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Spring and Summer Proliferation of Floating Macroalgae in a Mediterranean Coastal Lagoon (Tancada Lagoon, Ebro Delta, NE Spain)
Estuarine, Coastal and Shelf Science (2000) 51, 215–226 doi:10.1006/ecss.2000.0637, available online at http://www.idealibrary.com on
Spring and Summer Proliferation of Floating Macroalgae in a Mediterranean Coastal Lagoon (Tancada Lagoon, Ebro Delta, NE Spain) M. Mene´ndeza and F. A. Comı´n Department of Ecology, University of Barcelona, Av. Diagonal 645, 08028 Barcelona, Spain Received 6 September 1999 and accepted in revised form 27 March 2000 During the last 10 years, a drastic change in the structure of the community of primary producers has been observed in Tancada Lagoon (Ebro Delta, NE Spain). This consisted of a decrease in the abundance of submerged rooted macrophyte cover and a spring and summer increase in floating macroalgae. Two spatial patterns have been observed. In the west part of the lagoon, Chaetomorpha linum Ku¨tzing, dominated during winter and decreased progressively in spring when Cladophora sp. reached its maximum development. In the east part of the lagoon, higher macroalgal diversity was observed, together with lower cover in winter and early spring. Cladophora sp., Gracilaria verrucosa Papenfuss and Chondria tenuissima Agardh, increased cover and biomass in summer. Maximum photosynthetic production was observed in spring for G. verrucosa (10·9 mg O2 g 1 DW h 1) and C. tenuissima (19·0 mg O2 g 1 DW h 1) in contrast with Cladophora sp. (15·9 mg O2 g 1 DW h 1) and Chaetomorpha linum (7·2 mg O2 g 1 DW h 1) which reached maximum production in summer. Increased conductivity from reduced freshwater inflow, and higher water temperatures during periods of lagoon isolation, mainly in summer, were the main physical factors associated with an increase in floating macroalgal biomass across the lagoon. Reduced nitrogen availability and temperature-related changes in carbon availability during summer were related to a decrease in abundance of C. linum and increases in G. verrucosa and Cladophora sp. 2000 Academic Press Keywords: biomass; production; macroalgae; coastal lagoon; eutrophication; NE Spain
Introduction There is increasing eutrophication of coastal aquatic ecosystems worldwide which is associated with human activities, such as runoff from intensely fertilized agricultural fields, direct wastewater discharges, and disturbances of natural water flows (Valiela et al., 1992; Sfriso et al., 1992; McComb & Humphries, 1992; Taylor et al., 1995; Morand & Briand, 1996). In coastal lagoons, the most frequently reported consequences of eutrophication are changes in biogeochemical processes and the structure of biological communities (Taylor et al., 1995), including macroalgal blooms (Morand et al., 1990; Lavery & McComb, 1991; Viaroli & Pugnetti, 1992; Taylor et al., 1995; Anderson et al., 1996). Increased nitrogen inputs in such ecosystems have been associated with macroalgal blooms, particularly in temperate zones where high temperature and solar radiation favour the vernal proliferation of fast-growing species (Nixon et al., 1986; Howarth, 1988). Tancada Lagoon is a confined coastal body of water in NE Spain. During the last 10 years, a drastic 0272–7714/00/080215+12 $35.00/0
change in the structure of the community of primary producers has occurred in this lagoon, which has induced decreases in cover and biomass of submerged rooted macrophytes and overwhelming increases in the abundance of floating macroalgae during late spring and summer (Comin et al., 1995). This paper describes spring and summer proliferation of ephemeral macroalgae in Tancada Lagoon resulting from water eutrophication and confinement caused by the impact of agricultural practices in nearby rice fields during recent years. Water conductivity and nutrient concentrations were used as indicators of the environmental conditions under which algae growth took place. The nutrient content of the algae was analysed to evaluate limitation or excess of nitrogen. The photosynthetic performance of several species was determined to establish its relevance for development at different times during the growing season. The aim of this paper is to provide quantitative data on the temporal changes of the spatial distribution of ephemeral algae, related to their photosynthetic characteristics, in a shallow Mediterranean lagoon. 2000 Academic Press
216 M. Mene´ ndez and F. A. Comı´n
N Canal Vell Buda Encanyissada
Tancada Mediterranean Sea 0
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TAW TAE
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F 1. Map of the Ebro Delta (NE Spain) and Tancada Lagoon showing the distribution of macroalgae in summer 1997 and the location of the transects for macroalgae biomass sampling. TAE: Tancada East basin, TAW: Tancada West basin. t1: transect 1 t2: transect 2. The location of physicochemical samples is also shown ( ).
Material and methods Study area Tancada is a small, shallow coastal lagoon located in the Ebro River Delta, NE Spain (Figure 1), with an area of 1·8 km2 which is distributed in two basins (called East and West here) and has an average depth of 37 cm (Comin, 1984). During the 1970s and 1980s it received freshwater inflows from irrigated rice fields from May to October which led to relatively low water conductivity (Comin, 1984; Menendez & Comin, 1989). In the last 10 years, freshwater inflows have decreased progressively due to changes in agricultural
management practices and this has resulted in two differentiated zones. Increased conductivity has been observed in the East basin, which rarely received freshwater inputs. In contrast, lower conductivity has become apparent in the West basin which received most of the nutrient rich freshwater inputs from rice fields. These long-term hydrological changes have altered the macrophyte vegetation. In 1987, this lagoon was mostly occupied by a dense Ruppia cirrhosa Petagna (Grande) meadow with a small area in the central part of the West basin covered by Potamogeton pectinatus L. (Menendez & Comin, 1989). By 1989 P. pectinatus had completely disappeared and a
Floating macroalgae in a Mediterranean coastal lagoon 217
progressive increase in floating macroalgal growth was observed (Comin et al., 1995). During the mid1990s, macroalgal biomass and cover increased greatly during spring and summer due to the proliferation of Cladophora spp. and Chaetomorpha linum (O. F. Mu¨ ller) Ku¨ tzing in the West basin and Chondria tenuissima (Goodennough and Woodward) C. Agardh, Cladophora spp., and Gracilaria verrucosa (Hudson) Papenfuss in the East. Environmental variables Water transparency, conductivity, pH, dissolved oxygen and nutrient concentrations were measured monthly at four sites in the lagoon (Figure 1). Conductivity, pH and dissolved oxygen were measured in situ with portable apparatus. Nitrate, nitrite and ammonium nitrogen concentrations were determined from water samples (using Whatman GF/C filters combusted at 500 C) following Grashoff et al. (1983) in a Technicon Autoanalyzer. Light extinction coefficient was measured with a radiometer and quantum spherical sensor (Li-Cor, Lambda Instruments). Macroalgal biomass sampling The degree of cover and biomass of floating macroalgae were assessed on five occasions during 1997. Because the species of macroalgae studied are in unattached mats, increases in biomass may be due to both in situ growth and redistribution by water movements. In winter the prevalent wind in Tancada Lagoon is from the north-west and macroalgae accumulate mainly in the south part of the lagoon. In spring and summer there is a time of high stability in this area, only a light breeze from the south-east is observed from midday to sunset. A sampling strategy based on transects which are perpendicular to the shore was chosen, because it covers the spatial variability observed in this lagoon better than random sampling design. Biomass samples were collected in long transect lines in the East and West basins (Figure 1). In the West basin, macroalgal samples were collected every 8 m along a transect line that extended northwards from the central part of the southern shore, to the inner part of the lagoon, until no macroalgae were found. In the East basin, two transects were established because of differences observed in the distribution of macroalgae in this part of the lagoon, as thick mats were observed in the first 3 m near the shore line and with at least two species of macroalgae, and a less dense distribution towards the centre of the lagoon, with only one or two species (Figure 1): (a) transect 2 was located near the shore
