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Relationships between macroalgal biomass and nutrient concentrations in a hypertrophic area of the Venice Lagoon
.~larme Enrironmental Research 22(1987} 297-312
Relationships Between Macroalgal Biomass and Nutrient Concentrations in a Hypertrophic Area of the Venice Lagoon A. Sfriso, A. Marcomini & B. Pavoni Department of Environmental Sciences. University of Venice. Calle Larga S. Marta 2137. 30123 Venice. haty [Received 3 October 1986: revised version received 8 June 1987: accepted 9 June 1987) ABSTRACT
Macroalgae hiomuss and concentrutions of nitrogelz, phosphoru.s and chlorophyll a were determhwd weekly or hiweekh" hz water and sediments, ~htring the spring-summer of 1985 in a hypertrophic area of the lagoon 0/ Venice. Remarkable hiomass prothwtitm (up to 2 8 6 g m - 2 &tv-", wet weight), was interrupted ehtring three periods r?/"emo.v&, w/ten ttlaO'ou/gal decomposition (rate: up to lO00gm-'- day -1 ) released e.vtraordinarv amouHts q/mttrients. Depending on the macroalgrw distribution in the water colunm, the ntttrients released #~ water t,ar&,d./i'om 3"3 to 19" I Itg-at litre/or total htorganic nitrogen and./i'om 1"8 to 2"71tg-at litre-t /or reactice phosphorus. Most nutrients, howet:er, accumulated ht the .stu?]icial .vedhltent (up to 0"640 aml to 3 . 0 6 m g g - t . [ o r P and N respecticely) rc~hmhliHg the amotott.v ah'eadv stored under aerobic conditions. Phytoplank tern..~v.vtematitally Below 5 mg m - 3 as Chl. a, sharply increased up to 100 mg m - 3 otll.t" qlter the release of nutrients in water by anaerobic macroulgal decompo.~ition. During the algal growth periods, the N: P atomic ratio in water dt'crca.sed to 0"7, sttgge.s'ting that nitrogen is a growth-limiting [ktctor. This ratio /br surficial sediment was between 6.6 and 13"1, similar to that 0[" macr~mlgae (8.6-12"0).
INTRODUCTION
In shallow waters, macroalgae play an important role in the variation of nutrient concentrations. Many studies have related inputs and enrichment of nitrogen and phosphorus compounds to macroalgal blooms 297 Marine Enriron. Res. 0141-1136/87/503.50 C. Elsevier Applied Science Publishers Ltd. England, 1987. Printed in Great Britain
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A, Sfriso, ,4. Marcornini, B. Pavoni
(Harlin & Thorne-Miller, 1981: Kindig & Littler, 1980: Guist & Humm, 1976; Waite & Mitchell, 1972: Rosenberg, 1985). However, the influence of macroalgal growth (Chapman & Craige, 1977) and decomposition (Zimmermann & Montgomery, 1984) on the variation of nutrient concentrations has not been well studied in water bodies with restricted circulation. Rosenberg (1985) carried out investigations on poorly exchanged marine waters surrounding Sweden. Mortalities of benthic animals were observed and related to local and regional effects of increased macroalgal biomass and decreased oxygen concentrations in bottom water. The situation in the lagoon of Venice is more extreme and similar to situations referred to as "hypertrophic' by Fonselius (1978). For this reason the lagoon of Venice ecosystem has peculiar features compared to the few lagoons reported in the literature (Harlin & Thorne-Miller, 198 I: Charner Benz et al., 1979; Conover, 1964). With an expanse of 549km 2 and an average depth of l m, the lagoon is hydrographically subdivided into northern, central and southern basins (276, 162, 111 km2; see Fig. 1). The
Fig. !.
Map of the central part of tile lagoon of Venice and the sampling site.
