In 1995 the seasonal development of concentrations of both phytoplankton and larvae of the bivalve Macoma balthica was studied in the coastal zone behind the back-barrier island of Spiekeroog (German Wadden Sea). In July=August larvaereached maximum concentrations of about 1000 to 4200 ind. 

Bittkau, A.

Boysen-Ennen, E.

Fetzer, Ingo

Günther, C.-P.

Hasemann, Christiane

Heuers, J.

Jaklin, S.

Nacken, M.

Niesel, V.

Schlüter, Michael

English

Electronic Publication Information Center

ELSEVIER Journal of Sea Research 40 (1998) 347–351Short communicationObservations of a mass occurrence of Macoma balthica larvae inmidsummerC.-P. Gu¨nther a,, E. Boysen-Ennen b, V. Niesel c, C. Hasemann d, J. Heuers d, A. Bittkau d,I. Fetzer d, M. Nacken d, M. Schlu¨ter d, S. Jaklin da c=o Alfred-Wegener-Institute for Polar and Marine Research, Columbusstr., 27568 Bremerhaven, Germanyb Forschungsinstitut Senckenberg, c=o Institut fu¨r Hydrobiologie, Abteilung Biologische Ozeanographie, Zeiseweg 9,22765 Hamburg, Germanyc Forschungszentrum Terramare, Schleusenstr. 1, 26382 Wilhelmshaven, Germanyd Universita¨t Bremen, c=o Alfred-Wegener-Institut fu¨r Polar- und Meeresforschung, Columbusstr., 27568 Bremerhaven, GermanyReceived 13 January 1998; accepted 5 August 1998AbstractIn 1995 the seasonal development of concentrations of both phytoplankton and larvae of the bivalve Macoma balthicawas studied in the coastal zone behind the back-barrier island of Spiekeroog (German Wadden Sea). In July=August larvaereached maximum concentrations of about 1000 to 4200 ind. m 3 (depending on the sampling site and tidal period),probably in relation to a phytoplankton bloom in July. This observation of an unusually late maximum of Macoma larvaeis discussed in detail in connection with the recent literature available about spawning of M. balthica in the Wadden Sea. 1998 Elsevier Science B.V. All rights reserved.Keywords: Macoma balthica; spawning; seasonal development1. IntroductionAround the North Sea, intertidal populations ofMacoma balthica (L.) are known to spawn oncea year in spring (Caddy, 1967; Lammens, 1967).Subsequent gonadal redevelopment continues intoautumn or even the beginning of winter (Caddy,1967; Lammens, 1967; Chambers and Milne, 1975;Madsen and Jensen, 1987). The rise in water tem-perature in spring to above 10ºC appears to triggerthe spawning (Lammens, 1967). Experiments carriedout by Honkoop and Van der Meer (1997) suggestthat this trigger is pertinent only when the gonads Corresponding author: E-mail: carmen.guenther@uba.deare completely ripe. The process of gonad ripeningin M. balthica is still not completely understood. InMytilus edulis L. gonad ripening is accelerated by theincrease in phytoplankton density (Kautsky, 1982).Comparable studies for M. balthica are lacking.In contrast to those in the North Sea, intertidal M.balthica from the southern limit of its distribution(Gironde Estuary, France) are known to spawn twicea year: in late spring=early summer and again fromSeptember to November after a rapid redevelopmentof the gonads (Bachelet, 1986).Among the intertidal bivalves of the Wadden Sea,M. balthica and possibly Scrobicularia plana daCosta are the only species thought to spawn oncea year. In contrast, Cerastoderma edule (L.) and Mya1385-1101/98/$ – see front matter  1998 Elsevier Science B.V. All rights reserved.PII: S 1 3 8 5 - 1 1 0 1 ( 9 8 ) 0 0 0 3 4 - 3348 C.