and was used to sample the shallowest part of the East basin; sampling points were fixed 50 cm apart along 3 m, (b) transect 1 was a longer transect and sampling points were located every 2 m until no macroalgae were observed. Macroalgal samples were collected from the whole water column using a plastic cylinder with a basal area of 64 cm2 which was introduced in the water column and firmly pressed into the sediment. Epibionts attached to algae mat were sorted and counted and macroalgae were dried to constant weight at 60 C. Sampling was carried out in March, April, June, July and August 1997. Nutrient content and chlorophyll Carbon (C) and nitrogen (N) content of macroalgae were measured in subsamples taken from biomass collected during the study period. Macroalgal subsamples were ground to a powder (<0·5 mm diameter) and analysed for total N using a Carlo Erba Autoanalyzer. Fragments of macroalgae were collected for chlorophyll analysis in spring (April) and summer (July). These samples were frozen (11 C) and transported to the laboratory where pigments of triplicate samples were extracted in 90% acetone according to procedures described by Sestak (1971). Determinations of chlorophyll a and b were based on equations reported by Jeffrey and Humphrey (1975). Photosynthesis vs. irradiance measurements Measurements of macroalgae photosynthesis were carried out in spring (April) and summer (July). Water and algae were collected from the lagoon. Fresh growing parts of macroalgae were collected by hand and kept in aerated lagoon water at the same temperature (1 C) and with light/dark pattern as in sampling site, for no longer than 5 days prior to photosynthesis incubations, following Evans et al. (1986). Incubations were performed in filtered (0·45 m mesh size) lagoon water in 100 ml glass stoppered bottles. Approximately 0·2 g fresh weight of whole algal thalli were incubated in each bottle. Dry weight was determined after each experiment by drying the algae at 60 C to constant weight. The bottles were placed in incubators at a controlled temperature and stirring bars (c. 200 rpm) were used to breakdown diffusion gradients and decrease errors resulting from internal oxygen storage. All experiments were performed at ambient water temperatures (20 C and 30 C in April and July, respectively) and dissolved inorganic carbon levels (3·07 and 1·79 mmol l 1 in April and July, respectively). Daylight fluorescent tubes (400–700 nm waveband) were used, and the irradiance was adjusted by covering the bottles with
218 M. Mene´ ndez and F. A. Comı´n
Statistical analysis To test the effect of seasonality on Pm, R and in each species, analysis of variance (one-way ANOVA) was used. Similarly, differences between species were tested with data obtained in April and July. The fitted characteristics of the lines and curves were log transformed to obtain homogeneity of variances and determined to be normally distributed (Lilliefors test) before the analyses were conducted. The CSSStatistica computer program was used for statistical analysis. Results Environmental variables The West basin of Tancada lagoon received freshwater inflows from rice fields during spring and summer. This caused a decrease in water conductivity from 37·6 mS cm 1 in March to 22 mS cm 1 in April which then remained around 30 1·57 mS cm 1 until September (mean annual conductivity 29·2 mS cm 1, range: 12·38–37·6 mS cm 1). An increase in the concentration of dissolved inorganic nitrogen (DIN) from 21·37 mol l 1 in March to 73·83 mol l 1 in April, mainly in nitrate (52% and 71% of the DIN, in March and April respectively) was observed during the period of freshwater inflows (Figure 2). This coincided with an increase in light attenuation (from a
NO3 + NO2 (mmol l–1)
60 50 40 30 20 10
NH 4 (mmol l–1)
0 50 40 30 20 10 0 5 RSP (mmol l–1)
neutral filters to assess photosynthesis-irradiance relationships (between 0 and 830 mol photon m 2 s 1). Photosynthetically active radiation (PAR) was measured with a radiometer and quantum spherical sensor (Li-Cor, Lambda Instruments). After 2 h of incubation, dissolved oxygen (DO) concentrations were measured to the nearest 0·01 mg using an oxygen electrode (WTW), and compared with DO concentrations in control bottles (N=3) without plants. All the results were expressed in mg O2 g 1 dry weight h 1. Three replicates of each experimental condition were used. Parameters describing the photosynthesis vs. irradiance response (P-I) were determined for each incubated species using the Enzfitter program (Menendez & Sanchez, 1998). The maximum rates of net photosynthesis (Pm) were determined by averaging points on the light-saturated portion of each P vs. I curve (e.g. as the slope approached zero). Respiration rates (R) were determined by measuring oxygen consumption in dark bottles. A linear regression of photosynthetic rates at light-limiting irradiance (0, 30 and 60 mol m 2 s 1) was used to calculate the initial slope ().
4 3 2 1 0
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A M 1997
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F 2. Nutrient concentrations in the water column in Tancada lagoon in 1996 and 1997. TAE(circles): East basin, TAW(squares): West basin. Data points are mean valuesstandard errors from four sampling stations in the two basins (see Figure 1).
water extinction coefficient of 0·039 cm 1 in March to 0·76 cm 1 in April). During March and April, the number of bivalves and anemones (Paranemonia cinerea) attached to C. linum mats decreased from 3182 to 1638 ind m 2 and from 1414 to 0 ind m 2 respectively. From May onwards the DIN concentration in the West basin decreased progressively to 0–2·5 mol l 1 in summer, and light penetration increased with extinction coefficient values around 0·0035 cm 1. In the East basin, conductivity remained high at about 45 mS cm 1 (between 34·6 and 51·8) during spring and summer, as freshwater inflows in this part of the lagoon were much lower than in the West basin (mean annual conductivity: 41·4 mS cm 1, range: 19·6–51·8 mS cm 1). In the East basin water inputs from the bay were considerable in winter. Maximum values of NH4 concentration were observed in late autumn and winter, probably due to remobilization of
Floating macroalgae in a Mediterranean coastal lagoon 219
mineralized organic matter accumulated in the sediment–water interface during the growing period which was favoured by strong winds which are common in this geographic zone in winter (Vidal & Morguı´, 1995).
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Nitrogen and carbon content of G. verrucosa were higher than those of Cladophora sp., Ulva sp. and C. linum (ANOVA F=362, P<10 6). N and C content of G. verrucosa were around 3% of the dry weight for N and 30% of the dry weight for C in early summer but fell to 2·3% and 23% respectively in August (Figure 5) (ANOVA, P<0·0001). N concentrations in the tissue of Cladophora sp. varied from 2·23% N in April to 1·3% N in August. This decrease in N was also reflected by reduced pigmentation in Cladophora sp., which appeared pale and yellowish in late summer. Chaetomorpha linum had a N content of around 1·2% of dry weight until July which increased to 1·45% in August. Ash content was, in general, higher in Cladophora sp. and C. linum (between 45–55%) than in G. verrucosa (30%). Similar ash contents were, however,
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Two spatial patterns were observed. In the West basin, C. linum dominated during winter (maximum winter mean biomass 32144·19 g DW m 2, n=5 in February 1997) and early spring (Figure 3) and decreased progressively in late spring and summer. After May, this species was replaced by Cladophora sp., which reached maximum development in July (Figure 3). At the end of the summer, Cladophora biomass and cover decreased, while the biomass of the rooted macrophyte R. cirrhosa reached a maximum of 1375 g DW m 2. Neither C. tenuissima nor G. verrucosa were observed in the West basin during the study period. In the East basin more species of macroalgae were observed. During winter and early spring macroalgal cover and biomass were low (Figure 4) and consisted mostly of Cladophora sp., C. linum and G. verrucosa. By June, C. tenuissima was absent, while G. verrucosa and Cladophora increased their cover and biomass and C. linum was confined to the shores of the lagoon (Figure 4). In July, maximum biomasses of both G. verrucosa (179·675·7 g DW m 2) and Cladophora (187·666·4 g DW m 2) were observed (Figure 4). By the end of summer, C. linum, had increased, reaching a maximum biomass of 238·2 44·5 g DW m 2 (Figure 4).
200
0
20
40
60 80 100 Metres from shoreline
120
140
F 3. Macroalgae biomass, between April and August 1997, in the sampling transect in the West basin of Tancada Lagoon shown in Figure 1. Chaetomorpha linum: open bars; Ruppia cirrhosa: grey bars; Cladophora: closed bars.
observed in August when the ash content of G verrucosa reached a maximum of 47% (Figure 5). Photosynthesis vs. irradiance (P-I) measurements The photosynthetic parameters calculated from the P-I curves differed between April and July (Figure 6). In April, Pm, R and initial slope values were significantly higher (ANOVA; P<0·01) in incubations made with C. tenuissima than with the other species of algae studied (Table 1). The Pm/R ratio of this species was lower than that calculated for Cladophora sp., C.
220 M. Mene´ ndez and F. A. Comı´n Transects 1 and 2 TAE 600
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1 2 4 Metres from shoreline
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F 4. Macroalgae biomass, between April and August 1997 and in March 1998, in the sampling transects in the East basin of Tancada Lagoon shown in Figure 1. X-axis scales are not the same because transect lengths varied each season. Differences in transect lengths were related to the cover of macroalgae at the time of sampling. Chaetomorpha linum: ; Ruppia cirrhosa: ; Cladophora: ; Ulva: ; Gracilaria verrucosa: ; Chondria tenuissima: .
Floating macroalgae in a Mediterranean coastal lagoon 221
O2 g 1 DW h 1 in July, although we observed a significant increase in initial slope from 0·023 to 0·038 mg O2 g 1 DW h 1 per mol m 2 s 1 (ANOVA; P<0·009 and a decrease in the Pm/R ratio from 7·49 in April to 4·49 in July (ANOVA; P<0·05). Pm and values calculated from the C. linum P-I curves in July were significantly higher than those obtained in April, from 3·53 mg O2 g 1 DW h 1 in April to 7·15 mg O2 g 1 DW h 1 in July (Pm) and from 0·014 mg O2 g 1 DW h 1 per mol m 2 s 1 in April to 0·024 mg O2 g 1 DW h 1 per 2 1 mol m s in July () (ANOVA; P<0·02, Table 2) (Figure 6). No differences were observed for the Pm/R or R values between the two dates.
