NETHERLANDSJOURNALOFAQUATICECOLOGY29(3-4) 341-347(1995)

SPORULATIONOF ENTEROMORPHASPP. (CHLOROPHYTA) AND OVERWINTERINGOF SPORESIN SEDIMENTS OF THE WADDENSEA, ISLANDSYLT, NORTHSEA DIRK SCHORIES

KEYWORDS: Enteromorpha spp; spores; algal mats; Wadden Sea; intertidal sandflat; settlement; dark resistance; overwintering; germination.

ABSTRACT For the last two decades dense mats of species of the filamentous green algae Enteromorphaspp. have reguiary occurred on tidal flats of KGningshafen Bay (island Sylt, North Sea, FRG). In calm areas overwintering of adult plants or plant fragments is a common process to guarantee the mass development during the next season. In contrast, the distribution of Enteromorpha on exposed sandy tidal flats depends on recruitment by juvenile stages. In 1993 Enteromorpha spore settlement was recorded regularly in the field. Polyethylene dishes were placed in the field and left for a period of seven days and lateron cultivated in the laboratory to check Enteromorpha germling development. During summer 1993 - at a minimum distance of 200 m to the nearest adult Enteromorphapopulations - a total of at least 82 x 106 spores m-2 settled. During winter the number of spores attached to the collecting dishes was close to zero and the adjacent sand flats were free of any visible Enteromorpha plants. In further experiments it was shown that the development of Enteromorpha juveniles in the next spring depended on the overwintering capacity of spores. More than 2 x 106 spores m-2 attached to large sand grains and other substrata (e.g. Hydrobia ulvae) survived the winter. In a laboratory experiment several species of Enteromorphawere able to survive in total darkness for at least 10 months.

INTRODUCTION Up to the 1970s macroscopic green algae were a conspicuous element on sandy or muddy intertidal flats near the island of Sylt (Kuckuck, 1896-1903 unpubl, data; NIENBURG,1927; WOHLENBERG,1937; KORNMANN, 1952; Kornmann and Sahling, 19481958, unpubl, data), but have never occurred in thick mats before 1979 (REISE, 1983; REISEet aL, 1989; SCHORIESand REiSE,1993). Within the last 25 years, excessive growth of green macroalgae, namely Cladophora spp., Enteromorpha spp. and Ulva spp., has become an increasingly common phenomenon and a problem in sheltered bays (PERKINSand ABBOI-r1972; MONTGOMERYand SOULSBY, 1981; SFRISOet aL, 1987; RAEFAELLIet aL, 1989). 341

Eutrophication in estuaries and coastal waters is well documented and may explain the extensive growth of certain macroalgae, which take advantage of these conditions (SOULSBYet aL, 1982; SOULSSYet aL, 1985; SFRiSOetaL, 1987). FLETCHERand CALLOW(1992) reviewed the settlement, attachment and establishment of marine algal spores in general. It is supposed that the development of green algal mats on intertidal sandand mudflats in spring is commonly achieved by (1) overwintering and regrowth of adult plants, which persist partly embedded in the sediment or (2) the formation and detachment of propagules from the parent plants. Propagules of Enteromorpha spp., can take the form of ordinary vegetative fragments, which are detached from the adult plants

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by various physical and biological forces (SANTELICES,1990). This kind of propagules is able to continue growth in the water column and form freefloating aggregates through entanglement with each other. These are often secondarily anchored (CLOKIE and BONEY,1980; REISE,1983; SCHORIESand REISE, 1993). Spores as dispersal agents of Enteromorpha spp. can be found in the water column in large quantities in nearly all coastal regions of the world (JONSSON,1972; AMSLERand SEARLES,1980; ZECHMAN and MATNIESON,1985). They are able to survive up to 8 days in the water column depending on the suitability of environmental factors (JONES and BABB, 1968). NIENBURG(1927) described the settlement and direct development of Enteromorphaspores to juvenile plantlets on sand grains in K6nigshafen Bay. He suggested that these stages overwinter and guarantee the Enteromorphadevelopment in the following year. In spring Enteromorpha juveniles increase in length, become dislocated and continue growth in the same way as described above for fragments. Nowadays, overwintering of juveniles cannot be the missing link between Enteromorpha mats in summer and a renewed development the following spring, because their number in winter is too low. In this study, the aspects of overwintering of Enteromorpha spp. spores on sand grains are described in more detail. It is hypothesized that (1) Enteromorpha spores attached to coarse sediment or benthic organisms (Le. Hydrobia ulvae, Cerastoderma edule) can play an essential role in Enteromorpha development, (2) the availability of spores is not the bottleneck for the development of algal mats, and (3) overwintering of spores in the sediment is a good survival strategy against herbivorous grazing pressure.