-P. Gu¨nther et al. / Journal of Sea Research 40 (1998) 347–351arenaria L. and Mytilus edulis are reported to haveat least the potential of two annual spawning pe-riods (Pfitzenmeyer, 1965; Hummel and Boogards,1989; Pulfrich, 1997), suggesting that gametogene-sis proceeds more rapidly than in M. balthica. Thespring spawning stimulus in these species is simi-larly thought to be a rise in water temperature, butthe trigger of the autumn spawning is yet unknown.In the German part of the Wadden Sea after thesevere winter of 1985=1986, Gu¨nther (1990) ob-served only one larval peak in M. balthica, while in1982 and 1983, following moderate winters, Heiber(1988) reported a small autumn peak represented inboth years by one observation date. Although a sim-ilar observation was made by Boysen-Ennen in 1994(same area of investigation as in the present study,unpublished data), evidence for late spawning in thisspecies was still weak. The present paper describes acase history of a mass occurrence in 1995 of larvaeof M. balthica as late as July=August, emphazising(1) the need for more information on gonad ripeningand spawning stimuli and (2) the high plasticity oftemporal patterns in the reproduction of M. balth-ica.2. Material and methods2.1. Area of investigationThe area of investigation was the coastal zonebehind the barrier island of Spiekeroog, situated onthe southern North Sea coast, in the German Bight(Fig. 1). In 1995 meroplankton sampling was carriedout at two locations, one situated in the OtzumerBalje tidal inlet (A), and the other in the harbour ofNeuharlingersiel (B). At high tide, 70% of the waterin the Spiekeroog back-barrier flats is transportedvia the Otzumer Balje (A), while in the harbour (B)the water exchange by the tides is probably limited.Sampling of phytoplankton was also carried out atthe Otzumer Balje station (A), concurrent with themeroplankton sampling. Benthos sampling was car-ried out at the Gro¨ninger Plate (station C), a mainlysandy intertidal flat situated between the mainlandand the island of Spiekeroog. At this sampling sitemixed sediments occurred and the benthic fauna wasdominated by the polychaetous worms Heteromastusfiliformis and Aphelochaeta marioni (former name:Tharyx marioni).2.2. PhytoplanktonPhytoplankton samples were taken from the watersurface at station A. Sampling was carried out twohours before high tide. The material was preservedin 4% formalin. Phytoplankton was counted accord-ing to the Utermo¨hl technique (Utermo¨hl, 1958) involumes of 3 to 10 cm3. As bivalve larvae consumephytoplankton cells <30 µm (Balwin and Newell,1991), only data for this algal fraction are presentedhere.2.3. Meroplankton2.3.1. Otzumer Balje (Station A)Meroplankton samples were collected fromMarch to November 1995 at intervals of 2 to 8weeks. Sampling was carried out two hours beforehigh and low tides by filtering 50 dm3 pumped sea-water (water depth 6–7 m) over 125-µm meshes. Byusing this mesh size, small unidentifiable stages ofbivalve larvae were caught as well as larger stageswhich could be identified from a length of 150 to175 µm onwards. Thus, in general the maximumlarval density of M. balthica may have been under-estimated. Samples were preserved in a 4% bufferedKorsolin seawater mixture. In the laboratory sampleswere sorted and bivalve larvae were identified tospecies level.2.3.2. Neuharlingersiel Harbour (Station B)Meroplankton samples were collected from Aprilto September 1995 (represented are data from Mayto the end of August) at intervals of between 6 and20 days. Sampling was carried out at high tide usingan Apstein net (125-µm mesh size, opening diameter10 cm) hauled vertically through the water column.The water depth at mean high tide was about 4 m.Three repeated hauls were pooled into one sample.The volume filtered was determined via a flow meterand ranged between 75 and 100 dm3. The sampleswere fixed with 4% buffered formalin and sorted inthe laboratory. Some of them were subdivided usinga plankton splitter according to Kott (1953).For identification, comparison material analysedC.