% Nitrogern
4 3 2 1 0 35
% Carbon
30 25 20 15 10
Chlorophyll contents
5
The chlorophyll a concentrations of C. linum and Cladophora sp. increased from spring (0·21 and 0·10 mg total chlorophyll g 1 fresh weight for these two species respectively) to summer (0·34 and 0·19 mg total chlorophyll g 1 fresh weight, respectively). A 50% decrease in Chl a/Chl b was observed in C. linum, from 2·99 in April to 1·47 in July. The chlorophyll concentration of G. verrucosa remained fairly constant between April and July (Table 3).
0 60
% Ash
50 40 30 20 10 0
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June
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August
F 5. Percentage of nitrogen, carbon and ash in macroalgae tissues. Vertical bars are standard errors (N=3). Cladophora: ; Chaetomorpha linum: ; Ulva: ; Gracilaria verrucosa: .
linum and G. verrucosa. Pm, R, and for Cladophora sp. and G. verrucosa were similar (Figure 6) however the Pm/R ratio was significantly higher in Cladophora sp. (ANOVA; P<0·05, Table 1) than in G. verrucosa. In incubations made with algae collected in July, we observed significant differences in all the photosynthetic parameters calculated, Pm, R, initial slope and Pm/R ratio (ANOVA; P<0·0035, Table 1). Cladophora sp. showed a significant increase (ANOVA; P<0·02, Table 2) in Pm, R, and in July, in relation to values calculated in April: Pm changed from 11·85 mg O2 g 1 DW h 1 in April to 15·9 mg O2 g 1 DW h 1 in July, R changed from 1·07 mg O2 g 1 DW h 1 in April to 2·38 mg O2 g 1 DW h 1 in July, and changed from 0·022 mg O2 g 1 DW h 1 per mol m 2 s 1 in April to 0·058 mg O2 g 1 DW h 1 per mol m 2 s 1 in July. A decrease in the Pm/R ratio from 11·07 in April to 6·68 in July was observed (Figure 6). Pm values in incubations made with G. verrucosa decreased from 10·87 mg O2 g 1 DW h 1 to 4·9 mg
Discussion Spatial distribution Differences in the macroalgal distribution in the two basins of Tancada Lagoon were related to the distinct hydrological regimes. Water conductivity is an indicator of fresh- and sea-water mixing in this lagoon (Comin & Valiela, 1993). As a reference, the water conductivity in the sea close to the lagoon is around 55 mS cm 1. Gracilaria verrucosa and C. tenuissima were not observed in the West basin where conductivity was always lower than 38 mS cm 1 (approximate salinity 20), which indicates that a strong freshwater inflow takes place in this part of the lagoon. This trend of reduced diversity in the upper reaches of estuaries is ascribed to a combination of two factors, changes in salinity and light attenuation (Lavery, 1997). An increase in water transparency in zones of the lagoon without macroalgae in May, after freshwater inflows with high DIN concentrations, is related to the bloom of Cladophora sp. observed in the West basin. Thybo-Christesen et al. (1993) showed that mats of Cladophora sp. were responsible for the consumption of 95% and 85%, respectively, of the available N and P in a shallow Danish bay, resulting in clear water. During summer, Cladophora sp.
222 M. Mene´ ndez and F. A. Comı´n 4
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F 6. Estimated values of photosynthetic parameters and Pm/R ratios in macroalgae from Tancada Lagoon in spring and summer. Vertical bars are standard errors (n=3). Chaetomorpha linum: ; Cladophora: ; Gracilaria verrucosa: ; Chondria: .
dominated Tancada lagoon whereas C. linum biomass and spatial coverage decreased and accumulated in dense beds of algae, overlying a dark zone of decomposing algae and anoxic sediment near the shore, which probably served as a nutrient source for the algae. This distribution may be an adaptation to low nutrient content in the water column in summer. Macroalgal canopies over the sediment–water interface partially intercept ‘ old ’ nutrients released by regeneration from sediments (Valiela et al., 1997). The macroalgal canopies would sequester nutrients that could otherwise enter the water column and enhance the recycling of nutrients near the sediment surface (Lavery & McComb, 1991b). The distribution of C. linum coincides with a 50% reduction in the Chl a/Chl b ratio in plant tissues and an increase of initial slope of the P-I curve showing adaptation to low
radiation. In contrast, during winter, early spring and autumn C. linum mats are commonly observed floating in the water column and mat morphology is quite slack while the ammonium concentration in the column is relatively high (9–46 mol l 1, Figure 2). By mid-summer, an increase in water conductivity (up to 34·3 mS cm 1) was observed coinciding with the decrease in biomass and coverage of Cladophora sp. and the increase, both in biomass and coverage of R. cirrhosa (West basin) and C. linum (East basin). A similar decrease in Cladophora sp. at the end of the summer has been described by Peckol et al. (1994) in Waquoit Bay in Massachusetts. According to Rivers and Peckol (1995), this decrease was due to the low concentration of dissolved CO2 and the high pH observed in summer under conditions of saturating photon flux densities and high
Floating macroalgae in a Mediterranean coastal lagoon 223 T 1. Summary of the analysis of variance (one-way ANOVA) in the variables Pm, R, Pm/R and obtained in spring and summer incubations. Independent variable was species (Cladophora, G. verrucosa and C. linum) Variable April
July
Pm, (mg O2 g 1 DW h 1) R, (mg O2 g 1 AFDW h 1) Pm/R (mg O2 g 1 DW h 1 per mol m 2 s 1) Pm, (mg O2 g 1 DW h 1) R, (mg O2 g 1 AFDW h 1) Pm/R (mg O2 g 1 DW h 1 per mol m 2 s 1
Factor Species Error Species Error Species Error Species Error Species Error Species Error Species Error Species Error
df
MS
F
P
3 8 3 8 3 8 3 8 2 6 2 6 2 6 2 6
129·77 0·3032 5·11 0·052 16·78 0·6438 0·0066 0·000015 99·52 0·757 2·2698 0·0659 12·56 0·7646 0·00072 0·000057
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26·06
0·00017
428·51
10 6
131·43
0·00001
34·41
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16·34
0·0036
12·65
0·007
n.s.: no significant differences.
T 2. Summary of the analysis of variance (one-way ANOVA) in the variables Pm, R, Pm/R and obtained in Cladophora, G. verrucosa and C. linum incubations. Independent variable was seasonality (spring and summer) Variable Cladophora
Gracilaria
Chaetomorpha
Pm, (mg O2 g 1 DW h 1) R, (mg O2 g 1 AFDW h 1) Pm/R (mg O2 g 1 DW h 1 per mol m 2 s 1) Pm, (mg O2 g 1 DW h 1) R, (mg O2 g 1 AFDW h 1) Pm/R (mg O2 g 1 DW h 1 per mol m 2 s 1) Pm, (mg O2 g 1 DW h 1) R, (mg O2 g 1 AFDW h 1) Pm/R (mg O2 g 1 DW h 1 per mol m 2 s 1)
Factor Month Error Month Error Month Error Month Error Month Error Month Error Month Error Month Error Month Error Month Error Month Error Month Error
df
MS
F
P
1 4 1 4 1 4 1 4 1 4 1 4 1 4 1 4 1 4 1 4 1 4 1 4
24·64 0·5017 2·58 0·094 31·19 0·5253 0·018 0·00008 53·64 0·4004 0·225 0·0289 13·98 1·1079 0·00033 0·000015 19·7 0·5684 0·25 0·021 1·505 1·011 0·00015 0·000011
49·12
0·0021
26·98
0·0065
59·37
0·0015
22·11
0·0015
133·97
0·00031
7·79
0·049
12·62
0·023
23·27
0·0084
34·66
0·0041
11·51
0·027
1·48
n.s.