METHODS Habitat Investigations were carried out on a sandy flat in 'K6nigshafen', a shallow tidal bay near the island of Sylt (North Sea, FRG). Hydrography and macrofauna have been described by REISE(1985), benthic macroflora by NIENBURG (1927) and KORNMANN (1952), sediment by AUSTEN(1992). The investigation site is located at mid-tide level (organic content, measured as weight loss through ignition: 0,04% of dry weight; silt content <4%; median of particle size: 324 pm).

Experiments

Settlement of spores Over a period of 14 months (March 1993 - April 1994) every month 6 polyethylene dishes (9 cm in diameter) were placed and left in the field for seven days (starting from spring tide) to allow Enteromorpha spore settlement. Afterwards, the dishes were returned to the laboratory and then transferred to containers, filled with 800 ml autoclaved and nutrient-enriched seawater (PROVASOLI, 1968). The dishes were kept in a culture room at 15~ at irradiance between 80 and 100 pEm -2 sec-1 supplied at a 12:12 h light to dark cycle. After two weeks of growth, the number of juvenile Enteromorpha plantlets was counted under 25-fold magnification. Ten subsamples of 4 x 4 mm, taken at random, were analysed on each polyethylene dish.

Dark resistance of spores Starting in August 1993 the dark resistance of

Enteromorpha spp. spores was tested experimentally. Again, polyethylene dishes served as a substratum for Enteromorphaspores in the field. They were left outside over two tidal cycles and then transferred into containers with 800 ml autoclaved seawater and stored in the dark, one group at 5~ and the other group at 15~ After O, 1, 2, 4, 6, 8 and 10 months respectively, 4 dishes of each group were returned to the light and cultivated and analysed as described above. At the beginning (0 months in the dark) and at the end of the experiment (10 months in the dark) sub-samples of Enteromorpha plantlets were identified to species.

Depth distribution of propagules Eight sediment samples of 6.9 cm2 area and 5 cm depth were taken in February 1994 and portioned in 1 cm depth sections in order to estimate the content of Enteromorpha fragments and spores in the different sediment layers. Firstly, the sediment cores were transferred to petri dishes and inspected under 25-fold magnification to estimate and remove the fragments from the sediment. Afterwards, the sediment was cultivated (see above) to allow germination of Enteromorpha spores attached to sand grains.

Optimal grain size for germination of spores Sediment, taken from the field in August 1993, was dried at 80~ for 72 h and graded by size through 1000 pro, 500 pro, 250 pro, 125 pm and 63 pm sieves. Enteromorpha prolifera sporophytes were collected in the field and kept overnight in

Enteromorpha spores in the Wadden Sea plastic bags in a culture room at 15~ The following morning, selected and cleaned plants released zoospores after being transferred into autoclaved seawater. This spore suspension was used to inoculate subsamples (dry weight = 4.00 g) of the different sediment fractions. Eight replicate petri dishes for 5 grain sizes, filled with 60 ml autoclaved, enriched seawater and sand grains, were cultivated (see above). The effect of sand grain size on the development of zoospores was evaluated with 25fold magnification by using a grid of 100 units. The number of units containing juvenile Enteromorpha plantlets was estimated for 10 subsamples, taken at random, for each petri dish.

--

RESULTS Spore settlement

The mean density of juvenile Enteromorpha spp. plantlets developing on the collecting dishes, was highest during late spring and summer (Fig. 1). A reduced settlement of spores was observed in autumn, and in winter months and early spring the spore number was close to zero. Mean changes in Enteromorpha germling densities between collecting dates (Le. net recruitment) were highest from June to July (increased settlement) and from July to August (decreased settlement). Changes of spore settlement coincided with changes of Enteromorpha biomass of adult plants (max. standing crop as dry weight 18 g m-2) in adjacent areas (distance = 200 m), whose development was poor in comparison to

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Fig. 1. Mean (_+ 1 St. Dev.) spore settlement of Enteromorphaspp. on polyethylene dishes at a sandy intertidal station (n = 6).

