- Email: [email protected]
Producer-consumer relationships in the sea. II. Correlation between Mytilus pigmentation and the density and composition of phytoplanktonic populations in inshore waters
J. exp. mar. Biol. Ecol., 1970, Vol. 5,
pp. 246-253; North-Holland
PRODUCER-CONSUMER
Publishing Company, Amsterdam
RELATIONSHIPS IN THE SEA.
II. CORRELATION BETWEEN MYTZLUS PIGMENTATION AND THE DENSITY AND COMPOSITION
OF PHYTOPLANKTONIC
POPULATIONS
IN INSHORE WATERS ARNEJENSEN Norwegian
Institute
of Seaweed
Research,
Trondheim,
Norway
and
EGILSAKSHAUG The Royal Norwegian
Society
of Sciences and Leiters,
The Museum,
Trondheim,
Norway
Abstract: A simple, automatic water sampler has been constructed and used to study in detail the variations in phytoplanktonic densities around populations of the edible mussel (Myti~~~ edzdis L.). Very rapid fluctuations were observed in the plankton counts. A good correlation between these and the total carotenoid content of the mussels was found, together with considerable seasonal variation in the pigmentation of the mussels. Analyses of the pigments strongly indicated that the large dinoflagellates are at least partly assimilated by the edible sea mussel.
INTRODUCTION
A preliminary study has established a reasonable correlation in the Trondheimsfjord between the density of phytoplankton and the concentration of pigments in the edible mussel, &I~tilus edulis L. (Jensen & Sakshaug, 1970). To study this relationship in more detail, it was necessary to develop an automatic water sampler which pumps sub-samples every half-hour from the water surrounding the mussel population. The present paper describes the water sampler, gives the data for phytoplankton densities obtained with it, and deals with the relationship between these data and the pigment concentration in the mussels.
METHODS AND MATERIALS
The apparatus for the sampling of sea water is shown in Fig. 1, and consisted of an LKB fraction coilector and timer unit (Rotator 3401 B, turntable disk 3406 A, guide plate 3410 B, spiral guide 3413 A and controller 3403 B from LKB-Produkter AB, Stockholm, Sweden) a Jabsco pump (Model AL-$-200 from Jabsco Pump Company Ltd., Cheshunt, Herts., England) fitted with a + HP motor giving approximately 300 rpm, and an adjustable time-delay switch. A special device for discarding hold-up water in the suction hose and the pump consisted of a horizontal brass tube (15 mm inner diameter) with one inlet and three outlets. The first outlet was connected 246
PRODUCER-CONSUMER
tII
RELATIONSHIPS
IN THE SEA. II.
Fig. 1. Automatic sea water sampler: for explanation
247
see text.
to a plastic bottle (A) of - 250 ml capacity, which was stoppered tightly and fitted with a narrow siphon. The second outlet was shaped as a vertical brass cylinder (B), 100 x 15 mm, which ended in a glass capillary of - 1 mm internal diameter. Surplus water left the system through the third outlet (D). On a signal from the controller unit, the pump started and at the same time the turntable moved one step forward. The pump first filled the discarder flask (A) and when this was full, water flowed over into the sampling cylinder (B) and through the capillary into a test tube in the fraction collector. The pumping period and capacity was regulated so that there was a good overflow at D. After a suitable period, the time-delayed switch (C) stopped the pump, and flask A was slowly emptied through the siphon. In order to preserve the samples, all test tubes in the fraction collector contained 0.5 ml of 10 ‘A, neutralized formalin solution. The water sampler was placed on the quay in the Muruvik Bay in the Trondheimsfjord with the sampling hose (vacuum rubber tubing) extending into the mussel population growing on the wooden construction underneath. The intake was kept in a fixed position, - 1 m below the lowest tide mark. From the beginning of April, 1969 and throughout June, water samples each of - 30 ml were taken every 30 min. Later this interval was increased to 1 h. The sub-samples were pooled (12 x 12) giving four and two samples per day, respectively. Pooling was carried out every 5th and 10th day, respectively, and the samples were brought to the laboratory for counting by the Utermohl technique (Utermiihl, 1931). Mussel samples were obtained every week from the population surrounding the pump intake. Pigment analysis was carried out on 10-15 adult individuals as described by Jensen & Sakshaug (1970). In addition to the concentration and composition of carotenoids the content of chlorophyll-like pigments was determined by paper chromatography in cases were the epiphase showed traces of a green colouration. The
ARNE JENSEN AND EGIL SAKSHAUG
248
quantitative estimation was based on an estimated (St011 & Wiedemann, 1959).
