Distribution and growth dynamics of ephemeral macroalgae in shallow bays on the Swedish west coast

169

Journal of Sea Research 35 (1-3): 169-180 (1996)

D I S T R I B U T I O N A N D G R O W T H D Y N A M I C S OF E P H E M E R A L M A C R O A L G A E IN S H A L L O W BAYS ON T H E S W E D I S H W E S T C O A S T

LEIF PIHL 1, GUNILLA MAGNUSSON 1,2, INGELA ISAKSSON 1 and INGER WALLENTINUS 2 1GSteborg University, Kristineberg Marine Research Station, S-450 34 Fiskeb~ckskil, Sweden 2GSteborg University, Department of Marine Botany, Carl Skottsbergs gatan 22, S-413 19 GSteborg, Sweden

ABSTRACT

Distribution and growth dynamics of ephemeral macroalgae were investigated in some shallow (0-1 m) bays on the Swedish west coast during the period 1992 to 1994. Variation in cover and biomass was assessed in nine bays, and in one of them the seasonal dynamics of these algae was followed intensively over three years. Frequent measurements were taken of algal biomass, degree of cover, in situ growth, variable fluorescence and C/N-ratios. Irradiance and water nutrient concentrations were measured concurrently with the growth measurements. Ephemeral macroalgae were dominated by C/adophora and Enteromorpha species and occurred in all sampled bays, except one, covering 10 to 100% of the bottom sediment. Generally, a rapid biomass increase was recorded from mid-May, which peaked after six weeks at 400-600 g dwt-m "2. Later in the season, strong variations in biomass, cover and species composition were observed, suggesting that these opportunistic algae form a highly dynamic community. Initial growth rates estimated from biomass samples were similar to those recorded from in situ cage experiments, and also agreed with growth rates calculated from a model. For all species studied growth rate was within the range 10 to 30 g dwt.m'2.d "1, irrespective of method used. Low algal C/N-ratios (mean = 12.7) in 1993 (cold and rainy summer) indicated that growth was not limited by nutrients, but rather by light. In 1994 (warm and sunny summer), mean C/N-ratios were 20, reflecting the opposite situation. The appearance of these opportunistic algae in shallow bays which historically had been without macroalgal communities has changed the characteristics of these areas by altering habitat complexity. This could have important consequences for trophic interactions involving many species, thereby altering community structure and function.

Key words: green algae, macroalgal mats, eutrophication, nutrients, biomass, C/N ratios, growth model, variable fluorescence, Skagerrak, ecosystem changes

1. INTRODUCTION Eutrophication is a global phenomenon in marine coastal environments and is thought to be the cause of structural and functional changes in pelagic as well as benthic ecosystems (e.g. Officer et al., 1984; Eimgren, 1989; Rosenberg et aL, 1990). In the phytal system functional and structural changes are similar worldwide, although species may differ. This implies a shift in the composition, from a dominance of late successional algae to opportunistic ones, which may have a strong impact on the macrofauna and fish by reducing the architecturally important 3-dimensional structure of the vegetation into a more or less homogenous 2-dimensional one (cf. Duarte & Roff, 1991). A common symptom of elevated nutrient supply

observed in estuaries and coastal bays is the occurrence of large macroalgal 'blooms' dominated by drifting filamentous, tubular or sheet-like green algae such as species of Cladophora, Enteromorpha and Ulva, which seem to have increased over the last decades (e.g. Reise et aL, 1989; Lavery et aL, 1991; Bonsdorff, 1992; Hardy et al., 1993). Ephemeral algae with high surface area to volume ratios are characterized by fast rates of production and nutrient uptake compared to the much slower rates of the late successional species such as fucoids (e.g. Wallentinus, 1984a, 1984b and references therein). Fixing of solar energy and nutrients is thus mainly bound into ephemeral algae and no longer goes into the comparatively large biomasses of the long-lived perennial seaweeds or phanerogams.

170

L. PIHL, G. MAGNUSSON, I. ISAKSSON & I. WALLENTINUS

\ NOF~ Lly 59

58

Area E

atmospheric depositions, and are now considered eutrophic (Rosenberg, 1985). However, nutrients are also brought from the North Sea by deep-water influxes (e.g. Rydberg et al., 1990). The supply of nitrogen to the Kattegat and the Skagerrak has increased fourfold since 1930 and has doubled after 1970 (Rosenberg et al., 1990). Extended occurrence of filamentous macroalgae in the Kattegat-Skagerrak area was first recorded in the mid 1970s (Wennberg, 1987), and during the 1980s these algae have been commonly observed in bays and estuaries along the Swedish west coast (Isaksson & PiN, 1992; Utterstr6m-Gustavsson, 1993; Pihl et al., 1994; Wallentinus, 1995). The aim of this investigation was to provide quantitative data on distribution and seasonal growth and nutrient dynamics of ephemeral algae in shallow soft-bottom bays on the Swedish west coast. Since increases in biomass might be due both to growth and redistribution of algae by water movements, growth rates of some dominant algal species were measured individually in one bay, in which nutrient concentrations in the water were recorded frequently. To reveal the possibility of using physiological models to estimate growth and nutrient uptake more conveniently, in situ growth rates were compared with theoretical carbon uptake calculated from light measurements and variable fluorescence by the algae. Contents of C and N in the algae were used to evaluate limitation or excess of nitrogen as well as to estimate nitrogen uptake rates by using data from the model.