14·04
0·019
n.s.: no significant differences.
algal biomass. These authors remarked that Cladophora vagabunda showed a clear preference for dissolved CO2. Beer and Eschel (1983) found that the reduced rates of carbon fixation measured for algae in
dense stands probably result from a combination of shelf-shading, increased stability of boundary layers, and severe dissolved inorganic carbon (DIC) depletion. In Tancada lagoon, a high pH (9·54) and low
224 M. Mene´ ndez and F. A. Comı´n T 3. Chlorophyll a and b concentrations, Chlorophyll a b ratio and 430/665 index in floating macroalgae in spring and summer (meanstandard error, n=3)
April Chaetomorpha linum Gracilaria verrucosa Cladophora sp. July Chaetomorpha linum Gracilaria verrucosa Cladophora sp.
mg Chl a g 1 FW
mg Chl b g 1 FW
Chl a/Chl b
430/665
0·15780·012 0·13300·008 0·08400·031
0·05270·003 0 0·02050·009
2·99 — 4·09
2·990·08 1·700·01 2·030·09
0·20540·018 0·10820·002 0·14370·033
0·13890·036 0·00770·003 0·05300·009
1·47 14·05 2·71
1·930·04 1·780·01 2·050·03
CO2 concentration (0·05% of the total DIC) were observed by the end of July within the Cladophora sp. mats. These characteristics, together with the decrease in available light from 2171 mol m 2 s 1 at the water surface to 85 mol m 2 s 1 within the Cladophora sp. mats, may be responsible for the decline of this species by the end of the summer. The high uptake rates of C. linum for other forms of dissolved inorganic carbon, such as HCO3 , the fact that its maximum production value is between pH 6·5 and 8·5, (Menendez, unpubl. data), and its high resistance to environmental fluctuations (Orlandini, 1994; Lavery, 1997; McGlatery & Pedersen, 1999) may also contribute to the displacement of Cladophora sp. by C. linum. Thybo-Christesen et al. (1993) described the same specific change in coastal waters of Denmark at the end of the summer. The disappearance of Cladophora sp. in large areas of Tancada lagoon covering R. cirrhosa meadows, favours the development of the submerged rooted macrophyte. The prevailing conditions in the East basin (relatively high and constant conductivity and high water stability) favour the proliferation of G. verrucosa and Cladophora sp. which occupy preferentially shallow but permanently damp zones (Morand & Briand, 1996), where relatively low oxygen and high H2S concentrations, to which the two species are resistant (Peckol & Rivers, 1995), occur frequently. Gracilaria verrucosa and Cladophora mostly accumulated in very shallow (about 10 cm deep) zones of the East basin during spring and summer. At this time, the water column is relatively stable (a gradient in water temperature was observed between algal mat during July from 29·3 C at the bottom to 34·3 C at the surface), because of the absence of winds, which are relatively frequent and strong during autumn and winter. In contrast, C. linum occupies the open zones of the lagoon, where the water depth ranges between 30 and 80 cm.
Ecophysiological features In general, macroalgae in estuaries with increased nutrient supply show high nutrient uptakes rate, nutrient tissue content, initial slopes of the P-I curve () and maximum photosynthetic rates, Pm, and growth rates (Valiela et al., 1997). This high production in shallow zones may be related to high solar radiation (about 2000 mol m 2 s 1) and temperature (30 C) in summer, which can result in limited production due to decreased carbon and nitrogen availability and photoinhibition. In April both species are mixed, without any defined pattern. However, in July Cladophora sp. occupies the upper parts of the water column of the algal mat while G. verrucosa is located in the lower part, close to the sediment. This distribution may be related to the increase of Pm and R observed in July in Cladophora which shows an adaptation to high solar radiation, in contrast with the decrease of Pm calculated in incubations of Gracilaria. By mid summer to August, non-coloured fragments of G. verrucosa are observed in the upper parts of the water column and over Cladophora sp. indicating photoinhibition and the destruction of G. verrucosa at high temperatures. This is related to the low Pm values and high initial slopes of G. verrucosa observed in the laboratory incubations in July, which indicate the adaptation of this species to low light intensities imposed by the shading effect of the Cladophora sp. mats.
Conclusion The pattern of seasonal variation of macroalgal populations in Tancada lagoon has been characterised during the last years by the dominance of C. linum in autumn and winter. This species is acclimated to estuarine environments in which both light and nutrient conditions are highly variable mainly due to
Floating macroalgae in a Mediterranean coastal lagoon 225
freshwater inputs and wind perturbations (Orlandini, 1994; McGlatery & Pedersen, 1999). Growth was supported by high concentrations of dissolved ammonium in the water column which derived from the mineralization of organic matter accumulated in the lagoon during spring, summer and fall and from seawater inputs which were rich in nitrogen from the adjacent bay (Menendez, unpubl. data). When the water temperature and solar radiation increases in spring and summer, other species, Cladophora sp. in the upper part of water column and G. verrucosa in the lower part proliferate as they can adapt to high temperatures and solar radiation (Cladophora) and decreasing nutrient availability (Gracilaria) due to its uptake by photosynthetic organisms. A decrease of freshwater inflows, mainly in the East basin in Tancada lagoon, had produced a significant decrease in the depth of the water column (from 54·409·55 cm in 1979 to 32·52·69 cm in 1999) and in its turnover rate (water conductivity in spring and summer between 3·6 and 22·9 mS cm 1 in 1979 and between 44·1 and 61·9 mS cm 1 in 1998). This contributes to the stability and proliferation of fast growing species such as floating macroalgae and to a more heterotrophic stage, dominated by an excess of organic matter accumulation and decomposition, which is characteristic of eutrophic coastal lagoons.
References Anderson, R. J., Monteiro, P. M. S. & Levitt, G. J. 1996 The effect of localised eutrophication on competition between Ulva lactuca (Ulvaceae, Chlophyta) and a commercial resource of Gracilaria verrucosa (Gracilariaceae, Rhodophyta). Hydrobiologia 326/327, 291–296. Beer, S. & Eschel, A. 1983 Photosynthesis of Ulva sp. III. O2 effects carboxylase activities, and the CO2 incorporation pattern. Plant Physiology 81, 937–938. Comin, F. A. 1984 Caracterı´sticas fı´sicas y quı´micas y fitoplancton de las lagunas costeras Encanyizada, Tancada y Buda (Delta del Ebro). Oecologia Aquatica 7, 79–162. Comin, F. A. & Valiela, I. 1993 On the controls of phytoplankton abundance and production in coastal lagoons. Journal of coast Research 9, 895–906. Comin, F. A., Martin, M., Mene´ ndez, M., Romero, J. A., & Herrera-Silveira, J. 1995 Integrated management of a Coastal lagoon in the Ebro Delta. In Proceedings of the Second International Conference on the Mediterranean Coastal Environment (Ozhan, ed.). Tarragona, Spain, pp. 883–895. Evans, A. S., Webb, K. L. & Penhale, P. A. 1986 Photosynthetic temperature acclimation in two coexisting seagrasses, Zostera marina L. and Ruppia maritima L. Aquatic Botany 24, 185–197. Grasshoff, K., Ehrhardt, M. & Kremling, K. 1983 Methods of Seawater Analysis. Chemie, Weinheim. Howarth, R. W. 1988 Nutrient limitation of net primary production in marine ecosystems. Annual Revue Ecological Systems 19, 89– 110. Jeffrey, S. W. & Humphrey, G. F. 1975 New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochemistry Physiologie Pflanzen 167, 191–194.