Macroalgal biomass and nutrient concentrations in ~emce Lagoon
299
lagoon receives untreated and treated municipal selvage from Venice, Mestre and Chioggia (300 000 inhabitants}, industrial waste from Marghera and fresh water from 24 canals and small rivers draining an intensively cultivated region of 2000 km 2 iBernardi et al., 1986). Tidal exchange is very important: during a half fide cycle, 1.6-5"2 108 m 3 of water are exchanged with the northern Adriatic Sea through the port entrances of kido, Malamocco and Chioggia {Ministry of Public Works, 1979). The salinity is in the 25-35%0 range. In extended areas of the lagoon the water exchange is poor, due to the presence of islands and channels and to some changes in hydrodynamics, carried out to favour waterway access to the industrial area te.g., the Malamocco-Marghera canal). Until the late 1970s, macroalgal biomass production would typically start at the end of February. When the water temperature increased above 10-1TC and the photoperiod was optimal, seaweeds grew quickly and populated all the available space ISfriso & Cavolo, 1983). After initial rapid growth and dominance of Enteromorpha sp. pl., Ulva rigida C. Ag. prevailed. Large algal biomass fluctuations occurred for periods of a few days to two weeks, depending on climatic conditions, mainly wind and storms. The biomass of Ulca rigida was maximal from April to May; afterwards the biomass fluctuated and declined in summertime, usually becoming negligible in autumn and winter. Such processes always occurred under aerobic conditions (Sfriso & Cavolo, 1983). Since ten vears ago. however, this typical seasonal trend appears to have been changing. As a predominant consequence of hydrodynamical changes, a poor water exchange occurs in more extended areas, and an extraordinary growth of macroalgae is supported by hypertrophic conditions (Sfriso & Cavolo, 1983; Alberotanza & Piergallini, 1986) and anaerobic conditions are established. So tklr no integrated chemical-biological approach has been applied to study the lagoon. Some papers report systematical studies on the lagoon macroalgal species and associations (Schiffner & Vatova, 1938: Pignatti, 1962: Sfriso, 1987) and others deal with the content of nutrients ICossu eta/., 1983; 1984) in water and sediments. Study of the eutrophication in the lagoon water has so far been based mainly on the approach which emphasizes the role of the nutrient concentrations in determining phytoplankton blooms (Facco et al., 1986). However. since macroalgal biomass of many kg m - 2 (even more than 10 kg m - 2 wet weightl occupies a major part of the lagoon during the February-October period (Sfriso & Cavolo, 19831 and the phosphorus and nitrogen contents in macroalgae range from 1"34 to 3.17mgg -~ and from 17.6 to 4 3 m g g -~ tdry weight) respectively (Kornfeldt, 1982), we thought it worthwhile to study fluctuations of macroalgae and concentrations of nutrients in water and sediment.
300
.4. Sl~"so, .4. Marcomini, B. Patoni
MATERIALS AND METHODS
Sampling and analytical procedures Since macroalgal blooms had been observed in the spring-summer period (Sfriso & CavoIo. 1983: Alberotanza & Piergallini, 1986) twenty sampling sessions were carried out from April 21 to August 12, 1985, at a station 1300m 2 wide), located some hundred meters from the Lido island (Fig. 1). The sampling area is immediately south of the watershed dividing the northern basin from the central one, in a highly productive area of the Venice Lagoon. The mean water depth at the station was 0.9 m with a mean tide difference of + 3 0 c m lsee also Pirazzoli, 1974). To measure macroalga[ biomass, 4-6 adjacent spots of the bottom were isolated by a metallic cylinder (45-cm i.d.) lowered from the surface. Algae fronds trapped by the cylinder walls were cut by a stainless steel blade, collected with a landing-net and weighed wet. The mean and standard deviation of the recorded macroalgal weights were scaled to a square meter. The thickness of the macroalgae layer was measured as a percentage of height with respect to the water column. Macroalgae samples were stored in polyethylene foils, frozen at - 25-C and freeze-dried for dry weight, total phosphorus IP~,,t) and total nitrogen (Nt,,0 determinations. Three liters of water were sampled using a Kemmerer bottle at 20-30cm from the surface and filtered through Whatman G F F glass fibre filters for the analyses of