I

Fig. 1. The Swedish west coast showing the position of the shallow bays investigated. Sub-areas (1, 2, 3) and stations for nutrient samples in water (w) are shown for the intensively studied bay E, Tr~lebergskile. Since the ephemeral algae fluctuate considerably over the year, they give pulsed releases of nutrients back to the water by decomposing, and thereby influence the nutrient dynamics (cf. Lavery & McComb, 1991; Sfriso et al., 1992) causing reduced stability of the marine ecosystem. Nutrient enrichment favouring the opportunistic macroalgae also has an impact by increasing the amounts of epiphytes on the plants or by promoting organic material in the water which sediment on the thalti or seagrass leaves. The accumulation of drifting macroalgae further affects other subsystems such as the structure and function of the microbenthic communities in shallow sediments (Sundb&ck et al., 1990) or by converting sediment areas to communities dominated by loose macroalgae (Nilsson et aL, 1991). Swedish coastal waters have received increasing amounts of nutrients over the last five decades from several sources such as direct loads from discharges (sewage, industries and fish farms), land run-off and

2. MATERIALS AND METHODS 2.1. DEGREE OF COVER AND ALGAL BIOMASS Degree of cover and mean biomass of ephemeral algae were assessed and dominant species were identified on four occasions during 1992 in three shallow (0-1 m) soft-bottom bays (E, G and H) on the Swedish west coast (Fig. 1). With the aim to study geographic variation, the investigation was extended in 1993 to include nine bays, that year sampled on three occasions. Four exposed (C, E, F and H) and five sheltered (A, B, D, G and I) small (1 to 10 ha) soft-bottom, low-tidal (amplitude < 0.2 m) bays were chosen, and these areas were considered representative of the northern part of the Swedish west coast (Fig. 1). In co-operation with the Swedish coastguard, aerial photos of bays were taken on each sampling occasion to identify different types of vegetation (seagrasses, fucoids and ephemeral algae) in the nine bays and the areal extension of ephemeral algae was estimated. In each bay, an area of 10 000 m ~ (100 x 100 m) was marked so that it could be identified on the aerial photos. Slides were later analysed for percentage cover of ephemeral algae within the defined

EPHEMERAL MACROALGAL DISTRIBUTION AND DYNAMICS

areas by using a Jandel Opaque Tablet and Sigma-Scan computer program. Ground truth sampling in each bay in connection with the aerial photo documentation provided data on mean algal biomass and species composition and helped to interpret the information in the photos. On each occasion, five samples were taken in areas covered with vegetation in each bay at depths between 0.2 and 0.7 m. Vegetation was collected inside a 0.03 m 2 cylinder, which was thrown backwards overhead at randomly selected sites. Growth rates were calculated by difference in biomass data over time. Seasonal dynamics of the ephemeral algae was followed more frequently from spring to autumn from 1992 to 1994 in one bay, Tr~.lebergskile (E). Algal cover and mean biomass were estimated and dominant species were identified on five occasions during 1992 and almost weekly from April to August 1993 and 1994. In 1994, samples were also taken once in September and in October. In addition, seasonal succession in species composition was followed independently in three sub-areas within the bay during 1994 (Fig. 1). Organic matter contents of sediments were determined as loss of ignition in August 1993 in each bay by randomly taking five samples from the upper 5 cm of sediment, drying them to a constant weight at 60°C and then combusting them for 5 h at 550°C (Crisp, 1971). In this study exposed bays were defined by having a sandy-silt sediment with an organic-matter content varying between 0.6 and 1.4%, while sheltered bays had a clay-silt sediment and an organicmatter content varying from 5.0 to 11.8%. 2.2. NUTRIENTS AND IRRADIANCE Nutrient concentrations (pM NO3-, NH4 + and PO4-) in the water were measured in TrAlebergskile (bay E) at four stations (w, Fig. 1) from the end of May until August in 1993 and 1994. The stations sampled represented a transect from the inner part (water depth approximately 0.2 m) to the outer part of the bay (water depth approximately 0.7 m). Samples were taken in triplicate in the middle of the water column, in 1993 twice a week and in 1994 once a week, and were measured on an auto-analyser (Technicon Auto Analyser II). Data on total incident irradiance (Wh.m-2), measured with a pyroheliometer at G6teborg, were acquired from the Swedish Meteorological and Hydrological Institute. Assuming a reflection at the water surface of 3% and that PAR (Photosyntetic Active Radiation) constitutes 50% of total irradiance (Kirk, 1983), the incident irradiance (h v PAR, p.mol photons.m 2 .s- 1 ) was calculated by using the following factor conversion (LL~ning, 1981 ): 1 W.m -2 = 2.5 * 1018 quanta.m-2-s -1 = 4.2 pmol photons-m-2-s -1.