Lavery, P. S. & McComb, A. J. 1991 a The nutritional ecophysiology of Chaetomorpha linum and Ulva rigida in Peel Inlet, Western Australia. Botanica Marina 34, 251–260. Lavery, P. S. & McComb, A. J. 1991 b Macroalgal-sediment nutrient interactions and their importance to macroalgal nutrition in a eutrophic estuary. Estuarine, Coastal and Shelf Science 32, 281–295. Lavery, P. S. 1997 Waychinicup Estuary, Western Australia: the influence of freshwater inputs on the benthic flora and fauna. Journal of the Royal Society of Western Australia 80, 63–72. McComb, A. J. & Humphries, R. 1992 Loss of nutrients from catchments and their ecological impacts in the Peel-Harvey estuarine system. Estuaries 15, 529–537. McGlatery, K. J. & Pedersen, M. F. 1999 The effect of growth irradiance on the coupling of carbon and nitrogen metabolism in Chaetomorpha linum (Chlorophyta). Journal of Phycology 35, 721– 731. Menendez, M. & Comin, F. A. 1989 Seasonal patterns of biomass variation of Ruppia cirrhosa (Petagna) Grande and Potamogeton pectinatus L. in a coastal lagoon Scientia Marina 53, 633–638. Menendez, M. & Comin, F. A. 1990 Seasonal patterns of biomass variation of Ruppia cirrhosa (Petagna) Grande and Potamogeton pectinatus L. in a coastal lagoon. Scientia Marina 53, 633–638. Mene´ ndez, M. & Sa´ nchez, A. 1998 Seasonal variations in P-I responses of Chara hispida L. and Potamogeton pectinatus L. from stream mediterranean ponds. Aquatic Botany 61, 1–15. Morand, P., Charlier, R. H. & Maze´ , J. 1990 European bioconversion projects and realizations for macroalgal biomass: Sant-Cast-Le Guildo (France). In Proceedings of the Thirteenth International Seaweed Symposium (Lindstrom, S. C. & Gabrielson, P. W. eds). Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 301–308. Morand, P. & Briand, X. 1996 Excessive growth of macroalgae: a symptom of environmental disturbance. Botanica Marina 39, 491–516. Nixon, S. W., Owiat, C. A., Frithsen, J. & Sullivan, B. 1986 Nutrients and the productivity of estuarine and coastal marine systems. Journal Limnology Society of South Africa 12, 43–71. Orlandini, M. 1994 Anaerobic digestion of Chaetomorpha linum collected from Orbetello lagoon (Italy). In Production and Exploitation of Entire Seaweeds (Dele´ pine, R. & Morand, P. eds). Proceedings of the third COST 48-subgroup 3 Workshop, Paimpol-St. Malo, France, pp. 76–79. Peckol, P., DeMeo-Anderson, B., Rivers, J., Valiela, I., Maldonado, M., Weiner J. & Yates, J. 1994 Growth, nutrient uptake capacities, and tissue constituents of the macroalgae, Gracilaria tikvahiae and Cladophora vagabunda, related to site-specific nitrogen loading rates. Marine Biology 121, 175–185. Peckol, P. & Rivers, J. S. 1995 Physiological responses of the opportunistic macroalgae Cladophora vagabunda (L.) van den Hoek and Gracilaria tikvahiae (McLachlan) to environmental disturbances associated with eutrophication. Journal Experimental Marine Biology Ecology 190, 1–16. Rivers, J. S. & Peckol, P. 1995 Interactive effects of nitrogen and dissolved inorganic carbon on photosynthesis, growth, and ammonium uptake of the macroalgae Cladophora vagabunda and Gracilaria tikvahiae. Marine Biology 121, 747–753. Sestak, Z. 1971 Determination of chlorophylls a and b. In Plant Photosynthetic Production Methods (Sestak, Z., Catsky, J. & Jarvis, P. G. eds). Academic Press, New York. pp. 672–701. Sfriso, A., Pavoni, P., Marcomini, A. & Orio, A. A. 1992 Macroalgae, nutrient cycles, and pollutants in the Lagoon of Venice. Estuaries 15, 517–528. Taylor, D. I., Nixon, S. W., Granger, S. L., Buckley, B. A., McMahon, J. P. & Lin, H. J. 1995 Responses of coastal lagoon plant communities to different forms of nutrient enrichment–a mesocosm experiment. Aquatic Botany 52, 19–34. Thybo-Christesen, M., Rasmussen, M. B. & Blackburn, T. H. 1993 Nutrient fluxes and growth of Cladophora sericea in a shallow Danish bay. Marine Ecology Progress Series 100, 273– 281.
226 M. Mene´ ndez and F. A. Comı´n Valiela, I., Foreman, K., La Montagne, M., Hersh, D., Costa, J., Peckol, P., DeMeo-Anderson, B, d’Avanzo, C., Babione, M., Sham, C. H., Brawley, J. & Lajtha, K. 1992 Coupling of watersheds and coastal waters: sources and consequences of nutrient enrichment in Waquoit Bay, Massachusetts. Estuaries 15, 443–457. Valiela, I., McClelland, J., Hauxwell, J., Behr, P. J., Hersh, D. & Foreman, K. 1997 Macroalgal blooms in shallow estuaries: Controls and ecophysiological and ecosystem consequences. Limnology Oceanography 42, 1105–1118.
Viaroli, P. & Pugnetti, A. 1992Ulva rigida growth and decomposition processes and related effects on nitrogen and phosphorus cycles in a coastal lagoon (Sacca di Goro, Po River Delta). In Marine Eutrophication and Population Dynamics (Colombo, G., Ferrari, I., Cecchereli, V. U. & Rossi, R. eds). Olsen & Olsen, Fredensborg, Denmark, pp. 77–84. Vidal, M. & Morguı´, J. A. 1995 Short-term pore water ammonium variability coupled to benthic boundary layer dynamics in Alfacs Bay, Spain (Ebro Delta, NW Mediteranean). Marine Ecology Progress Series 118, 229–236.
Spring and Summer Proliferation of Floating Macroalgae in a Mediterranean Coastal Lagoon (Tancada Lagoon, Ebro Delta, NE Spain) M. Mene´ndeza and F. A. Comı´n Department of Ecology, University of Barcelona, Av. Diagonal 645, 08028 Barcelona, Spain Received 6 September 1999 and accepted in revised form 27 March 2000 During the last 10 years, a drastic change in the structure of the community of primary producers has been observed in Tancada Lagoon (Ebro Delta, NE Spain). This consisted of a decrease in the abundance of submerged rooted macrophyte cover and a spring and summer increase in floating macroalgae. Two spatial patterns have been observed. In the west part of the lagoon, Chaetomorpha linum Ku¨tzing, dominated during winter and decreased progressively in spring when Cladophora sp. reached its maximum development. In the east part of the lagoon, higher macroalgal diversity was observed, together with lower cover in winter and early spring. Cladophora sp., Gracilaria verrucosa Papenfuss and Chondria tenuissima Agardh, increased cover and biomass in summer. Maximum photosynthetic production was observed in spring for G. verrucosa (10·9 mg O2 g 1 DW h 1) and C. tenuissima (19·0 mg O2 g 1 DW h 1) in contrast with Cladophora sp. (15·9 mg O2 g 1 DW h 1) and Chaetomorpha linum (7·2 mg O2 g 1 DW h 1) which reached maximum production in summer. Increased conductivity from reduced freshwater inflow, and higher water temperatures during periods of lagoon isolation, mainly in summer, were the main physical factors associated with an increase in floating macroalgal biomass across the lagoon. Reduced nitrogen availability and temperature-related changes in carbon availability during summer were related to a decrease in abundance of C. linum and increases in G. verrucosa and Cladophora sp. 2000 Academic Press Keywords: biomass; production; macroalgae; coastal lagoon; eutrophication; NE Spain
Introduction There is increasing eutrophication of coastal aquatic ecosystems worldwide which is associated with human activities, such as runoff from intensely fertilized agricultural fields, direct wastewater discharges, and disturbances of natural water flows (Valiela et al., 1992; Sfriso et al., 1992; McComb & Humphries, 1992; Taylor et al., 1995; Morand & Briand, 1996). In coastal lagoons, the most frequently reported consequences of eutrophication are changes in biogeochemical processes and the structure of biological communities (Taylor et al., 1995), including macroalgal blooms (Morand et al., 1990; Lavery & McComb, 1991; Viaroli & Pugnetti, 1992; Taylor et al., 1995; Anderson et al., 1996). Increased nitrogen inputs in such ecosystems have been associated with macroalgal blooms, particularly in temperate zones where high temperature and solar radiation favour the vernal proliferation of fast-growing species (Nixon et al., 1986; Howarth, 1988). Tancada Lagoon is a confined coastal body of water in NE Spain. During the last 10 years, a drastic 0272–7714/00/080215+12 $35.00/0
change in the structure of the community of primary producers has occurred in this lagoon, which has induced decreases in cover and biomass of submerged rooted macrophytes and overwhelming increases in the abundance of floating macroalgae during late spring and summer (Comin et al., 1995). This paper describes spring and summer proliferation of ephemeral macroalgae in Tancada Lagoon resulting from water eutrophication and confinement caused by the impact of agricultural practices in nearby rice fields during recent years. Water conductivity and nutrient concentrations were used as indicators of the environmental conditions under which algae growth took place. The nutrient content of the algae was analysed to evaluate limitation or excess of nitrogen. The photosynthetic performance of several species was determined to establish its relevance for development at different times during the growing season. The aim of this paper is to provide quantitative data on the temporal changes of the spatial distribution of ephemeral algae, related to their photosynthetic characteristics, in a shallow Mediterranean lagoon. 2000 Academic Press
216 M. Mene´ ndez and F. A. Comı´n
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F 1. Map of the Ebro Delta (NE Spain) and Tancada Lagoon showing the distribution of macroalgae in summer 1997 and the location of the transects for macroalgae biomass sampling. TAE: Tancada East basin, TAW: Tancada West basin. t1: transect 1 t2: transect 2. The location of physicochemical samples is also shown ( ).