chlorophyll a/Chl, a) and nutrients. Water samples were immediately frozen and stored at -25~C. Chlorophyll a was measured after acetone extraction of the total suspended matter by a fluorescence spectrophotometer (PerkinElmer MPG-44B, Norwalk, Connecticut), according to Strickland & Parsons (19721. Ammonia (NH2), nitrite (NOy), nitrate (NO3) and reactive phosphorus (RP) concentrations were determined, as soon as possible, using a Perkin-Elmer 320 or 156 spectrophotometer (Strickland & Parsons, 1972). The sum of NH2, NO 3 and N O ; is referred to as total inorganic nitrogen (TIN). Air and water temperatures, water transparency, redox potential (Eh) and pH were measured in situ with a mercury thermometer, Secchi disk and laboratory instruments adapted for field work (Orsenigo & Co., Milan, Italy), respectively. The water parameters reported were measured at 20-30cm from the surface; occasionally also the values at the bottom were monitored. Water samples for dissolved oxygen (DO) and sulfide analyses were immediately stabilized and analyzed as soon as possible by titration according to Strickland & Parsons (1972) and A P H A - A W W A - W P C F (1975). After measuring Eh and pH of the surface sediments, the 5-cm surface layer was
:l,lacroalgal biomass and nutrient concentrations m Venice Lagoon
301
sampled with a 10cm i.d. plexiglas corer, homogenized, wrapped in polyethylene foils and stored frozen at - 2 5 ° C for nutrient analyses. Total nitrogen (N,o t) was determined on freeze-dried macroalgae and sediment using a Perkin-Elmer 240B Elemental Analyzer. Inorganic (Pml and total phosphorus (P~o~)in sediment were determined by the phosphomol.vbdenum blue method (Aspila et al., 1976) before and after combustion at 550:C, respectively. Organic phosphorus (Po~g) was calculated by difference. Total phosphorus of macroalgae was determined with the same method after digestion by HCIO,~/HNO>4/1, according to Kornfeldt i 1962). All analyses were repeated at least twice.
RESULTS AND DISCUSSION The sampling was carried out from the end of April through mid-August, when macroalgal biomass became negligible {i.e. <0"01 kgm-:). Figure 2 shows the seasonal change in the chemical-physical parameters in water and surficial sediment. Dissolved oxygen (DO) content, pH and,:Eh of water appear to follow similar trends. Dissolved oxygen showed three minima: 2.3, 0-5 and 0 . 0 m g l - ' , corresponding to 46, 10, and 0% of saturation, on May 19, June 2 and July 20. In such anoxic conditions macroalgal biomass and chemical-physical parameters had comparable variations. During this period pH and Eh in water, from the average values of 85 and 300mV, measured under aerobic conditions !(DO% > 100), dropped to about 7 and 0mV, respectively, and water transparency decreased to 40% of the depth. Similarly, pH and Eh in surficiaI sediment decreased from about 7.5 and - 5 0 m V to 68 and - 1 7 0 m V , respectively, between April 21 and May 19, when conditions were aerobic. In Figs 3a, 3b and 4, the biomass, the fluctuations and the vertical distribution of the macroalgae are graphically represented. The dominant species (almost 100%) was Ulva rigida C. Ag. The precision of the biomass measures (standard deviation, SD) reported in Fig. 3a, reflected the pattern of macroalgal dispersion on the sediment surface, which was never homogeneous. In fact, macroalgae began to grow progressively from new plants or from fronds accumulated by currents in depressions of the lagoon floor. At the beginning of the productive period, macroalgae were irregularly distributed on the lagoon sediment., and biomass estimates had high SD. After the second anoxia, macroalgae were distributed more uniformly, because they grew from fronds almost equally spaced, and the SD was lower. Standard deviation was also low at the end of April when macroalgae were sampled after a wind storm, which improved the uniform distribution over the bottom. The biomass of UIt'a ranged between 6 and 9 kg m - -" before the