Statistics

Between treatment differences for the experiments (3) and (4) were analysed using a single factor analysis of variance (ANOVA),after square root (exp. 3) or arc-sine transformation (exp. 4) of the dependent variable (mean of the 10 subsamples). A 2-way ANOVAwas used for experiment (2), after log transformation of numbers (mean of the 10 subsamples). Homogeneous subsets of treatments were defined using the STUDENT - NEWMAN - KEULS procedure (SOKALand ROHLF,1981), which performed a multiple comparison between the treatment means for determining differences between treatments at the 5% level. Homogeneity of variances was tested by the COCHRANtest (UNDERWOOD,1981). In experiment (3), after transformation of data variances appeared still heterogeneous (P = 0.038), but nevertheless analysis of variance was done. Explications for this procedure are discussed by UNDERWOOD(1981, p. 534-535).

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6

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previous years and restricted to the upper eulittoral from 10 cm below to 30 cm above mean high water. In winter no adult plants of Enteromorpha were present nearby the investigation area. It was calculated that from April 1993 to October 1993 a total of at least 82 x 106 spores m-2 were deposited. However, the number of spores attached to the petri dishes during winter time was zero or close to zero: no more than 0.008 x 106 spores could have settled onto the sediment surface. In spite of monthly variations in the quantitative species composition of Enteromorpha (LOFZE,1994), 5 species of Enteromorpha were regularly present on the dishes during summer months. These were Enteromorpha radiata and E. prolifera (both very frequent), E. flexuosa (frequent) and E. clathrata and E torta (both rare).

Dark resistance

Both temperature and exposure time influenced

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SCHORIES

the survival rate of Enteromorphaspp. spores stored in the dark (Fig. 2). The potential for germination of spores stored in the dark at 5~ was significantly higher (P <0.01) than germination of spores at 15~ Over time the total number of spores, which were able to germinate, also decreased significantly (P <0.001). Nevertheless, germination of spores at 5~ and 15~ was still successful after 10 months. At the end of the experiment the same 5 Enteromorpha species (see above) could be identified as before. Two homogeneous subsets of treatment means were obtained when data were ranked at P = 0.05 level (Fig. 2).

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Depth distribution of propagules

Thallus fragments of Enteromorphaspp. were not present in the sediment samples. Only in one case a single filament was found at 4-5 cm depth. Yet the sediment was absolutely stuffed with Enteromorphaspores. Up to a depth of 5 cm a great number of Enteromorphaplantlets developed directly from the sand grains (Fig. 3). Considering also multiple growth of Enteromorpha filaments on a single sand grain, the total number of Enteromorpha plantlets was higher than the numbers of overgrown sand grains presented in Fig. 3. The average number of Enteromorpha filaments attached to one sand grain was 1.40 (number of analysed sand grains, independent of depth = 530). From these results it is calculated that at least 2 x 106 spores m-2 were present in the upper 5 cm of the sediment during winter. Nevertheless, the number of spores, that germinated on sediment grains, decreased significantly with increasing sediment depth (P <0.0001), but the first three centimetres of the sediment formed a homogeneous subset. Optimal grain size for germination of spores

The laboratory experiment showed that germination of Enteromorpha prolifera zoospores was significantly influenced by the grain size of sediment (P <0.0001). Three homogeneous subsets of treatment means were obtained when data were ranked at P = 0.05 level (Fig. 4). Coarse sediment (>250 pro) was very suitable as a substratum for zoospores and subsequent germination. Relative germination of zoospores did not differ significantly between sand grain size classes of 0-1.0 PHI (500 1000 pm) and 1.0 - 2.0 PHI units (250 - 500 pro). On the other hand, the germination potential of Enteromorpha was reduced significantly on finer sediment particles. Relative abundance of young Enteromorphaplantlets was very low on sand grains smaller than 125 pm. When these results are corn-

2-3 cm

3-4 cm

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Fig. 4. Success of germination of Enteromorpha profifera zoospores on different sized sand grains. Homogeneous subsets are defined by shading (n = 8; means _+1 SD). Mean % (_+1 St. Dev.) of grid elements.

pared with the sediment composition at the investigation area, nearly 70% of the sediment size class >250 pm seems to be suitable for Enteromorpha germination.