Material and methods Study area Tancada is a small, shallow coastal lagoon located in the Ebro River Delta, NE Spain (Figure 1), with an area of 1·8 km2 which is distributed in two basins (called East and West here) and has an average depth of 37 cm (Comin, 1984). During the 1970s and 1980s it received freshwater inflows from irrigated rice fields from May to October which led to relatively low water conductivity (Comin, 1984; Menendez & Comin, 1989). In the last 10 years, freshwater inflows have decreased progressively due to changes in agricultural
management practices and this has resulted in two differentiated zones. Increased conductivity has been observed in the East basin, which rarely received freshwater inputs. In contrast, lower conductivity has become apparent in the West basin which received most of the nutrient rich freshwater inputs from rice fields. These long-term hydrological changes have altered the macrophyte vegetation. In 1987, this lagoon was mostly occupied by a dense Ruppia cirrhosa Petagna (Grande) meadow with a small area in the central part of the West basin covered by Potamogeton pectinatus L. (Menendez & Comin, 1989). By 1989 P. pectinatus had completely disappeared and a
Floating macroalgae in a Mediterranean coastal lagoon 217
progressive increase in floating macroalgal growth was observed (Comin et al., 1995). During the mid1990s, macroalgal biomass and cover increased greatly during spring and summer due to the proliferation of Cladophora spp. and Chaetomorpha linum (O. F. Mu¨ ller) Ku¨ tzing in the West basin and Chondria tenuissima (Goodennough and Woodward) C. Agardh, Cladophora spp., and Gracilaria verrucosa (Hudson) Papenfuss in the East. Environmental variables Water transparency, conductivity, pH, dissolved oxygen and nutrient concentrations were measured monthly at four sites in the lagoon (Figure 1). Conductivity, pH and dissolved oxygen were measured in situ with portable apparatus. Nitrate, nitrite and ammonium nitrogen concentrations were determined from water samples (using Whatman GF/C filters combusted at 500 C) following Grashoff et al. (1983) in a Technicon Autoanalyzer. Light extinction coefficient was measured with a radiometer and quantum spherical sensor (Li-Cor, Lambda Instruments). Macroalgal biomass sampling The degree of cover and biomass of floating macroalgae were assessed on five occasions during 1997. Because the species of macroalgae studied are in unattached mats, increases in biomass may be due to both in situ growth and redistribution by water movements. In winter the prevalent wind in Tancada Lagoon is from the north-west and macroalgae accumulate mainly in the south part of the lagoon. In spring and summer there is a time of high stability in this area, only a light breeze from the south-east is observed from midday to sunset. A sampling strategy based on transects which are perpendicular to the shore was chosen, because it covers the spatial variability observed in this lagoon better than random sampling design. Biomass samples were collected in long transect lines in the East and West basins (Figure 1). In the West basin, macroalgal samples were collected every 8 m along a transect line that extended northwards from the central part of the southern shore, to the inner part of the lagoon, until no macroalgae were found. In the East basin, two transects were established because of differences observed in the distribution of macroalgae in this part of the lagoon, as thick mats were observed in the first 3 m near the shore line and with at least two species of macroalgae, and a less dense distribution towards the centre of the lagoon, with only one or two species (Figure 1): (a) transect 2 was located near the shore
and was used to sample the shallowest part of the East basin; sampling points were fixed 50 cm apart along 3 m, (b) transect 1 was a longer transect and sampling points were located every 2 m until no macroalgae were observed. Macroalgal samples were collected from the whole water column using a plastic cylinder with a basal area of 64 cm2 which was introduced in the water column and firmly pressed into the sediment. Epibionts attached to algae mat were sorted and counted and macroalgae were dried to constant weight at 60 C. Sampling was carried out in March, April, June, July and August 1997. Nutrient content and chlorophyll Carbon (C) and nitrogen (N) content of macroalgae were measured in subsamples taken from biomass collected during the study period. Macroalgal subsamples were ground to a powder (<0·5 mm diameter) and analysed for total N using a Carlo Erba Autoanalyzer. Fragments of macroalgae were collected for chlorophyll analysis in spring (April) and summer (July). These samples were frozen (11 C) and transported to the laboratory where pigments of triplicate samples were extracted in 90% acetone according to procedures described by Sestak (1971). Determinations of chlorophyll a and b were based on equations reported by Jeffrey and Humphrey (1975). Photosynthesis vs. irradiance measurements Measurements of macroalgae photosynthesis were carried out in spring (April) and summer (July). Water and algae were collected from the lagoon. Fresh growing parts of macroalgae were collected by hand and kept in aerated lagoon water at the same temperature (1 C) and with light/dark pattern as in sampling site, for no longer than 5 days prior to photosynthesis incubations, following Evans et al. (1986). Incubations were performed in filtered (0·45 m mesh size) lagoon water in 100 ml glass stoppered bottles. Approximately 0·2 g fresh weight of whole algal thalli were incubated in each bottle. Dry weight was determined after each experiment by drying the algae at 60 C to constant weight. The bottles were placed in incubators at a controlled temperature and stirring bars (c. 200 rpm) were used to breakdown diffusion gradients and decrease errors resulting from internal oxygen storage. All experiments were performed at ambient water temperatures (20 C and 30 C in April and July, respectively) and dissolved inorganic carbon levels (3·07 and 1·79 mmol l 1 in April and July, respectively). Daylight fluorescent tubes (400–700 nm waveband) were used, and the irradiance was adjusted by covering the bottles with
218 M. Mene´ ndez and F. A. Comı´n
Statistical analysis To test the effect of seasonality on Pm, R and in each species, analysis of variance (one-way ANOVA) was used. Similarly, differences between species were tested with data obtained in April and July. The fitted characteristics of the lines and curves were log transformed to obtain homogeneity of variances and determined to be normally distributed (Lilliefors test) before the analyses were conducted. The CSSStatistica computer program was used for statistical analysis. Results Environmental variables The West basin of Tancada lagoon received freshwater inflows from rice fields during spring and summer. This caused a decrease in water conductivity from 37·6 mS cm 1 in March to 22 mS cm 1 in April which then remained around 30 1·57 mS cm 1 until September (mean annual conductivity 29·2 mS cm 1, range: 12·38–37·6 mS cm 1). An increase in the concentration of dissolved inorganic nitrogen (DIN) from 21·37 mol l 1 in March to 73·83 mol l 1 in April, mainly in nitrate (52% and 71% of the DIN, in March and April respectively) was observed during the period of freshwater inflows (Figure 2). This coincided with an increase in light attenuation (from a
NO3 + NO2 (mmol l–1)
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neutral filters to assess photosynthesis-irradiance relationships (between 0 and 830 mol photon m 2 s 1). Photosynthetically active radiation (PAR) was measured with a radiometer and quantum spherical sensor (Li-Cor, Lambda Instruments). After 2 h of incubation, dissolved oxygen (DO) concentrations were measured to the nearest 0·01 mg using an oxygen electrode (WTW), and compared with DO concentrations in control bottles (N=3) without plants. All the results were expressed in mg O2 g 1 dry weight h 1. Three replicates of each experimental condition were used. Parameters describing the photosynthesis vs. irradiance response (P-I) were determined for each incubated species using the Enzfitter program (Menendez & Sanchez, 1998). The maximum rates of net photosynthesis (Pm) were determined by averaging points on the light-saturated portion of each P vs. I curve (e.g. as the slope approached zero). Respiration rates (R) were determined by measuring oxygen consumption in dark bottles. A linear regression of photosynthetic rates at light-limiting irradiance (0, 30 and 60 mol m 2 s 1) was used to calculate the initial slope ().
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water extinction coefficient of 0·039 cm 1 in March to 0·76 cm 1 in April). During March and April, the number of bivalves and anemones (Paranemonia cinerea) attached to C. linum mats decreased from 3182 to 1638 ind m 2 and from 1414 to 0 ind m 2 respectively. From May onwards the DIN concentration in the West basin decreased progressively to 0–2·5 mol l 1 in summer, and light penetration increased with extinction coefficient values around 0·0035 cm 1. In the East basin, conductivity remained high at about 45 mS cm 1 (between 34·6 and 51·8) during spring and summer, as freshwater inflows in this part of the lagoon were much lower than in the West basin (mean annual conductivity: 41·4 mS cm 1, range: 19·6–51·8 mS cm 1). In the East basin water inputs from the bay were considerable in winter. Maximum values of NH4 concentration were observed in late autumn and winter, probably due to remobilization of
Floating macroalgae in a Mediterranean coastal lagoon 219
mineralized organic matter accumulated in the sediment–water interface during the growing period which was favoured by strong winds which are common in this geographic zone in winter (Vidal & Morguı´, 1995).