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first occurrence ofanoxia (May 19) and was undetectable after the anoxia of July 20. The highest biomass was measured in the last ten days of April, when Ulva fronds, some up to 2-3 m 2 in size, were almost equally distributed through the water column (Fig. 4). Oxygen bubbles were very abundant and helped to lift Uh'a toward the surface. The sudden drop of biomass before May 19 was due to a storm which dispersed the algal fronds located 30-40cm above the bottom. Conditions of oxygen supersaturation were re-established after this meteorological perturbation, and Uh'a grew again through May l l, then decreased till the second anoxia, on June 2. Macroalgal biomass grew again in mid-June up to 6.8kgm--', and decreased very sharply to 0 . 0 k g m -2 during the third anoxia on July 20. Afterwards, for 20days, no seaweeds were observed. In Fig. 3b the macroalgal biomass daily growth or degradation rate per square meter is given. Due to the short time between the first and second anoxia a continuot, s macroalgal biomass decomposition, with a mean rate up to 7 0 0 g m - 2 d a y - t , was observed from mid-May through the first ten days of June. The third anoxia reached a mean macroalgal degradation rate of 1000 g m - 2 day - t. Between June and July, macroalgal biomass increased up to 6 k g m -2 (Fig. 3a) and highly productive periods labove 2 5 0 g m -2 day- t) alternated with low reductions in biomass (O-50gm- 2 day- t). The results reported in Figs 2, 3 and 4 can be interpreted as follows. When water temperature exceeded 20'~C and a macroalgal bloom filled the water column, dramatically decreasing the already poor water exchange, the dissolved oxygen, produced in s i t . by photosynthetic processes, was inadequate to support night respiration. Then, anoxic conditions were
?,Iacroalgal biomass and nutrient concentrations in Venice Lagoon
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established and macroalgal biomass started to decompose. Hydrogen sulfide concentrations in water were in the range 1-8-9-6 mg 1 - Las S-" -. Before the 1980s, when the circulation of tidal waters was more active and supplied oxygen adequately, anoxic conditions were prevented, even if macroalgal blooms produced large amounts of biomass. The anoxic conditions of July 20 lasted some days and killed all the macrofauna, except chironomid larvae (Chironomus salinarius Kieff: Ceretti et al., 1985). This species has an anaerobic metabolism enabling its survival, ~vhile its predators die off. In August 1985 swarms of such Diptera invaded Venice, hindering railway and airport activities. Seaweeds were again sampled after 20 days. Some Cladophorae species, typical of the summer season (Sfriso, 1987) were sampled, but Ult'a was no longer present. The graphs of Fig. 5 show nutrient and chlorophyll a concentrations in water. The trends in the inorganic nitrogen compounds (Fig. 5a-e) were similar, in that maximum concentrations occurred after the first, second and, possibly, third anoxic events. A m m o n i a reached values above 14~g-at litre-t and nitrite and nitrate concentrations were concurrently detected above 06 and 3.5lLg-at litre-~. Two maxima of nitrate concentrations (Fig. 5c) had also been detected before the first anoxia. These may be attributable to the fluctuations of macroalgae biomass during oxic periods (Fig. 3b), which led to release of nitrogen as NO;- (Fig. 5c). Reactive phosphorus IFig. 5e) also increased, during the three anoxic periods, to 2.7. 1.9 and l81~g-at litre -t. In Fig. 5, the appearance of concentration maxima in the profile is closely related to the different biodegradation of nitrogen and phosphorus organic compounds. Since the phosphorus regeneration is faster (Golterman, 1973) the reactive phosphorus peak appeared immediately, as soon as anoxic conditions ,,,,ere established. Nitrogen concentrations increased later. Figure 5fshows the seasonal change of phytoplankton. Before the anoxia of May 19, phytoplankton was constantly below 511g litre-t of Chl a. A phytoplanktonic bloom (Chl. a above 100 llg litre - ~ occurred only after this first anoxic period, when the decomposing algal biomass released a large quantity of nutrients. Phytoplankton continued to bloom during the second anoxia of June 2. Chl. a concentrations decreased until the next macroalgal growth period and a slight increase was only detected after the anoxia of July 20{Ch1. a: from 21 to 10.1 l~g litre- ~. The low RP and TIN values recorded in water samples collected on June 2 were strictly related to concurrent occurrences of abnormal phytoplankton bloom, which delayed the TIN and RP maxima for two weeks. After the extra nutrients in ~'ater were depleted, phytoplankton Chl. a concentrations decreased to 2-2 and 5-2 l~g litre - ' on June 2 and July 20, respectively.