Ei ci of 890, as for chlorophyll
a
RESULTS
Some sub-samples were lost because of frost, interruptions of the power supply, and for mechanical reasons. Complete samples were obtained for 156 out of the 186 days covered by the present investigation. The phytoplankton counts for each day were grouped into the following classes: total number of diatoms; total number of dinoflagellates; Phaeocystis pouchetii (Hariot) Lagerheim, and Coccolithus huxleyi (Lohmann) Kamptner. Fig. 2 shows the more pronounced variations in plankton
APRIL
MA”
JUNE
JULY
AUGUST
SEPTEMBER
OCTOBER
Fig. 2. Phytoplankton counts (cells/l), total carotenoids and ‘chlorophyll’ in Myrilus edulis L. (mg/kg of acetone extracted dry matter) at Muruvik 1969: l total carotenoids; x ‘chlorophyll’; 0 Coccolithus huxleyi; 0 total diatoms; A Phaeocystic pouchetii; 0 total dinoflagellates.
counts given as the logarithm of the number of organisms per litre of sea water. The content of total carotenoids and chlorophyll-like pigment in the mussels are also given in this Figure. The variation in the composition of the carotenoid pigments is given in Fig. 3, in which the percentage of the three main components is shown as a function of time. These groups of pigments are the same as found previously (Jensen & Sakshaug, 1970). In all, six zones were found on the paper chromatograms; but zones 1, 2 and
60 -
I FEBRUARY
I
I
I MARCH
PlPRlL
MAY
1 JUNE
I JULY
A”G”ST
I SEPTEMBER
I OCTOBER
Fig. 3. Seasonal variation of the main carotenoid groups in lwyfiZus e&is L., expressed as %total carotenoids, Muruvik 1969: 0 Group 3 pigments; 0 Group 4 pigments; x Group 6 pigments; ,JJ tota carotenoids in mgjkg of acetone extracted dry matter.
5 made up 5-10 % each of the total and remained nearly constant throughout whole period.
the
DISCUSSION
In the preceding paper of the present series (Jensen & Sakshaug, 1970) it was shown that the seasonal variation in the content of total carotenoids in mussels followed the gross changes in phytoplankton density in the fiord. It was evident, however, that very frequent sampling of the plankton would be required to allow more detailed studies to be carried out, and that this should preferably be done in the inshore water surrounding the mussels. The sampling method used in the present study was not expected to give an estimate of the phytoplankton population in the whole water column, since the samples were taken exclusively in the 1-4 m layer (depending on the tidal movements), but it should have given representative samples of the body of water available to the mussel population in question. It may be seen from Fig. 2 that the density of phytoplankton in the water which surrounded the mussels underwent rapid changes. The experiment started in early April during the rapid decline of the early spring bloom, which consisted of a mixed population of Phaeocystis pouchetii and diatoms, mainly Chaetoceros debilis Cleve, C. decipiens Cleve, ~keletone~a co~t~t~~ (Grev.) Cleve, and T~~la~s~o~ira~rovi~
250
ARNE
JENSEN
AND
EGIL
SAKSHAUG
Cleve. Phareocystis dropped from 140 000 to virtually zero cells/l in 4 days. After a minimum period in late April, a diatom bloom took place in May with Chaetoceros ~~nstr~ct~sG-an predominating (m~imum 19th May, 103 500/l). It coincided with a small dinoflagellate maximum made up of Peridinium truchoideum (Stein) Lemmermann (max. 16th May, 11200/l), together with minute amounts of Govlyaulax tamarensis Lebour and Peridinium ovatum (Pouchet) Schiitt. Tn summer, Nitzschia delicatissima-type cells (max. 16th June, 264 000/l>, Thalassionema nitzschioides and C~ccu~~th~s huxleyi (max. 6th July, ~runow (max. 17th June, 294~/1), 1 172000/l) populated the water for variable periods. The sparse phytoplankton population in autumn consisted practically only of dinoflagellates, mainly Ceratium ,fusus (Ehrenberg) Dujardin (max. 8th Sept., 4260/l). We regard the events mentioned above as regular blooms which took place in the water surrounding the mussels, and the planktonic organisms were available for the mussels to feed upon for a considerable period. Tn some cases the bloom was followed by very irregular peaks in the density of the phytoplankton. In three instances the concentration of Thalassionema rose from a background level of 20 000 to nearly 200 000 cells/l in one day and dropped back again to the 20 000 cells/l the next day. The peaks did not coincide with spring tides allowing the pump to sample deeper strata; it is, therefore, suggested that they have hydrographical causes. Water rich in phytoplankton