171

The irradiance penetrating to the depths of the cages (see section 2.3.) at Tr~.lebergskile was measured with a spherical sensor (Biospherical Instruments) and was calculated as percentage of incident irradiance (h v PAR) at the water surface. 2.3. ALGAL GROWTH RATES, FLUORESCENCE AND C/N-RATIOS

In situ growth rate, variable fluorescence and C/N-ratios of ephemeral algae were measured in the intensively studied bay Tr~.lebergskile (E). In 1993, growth rates of four green algal species were evaluated from in situ cage experiments. The species tested were dominant during different parts of the season and consequently experiments were run during different periods for each species: Cladophora cf. vagabunda (L.) Hoek between May 25 and June 28, Percursaria percursa (C. Ag.) Bory between June 17 and July 21, Enteromorpha flexuosa (Wulfen ex Roth) J. Ag. between June 28 and August 2 and Enteromorpha linza (L.) J. Ag. between July 21 and August 11. The cages were constructed from half of an acrylic glass cylinder mounted on a PVC frame (20 x 20 cm) and had nets (2 mm mesh) at the sides and at the bottom (Gertz-Hansen & Sand-Jensen, 1992). For each species, five cages were placed on the bottom at 0.5 m depth. Algal samples (2.5 g fresh weight of each species) collected in the bay and placed in the cages were harvested after a week and weighed. This was repeated for five weeks for C. cf. vagabunda and P. percursa, and for six and three weeks for E. flexuosa and E. linza, respectively. The algae were dried in a circotherm oven at 60°C and weighed to obtain dry weight to fresh weight ratios. In addition, growth rates of the four species used in the cage experiments were estimated by using the formula described by Magnusson et al. (1994). In this formula incident irradiance (h v PARin situ; see further 3.2.) and the capacity of the plant to use light for carbon binding (o~ net) is used. Under ideal conditions o~ net is set at 0.03 (i.e. 30% of the light is used for photosynthesis) and the maximum value of Fv/Fm (i.e. when no photoinhibition occurs) at 0.83 (Magnusson et al., 1994). The value of c3net was corrected for photoinhibition by measuring variable fluorescence: cqnet=0.03 * (Fv/Fm)measure d / 0.83 C net: cqnet * hv PARin situ C net was converted into biomass by using the percentage of C in the algae on each occasion. By combining the formula above and the C/N-ratios of the algae, the potential algal nitrogen uptake per unit sea surface area was calculated. Carbon, total nitrogen and variable fluorescence were measured for algae used in cage experiments during 1993 and for Cladophora sp., Percursaria percursa, Enteromorpha linza and Enteromorpha flexu-

172

L. PIHL, G. MAGNUSSON, I, ISAKSSON & I. WALLENTINUS

1993 5

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4OO H 200

70.

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0 May

June

July

August

0 6O0 40O 2OO 0

j/

90

75

April

June

August

Fig. 2. Mean biomass (g dwt-m -2) and SE of ephemeral algae in nine shallow bays on the Swedish west coast in 1992 and 1993. Numbers above curves indicate the percentage vegetation cover of the bottom area (100x100 m).

EPHEMERAL MACROALGAL DISTRIBUTION AND DYNAMICS

osa collected weekly in Tr#.lebergskile during 1994. Carbon and nitrogen contents were measured in duplicate on about 5 mg dried algae on a carbon nitrogen analyser (Fison NA 1500 NC), from which molar C/N-ratios were calculated. Fluorescence was measured with a Plant Stress Meter (BioMonitor AB SC. Am, Sweden; Oquist & Wass, 1988). Plant material was placed in a leaf-clamp cuvette for dark adaptation for ten minutes before measurements. The nomenclature of Van Kooten & Snel (1990) was used; the parameters measured were Fo, non-variable fluorescence, and Fro, maximal fluorescence. From these values Fv, variable fluorescence, i.e. Fm-Fo, and the ratio Fv/Fm were calculated. 3. RESULTS 3.1. DEGREE OF COVER, ALGAL BIOMASS AND DOMINANT TAXA Percentage bottom area covered by ephemeral algae was highest in June (50-85%) in all areas studied in 1992, and decreased thereafter in July and August (Fig. 2). In 1993 four out of nine bays investigated had low percentage cover of ephemeral algae (0-15%) throughout the study period. In all other bays, except one, highest cover of ephemeral algae was measured in August with values between 20 and 100% (Fig. 2). In bay H the bottom area was almost completely covered with ephemeral algae during both June and August. There was no significant difference (p>0.05, Mann-Whitney U4est) in cover of ephemeral algae between exposed and sheltered bays. In 1994, the bottom sediment in bay E, Tr&lebergskile, was already covered between 5 and 15% by ephemeral algae in mid-May, and by the end of June the cover had increased to 40%. From July to September percentage cover varied between 15 and 25%, and increased thereafter to 65% in October. All three bays investigated in 1992 were devoid of ephemeral algae at the beginning of the study in early May. Biomass of ephemeral algae was similar in bay E and H during June to Augus~ with mean values between 127 and 250 g dwt-m- (Fig. 2). In bay G there was a rapid biomass increase already in June, reaching 442 _+77 (SE) g dwt.m -2. Biomass was lower in July (94+34 g dwt-m -~) in this bay, and increased again thereafter to 317+39 g dwt.m -~ in August. During the first sampling occasion in April 1993, ephemeral algae were not found in any of the nine bays investigated (Fig. 2). In June they were present in all bays, except G, and mean biomass varied between 54 and 501 g dwt.m -2. In August, biomasses were comparable to those recorded in June in three bays, whereas an increase in biomass was found in two bays. In the remaining three bays ephemeral algae had disappeared from the sampling area. Biomass did not differ significantly (p>0.05, Mann-Whitney U-test) between exposed and sheltered bays.