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Nitrogen and carbon content of G. verrucosa were higher than those of Cladophora sp., Ulva sp. and C. linum (ANOVA F=362, P<10 6). N and C content of G. verrucosa were around 3% of the dry weight for N and 30% of the dry weight for C in early summer but fell to 2·3% and 23% respectively in August (Figure 5) (ANOVA, P<0·0001). N concentrations in the tissue of Cladophora sp. varied from 2·23% N in April to 1·3% N in August. This decrease in N was also reflected by reduced pigmentation in Cladophora sp., which appeared pale and yellowish in late summer. Chaetomorpha linum had a N content of around 1·2% of dry weight until July which increased to 1·45% in August. Ash content was, in general, higher in Cladophora sp. and C. linum (between 45–55%) than in G. verrucosa (30%). Similar ash contents were, however,
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Two spatial patterns were observed. In the West basin, C. linum dominated during winter (maximum winter mean biomass 32144·19 g DW m 2, n=5 in February 1997) and early spring (Figure 3) and decreased progressively in late spring and summer. After May, this species was replaced by Cladophora sp., which reached maximum development in July (Figure 3). At the end of the summer, Cladophora biomass and cover decreased, while the biomass of the rooted macrophyte R. cirrhosa reached a maximum of 1375 g DW m 2. Neither C. tenuissima nor G. verrucosa were observed in the West basin during the study period. In the East basin more species of macroalgae were observed. During winter and early spring macroalgal cover and biomass were low (Figure 4) and consisted mostly of Cladophora sp., C. linum and G. verrucosa. By June, C. tenuissima was absent, while G. verrucosa and Cladophora increased their cover and biomass and C. linum was confined to the shores of the lagoon (Figure 4). In July, maximum biomasses of both G. verrucosa (179·675·7 g DW m 2) and Cladophora (187·666·4 g DW m 2) were observed (Figure 4). By the end of summer, C. linum, had increased, reaching a maximum biomass of 238·2 44·5 g DW m 2 (Figure 4).
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F 3. Macroalgae biomass, between April and August 1997, in the sampling transect in the West basin of Tancada Lagoon shown in Figure 1. Chaetomorpha linum: open bars; Ruppia cirrhosa: grey bars; Cladophora: closed bars.
observed in August when the ash content of G verrucosa reached a maximum of 47% (Figure 5). Photosynthesis vs. irradiance (P-I) measurements The photosynthetic parameters calculated from the P-I curves differed between April and July (Figure 6). In April, Pm, R and initial slope values were significantly higher (ANOVA; P<0·01) in incubations made with C. tenuissima than with the other species of algae studied (Table 1). The Pm/R ratio of this species was lower than that calculated for Cladophora sp., C.
220 M. Mene´ ndez and F. A. Comı´n Transects 1 and 2 TAE 600
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F 4. Macroalgae biomass, between April and August 1997 and in March 1998, in the sampling transects in the East basin of Tancada Lagoon shown in Figure 1. X-axis scales are not the same because transect lengths varied each season. Differences in transect lengths were related to the cover of macroalgae at the time of sampling. Chaetomorpha linum: ; Ruppia cirrhosa: ; Cladophora: ; Ulva: ; Gracilaria verrucosa: ; Chondria tenuissima: .
Floating macroalgae in a Mediterranean coastal lagoon 221
O2 g 1 DW h 1 in July, although we observed a significant increase in initial slope from 0·023 to 0·038 mg O2 g 1 DW h 1 per mol m 2 s 1 (ANOVA; P<0·009 and a decrease in the Pm/R ratio from 7·49 in April to 4·49 in July (ANOVA; P<0·05). Pm and values calculated from the C. linum P-I curves in July were significantly higher than those obtained in April, from 3·53 mg O2 g 1 DW h 1 in April to 7·15 mg O2 g 1 DW h 1 in July (Pm) and from 0·014 mg O2 g 1 DW h 1 per mol m 2 s 1 in April to 0·024 mg O2 g 1 DW h 1 per 2 1 mol m s in July () (ANOVA; P<0·02, Table 2) (Figure 6). No differences were observed for the Pm/R or R values between the two dates.
% Nitrogern
4 3 2 1 0 35
% Carbon
30 25 20 15 10
Chlorophyll contents
5
The chlorophyll a concentrations of C. linum and Cladophora sp. increased from spring (0·21 and 0·10 mg total chlorophyll g 1 fresh weight for these two species respectively) to summer (0·34 and 0·19 mg total chlorophyll g 1 fresh weight, respectively). A 50% decrease in Chl a/Chl b was observed in C. linum, from 2·99 in April to 1·47 in July. The chlorophyll concentration of G. verrucosa remained fairly constant between April and July (Table 3).
0 60
% Ash
50 40 30 20 10 0
April
June
July
August
F 5. Percentage of nitrogen, carbon and ash in macroalgae tissues. Vertical bars are standard errors (N=3). Cladophora: ; Chaetomorpha linum: ; Ulva: ; Gracilaria verrucosa: .
linum and G. verrucosa. Pm, R, and for Cladophora sp. and G. verrucosa were similar (Figure 6) however the Pm/R ratio was significantly higher in Cladophora sp. (ANOVA; P<0·05, Table 1) than in G. verrucosa. In incubations made with algae collected in July, we observed significant differences in all the photosynthetic parameters calculated, Pm, R, initial slope and Pm/R ratio (ANOVA; P<0·0035, Table 1). Cladophora sp. showed a significant increase (ANOVA; P<0·02, Table 2) in Pm, R, and in July, in relation to values calculated in April: Pm changed from 11·85 mg O2 g 1 DW h 1 in April to 15·9 mg O2 g 1 DW h 1 in July, R changed from 1·07 mg O2 g 1 DW h 1 in April to 2·38 mg O2 g 1 DW h 1 in July, and changed from 0·022 mg O2 g 1 DW h 1 per mol m 2 s 1 in April to 0·058 mg O2 g 1 DW h 1 per mol m 2 s 1 in July. A decrease in the Pm/R ratio from 11·07 in April to 6·68 in July was observed (Figure 6). Pm values in incubations made with G. verrucosa decreased from 10·87 mg O2 g 1 DW h 1 to 4·9 mg
Discussion Spatial distribution Differences in the macroalgal distribution in the two basins of Tancada Lagoon were related to the distinct hydrological regimes. Water conductivity is an indicator of fresh- and sea-water mixing in this lagoon (Comin & Valiela, 1993). As a reference, the water conductivity in the sea close to the lagoon is around 55 mS cm 1. Gracilaria verrucosa and C. tenuissima were not observed in the West basin where conductivity was always lower than 38 mS cm 1 (approximate salinity 20), which indicates that a strong freshwater inflow takes place in this part of the lagoon. This trend of reduced diversity in the upper reaches of estuaries is ascribed to a combination of two factors, changes in salinity and light attenuation (Lavery, 1997). An increase in water transparency in zones of the lagoon without macroalgae in May, after freshwater inflows with high DIN concentrations, is related to the bloom of Cladophora sp. observed in the West basin. Thybo-Christesen et al. (1993) showed that mats of Cladophora sp. were responsible for the consumption of 95% and 85%, respectively, of the available N and P in a shallow Danish bay, resulting in clear water. During summer, Cladophora sp.
222 M. Mene´ ndez and F. A. Comı´n 4
10
5
0
α (mg O2 g–1 DW h–1 per µmol m–2 s–1)
R (mg O2 g–1 DW h–1)
15
April
3
2
1
0
July
0.12
12
0.10
10
0.08
8 Pm/R
Pm (mg O2 g–1 DW h–1)
20
0.06
4
0.02
2
April
July
July
April
July
6
0.04
0.00
April
0
F 6. Estimated values of photosynthetic parameters and Pm/R ratios in macroalgae from Tancada Lagoon in spring and summer. Vertical bars are standard errors (n=3). Chaetomorpha linum: ; Cladophora: ; Gracilaria verrucosa: ; Chondria: .