-P. Gu¨nther et al. / Journal of Sea Research 40 (1998) 347–351 349Fig. 1. The area of investigation. (A) The station in the Otzumer Balje; (B) the Neuharlingersiel harbour station; (C) the benthos samplingstation at the Gro¨ninger Plate.by K.W. Ockelmann was used. Cross checking of thebivalve larvae from the Otzumer Balje and Neuhar-lingersiel Harbour was also done. Because we recog-nised the larvae of Tellina sp. in the Otzumer Balje,it is not likely that the two species were confused.2.3.3. Gro¨ninger Plate (Station C)Benthos sampling was carried out at the southernborder of the Gro¨ninger Plate. Here mixed sedimentsoccur, in which settlement of bivalves regularly takesplace (Gu¨nther, 1990; Jaklin et al., in prep.). Sampleswere collected from April to August in time intervalsof 1 to 3 weeks. One additional sampling was carriedout on 18 December 1995.Five parallel samples were taken with a corer of33 cm2 area and preserved intact in 5% bufferedformalin. Sorting and identification of postlarvaewas carried out in the laboratory after sieving of thesediment on a sieve column of 500, 250 and 125 µm.To demonstrate settlement of larvae, only the meanabundance of postlarvae <500 µm will be presented.3. Results and discussionFig. 2a presents the density of algae <30 µmpotentially contributing to the diet of bivalve larvae.With less than 6  109 cells m 3, the spring phy-toplankton bloom in 1995 was extraordinarily smallwhile later peaks in summer reached the magnitudeof a ‘normal’ spring bloom. In the North FrisianWadden Sea a delay of the 1995 spring bloom wasobserved with increasing phytoplankton densities oc-curring as late as May. This irregular seasonal devel-opment was assumed to be related to a shortage inlight available for the algae due to the high turbidityof the water column in spring 1995 (Tillmann andHesse, pers. comm., 1998).The density of M. balthica larvae in the mero-plankton was similarly low during the spring spawn-ing period (Fig. 2b), although larval abundances usu-ally peak at this time of year (Heiber, 1988; Gu¨nther,1990, 1991). Due to the lack of data it cannot com-pletely be excluded that M. balthica had spawned350 C.-P. Gu¨nther et al. / Journal of Sea Research 40 (1998) 347–351Fig. 2. Density of (a) small phytoplankton (<30 µm), of (b) M.balthica larvae, and (c) of M. balthica postlarvae in 1995. For thelarvae, results from two sampling locations (Station A: OtzumerBalje; Station B: Neuharlingersiel harbour) are presented.already before April. But the trigger water tempera-ture of 10ºC was reached only in the second half ofApril 1995 (data: Deutscher Wetterdienst), implyingthat no spawning will have taken place before thatdate.In contrast to data found in 1994 and 1996 (Jak-lin et al., in prep.), larval densities increased againat both sampling locations in July (Station B) andAugust 1995 (29 August; Stations A and B), indicat-ing summer spawning of M. balthica in the WaddenSea. This contradicts the results of Lammens (1967),who concluded from studies on gonad developmentof intertidal M. balthica that they spawn only oncea year in spring. Also the results of Honkoop andVan der Meer (1997) imply a single spring spawningin intertidal populations, suggesting that spawningintensity is related to preceding winter temperatureregimes and food availability during gametogenesis.Though the larval densities in spring were low,a clear settlement peak was observed in May in thebenthos of the Gro¨ninger Plate (Fig. 2c). The secondperiod of occurrence of M. balthica larvae in 1995was reflected in an increase of postlarval abundancein August and particularly in an extraordinarily highdensity of postlarvae (mostly smaller than 800 µm)as late as December 1995.The observations reported here point to the occur-rence in certain years of repeated spawning events inM. balthica in the Wadden Sea, a phenomenon previ-ously reported for populations close to the southernlimit of the geographical distribution of this species(Bachelet, 1986). Which part of the population (sub-tidal or