173

Tr~ilebergskile (E)

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olO. oo. e. . * ' ~ ~ '~s~pt ' ~ April May 'J-ne JUly'Augl . . . . i Fig. 3. Mean biomass values (g dwt.m-2) with SE of ephemeral algae sampled five times in 1992 and almost weekly in 1993 and 1994 in the intensively studied bay Tr#.lebergskile (E in Fig. 1). Values are based on five random samples within algal mats. Stars indicate strong winds (15-20 m.sq) for several days. In the intensively studied bay E (Tr&lebergskile), seasonal development in ephemeral algal biomass was quite similar during the three years of investigation. In April and early May no ephemeral algae were found in the area (Fig. 3). A rapid increase in biomass was observed from mid-May, and peak mean values (250 - 626 g dwt.m -2) were recorded in late June to early July. In August 1992 mean biomass values were 160 g dwt.m -2, while in 1993, after a week with strong winds in the middle of July, the area was free from vegetation. During August 1993 ephemeral algae biomass increased again and a mean biomass of 432+45 g dwt.m -2 was recorded at the end of the month. Also in 1994, biomass of ephemeral algae decreased suddenly after one week with strong winds in late June and considerable amounts of algae were found on land. That year, no second peak in biomass was measured, instead mean biomass values varied between 26 and 78 g dwt.m -2 until the end of the investigation in October. Cladophora spp. dominated among the ephemeral algae in June and July in the three bays investigated in 1992. In August there was a shift in dominance to Enteromorpha flexuosa in all areas. Both in June and August 1993 different species of Enteromorpha (in

174

L. PIHL, G. MAGNUSSON, I. ISAKSSON & I. WALLENTINUS

morpha sp. and Chaetomorpha linum prevailed together with P. percursa, while in July the latter species disappeared from this sub-area. From August until September there was a shift in dominance to Cladophora sp. and Enteromorpha sp. In October no vegetation was found in this sub-area. In sub-area 3, Cladophora sp. and R percursa were the dominant drift algae during May; in June together with Enteromorpha sp. In July, all three algae dominated together with Ulothrix sp. From August until the end of the investigation in October Enteromorpha sp. was the only species, except in September when it occurred together with Cladophora sp.

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3.2. NUTRIENTS AND IRRADIANCE ,u

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Fig. 4. Nutrient concentrations in the water column in Tr&lebergskile in 1993 and 1994. NH4+ (filled circles), NO3- (open circles) and PO4- (squares). Datapoints are mean values + SD from four sampling stations in the bay (see Fig. 1). most cases E. flexuosa) dominated the ephemeral vegetation in all bays, except in D and I, where in August the dominant species were the brown alga Spermatochnus paradoxus (Roth) KL~tz. and the green alga Chaetomorpha linum (O.E M~Jller) KLitz., respectively. During 1994, species succession of ephemeral algae was followed in three sub-areas within the Tr#,lebergskile bay (Fig. 1). In area 1 all species found were growing attached to the substrate (blue mussels, cobbles and Fucus serratus L.) while both in area 2 and 3 the ephemerals were mainly drifting algae. In sub-area 1, Cladophora sp. dominated during the beginning of the season and in July it was the dominant species together with Percursaria percursa. From late July until August there was a shift in dominance to Enteromorpha sp. In September and October, no vegetation was found in this sub-area. In sub-area 2 R percursa was dominating the drifting mats in May. During June, Cladophora sp., Entero1994

1993 3O 20 OZ

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Fig. 5. Surface water N/P-ratios in Tr&lebergskile during 1993 and 1994. The figures are the mean values +_SD from four sampling stations in the bay (see Fig. 1).

Nutrient concentrations in the water column did not differ significantly (p>0.05, 1-way ANOVA) between sampling stations in Tr~lebergskile, and data presented in Fig. 4 are the mean values for the four stations. In 1993, NO3--concentrations fluctuated between 0 and 10.5 #M with a peak value in July, and were less than 1 l.tM most of the time (but with slightly higher values at the beginning and the end of the summer). NH4+-concentrations varied between 0.5 and 10 ~tM, generally being about 1.5 I~M with increasing values at the end of July. PO4--concentrations varied between 0 and 1.6 #M and were relatively stable around 0.2 #M throughout the summer with a peak in July. In 1994, low concentrations of NO 3- were recorded throughout the season, except for two minor peaks in early June and late August. The amounts of NH4+ were also low during the summer with only one peak at the beginning of July. The mean concentration of PO 4- was 0.2 #M throughout the summer with one minor peak in early June. The molar N/P-ratios in the water varied between 0 and 10 (mean = 6.1) in 1993 with one peak of 30 in July. In 1994 the mean N/P-ratio was 7.5 with a seasonal variation from 0 to 20 (Fig. 5). The mean irradiance (hVpAR) during the different experimental periods varied between 25.7 and 46.7 mol photons m-2.d-1 in 1993 and 1994 (Table 1). Light penetrating to the depths of the cages fluctuated between 12 and 96% of the incident irradiance, depending on the time of the day and on weather conditions, giving an estimated mean of 70%. Because of the large fluctuations this mean value was used together with incident irradiance, when calculating growth according to the theoretical model (Magnusson et aL, 1994). A mean of 70% has generally been used in shallow coastal waters (LL~ning & Dring, 1979). 3.3. ALGAL GROWTH RATES, FLUORESCENCE AND C/N-RATIOS In 1993 and 1994 a continuous increase in biomass of ephemeral algae was recorded from field sampling