may have been brought up within reach of the pump during a local upwelling situation, or it may have been brought to the pump by rapid horizontal transport of water. In this connection it may be mentioned that, in the open fiord, several of the blooms tended to last longer at greater depths than in surface water during the warm summer of 1969. The bloom of Chaetoceros constrictus in May gave rise to a very pronounced peak in the concentration of pigments in the mussels, while the large amount of Phaeocystis pouchelii of the spring bloom did not seem to be similarly effective. The latter organism belongs to the group which Yonge (1926) would characterize as “many small particles imbedded in mucus” and which would tend to be rejected by the mussels. This may partly explain why the occurrence of this planktonic species did not result in a corresponding increase of mussel pigmentation. It should be noticed that the green, chlorophyll-like pigments were found in the mussels only during the blooms of Phaeocystis pouchetii and Chaetoceros constrictus. The first part of the summer was characterized by blooms of Nitzschia and Thalassionema, neither of which was reflected in the pigment content of the mussels. A population of Coccolithus huxleyi, also invaded the water during the middle of the summer without affecting the mussel pigmentation. All these species are very small and with little pigmentation and thus represented negligible quantities of pigments as well as a small biomass. The rest of the period was dominated by dinoflageliates, although their number remained rather low, at less than 6000 cells/l. The small variations that occurred were, however, immediately followed by changes in the pigmentation of the mussels.
PRODUCER-CONSUMER
RELATIONSHIPS
IN THE SEA. II.
251
Since the dinoflagellates were relatively large and heavily pigmented, and since the variations in plankton density and pigment concentration in the mussels followed each other closely, we are led to believe that the observed correlation is real and that the mussels were able to respond to the low concentrations of dinoflagellates observed. It has been indicated in the literature (Kellogg, 1915; Loosanoff & Engle, 1947; Davids, 1964) that low particle contents lead to better utilization by the mussels, and this may help to explain the high efficiency of the dilute plankton populations in autumn relative to the low effect of the rather dense blooms that occurred in spring and summer. These observations are in apparent conflict with those of Coe (1947) who could not find any traces of the larger dinoflagellates among the stomach contents of mussels, a finding which led Boje (1965) to assume that these and other large and spiny species are not utilized by mussels. The fact that the ~arotenoid content of the mussels increased rapidly during blooms of large dinoflagellates as demonstrated by us for two consecutive years, strongly indicates that these plants are indeed both removed from the water, and retained, by the mussel. There, was no sign of chlorophylls or their derivatives in the mussels during the autumn blooms which implies that the major part of the ingested dinoflagellates were dead when the mussels were collected. It is, therefore, not possible that they had been merely filtered off and were awaiting rejection in a more or less intact state as pseudo-faeces. The quantitative aspects of the process also strongly indicate that the mussels must have accumulated the algae over several days in order to produce the increase observed in the pigment content. Furthermore, the composition of the mussel pigments was always different from that of the algae in the surrounding water masses. We are, therefore, led to conclude that the edible mussel is able to assimilate rather efficiently at least the carotenoid pigments of large dinoflagellates such as Ceratium fusus. The well known fact that mussels can accumulate toxin very rapidly from Gonyaulax species also shows that molluscs must have an efficient mechanism for the assimilation of other dinoflagellates. The literature contains conflicting reports regarding the influence of season on the content of carotenoids in molluscs. While Scheer (1940) found no marked seasonal variation in any of the carotenoids of the California sea mussel (Myth californianus), Lederer (1938) reported that the carotenoid content of the scallop (Pecten maximus) varied greatly with the season. The seasonal variations established for the edible mussel by us in both the preceding and present study