intertidal) generally contributes to such a latespawning in the Wadden Sea can only be determinedby studying the seasonal gonad development of bothtidal and subtidal M. balthica. However, the highlarval density of M. balthica observed in summerin the present study (the highest reported to date)suggests that a considerable part of the populationhad spawned.The late spawning event observed in the presentstudy raises questions as to the causative factors.The possibilities are: (1) In 1995 the abiotic aswell as food conditions in the Wadden Sea weresimilar to those in the Gironde Estuary, thus allow-ing two spawning periods. The winter 1994=95 wasextremely mild and the water temperature duringsummer was extraordinarily high. In June–Augusta positive temperature anomaly was observed withvalues up to 3 standard deviations higher than the25-y average (Umweltbundesamt, 1996). Simultane-ously the seasonal development of the phytoplanktonwas unusual, with a heavy bloom occurring as lateas July–September. Such late blooms are assumedto play a key role in the occurrence of two growingperiods of M. balthica in the Seine estuary (Beukemaand Deprez, 1986) and are most likely to be the causeof two spawning periods in this region as well. (2)This unusually heavy and late phytoplankton bloommay have triggered a second spawning in M. balthicaas well as in other dominant bivalves of the Wad-den Sea (Jaklin et al., in prep.). That phytoplanktonC.-P. Gu¨nther et al. / Journal of Sea Research 40 (1998) 347–351 351blooms may induce spawning events was describedby Himmelmann (1975) and Starr et al. (1991), viz.for sea urchins and mytilid bivalves. As such in-tense and delayed phytoplankton blooms occur onrare occasions only, their effect on the reproductivebehaviour of bivalves has not yet been determined.Future research on M. balthica should thus focuson: (1) what drives=accelerates gonad development,(2) when does the subtidal part of the M. balthicapopulation in the Wadden Sea spawn, and finally(3) what triggers summer=autumn spawning in M.balthica or in other bivalve species.AcknowledgementsThe study was supported financially by theBundesministerium fu¨r Bildung, Wissenschaft,Forschung und Technologie (BMBF) under grant03F0112A. This is publication no. 69 of the project‘Ecosystem Research Wadden Sea’. We gratefullyacknowledge the valuable comments of the threereferees and the helpful comments of one of theeditors.ReferencesBachelet, G., 1986. Recruitment and year-to-year variability in apopulation of Macoma balthica (L.) Hydrobiologia 142, 233–248.Balwin, B.S., Newell, R.I.E., 1991. Omnivorous feeding byplanktotrophic larvae of the eastern oyster Crassostrea vir-ginica. Mar. Ecol. Prog. Ser. 78, 285–301.Beukema, J.J., Deprez, M., 1986. Single and dual growing sea-sons in the tellinid bivalve Macoma balthica (L.) J. Exp. Mar.Biol. Ecol. 102, 35–45.Caddy, J.F., 1967. Maturation of gametes and spawning in Ma-coma balthica (L.) Can. J. Zool. 45, 955–965.Chambers, M.R., Milne, H., 1975. The production of Macomabalthica (L.) in the Ythan estuary. Estuar. Coast. Shelf Sci. 3,443–455.Gu¨nther, C.-P., 1990. Zur O¨ kologie von Muschelbrut im Watten-meer. Ph.D. thesis, University of Bremen, 183 pp.Gu¨nther, C.-P., 1991. Settlement of Macoma balthica on anintertidal sandflat in the Wadden Sea. Mar. Ecol. Prog. Ser. 76,73–79.Heiber, W., 1988. Die Faunengemeinschaft einer großen Strom-rinne des Wurster Wattengebietes (Deutsche Bucht). Ph.D.thesis, University of Bonn, 398 pp.Himmelmann, J.H., 1975. Phytoplankton as a stimulant forspawning in three marine invertebrates. J. Exp. 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Observations of a mass occurrene of Macoma balthica larvae in midsummer

Observations of a mass occurrene of Macoma balthica larvae in midsummer

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