matter
50
K. ESSINK & A.H. BOS
concentrations frequently surpass this value. The same may be the case at Site 2 due to resuspension of relatively muddy sediment. In laboratory experiments with mussels fed with algal cells WINTER (1976) found the filter feeding activity stimulated by low quantities of suspended silt. These findings, however, were obtained at low total suspended matter contents (less than 13 g.m-3). In Mya arenaria the organic matter content of the suspended matter seems to play a part in growth. This species tolerates low salinities and is relatively abundant in the central part of the Dollard (VAN ARKEL & MULDER, 1979, 1982), but the animals are relatively small here. MATTHIESEN (1960) found growth of Mya to be dependent on salinity. Highest densities, especially of young specimens, are normally found in fine sediments (KOHL, 1952; JEPSEN, 1965; WOLFF, 1973; ESSINK, 1978). Therefore, this species may be well adapted to high suspended matter concentrations. But, as Mya is reported to be a slow suspension feeder (THAMDRUP, 1935; MANN, 1952), the quality of the suspended matter is likely to be more important for growth than the quantity. As a matter of fact all 3 mollusc species showed significant correlations between growth and the organic matter content of the suspended matter during the last 3 months of the experiment (Table 1). However, the loss-of-weight-onignition method used for determining the organic matter content of the suspended matter is a rather crude one (DANKERS & LAANE, 1983). VAN ES & LAANE (1983) are of the opinion that the labile fraction of POC gives a better indication of food availability for filter feeders than total POC. They found that during the growing season of filter feeders the labile POC concentration as well as the ratio of labile POC to total POC increased from low values in the Dollard to high values in the outer part of the estuary. The work by VRINS (1978) on Cerastoderma edule also indicates that differences in quality of food play a part in the growth of this filter feeder. 6. REFERENCES
ANON., 1980. Kwaliteitsonderzoek in de rijkswateren. Verslag van de resultaten over 1980. Rijkswaterstaat, Rijksinstituut voor de Volksgezondheid, Rijksinstituut voor Drinkwatervoorziening, Lelystad. ARKEL, M.A. VAN & M. MULDER, 1979. Inventarisatie van de macrobenthische fauna van het Eems-Dollard estuarium. Publikaties en Verslagen Biologisch Onderzoek Eems-Dollard Estuarium, 1979-2.
, 1982. Macrobenthische fauna van het EemsDollard estuarium: een qualitatieve survey (1978); een quantitatieve survey (1979) veranderingen in een periode van vijf jaar. Publikaties en Verslagen Biologisch Onderzoek Eems-Dollard Estuarium, 1982-7. BAYNE, B.L., R.J. THOMPSON& J. WIDDOWS, 1976. Physiology I. In: B.L. BAYNE. Marine mussels: their ecology and physiology. Cambridge: 121-206. BAYNE, B.L., J. WIDDOWS & R.I.E. NEWELL, 1977. Physiological measurements on estuarine bivalve molluses in the field. In: B.F. KEEGAN, P.O'CEIDIGH & P.J.S. BOADEN. Biology of benthic organisms. Pergamon Press, Oxford: 57-68. CADEE, G.C. & J. HFGEMAN, 1974. Primary production of phytoplankton in the Dutch Wadden Sea.--Neth. J. Sea Res. 8: 240-259. COLIJN, F., 1983. Primary production in the EemsDollard estuary. Publikaties en Verslagen Biologisch Onderzoek Eems-Dollard estuarium, 1983-2 (Ph.D. thesis). DANKERS, N. & R.W.P.M. LAANE, 1983. A comparison of wet oxidation and loss on ignition of organic material in suspended matter.--Environm. Technol. Letters 4: 283-290. DAVIDS, C., 1964. The influence of suspensions of micro-organisms of different concentrations on the pumping and retention of food by the mussel (Mytilus edulis L.).--Neth. J. Sea Res. 2: 233-249. DITTMER, J.D., 1981, The distribution of subtidal macrobenthos in the estuaries of the rivers Ems and Weser. In: N. DANKERS,H. K(JHL & W.J. WOLFF. Invertebrates of the Wadden Sea. Balkema, Rotterdam: 189-206. DRAL, A.D.G., 1967. The movements of the laterofrontal cilia and the mechanism of particle retention in the mussel (Mytilus edulis L.).--Neth. J. Sea Res. 3." 391-422. EISMA, D., 1965. Shell characteristics of Cardium edule as indicators of salinity.--Neth. J. Sea Res. 2: 492-540. ES, F.B. VAN, 1977. A preliminary carbon budget for a part of the Ems estuary: the Dollard.-Helgol,~nder wiss. Meeresunters. 30: 283-294. Es, F.B. VAN & R.W.P.M. LAANE, 1982. The utility of organic matter in the Ems-Dollard estuary.--Neth. J. Sea Res. 16: 300-314. ESSINK, K., 1978. The effects of pollution by organic waste on macrofauna in the eastern Dutch Wadden Sea. Publication Series Netherlands Institute for Sea Research 1: 1-135. FOSTER-SMITH, R.L., 1975. The effect of concentration of suspension on the filtration rates and pseudofaecal production for Mytilus edulis L., Cerastoderma edule (L.) and Venerupis pullastra (Montagu).--J. exp. mar. Biol. Ecol. 17: 1-22. HELDER, W. & P. RUARDY,1982. A one-dimensional mixing and flushing model of the Ems-Dollard estuary: calculation of time scales at different river discharges.--Neth. J. Sea Res. 15: 293-312. JEPSEN, U., 1965. Die Struktur der WattenbiozSnosen im VormQndungsgebiet der Elbe.--Arch. Hydrobiol. 29: 252-370.