EPHEMERAL MACROALGAL DISTRIBUTION AND DYNAMICS

175

TABLE 1 Mean incident irradiation (hvpAR in mol photons.m-2.dl), mean variable fluorescence (Fv/Fm)and mean total carbon content (mg C gq dwt) for different algal species during their whole growth period. 70% of incident irradiation value was used when calculating carbon fixation in the model (see text). hVpAR F~/Fm mg C g-~ dwt species Cladophora cf. vagabunda/sp. Percursaria percursa Enteromorpha flexuosa Enteromorpha linza

1993 44.7+_13.6 35.4+15.1 30.1_+t5.0 25.7-+12.8

1994 44.9+]3.7 44.9_+]3.7 33.8_+]1.6 46.7+14.8

in Trb.lebergskile over a six-week period from mid-May through June, and in 1993 also for four weeks in August. During these initial phases, the growth rates estimated from biomass data were between 14 and 33 g dwt.m-2.d -1, resulting in a peak biomass of 425 to 625 g dwt.m -2 at the end of the periods (Fig. 3). Growth rates measured in the cages varied between 12 and 24 g dwt.m-2.d -1 for Cladophora cf. vagabunda, without any obvious trend over the five weeks, and did not differ significantly (p>0.05, Mann-Whitney U-test) from the theoretically calculated growth rate (Fig. 6). For Percursaria percursa both measured, 10-30 g dwt.m-2.d -1, and calculated growth rates were highest in the first weeks of the experiment. Calculated growth rates were significantly higher (p<0.01, Mann-Whitney U-test) than those measured in the cages. Enteromorpha flexuosa and E. finza showed no or little growth in the cage Cladophora cf. vagabunda

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1993 0.42_+0.07 0.53_+0.10 0.57_+0.10 0.68+0.06

1994 1993 1994 0.40_+0.08 255.5+P6.52 230.1+50.0 0.49_+0.08 183.1_+38.69 192.3_+32.06 0.47_+0.11 260.8_+34.18 196.0+32.06 0.50_+0.07 257.3-+15.31 182.2-+35.24

experiments, probably because they are sensitive to handling during transports and weight measurements in the laboratory. Their calculated growth rates were similar to those of C. cf. vagabunda. Overall, the daily growth estimated in the field, from biomass field samples and in situ cage experiments (excl. the Enteromorpha species for reasons given above), was in good agreement with the growth rate calculated theoretically from the model (12-60 g dwt.m-2.d-1). The total seasonal growth of ephemeral algae estimated from biomass changes in the field during the period May 15 to September 1 was 845 and 705 g dwt.m -2 in 1993 and 1994, respectively. However, growth calculated from the model for the same periods was much higher, giving values of 3150 and 2980 g dwt.m -2 in 1993 and 1994, respectively. The Fv/Fm ratios varied between 0.40 and 0.68 for the four algae studied in 1993 and 1994 (Table 1), indicating a considerable variation in photoinhibition over the growth periods. Although all algae showed somewhat lower ratios (i.e. more photoinhibition) in 1994, they were only significantly different for E. linza. The C/N-ratios for the four algae varied between 7.5 and 20.5 (mean 12.7) in 1993 and between 9.1 and 50.5 (mean 20.1) in 1994 (Fig. 7). C/N-ratios were significantly higher (p<0.05-0.01, Mann-Whitney U-test) in all species in 1994 than in 1993. The overall nitrogen uptake rates by Cladophora sp. and Enteromorpha spp., calculated by using C/N-ratios in the model, were 0.3-0.72 and 0.12-1.42 g N-m-2 day -1, respectively.

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Fig. 6. Mean growth rates -+ SD, estimated from in situ cage experiments (open circles) and calculated from a theoretical model (filled circles) (see Magnusson et aL, 1994 and part 2 of the present paper) of four dominant algae in Tr&lebergskile in 1993. Growth periods shown are: Cladophora cf. vagabunda from May 25 to June 28, Percursaria percursa from June 17 to July 21, Enteromorpha flexuosa from June 28 to August 2, Enteromorpha linza from July 21 to August 11.

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Fig. 7. Mean C/N-ratios _+ SD in four dominant algae in Tr~lebergskile during the summers of 1993 and 1994. Cladophora cf. vagabunda (11), Percursaria percusa (A), Enteromorpha flexuosa (O), and E. linza (~ ).