were quite significant. Scheer always kept the mussels for IO-20 h in clean sea water to clear them of faecal pellets, whereas in our studies the animals were analysed shortly after collection. This, however, should require only a small correction to the carotenoid contents found in the present studies, since it would have been necessary for the mussels to accumulate the pigments over several days in order to bring about the observed increases. The rapid decreases in pigment concentrations shown by the mussels when the plankton counts dropped must mean that at least a large fraction of these pigments has a high turnover. Part of the carotenoids could be lost during spawning. Yet the
252
ARNE JENSEN AND EGIL SAKSHAUG
dry weight content per mussel remained fairly constant throughout spring, summer, and autumn, indicating that no well-defined period of mass spawning occurred in 1969. Lande (1969) observed that the edible sea mussel spawned both in spring and in autumn in the inner part of the Trondheimsfjord. This rather extended spawning cannot explain the rapid variations in pigment concentration of the mussels. In agreement with previous findings (Jensen & Sakshaug, 1970) the pigments of the mussels were again found to be dominated by three groups of components, namely Groups 3,4 and 6 (see Fig. 3). Also Groups 3 and 4 again showed tendencies towards an inverse relationship. The pigments of Group 6 increased relatively more than did the others during blooms of Ph~eoc~sti~ pouchetii and Chaetoceros con~t$ict~s in spring and early summer. The pigment composition remained fairly constant during summer and autumn this year, a fact which may be related to the lack of a typical autumn bloom of phytoplankton in the water during the 1969 observations. The close correlation between mussel pigmentation and phytoplankton occurrence makes pigment analysis in plankton and filter-feeders a promising tool for studying the uptake and assimilation of the former by the latter organisms. Identification of carotenoids derived from peridinin in sea mussel tissue during blooms of large dinoflagellates would prove conclusively that the mussels can assimilate this food, even though a mechanism for this process is not known.
ACKNOWLEDGEMENTS The authors are indebted to the Norwegian Research Council for Science and the
Humanities and to Fiskerinreringens Forskningsfond for financial support. We are grateful to Meraker Smelteverk A/S, Muruvik for technical facilities and to Mrs. lngjerd Mehli for skilful technical assistance.
REFERENCES BOJE,R., 1965.Die Bedeutung von Nahrungsfaktoren fiir das Wachstum von Myriius edulis L. in der Kieler F&de und im Nerd-Ostsee-Kanal. Kkier ~ee~es~~~~c~., Bd 21, S. 81-100. COE, W. R., 1947. Nutrition, growth and sexuality of the Pismo clam (Tiuefa stttltoram). J. exp. Zooi., Vol. 104, pp. 1-14. DAVID%C., 1964. The influence of suspensions of microorganisms of different concentrations on the pumping and retention of food by the mussel (Mytilus edulis L.) Neth. J. Sea Res., Vol. 2, pp. 233-249.
JENSEN,A. &E. SAKSHAUG,1970. Producer-consumer relationships in the sea. I. Preliminary studies on phytoplankton density and Mytilus pigmentation. J. exp. mar. Biol. Ecol., Vol. 5, pp. 180-186. KELLOGG,J. L., 1915. Ciliary mechanisms of lametlibranchs with descriptions of anatomy. .I. Morph., Vol. 26, pp. 625-701. LANDE,E., 1969. En undersskelse av vekst, gyting og dodelighet hos btaskjell ~~~t~~/~~ edttlis L.) pa to iokaliteter i Trondheimsfjorden. Thesis, University of 0~10, 67 pp. LEDERER,E., 1938. Recherches sur les carotCno?ds des invertebres. Bull. Sm. Chim. bioi., T. 20, pp. 567-610.
LOOSANOFF, V. L. & J. B. ENGLE, 1947. Effect of different concentrations of micro-organisms feeding of oysters (Ostrea virginica). U.S. Fish Wildl. Serv. Bull., Vol. $1, pp. 31-57.
on the
PRODUCER-CONSUMER
RELATIONSHIPS
IN THE SEA. II.
253
SCHEER,B. T., 1940. Some features of the metabolism of the carotenoid pigments of the California sea mussel (Mytilus californianus). J. biol. Chem.. Vol. 136, pp. 275-299. STOLL, A. & E. WIEDEMANN,1959. Die kristallisierten natiirlichen Chlorophylle a und b. Helv. chim. Acta, Bd 42, S. 679-683. UTERMBHL,H., 1931. Neue Wege in der quantitativen Erfassung des Planktons. Verh. int. Verein. theor. angew. Limnol., Bd 5, S. 567-595. YONGE,C. M., 1926. Structure and physiology of the organs of feeding and digestion in Oshea edulis. J. mar. biol. Ass. U.K., Vol. 14, pp. 295-386.
pp. 246-253; North-Holland
PRODUCER-CONSUMER
Publishing Company, Amsterdam
RELATIONSHIPS IN THE SEA.