DISCUSSION

Consistent with previous observations of REISE

et aL (1989) and SCHORIESand REISE (1993) in K6nigshafen bay the development of Enteromorpha spp. mats showed a strong temporal pattern in 1993. The abundance of Enteromorphaspores was highest in those months with greatest biomass of adults. The results show a clear seasonality of total spore settlement, although adult plants of several Enteromorpha species might have differed in dispersal behaviour due to environmental conditions

Enteromorpha spores in the WaddenSea and changes in species composition (LOTZE,1994). In agreement with my findings FLAVIERand ZINGMARK (1993) found a minimum of ulvoid propagule densities settling on tiles during winter months. In 1993 a number of 82 x 106 spores m-2, able to germinate under cultivation conditions, were calculated to have settled in the investigation area. In comparison to other investigations on macroalgal spore production (summarised by SANTELICES,1990) this number appears to be very low. Two facts may explain this discrepancy: (1) not all spores released by adult Enteromorpha plants are vital (HOFFMANN and CAMUS, 1989); (2) the majority of spores are released by the incoming tide due to desiccation during ebb-tide and settle in close vicinity of parent plants; the remaining part disperses with the current in a progressively diluted cloud (DEYSHERand NORTON, 1982) and can be widely distributed (AMSLER and SEARLES, 1980). The nearest Enteromorpha populations were more than 200 m away from my investigation area. Therefore, it is not possible to calculate a posteriorifrom my results the total spore production of Enteromorphain K6nigshafen. Previous studies of SCHORIESand REISE(1993) showed that germination of Enteromorpha spp. spores was restricted to spring and then rapidly decreased. In this study the number of spores attached to the polyethylene dishes during winter time was zero or close to zero. The only possibility to guarantee the development of adult plants in spring in a sandy intertidal area, free of overwintering plants and fragments, must be the survival of already settled spores in winter. In the laboratory dark resistance of various Enteromorpha spp. spores was at least 10 months, and thus much higher than expected based on the results of su-ro (1950), but in the same order of magnitude as in findings of KYLIN (1947) and ARASAKI (1953). Low winter temperatures support survival of Enteromorphaspores, but restrict germination together with other environmental conditions (WOODHEAOand MOSS,1975). Sediment samples taken in February 1994, demonstrated, that even 6 months after the last considerable spore settlement, the sediment was stuffed wit Enteromorphaspores up to a depth of 5 cm. This observation coincided well with the yearly entrainment zone of the sediment in K6nigshafen bay (2-6 cm, BAYERL,1992). The spores seem to be well adapted to anoxic conditions in the sediment and protected against possibly toxic bacterial activities. Assuming that the calculated number of 82 x 106 spores m-2, which settled during 1993, also represents the real spore deposition onto the sediment surface in the investigated area, at least

345

4% of the spores survived winter. These spores were the prospective initiators of Enteromorpha spread in the following spring together with those settling onto on other substrata (SCHORIESand REISE, 1993). At first, it seems to be a disadvantage for a spore to be embedded in the sediment and thus be far away from the light. However, the advantages of being protected against dislocation due to storms and grazing, as known from the rocky intertidal zone, might be a good survival strategy. It is well documented, that littorinid snails efficiently graze Enteromorpha spores on rocks and thus can inhibit growth of adult plants (HAWKINSand HARTNOLL, 1983). Grazing by these snails would not be efficient in a sandy intertidal area, as this study implies: once snails grazed the spores off the sediment surface, the next recruits would come up immediately after sediment disturbance. It was shown that only coarse sediment was suitable as a substratum for Enteromorphaprolifera zoospores and subsequent germination. In comparison to other intertidal flats of the Frisian coast (FIGGEet aL, 1980) the sediments of K6nigshafen bay are extraordinarily rich of coarse sand grains (>250 pro) due to aeolian import from nearby dunes (GOLDSCHMIDTet HI., 1993). Generally, germination of Enteromorpha spores on sand grains seems to be restricted to areas with coarse surface sediment; in other places development of Enteromorpha spp., therefore, depends on the availability of biogenic substrata (BAUMERT,1924; KOEMAN,1975; SCHORIES and REISE,1993). It is concluded that (1) persistence of spores during winter provides the general potential for adult growth and (2) in most cases the availability of Enteromorphaspp. spores in coastal intertidal areas is not the bottleneck for the development of Enteromorpha mats. Instead, other abiotic or biotic factors determine whether an algal mat develops or not.

ACKNOWLEDGEMENTS I gratefully acknowledge the help of A. Albrecht and D. Lackschewitz. The investigation was supported by the F.R.G. Ministry of Research and Technology (Publication No. 175 of the Wadden Sea Ecosystem Project).

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Enteromorpha spores in the Wadden Sea

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Address of author:

Biologische Anstalt Helgoland,Wadden Sea Station, 25992 List / Sylt, Germany. Present address: Zentrum for Marine Tropen6kologie,KlagenfurterStr. GEO,28359 Bremen, Germany.