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Macroalgal biomass and nutrient concentrations in ['enice Lagoon
307
The amount of nutrients released into water, due to macroalgal decomposition, decreased drastically from the first to the third anoxia. The nutrient profiles in Fig. 5 show no apparent relationship with the amounts of macroalgal biomass decomposed (Fig. 3a) in the same periods. Vertical distribution of macroatgae during the three anoxia was very different (Fig. 4). In May, when macroalgae started to decompose, they occupied all the water column; therefore a high nutrient release in water was observed, The over-abundance of nutrients triggered a phytoplanktonic bloom which reduced water transparency {Fig. 2) and inhibited the growth of the macroalgae. A stratification in the water column occurred with a surficial, layer of phytoplankton superimposed on a macroalgae bed in contact with the sediment, greatly reducing the growth rate of macroalgae (Fig. 3). When the second and third anoxic periods occurred, macroalgae were bound to the bottom and a very small nutrient release to the water was observed. If we take into account the percentage of dry matter in the wet fronds of Uh,a rigida (Table 1), and the related phosphorus and nitrogen concentrations, we can estimate the amount of nutrients recycled by macroalgal decomposition. A kilogram of wet UIL'arigida corresponds to an average dry weight of 126g, and to 0-31 and 3.49g of phosphorus and nitrogen respectively. Therefore, considering the average water depth at the sampling site {0.9 m), each kilogram of decomposed Ult'a, can release (per square meter) 034 mg litre- t phosphorus and 3'88 mg litre- ~ nitrogen, i.e. about 11 and 277 llg-at litre- t respectively. These values are about 10 and 50 times higher than the mean nutrient concentrations detected in water at the beginning of field samplings (Fig. 5). Since the nutrient concentrations found in water were much lower, compared to the amounts of decomposed macrolagae, storage in sediments was implicated. The concentrations of P~., Por~, P,ot and Nto~ in the surficial sediment, and the N:P atomic ratios calculated in water and sediment are reported in Fig. 6. All the measures had standard deviations within 5%. During the investigation period P~, remained practically unchanged at about TABLE I Values of Nutrients F o u n d in U/ca r~ida
Dry weight (%) P,,,dmg g - J ) N,,,,{mg g - t) N : P atomic ratio
Range
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9-0-17-9 I. l-3.9 22-9-31-8 8-6-12-0
12.6 + 2"2 2"5 + 1.0 27.7 __ 4.3 10-2 '___3-2
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Macroalgal biomass and nutrient concentrations in Venice Lagoon
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0-3 me~-,,- L, whereas Po,~ ranged from below 0-1 me, g - t . at the beeinnin~,_ of the samplings, to above 0"3 mg g- t after the anoxic periods. Consequently, P,o, ranged from 0-368 to 0"679 m g g - t . Total nitrogen, which is mainly organic nitrogen (Keeney et al., 1970: Kemp & Mudrochova, 19721, increased from below 1.3 mg g- t to above 3 mg gAn accumulation of nutrients in sediment started at the beginning of the biomass fluctuations under aerobic conditions and continued until macroalgal biomass completely disappeared at the end of July (Fig. 3). Because of macroalgal stratification in the water column, some of the macroalgae lying near the bottom decomposed continuously, even under aerobic conditions. This steady-decomposition state supported a continuous increase of nutrient concentrations in sediment favoured by the poor vertical water mixing and temperature differences. Occasionally a surface-to-bottom temperature difference up to 2~C was measured. The nutrients released by anaerobic macroalgal decomposition accumulated in surficial sediment at a faster rate (Fig. 6). Chiaudani et al. (1983), have recently reviewed the literature on the N:P ratios in different Italian coastal waters. According to them, when the ratio decreases below 4.5, nitrogen is the limiting factor in the algal growth, whereas for N:P ratios higher than 7, phosphorus becomes the limiting factor. Tile N:P atomic ratios found in water and sediments are plotted in Fig. 6. In the periods preceding the first and third anoxia, the N:P ratio in water decreased to 2-0 and 0-7, respectively, indicating nitrogen as a possible growth-limiting factor (see also Ryther and Dunstan, 1971; Goldman et al., 1973: Keeney, 1973 and Rosenberg, 1975). In fact, macroalgae grew by taking up nutrients from the water and simultaneously decayed at the surface sediments. This led to a decrease in the N : P ratio in water and an increase in the ratio in the surficial sediment, where it progressively approached the values measured in UIt'a (Table 1). During anoxias, both water and sediment N : P ratios became even closer to macroalgae values. Water N : P ratios more suitable for algal growth were observed some days after the anoxic conditions when, in fact, macroalgal growth re-commenced.