176

L. PIHL, G. MAGNUSSON, I. ISAKSSON & I. WALLENTINUS

4. DISCUSSION Ephemeral algae first appeared in the bays studied in late May to early June. Generally, a rapid increase in biomass was recorded which peaked four to six weeks after the start of growth. The development of ephemeral algae later in the season was without any clear patterns, probably due to influences from several abiotic and biotic factors such as light, nutrient supply, wave exposure, winds, desiccation, degradation and grazing (cf. Lowthion etal., 1985; Pregnall & Rudy, 1985; Soulsby et aL, 1985; Gertz-Hansen et al., 1993; Den Hartog, 1994). The areal extension of ephemeral algae varied in time and space from a few percent to complete cover of the sediment in the bays. In bay G, a great difference in algal cover was observed between 1993 and 1994. In 1994, a high pressure front drained the shallow bay and the sediment was dry for several weeks in April and May, which might have hindered the establishment of ephemeral algae. Our peak biomass (425 to 625 g dwt.m -2) at the end of growth periods as well as the theoretical growth calculated from the model (3150 and 2980 g dwt-m -2 in 1993 and 1994) were in the same order of magnitude as data for other macroalgal mats. Pregnail & Rudy (1985) reported a mean biomass of approximately 300 g dwt'm "2 and estimated the annual production at 1100 g C.m -2 in the summer on a mud flat in Oregon, mainly composed of Enteromorpha spp. Owens & Stewart (1983) also calculated a theoretical growth three times higher than measured biomass of Enteromorpha sp, in a Scottish estuary. These results suggest that the model used in our study could be an alternative method for assessment of growth rate of macroalgae and a complement to traditional sampling techniques. Furthermore, the model can be used to assess the growth rate during periods with a stable biomass, when growth is partly balanced by factors such as erosion, degradation and grazing. As anticipated, total seasonal growth based on biomass changes was underestimated. Nutrient concentrations showed small seasonal variations during the sampling period in Tr&lebergskile and the means for NO3", NH4 ÷ and PO 4- were similar during the two years (0.84, 2.07 and 0.4 in 1993 and 0.82, 1.44 and 0.3 in 1994, respectively). However, in 1993 peaks in nutrient concentrations were recorded on some occasions in connection with heavy rain giving extra land run-off. Within a monitoring programme nutrient concentrations were measured biweekly in 1993 and 1994 at an offshore station approximately 15 km west of the bay. The corresponding mean concentrations for NO3-, NH4 + and PO 4- in the surface water during June through August were estimated at 0.2, 0.82 and 0.08 in 1993 and to 0.09, 0.33 and 0.04 in 1994 (O. Lindahl, pers. comm.), three to nine times lower than the nutrient concentrations recorded in the bay. The mean

N/P-ratios at the offshore station were 19.4 and 9.1 during 1993 and 1994, respectively. In the bay the corresponding values were 6.1 and 7.5. Thus, algae in the shallow bay have not only more nutrient-rich conditions than offshore phytoplankton available, but also comparatively more phosphate. NH4 ÷ was available most of the time even during 1994 when precipitation was close to zero during June and July and land run-off was at a minimum. The nutrients supplied from the sediment by recycling and/or by nutrient-rich ground water seaping out, as well as from degradation of plant and animal material thus may play an important role during summer (cf. Owens & Stewart, 1983; Sfirso etal., 1987; Lapointe & O'Connell, 1989; Lavery & McComb, 1991; Sfirso et al., 1992; Sundbb,ck et al., 1994). Differences in nutrient availability or a change in N/P-ratios may also contribute to the drastic seasonal shift in dominant species found in this study. The C/N-ratios in macroalgae can be used as an indicator of the nutrient status of the plants and the difference in ratios within the same species grown in different nutrient regimes is generally larger than between different taxonomic groups (e.g. Wallentinus, 1981 ). In this study the C/N-ratios in the algae varied between 7.5 and 50, the lower value being close to the Redfield ratio (6.6) for phytoplankton. However, optimal values for macroalgae are generally higher (Atkinsson & Smith, 1983; Neori et al., 1991). Our mean values were twice as high in 1994 as in 1993 (Fig. 7). During 1993, which had a cold and rainy summer, the algae were probably light limited, while during the sunny and warm summer of 1994 the algae probably had an excess of light and/or were limited by nutrients. The probability of nitrogen limitation in a mat-forming Cladophora sericea (Huds.) K0tz. in a shallow Danish bay during April to June was discussed by Thybo-Christesen & Blackburn (1993) and Thybo-Christesen et al. (1993), when the mean C/N ratio was 17 and C/N ratios in June reached 37. The estimated nitrogen uptake rates in this study (0.3-0.72 and 0.12-1.42 g N.m -2 .dq, for Cladophora sp. and Enteromorpha spp., respectively) compared well with other studies. Magnusson et al. (1994) estimated the nitrogen uptake by Ulva lactuca L. at 0.31 g m-2.d -1 and Owens & Stewart (1983) calculated an uptake of 0.18-0.42 g N,m-2.d -1 by Enteromorpha. However, resynthesis of nitrogen by Cladophora sericea (biomass 87 g dwt.m -2) was estimated by Thybo-Christesen et al. (1993) at only 0.05 g N.m- 2 -d- 1 , but constituted 95 oYoof the nitrogen available. The factors which determine the start of the algal growth and its seasonal and successional development in Swedish shallow bays might partly be the same as in other regions. The overwintering strategies of ephemeral algae have been considered to be highly important. For Cladophora glomerata (L.) KLitz. in the Great Lakes, Rosemarin (1982) suggested that