II. CORRELATION BETWEEN MYTZLUS PIGMENTATION AND THE DENSITY AND COMPOSITION
OF PHYTOPLANKTONIC
POPULATIONS
IN INSHORE WATERS ARNEJENSEN Norwegian
Institute
of Seaweed
Research,
Trondheim,
Norway
and
EGILSAKSHAUG The Royal Norwegian
Society
of Sciences and Leiters,
The Museum,
Trondheim,
Norway
Abstract: A simple, automatic water sampler has been constructed and used to study in detail the variations in phytoplanktonic densities around populations of the edible mussel (Myti~~~ edzdis L.). Very rapid fluctuations were observed in the plankton counts. A good correlation between these and the total carotenoid content of the mussels was found, together with considerable seasonal variation in the pigmentation of the mussels. Analyses of the pigments strongly indicated that the large dinoflagellates are at least partly assimilated by the edible sea mussel.
INTRODUCTION
A preliminary study has established a reasonable correlation in the Trondheimsfjord between the density of phytoplankton and the concentration of pigments in the edible mussel, &I~tilus edulis L. (Jensen & Sakshaug, 1970). To study this relationship in more detail, it was necessary to develop an automatic water sampler which pumps sub-samples every half-hour from the water surrounding the mussel population. The present paper describes the water sampler, gives the data for phytoplankton densities obtained with it, and deals with the relationship between these data and the pigment concentration in the mussels.
METHODS AND MATERIALS
The apparatus for the sampling of sea water is shown in Fig. 1, and consisted of an LKB fraction coilector and timer unit (Rotator 3401 B, turntable disk 3406 A, guide plate 3410 B, spiral guide 3413 A and controller 3403 B from LKB-Produkter AB, Stockholm, Sweden) a Jabsco pump (Model AL-$-200 from Jabsco Pump Company Ltd., Cheshunt, Herts., England) fitted with a + HP motor giving approximately 300 rpm, and an adjustable time-delay switch. A special device for discarding hold-up water in the suction hose and the pump consisted of a horizontal brass tube (15 mm inner diameter) with one inlet and three outlets. The first outlet was connected 246
PRODUCER-CONSUMER
tII
RELATIONSHIPS
IN THE SEA. II.
Fig. 1. Automatic sea water sampler: for explanation
247
see text.
to a plastic bottle (A) of - 250 ml capacity, which was stoppered tightly and fitted with a narrow siphon. The second outlet was shaped as a vertical brass cylinder (B), 100 x 15 mm, which ended in a glass capillary of - 1 mm internal diameter. Surplus water left the system through the third outlet (D). On a signal from the controller unit, the pump started and at the same time the turntable moved one step forward. The pump first filled the discarder flask (A) and when this was full, water flowed over into the sampling cylinder (B) and through the capillary into a test tube in the fraction collector. The pumping period and capacity was regulated so that there was a good overflow at D. After a suitable period, the time-delayed switch (C) stopped the pump, and flask A was slowly emptied through the siphon. In order to preserve the samples, all test tubes in the fraction collector contained 0.5 ml of 10 ‘A, neutralized formalin solution. The water sampler was placed on the quay in the Muruvik Bay in the Trondheimsfjord with the sampling hose (vacuum rubber tubing) extending into the mussel population growing on the wooden construction underneath. The intake was kept in a fixed position, - 1 m below the lowest tide mark. From the beginning of April, 1969 and throughout June, water samples each of - 30 ml were taken every 30 min. Later this interval was increased to 1 h. The sub-samples were pooled (12 x 12) giving four and two samples per day, respectively. Pooling was carried out every 5th and 10th day, respectively, and the samples were brought to the laboratory for counting by the Utermohl technique (Utermiihl, 1931). Mussel samples were obtained every week from the population surrounding the pump intake. Pigment analysis was carried out on 10-15 adult individuals as described by Jensen & Sakshaug (1970). In addition to the concentration and composition of carotenoids the content of chlorophyll-like pigments was determined by paper chromatography in cases were the epiphase showed traces of a green colouration. The
ARNE JENSEN AND EGIL SAKSHAUG
248
quantitative estimation was based on an estimated (St011 & Wiedemann, 1959).