GROWTH OF TRANSPLANTED BIVALVES
JONGE, V.N. DE, 1983. Relation between annual dredging activities, suspended matter concentrations, and the development of tidal regime in the Ems estuary.--Can. J. Fish. Aq. Sci. 40 (Suppl. 1): 289-300. J@RGENSEN, C.B., 1966. Biology of suspension feeding. Pergamon Press, New York. - - - - , 1975. On gill function in the mussel Mytilus edulis L - - O p h e l i a 13: 187-232. KOCK, W.C. DE & J.M. MARQUENIE, 1981. De experimenteie toepassing van de mossel, Mytilus edulis L., bij het meten van zware metalen en organische microverontreinigingen in Nederlandse kustwateren. TNO, Delft, Rapport MD-N & E 81/2. KUHL, H., 1952. 0ber die Siedlungsweise yon Mya arenaria.--Verh, dt. zool. Ges. 1951: 385-391. KOHL, H, & H. MANN, 1973. Untersuchungen zur Hydrobiologie der unteren Ems.--Arch. FischWiss. 23: 243-268. LAANE, R,W.P.M., 1980. Conservative behaviour of dissolved organic carbon in the Ems estuary and the western Wadden Sea.--Neth. J. Sea Res. 14: 192-199. LOOSANOFF, M.L. & F.D. TOMMERS, 1948. Effect of suspended silt and other substances on the rate of feeding of oysters.--Science, N.Y. 107: 69-70. MANN, H., 1952. Vergleichende Unterschungen an einigen Muscheln des Watts.--Zool. Anz. (Suppl.) 16: 374-378, MATTHIESSEN, G.C., 1960. Observations on the ecology
51
of the soft clam, Mya arenaria, in a salt pond.-Limnol. Oceanogr. 5: 291-300. THAMDRUP, H., 1935. Beitr&ge zur Okologie der Wattenfauna auf experimentelle Grundlage.--Meddr Kommn Danm. Fisk.-og Havunders. (Ser. Fisk.) 10: 1-125. THEEDE, H. & J. LASSIG, 1967. Comparative studies on cellular resistance of bivalves from marine and brackish waters.--Helgol&nder wiss. Meeresunters. 16: 119-129. VAHL, O., 1972. Efficiency of particle retention of Mytilus edulis L. of different sizes.--Ophelia 12: 45-52. VOGEL, K., 1959. Wachstumunterbrechungen bei Lamellibranchiaten und Brachiopoden.--Neues Jb. Geol. Pal&ont. Abh. 109: 109-129. VRINS, A., 1978. De groei van populatiedichtheid van kokkels op enkele plaatsen in de Eems-Dollard. Publikaties en Verslagen Biologisch Onderzoek Eems-Dollard Estuarium, 1978-6. WINTER, J.E., 1976. Feeding experiments with Mytilus edulis L. at small laboratory scale. II. The influence of suspended silt in addition to algal suspensions on growth. In: G. PERSOONE & E. JASPERS. Proceedings of the 10th European Symposium on Marine Biology 1: 583-600. WOLFF, W.J., 1973. The estuary as a habitat.--Zo61. Verh., Leiden: 1-242. WOLFF, P. DE, 1978. Effects of organic waste on primary and secondary production in the Ems-Dollard estuary.--Hydrobiol. Bull. 12: 260-272.