EPHEMERAL MACROALGAL DISTRIBUTION AND DYNAMICS the overwintering of the basal parts of the thalli (akinete formation) contributed to its success in comparison to Stigeoclonium tenue (Ag.) KL~tz. The latter should theoretically have been more competitive due to its higher metabolic rates, resulting from a larger surface to volume ratio, but was incapable of an early start in spring. In the German Wadden Sea, spores and filaments of Enteromorpha have been found attached to sand grains and to the shells of the mud snail Hydrobia (Schories & Reise, 1993). The growing season in the Wadden Sea started in May and extensive mats developed during summer. The mud snail Hydrobia was suggested to function as an additional substrate for the algal filaments, especially in areas with fine-grained sediments and excess of nutrients, thereby partly contributing to the rapid growth of ephemeral algae during early summer (Schories & Reise, 1993). The observed strong seasonal variation in cover, biomass and species composition of ephemeral algae suggests that this type of algal vegetation comprises a highly dynamic community in the shallow embayments on the Swedish west coast. In the nine shallow bays studied, six taxa of ephemeral algae were found in significant amounts. Different species dominated in different bays at the same time and in most areas shifts in species dominance occurred one or several times during one season. Thus, separate factors may be important during the initial growing phase of a species, and hereby influence its success as a competitor. In addition to distribution and occurrence of spores and overwintering thalli, the potential for growth of a species is to a large extent governed by competition. Uptake rates of nutrients may also vary between and within ephemeral species due to their internal concentrations (cf. Wallentinus, 1984a and references therein) as well as due to the nutrient availability per unit of time (continuously or in pulses). Furthermore, the capacities of the species to store energy and nutrients can shift (cf. Fujita, 1985; Carpenter, 1990; McGlathery, 1992; Wheeler & Bj6rns&ter, 1992). Besides different responses to light regimes (e.g. Gertz-Hansen & Sand-Jensen, 1992; Henley et aL, 1992; Magnusson et aL, 1994), another important feature might be that growth and uptake of carbon or nutrients are not directly coupled (cf. Henley, 1990). Thus the physiological status of the plants, determining the turnover rates, may also be used to reflect the degree of impact on the system. Wind-induced wave erosion often changed the distribution of ephemeral algae drastically and could clean a bay completely. Wind might therefore be an important factor for the seasonal succession of dominant species in shallow areas (Lowthion et al., 1985; Pregnall & Rudy, 1985). However, in this study, there were no overall differences in algal distribution, biomass or species composition between exposed and sheltered bays. Shallow (0-1 m) soft-bottom bays on the Swedish

177

Skagerrak coast were generally free from vegetation during the 1970s and ephemeral algae appeared only in the 1980s (Pihl, 1986; Isaksson & Pihl, 1992). During the last decade an increase in occurrence of ephemeral algae has been observed, and in 1990s large areas were found to be covered with algae. In a survey of 300 bays along the Skagerrak coast during June and August 1994 the percentage cover of ephemeral algae was estimated from aerial photographs. Seventy percent of the bays were found to have these opportunistic algae (>5% cover) and, on average, these bays had an algal cover of 52% (Moksnes & Pihl, 1995). This is in agreement with the increasing occurrence of ephemeral algae observed in many estuaries and coastal bays during the last decades (e.g. Breuer & Schramm, 1988; Reise et al., 1989; Hardy et al., 1993; Munda, 1993; Schramm et al., 1995 and references therein), and these changes have in most cases been related to enhanced nutrient loading to coastal waters (Buttermore, 1977; Van Montfrans et al., 1984; Sfriso et aL, 1987; Reise et al., 1989). Thus, proliferation by ephemeral algae may be regarded as a general sign of coastal eutrophication (cf. Sfriso et al., 1987). Shallow bays are important nursery and feeding areas for several fish species (Pihl, 1982; Pihl & Rosenberg, 1982; Pihl, 1989). The occurrence of ephemeral algae in shallow soft-bottom bays on the Swedish west coast during the last decade has changed the characteristics of these areas by altering habitat complexity. The changes involve many species and have a high impact on macrofauna and fish in the community, including effects on commercially important species, which often use the large plants for shelter and foraging (e.g. Reise, 1983; Hall & Bell, 1988; Reise et al., 1989; Raffaeli et al., 1991 ; Baden et aL, 1990; Isaksson & Pihl, 1992; Pihl et al., 1994). However, they also provide a huge magnification of the surface area available for epiphytic micro- and meiofauna as well as for smaller macrofauna, which to a certain extent might promote productivity. Isaksson & Pihl (1992) reported a shift in dominant fauna in a sandy bay and an eelgrass bed (Zostera marina), sampled from 1980 to 1990, when cover of ephemeral algae increased. In the sandy bay, epibenthic faunal biomass increased with a moderate cover (30 to 50%) of ephemerals, but was reduced at higher cover (90%). In the eelgrass bed faunal biomass was reduced at both moderate and high cover of ephemeral algae. Also the fish assemblage sampled at 19 stations in the archipelago of G6teborg (Pihl et al., 1994) was related to vegetation structure and both species number and biomass were found to be negatively affected by the occurrence of ephemeral algae. The timing of growth of ephemeral algae is important for the recruitment of fauna during spring and early summer. For example, plaice larvae (Pleuronectes platessa) are transported to coastal areas during spring, and after metamorphosis they settle in