Ei ci of 890, as for chlorophyll
a
RESULTS
Some sub-samples were lost because of frost, interruptions of the power supply, and for mechanical reasons. Complete samples were obtained for 156 out of the 186 days covered by the present investigation. The phytoplankton counts for each day were grouped into the following classes: total number of diatoms; total number of dinoflagellates; Phaeocystis pouchetii (Hariot) Lagerheim, and Coccolithus huxleyi (Lohmann) Kamptner. Fig. 2 shows the more pronounced variations in plankton
APRIL
MA”
JUNE
JULY
AUGUST
SEPTEMBER
OCTOBER
Fig. 2. Phytoplankton counts (cells/l), total carotenoids and ‘chlorophyll’ in Myrilus edulis L. (mg/kg of acetone extracted dry matter) at Muruvik 1969: l total carotenoids; x ‘chlorophyll’; 0 Coccolithus huxleyi; 0 total diatoms; A Phaeocystic pouchetii; 0 total dinoflagellates.
counts given as the logarithm of the number of organisms per litre of sea water. The content of total carotenoids and chlorophyll-like pigment in the mussels are also given in this Figure. The variation in the composition of the carotenoid pigments is given in Fig. 3, in which the percentage of the three main components is shown as a function of time. These groups of pigments are the same as found previously (Jensen & Sakshaug, 1970). In all, six zones were found on the paper chromatograms; but zones 1, 2 and
60 -
I FEBRUARY
I
I
I MARCH
PlPRlL
MAY
1 JUNE
I JULY
A”G”ST
I SEPTEMBER
I OCTOBER
Fig. 3. Seasonal variation of the main carotenoid groups in lwyfiZus e&is L., expressed as %total carotenoids, Muruvik 1969: 0 Group 3 pigments; 0 Group 4 pigments; x Group 6 pigments; ,JJ tota carotenoids in mgjkg of acetone extracted dry matter.
5 made up 5-10 % each of the total and remained nearly constant throughout whole period.
the
DISCUSSION
In the preceding paper of the present series (Jensen & Sakshaug, 1970) it was shown that the seasonal variation in the content of total carotenoids in mussels followed the gross changes in phytoplankton density in the fiord. It was evident, however, that very frequent sampling of the plankton would be required to allow more detailed studies to be carried out, and that this should preferably be done in the inshore water surrounding the mussels. The sampling method used in the present study was not expected to give an estimate of the phytoplankton population in the whole water column, since the samples were taken exclusively in the 1-4 m layer (depending on the tidal movements), but it should have given representative samples of the body of water available to the mussel population in question. It may be seen from Fig. 2 that the density of phytoplankton in the water which surrounded the mussels underwent rapid changes. The experiment started in early April during the rapid decline of the early spring bloom, which consisted of a mixed population of Phaeocystis pouchetii and diatoms, mainly Chaetoceros debilis Cleve, C. decipiens Cleve, ~keletone~a co~t~t~~ (Grev.) Cleve, and T~~la~s~o~ira~rovi~
250
ARNE
JENSEN
AND
EGIL
SAKSHAUG
Cleve. Phareocystis dropped from 140 000 to virtually zero cells/l in 4 days. After a minimum period in late April, a diatom bloom took place in May with Chaetoceros ~~nstr~ct~sG-an predominating (m~imum 19th May, 103 500/l). It coincided with a small dinoflagellate maximum made up of Peridinium truchoideum (Stein) Lemmermann (max. 16th May, 11200/l), together with minute amounts of Govlyaulax tamarensis Lebour and Peridinium ovatum (Pouchet) Schiitt. Tn summer, Nitzschia delicatissima-type cells (max. 16th June, 264 000/l>, Thalassionema nitzschioides and C~ccu~~th~s huxleyi (max. 6th July, ~runow (max. 17th June, 294~/1), 1 172000/l) populated the water for variable periods. The sparse phytoplankton population in autumn consisted practically only of dinoflagellates, mainly Ceratium ,fusus (Ehrenberg) Dujardin (max. 8th Sept., 4260/l). We regard the events mentioned above as regular blooms which took place in the water surrounding the mussels, and the planktonic organisms were available for the mussels to feed upon for a considerable period. Tn some cases the bloom was followed by very irregular peaks in the density of the phytoplankton. In three instances the concentration of Thalassionema rose from a background level of 20 000 to nearly 200 000 cells/l in one day and dropped back again to the 20 000 cells/l the next day. The peaks did not coincide with spring tides allowing the pump to sample deeper strata; it is, therefore, suggested that they have hydrographical