CONCLUSIONS in extended shallow water areas of the Venice Lagoon, under aerobic conditions, nutrients in water were assimilated almost completely by macroalgae during their spring and summer growth periods. When there was an imbalance in the production and consumption of oxygen, anoxic conditions occurred and large amounts of nutrients were released by the decomposition of macroalgae. The concentrations of nutrients in water
310
A. Sfriso. A. .~,larcomini. B. Pavoni
depended on the vertical distribution of the macroalgae in the water column. Most of the nutrients regenerated were accumulated in the sediments. Nutrients released in water were mostly depleted by phytoplankton, whose blooms were triggered by macroalgal decomposition. During the same spring-summer period, phytoplankton blooms were regulated by macroalgal biomass fluctuations, in hypertrophic lagoon areas with similar macroalgae crops.
A C K N O W L E D G E M ENTS The authors express their thanks to Jane Frankenfield Zanin of the I S D G M - C N R , Venice, for her suggestions in revising the manuscript. The research was supported by the Italian National Research Council (CNR) under Grants Nos 84.00175.03 and 86.01727.03.
REFERENCES Alberotanza. L. & Piergallini, G. (I 986). Biomassa algale nella laguna di Venezia. Amhiente Risorse Salute. 51, 45-7. Aspila, K. I.. Agemian, H. & Chau, S. J. (1976). A semi-automated method for the determination of inorganic, organic and total phosphorus in sediments. Anah'st. 101, 187-97. APHA, AWWA & WPCF (1975). Standard methods for the exanthlation oJ water and wastewater. Washington, 1193 pp. Bernardi, S., Cecchi, R., Costa, F., Ghermandi, G. & Vazzoler. S. (1986). Transferimento di acqua dolce e di inquim, nti nella laguna di Venezia. lnquinanwnto, !/2, 46-64. Ceretti, G., Ferrarese, U. & Scattolin, M. 11985). In: I chh'onomidi nelhl laguna di Venezia. Arsenale Editrice, Venice, 59 pp. Chapman, A. R. O. & Craige, J. J. (1977). Seasonal growth in Lambtariu longicruris: relations with dissolved inorganic nutrients and internal reserves of nitrogen. Mar. Biol., 40, 197-205. Charner Benz, M., Eiseman, N. J. & Gallaher, E. E. (1979), Seasonal occurrence and variation in standing crop of a drift algal community in the Indian river, Florida. Botanica Marhra. 22, 413-20. Chiaudani, G., Gaggino, G. F. & Vighi, M. 11983). Synoptic survey of the distribution of nutrients in Italian Adriatic coastal waters. Thula.ssia Jugoslulicu, 19(1-4), 77-86. Conover, J. T. (1964), The ecology, seasonal periodicity, and distribution of benthic plants in some Texas lagoons. Botunica Marina, 7(I), 4-41. Cossu, R., Degobbis, D., Donazzolo, R.. Maslowska, E., Orio, A. A. & Pavoni, B. (1983). Nutrient release from the sediments of the Venice lagoon, lngegneria Amhientule, 31(5 6), 16-23.