dominated Tancada lagoon whereas C. linum biomass and spatial coverage decreased and accumulated in dense beds of algae, overlying a dark zone of decomposing algae and anoxic sediment near the shore, which probably served as a nutrient source for the algae. This distribution may be an adaptation to low nutrient content in the water column in summer. Macroalgal canopies over the sediment–water interface partially intercept ‘ old ’ nutrients released by regeneration from sediments (Valiela et al., 1997). The macroalgal canopies would sequester nutrients that could otherwise enter the water column and enhance the recycling of nutrients near the sediment surface (Lavery & McComb, 1991b). The distribution of C. linum coincides with a 50% reduction in the Chl a/Chl b ratio in plant tissues and an increase of initial slope of the P-I curve showing adaptation to low
radiation. In contrast, during winter, early spring and autumn C. linum mats are commonly observed floating in the water column and mat morphology is quite slack while the ammonium concentration in the column is relatively high (9–46 mol l 1, Figure 2). By mid-summer, an increase in water conductivity (up to 34·3 mS cm 1) was observed coinciding with the decrease in biomass and coverage of Cladophora sp. and the increase, both in biomass and coverage of R. cirrhosa (West basin) and C. linum (East basin). A similar decrease in Cladophora sp. at the end of the summer has been described by Peckol et al. (1994) in Waquoit Bay in Massachusetts. According to Rivers and Peckol (1995), this decrease was due to the low concentration of dissolved CO2 and the high pH observed in summer under conditions of saturating photon flux densities and high
Floating macroalgae in a Mediterranean coastal lagoon 223 T 1. Summary of the analysis of variance (one-way ANOVA) in the variables Pm, R, Pm/R and obtained in spring and summer incubations. Independent variable was species (Cladophora, G. verrucosa and C. linum) Variable April
July
Pm, (mg O2 g 1 DW h 1) R, (mg O2 g 1 AFDW h 1) Pm/R (mg O2 g 1 DW h 1 per mol m 2 s 1) Pm, (mg O2 g 1 DW h 1) R, (mg O2 g 1 AFDW h 1) Pm/R (mg O2 g 1 DW h 1 per mol m 2 s 1
Factor Species Error Species Error Species Error Species Error Species Error Species Error Species Error Species Error
df
MS
F
P
3 8 3 8 3 8 3 8 2 6 2 6 2 6 2 6
129·77 0·3032 5·11 0·052 16·78 0·6438 0·0066 0·000015 99·52 0·757 2·2698 0·0659 12·56 0·7646 0·00072 0·000057
427·98
10 6
29·74
0·01
26·06
0·00017
428·51
10 6
131·43
0·00001
34·41
0·00051
16·34
0·0036
12·65
0·007
n.s.: no significant differences.
T 2. Summary of the analysis of variance (one-way ANOVA) in the variables Pm, R, Pm/R and obtained in Cladophora, G. verrucosa and C. linum incubations. Independent variable was seasonality (spring and summer) Variable Cladophora
Gracilaria
Chaetomorpha
Pm, (mg O2 g 1 DW h 1) R, (mg O2 g 1 AFDW h 1) Pm/R (mg O2 g 1 DW h 1 per mol m 2 s 1) Pm, (mg O2 g 1 DW h 1) R, (mg O2 g 1 AFDW h 1) Pm/R (mg O2 g 1 DW h 1 per mol m 2 s 1) Pm, (mg O2 g 1 DW h 1) R, (mg O2 g 1 AFDW h 1) Pm/R (mg O2 g 1 DW h 1 per mol m 2 s 1)
Factor Month Error Month Error Month Error Month Error Month Error Month Error Month Error Month Error Month Error Month Error Month Error Month Error
df
MS
F
P
1 4 1 4 1 4 1 4 1 4 1 4 1 4 1 4 1 4 1 4 1 4 1 4
24·64 0·5017 2·58 0·094 31·19 0·5253 0·018 0·00008 53·64 0·4004 0·225 0·0289 13·98 1·1079 0·00033 0·000015 19·7 0·5684 0·25 0·021 1·505 1·011 0·00015 0·000011
49·12
0·0021
26·98
0·0065
59·37
0·0015
22·11
0·0015
133·97
0·00031
7·79
0·049
12·62
0·023
23·27
0·0084
34·66
0·0041
11·51
0·027
1·48
n.s.
14·04
0·019
n.s.: no significant differences.
algal biomass. These authors remarked that Cladophora vagabunda showed a clear preference for dissolved CO2. Beer and Eschel (1983) found that the reduced rates of carbon fixation measured for algae in
dense stands probably result from a combination of shelf-shading, increased stability of boundary layers, and severe dissolved inorganic carbon (DIC) depletion. In Tancada lagoon, a high pH (9·54) and low
224 M. Mene´ ndez and F. A. Comı´n T 3. Chlorophyll a and b concentrations, Chlorophyll a b ratio and 430/665 index in floating macroalgae in spring and summer (meanstandard error, n=3)
April Chaetomorpha linum Gracilaria verrucosa Cladophora sp. July Chaetomorpha linum Gracilaria verrucosa Cladophora sp.
mg Chl a g 1 FW
mg Chl b g 1 FW
Chl a/Chl b
430/665
0·15780·012 0·13300·008 0·08400·031
0·05270·003 0 0·02050·009
2·99 — 4·09
2·990·08 1·700·01 2·030·09
0·20540·018 0·10820·002 0·14370·033
0·13890·036 0·00770·003 0·05300·009
1·47 14·05 2·71
1·930·04 1·780·01 2·050·03
CO2 concentration (0·05% of the total DIC) were observed by the end of July within the Cladophora sp. mats. These characteristics, together with the decrease in available light from 2171 mol m 2 s 1 at the water surface to 85 mol m 2 s 1 within the Cladophora sp. mats, may be responsible for the decline of this species by the end of the summer. The high uptake rates of C. linum for other forms of dissolved inorganic carbon, such as HCO3 , the fact that its maximum production value is between pH 6·5 and 8·5, (Menendez, unpubl. data), and its high resistance to environmental fluctuations (Orlandini, 1994; Lavery, 1997; McGlatery & Pedersen, 1999) may also contribute to the displacement of Cladophora sp. by C. linum. Thybo-Christesen et al. (1993) described the same specific change in coastal waters of Denmark at the end of the summer. The disappearance of Cladophora sp. in large areas of Tancada lagoon covering R. cirrhosa meadows, favours the development of the submerged rooted macrophyte. The prevailing conditions in the East basin (relatively high and constant conductivity and high water stability) favour the proliferation of G. verrucosa and Cladophora sp. which occupy preferentially shallow but permanently damp zones (Morand & Briand, 1996), where relatively low oxygen and high H2S concentrations, to which the two species are resistant (Peckol & Rivers, 1995), occur frequently. Gracilaria verrucosa and Cladophora mostly accumulated in very shallow (about 10 cm deep) zones of the East basin during spring and summer. At this time, the water column is relatively stable (a gradient in water temperature was observed between algal mat during July from 29·3 C at the bottom to 34·3 C at the surface), because of the absence of winds, which are relatively frequent and strong during autumn and winter. In contrast, C. linum occupies the open zones of the lagoon, where the water depth ranges between 30 and 80 cm.
Ecophysiological features In general, macroalgae in estuaries with increased nutrient supply show high nutrient uptakes rate, nutrient tissue content, initial slopes of the P-I curve () and maximum photosynthetic rates, Pm, and growth rates (Valiela et al., 1997). This high production in shallow zones may be related to high solar radiation (about 2000 mol m 2 s 1) and temperature (30 C) in summer, which can result in limited production due to decreased carbon and nitrogen availability and photoinhibition. In April both species are mixed, without any defined pattern. However, in July Cladophora sp. occupies the upper parts of the water column of the algal mat while G. verrucosa is located in the lower part, close to the sediment. This distribution may be related to the increase of Pm and R observed in July in Cladophora which shows an adaptation to high solar radiation, in contrast with the decrease of Pm calculated in incubations of Gracilaria. By mid summer to August, non-coloured fragments of G. verrucosa are observed in the upper parts of the water column and over Cladophora sp. indicating photoinhibition and the destruction of G. verrucosa at high temperatures. This is related to the low Pm values and high initial slopes of G. verrucosa observed in the laboratory incubations in July, which indicate the adaptation of this species to low light intensities imposed by the shading effect of the Cladophora sp. mats.
Conclusion The pattern of seasonal variation of macroalgal populations in Tancada lagoon has been characterised during the last years by the dominance of C. linum in autumn and winter. This species is acclimated to estuarine environments in which both light and nutrient conditions are highly variable mainly due to
Floating macroalgae in a Mediterranean coastal lagoon 225
freshwater inputs and wind perturbations (Orlandini, 1994; McGlatery & Pedersen, 1999). Growth was supported by high concentrations of dissolved ammonium in the water column which derived from the mineralization of organic matter accumulated in the lagoon during spring, summer and fall and from seawater inputs which were rich in nitrogen from the adjacent bay (Menendez, unpubl. data). When the water temperature and solar radiation increases in spring and summer, other species, Cladophora sp. in the upper part of water column and G. verrucosa in the lower part proliferate as they can adapt to high temperatures and solar radiation (Cladophora) and decreasing nutrient availability (Gracilaria) due to its uptake by photosynthetic organisms. A decrease of freshwater inflows, mainly in the East basin in Tancada lagoon, had produced a significant decrease in the depth of the water column (from 54·409·55 cm in 1979 to 32·52·69 cm in 1999) and in its turnover rate (water conductivity in spring and summer between 3·6 and 22·9 mS cm 1 in 1979 and between 44·1 and 61·9 mS cm 1 in 1998). This contributes to the stability and proliferation of fast growing species such as floating macroalgae and to a more heterotrophic stage, dominated by an excess of organic matter accumulation and decomposition, which is characteristic of eutrophic coastal lagoons.
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