causes. Water rich in phytoplankton may have been brought up within reach of the pump during a local upwelling situation, or it may have been brought to the pump by rapid horizontal transport of water. In this connection it may be mentioned that, in the open fiord, several of the blooms tended to last longer at greater depths than in surface water during the warm summer of 1969. The bloom of Chaetoceros constrictus in May gave rise to a very pronounced peak in the concentration of pigments in the mussels, while the large amount of Phaeocystis pouchelii of the spring bloom did not seem to be similarly effective. The latter organism belongs to the group which Yonge (1926) would characterize as “many small particles imbedded in mucus” and which would tend to be rejected by the mussels. This may partly explain why the occurrence of this planktonic species did not result in a corresponding increase of mussel pigmentation. It should be noticed that the green, chlorophyll-like pigments were found in the mussels only during the blooms of Phaeocystis pouchetii and Chaetoceros constrictus. The first part of the summer was characterized by blooms of Nitzschia and Thalassionema, neither of which was reflected in the pigment content of the mussels. A population of Coccolithus huxleyi, also invaded the water during the middle of the summer without affecting the mussel pigmentation. All these species are very small and with little pigmentation and thus represented negligible quantities of pigments as well as a small biomass. The rest of the period was dominated by dinoflageliates, although their number remained rather low, at less than 6000 cells/l. The small variations that occurred were, however, immediately followed by changes in the pigmentation of the mussels.
PRODUCER-CONSUMER
RELATIONSHIPS
IN THE SEA. II.
251
Since the dinoflagellates were relatively large and heavily pigmented, and since the variations in plankton density and pigment concentration in the mussels followed each other closely, we are led to believe that the observed correlation is real and that the mussels were able to respond to the low concentrations of dinoflagellates observed. It has been indicated in the literature (Kellogg, 1915; Loosanoff & Engle, 1947; Davids, 1964) that low particle contents lead to better utilization by the mussels, and this may help to explain the high efficiency of the dilute plankton populations in autumn relative to the low effect of the rather dense blooms that occurred in spring and summer. These observations are in apparent conflict with those of Coe (1947) who could not find any traces of the larger dinoflagellates among the stomach contents of mussels, a finding which led Boje (1965) to assume that these and other large and spiny species are not utilized by mussels. The fact that the ~arotenoid content of the mussels increased rapidly during blooms of large dinoflagellates as demonstrated by us for two consecutive years, strongly indicates that these plants are indeed both removed from the water, and retained, by the mussel. There, was no sign of chlorophylls or their derivatives in the mussels during the autumn blooms which implies that the major part of the ingested dinoflagellates were dead when the mussels were collected. It is, therefore, not possible that they had been merely filtered off and were awaiting rejection in a more or less intact state as pseudo-faeces. The quantitative aspects of the process also strongly indicate that the mussels must have accumulated the algae over several days in order to produce the increase observed in the pigment content. Furthermore, the composition of the mussel pigments was always different from that of the algae in the surrounding water masses. We are, therefore, led to conclude that the edible mussel is able to assimilate rather efficiently at least the carotenoid pigments of large dinoflagellates such as Ceratium fusus. The well known fact that mussels can accumulate toxin very rapidly from Gonyaulax species also shows that molluscs must have an efficient mechanism for the assimilation of other dinoflagellates. The literature contains conflicting reports regarding the influence of season on the content of carotenoids in molluscs. While Scheer (1940) found no marked seasonal variation in any of the carotenoids of the California sea mussel (Myth californianus), Lederer (1938) reported that the carotenoid content of the scallop (Pecten maximus) varied greatly with the season. The seasonal variations established for