.1,Ict¢'ro¢ll,~¢l[hirJrplclSS und nutrient concentrati~ms in [ cm~c La~o~m
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Cossu, R.. Degobbis. D., Donazzolo, R., Homme-Maslowska, E., Orio. A. A. & Pavoni, B. (1984). II ruolo dei sedimenti nella eutrofizzazione della laguna di Venezia. blgegneria Scmitaria, 32(4!, 1--9. Facco, S., Degobbis, D.. Sfriso, A. & Orio, A. A. (1986). Space and time x ariability of" nutrients in the Venice lagoon. In: Estuarine variability (Wolfe. D. A. (ed.)t, Academic Press, Rockville, Maryland, pp. 307-318. Fonselius. St. H. (1978). On nutrients and their role as production limiting factors in the Baltic. Acta Hvdrochim. H.v~b'ohicd., 614). 329-39. Goldman, J. C., Tenore. K. R. and Stanley. H. 1. ( 19731. Inorganic nitrogen removal from wastewater: effect on phytoplankton growth in coastal marine waters. Science. 180, 955-6. Golterman, A. L. (19731. Vertical movement of phosphate in freshwater. In: Encironmemal phosphorus hamthook (Griffith, E. J., Beeton, A., Spencer. J. M. and Mitchell, D. T. (eds)), Wiley-lnterscience. New York, 509-38, Guist, G. G. & Humm, H. J. (1976). Effect of sewage effluents on growth of Uh'a lactuca. Florida Sci., 39, 267-71. Harlin, M. M. & Thorne-Miller, B. (I 981 ). Nutrient enrichment ofseagrass beds in a Rhode island coastal lagoon. Mar. Biol., 65. 221-9. Keeney, D. R. (1973). The nitrogen cycle in sediment-water systems. J. Enciron. Quality, 2(I), 15-29. Keeney, D. R., Kourad, G. & Clesters, G. (1970). Nitrogen distribution in some Wisconsin lake sediments, ll"ater Poll. Control Fed., 42, 411-17. Kemp, A. L. W. & Mudrochova, A. (1972). Distribution and forms of nitrogen in a lake Ontario sediment core. Lbmtology cmd Oceanography, 17(16), 85567. Kindig, A. C, & Littler, M. M. (1980). Growth and primary productivity of marine macrophytes exposed to domestic sewage effluent. Mar. Ent'iropz. Res., 3, 81-100. Kornfeldt, R. A. (1982), Relation between nitrogen and phosphorus content of macroalgae and the waters of northern Oresund. Botanica Marimt, 25(4), 197-20 I. Ministry of Public Works (1979). Le correnti di mctrea nella laguna di I/enezia. lstituto Idraulica Padova, Padova, 95 pp. Pignatti, S. (1962). Associazioni di alghe marine sulla costa veneziana. Memorie lstituto Veneto Lettere Scienze Arti, 32(3), 1-134. Pirazzoli, P. (1974). Dati storici sul medio rnare a Venezia. ,4 tti Accademia Scienze Ls'tituto Bologna, 18(1), 124-48. Rosenberg, R. (I 985). Eutrophication. The future marine coastal nuisance. Marine Pollution Bulletin, 16(6), 227-31. Rhyther, J. H. & Dunstan, W. M. (1971). Nitrogen, phosphorus and eutrophication in the coastal marine environment. Science, 171,375-80. Schiffner, V. & Vatova, A. (1938). Le alghe della Laguna: Chlorophyceae, Phaeophyceae, Rhodophyceae, Myxophyceae. In: La lagttna di Venezia, vol. 3 (Minio, M. (ed.)), Venice, 250pp. Sfriso, A. (1987). Flora and vertical distribution of macroalgae in the lagoon of Venice: a comparison with previous studies. Giornale Botanico ltaliano, 121(1-2), 69-85. Sfriso, A. & Cavolo, S. (1983). La situazione delle alghe nella laguna di Venezia. Amhiente Risorse Sahtte, 16-17, 38-9.
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Strickland, J. D. H. & Parsons. T. R. (19721..-t practical handbook o/ seawater analyses [Stevenson, J. C. (ed.)), Fisheries Research Board Canada. Ottaw'a, 310pp. Waite, T. & Mitchell. R. (1972). The effect of nutrient fertilization on the benthic alga Uh'a lactuc'a. Botanica Murina, 15, 15 t-6. Zimmermann. C. F. & Montgomery, J. R. (1984). Effects of a decomposing drift algal mat on sediment pore water nutrient concentration in a Florida seagrass bed. Murine Ecoh~gy, 19, 299-302.