178

L. PIHL, G. MAGNUSSON, I. ISAKSSON & I. WALLENTINUS

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Fig. 8. A generalized and simplified model of storages and flows in shallow bays. Thick lines indicate impact by ephemeral macroalgae. --> are flows of energy and nutrients; - - -> are impact on storages and flows; circles = pools outside the system; 'bird hoses' = non-biological pools; 'bullet shaped' symbols = autotrophs; hexagons = heterotrophs; ,~. two-way flows and processes regulated by threshold values (Odum & Odum, 1976). Temperature effects and respiration are not included in the model. shallow bays with sandy substrate. Field sampling and laboratory experiments have shown that larvae and early benthic juvenile stages of plaice avoid substrate covered with ephemeral algae; in areas where ephemeral algae cover the bottom during the recruitment period a reduction in plaice density is found (Pihl & Van der Veer, 1992; Wennhage & Pihl, 1994). The fact that even some of the bays with sandy substrate had high biomasses of ephemeral algae during that season constitutes a threat also to migrating populations. The main flows of energy and nutrients in shallow bays on the Swedish west coast are depicted in Fig. 8, where the impact by ephemeral macroalgae on the structure and function of the ecosystem has been emphasized. The following storages and processes are mainly influenced: 1) formation of particulate organic matter and through decomposition processes the nutrient release and the consumption of oxygen; 2) competition for light, nutrients and space with other benthic primary producers;

3) 4)

food supply and space for grazing epifauna; recruitment and migration of macrofauna and fish. The main forcing functions on the establishment of ephemeral macroalgae are the availability of light, nutrients (incl. N/P ratios), wind dispersal and area available for growth (incl. areas provided by some macrofaunal species and macrophytes). 5. CONCLUSIONS Fast growing ephemeral algae can build up large biomasses within a couple of weeks, and in some areas they may cover a whole bay. Through their rapid metabolic rates and short life span these algae have a significant influence on carbon and nutrient dynamics in shallow embayments and on the stability of the ecosystem. In connection with strong winds, ephemeral algae may disappear from a shallow bay within a few days. These rapid and unpredictable changes of the habitat structure will strongly affect the faunal succession during the season.

EPHEMERAL MACROALGAL DISTRIBUTION AND DYNAMICS

Acknowledgements.--The Swedish Environmental Protection Agency has given financial support to the two projects (contracts to L.P. and I.W). Additional grants were obtained from the Hiertha-Retzius foundation. We are most obliged to the Swedish coast guard for making it possible to take the aerial photographs and to the Swedish Meteorological and Hydrological Institute in G6teborg for providing light data. Technical assistance was provided by Maria Bjurstr6mer, Bj6rn Fagerholm, Sven Nilsson, Per Moksnes and H&kan Wennhage. Dr. Mats Kuylenstierna kindly assisted in identifying some of the macroalgal species and Dr. Lennart Axelsson gave advice and comments on the manuscript and provided equipment for analysis. 6. REFERENCES Atkinson, M.J. & S.V. Smith, 1983. C:N:P ratios of benthic marine plants.--Limnol. Oceangr. 28: 568-574. Baden S.P., L.-O. Loo, L. Pihl & R. Rosenberg, 1990. Effects of eutrophication on benthic communities including fish: Swedish west coast.--Ambio 19: 113-122. Bonsdorff, E., 1992. Drifting algae and zoobenthos - effects on settling and community structure.--Neth. J. Sea Res. 30: 57-62. Breuer, G. & W. Schramm, 1988. Changes in macroalgal vegetation of Kiel Bight (western Baltic Sea) during the past 20 years.--Kieler Meeresforsch. 6: 241-255. Buttermore, R.E., 1977. Eutrophication of an impounded estuarine lagoon.--Mar. Poll. Bull. 8:13-15. Carpenter, C., 1990. Competition among marine macroalgae: a physiological perspective.--J. Phycol. 26: 6-12. Crisp, D.J., 1971. Energy flow measurements. In: N.A. Holme & A.D. Mclntyre. Methods for the study of marine benthos. Blackwell Sci. Publ., Oxford and Edinburgh: IBP Handbook 16: 197-279. Den Hartog, C., 1994. Suffocation of littoral Zostera bed by Enteromorpha radiata.--Aquat. Bot. 47: 21-28. Duarte, C.M. & D.A. Roff, 1991. Architectural and life history constraints to submersed macrophyte community structure: a simulation study.--Aquat. Bot. 42" 15-29. Elmgren, R., 1989. Man's impact on the ecosystem of the Baltic Sea. Energy flows today and at the turn of the century.--Ambio 18: 326-332. Fujita, RM., 1985. The role of nitrogen status in regulating transient ammonium uptake and nitrogen storage by macroalgae.--J, exp. mar. Biol. Ecol. 92: 283-301. Gertz-Hansen, O. & K. Sand-Jensen, 1992. Growth rates and photon yield of growth in natural populations of a marine macroalgae Ulva lactuca.--Mar. Ecol. Prog. Ser. 81: 179-183. Gertz-Hansen, O., K. Sand-Jensen, D.F. Hansen & A. Christiansen, 1993. Growth and grazing control of abundance of the marine macroalga, Ulva lactuca L. in a eutrophic Danish estuary.-Aquat. Bot. 46:101-109. Hall, M.O. & S.S. Bell, 1988. Response of small mobile epifauna to complexity of epiphytic algae on seagrass blades.--& mar. Res. 46" 613-630. Hardy, F.G., S.M. Evans & M.A. Tremayne, 1993. Long-term changes in the marine macroalgae of three polluted estuaries in north-east England.~. exp. mar. Biol. Ecol. 172: 81-92. Henley, W.J., 1990. Uncoupling of various measures of

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