the edible mussel by us in both the preceding and present study were quite significant. Scheer always kept the mussels for IO-20 h in clean sea water to clear them of faecal pellets, whereas in our studies the animals were analysed shortly after collection. This, however, should require only a small correction to the carotenoid contents found in the present studies, since it would have been necessary for the mussels to accumulate the pigments over several days in order to bring about the observed increases. The rapid decreases in pigment concentrations shown by the mussels when the plankton counts dropped must mean that at least a large fraction of these pigments has a high turnover. Part of the carotenoids could be lost during spawning. Yet the
252
ARNE JENSEN AND EGIL SAKSHAUG
dry weight content per mussel remained fairly constant throughout spring, summer, and autumn, indicating that no well-defined period of mass spawning occurred in 1969. Lande (1969) observed that the edible sea mussel spawned both in spring and in autumn in the inner part of the Trondheimsfjord. This rather extended spawning cannot explain the rapid variations in pigment concentration of the mussels. In agreement with previous findings (Jensen & Sakshaug, 1970) the pigments of the mussels were again found to be dominated by three groups of components, namely Groups 3,4 and 6 (see Fig. 3). Also Groups 3 and 4 again showed tendencies towards an inverse relationship. The pigments of Group 6 increased relatively more than did the others during blooms of Ph~eoc~sti~ pouchetii and Chaetoceros con~t$ict~s in spring and early summer. The pigment composition remained fairly constant during summer and autumn this year, a fact which may be related to the lack of a typical autumn bloom of phytoplankton in the water during the 1969 observations. The close correlation between mussel pigmentation and phytoplankton occurrence makes pigment analysis in plankton and filter-feeders a promising tool for studying the uptake and assimilation of the former by the latter organisms. Identification of carotenoids derived from peridinin in sea mussel tissue during blooms of large dinoflagellates would prove conclusively that the mussels can assimilate this food, even though a mechanism for this process is not known.
ACKNOWLEDGEMENTS The authors are indebted to the Norwegian Research Council for Science and the
Humanities and to Fiskerinreringens Forskningsfond for financial support. We are grateful to Meraker Smelteverk A/S, Muruvik for technical facilities and to Mrs. lngjerd Mehli for skilful technical assistance.
REFERENCES BOJE,R., 1965.Die Bedeutung von Nahrungsfaktoren fiir das Wachstum von Myriius edulis L. in der Kieler F&de und im Nerd-Ostsee-Kanal. Kkier ~ee~es~~~~c~., Bd 21, S. 81-100. COE, W. R., 1947. Nutrition, growth and sexuality of the Pismo clam (Tiuefa stttltoram). J. exp. Zooi., Vol. 104, pp. 1-14. DAVID%C., 1964. The influence of suspensions of microorganisms of different concentrations on the pumping and retention of food by the mussel (Mytilus edulis L.) Neth. J. Sea Res., Vol. 2, pp. 233-249.
JENSEN,A. &E. SAKSHAUG,1970. Producer-consumer relationships in the sea. I. Preliminary studies on phytoplankton density and Mytilus pigmentation. J. exp. mar. Biol. Ecol., Vol. 5, pp. 180-186. KELLOGG,J. L., 1915. Ciliary mechanisms of lametlibranchs with descriptions of anatomy. .I. Morph., Vol. 26, pp. 625-701. LANDE,E., 1969. En undersskelse av vekst, gyting og dodelighet hos btaskjell ~~~t~~/~~ edttlis L.) pa to iokaliteter i Trondheimsfjorden. Thesis, University of 0~10, 67 pp. LEDERER,E., 1938. Recherches sur les carotCno?ds des invertebres. Bull. Sm. Chim. bioi., T. 20, pp. 567-610.
LOOSANOFF, V. L. & J. B. ENGLE, 1947. Effect of different concentrations of micro-organisms feeding of oysters (Ostrea virginica). U.S. Fish Wildl. Serv. Bull., Vol. $1, pp. 31-57.
on the
PRODUCER-CONSUMER
RELATIONSHIPS
IN THE SEA. II.
253
SCHEER,B. T., 1940. Some features of the metabolism of the carotenoid pigments of the California sea mussel (Mytilus californianus). J. biol. Chem.. Vol. 136, pp. 275-299. STOLL, A. & E. WIEDEMANN,1959. Die kristallisierten natiirlichen Chlorophylle a und b. Helv. chim. Acta, Bd 42, S. 679-683. UTERMBHL,H., 1931. Neue Wege in der quantitativen Erfassung des Planktons. Verh. int. Verein. theor. angew. Limnol., Bd 5, S. 567-595. YONGE,C. M., 1926. Structure and physiology of the organs of feeding and digestion in Oshea edulis. J. mar. biol. Ass. U.K., Vol. 14, pp. 295-386.