Relationships Between Macroalgal Biomass and Nutrient Concentrations in a Hypertrophic Area of the Venice Lagoon A. Sfriso, A. Marcomini & B. Pavoni Department of Environmental Sciences. University of Venice. Calle Larga S. Marta 2137. 30123 Venice. haty [Received 3 October 1986: revised version received 8 June 1987: accepted 9 June 1987) ABSTRACT
Macroalgae hiomuss and concentrutions of nitrogelz, phosphoru.s and chlorophyll a were determhwd weekly or hiweekh" hz water and sediments, ~htring the spring-summer of 1985 in a hypertrophic area of the lagoon 0/ Venice. Remarkable hiomass prothwtitm (up to 2 8 6 g m - 2 &tv-", wet weight), was interrupted ehtring three periods r?/"emo.v&, w/ten ttlaO'ou/gal decomposition (rate: up to lO00gm-'- day -1 ) released e.vtraordinarv amouHts q/mttrients. Depending on the macroalgrw distribution in the water colunm, the ntttrients released #~ water t,ar&,d./i'om 3"3 to 19" I Itg-at litre/or total htorganic nitrogen and./i'om 1"8 to 2"71tg-at litre-t /or reactice phosphorus. Most nutrients, howet:er, accumulated ht the .stu?]icial .vedhltent (up to 0"640 aml to 3 . 0 6 m g g - t . [ o r P and N respecticely) rc~hmhliHg the amotott.v ah'eadv stored under aerobic conditions. Phytoplank tern..~v.vtematitally Below 5 mg m - 3 as Chl. a, sharply increased up to 100 mg m - 3 otll.t" qlter the release of nutrients in water by anaerobic macroulgal decompo.~ition. During the algal growth periods, the N: P atomic ratio in water dt'crca.sed to 0"7, sttgge.s'ting that nitrogen is a growth-limiting [ktctor. This ratio /br surficial sediment was between 6.6 and 13"1, similar to that 0[" macr~mlgae (8.6-12"0).
INTRODUCTION
In shallow waters, macroalgae play an important role in the variation of nutrient concentrations. Many studies have related inputs and enrichment of nitrogen and phosphorus compounds to macroalgal blooms 297 Marine Enriron. Res. 0141-1136/87/503.50 C. Elsevier Applied Science Publishers Ltd. England, 1987. Printed in Great Britain
298
A, Sfriso, ,4. Marcornini, B. Pavoni
(Harlin & Thorne-Miller, 1981: Kindig & Littler, 1980: Guist & Humm, 1976; Waite & Mitchell, 1972: Rosenberg, 1985). However, the influence of macroalgal growth (Chapman & Craige, 1977) and decomposition (Zimmermann & Montgomery, 1984) on the variation of nutrient concentrations has not been well studied in water bodies with restricted circulation. Rosenberg (1985) carried out investigations on poorly exchanged marine waters surrounding Sweden. Mortalities of benthic animals were observed and related to local and regional effects of increased macroalgal biomass and decreased oxygen concentrations in bottom water. The situation in the lagoon of Venice is more extreme and similar to situations referred to as "hypertrophic' by Fonselius (1978). For this reason the lagoon of Venice ecosystem has peculiar features compared to the few lagoons reported in the literature (Harlin & Thorne-Miller, 198 I: Charner Benz et al., 1979; Conover, 1964). With an expanse of 549km 2 and an average depth of l m, the lagoon is hydrographically subdivided into northern, central and southern basins (276, 162, 111 km2; see Fig. 1). The
Fig. !.
Map of the central part of tile lagoon of Venice and the sampling site.
Macroalgal biomass and nutrient concentrations in ~emce Lagoon
299
lagoon receives untreated and treated municipal selvage from Venice, Mestre and Chioggia (300 000 inhabitants}, industrial waste from Marghera and fresh water from 24 canals and small rivers draining an intensively cultivated region of 2000 km 2 iBernardi et al., 1986). Tidal exchange is very important: during a half fide cycle, 1.6-5"2 108 m 3 of water are exchanged with the northern Adriatic Sea through the port entrances of kido, Malamocco and Chioggia {Ministry of Public Works, 1979). The salinity is in the 25-35%0 range. In extended areas of the lagoon the water exchange is poor, due to the presence of islands and channels and to some changes in hydrodynamics, carried out to favour waterway access to the industrial area te.g., the Malamocco-Marghera canal). Until the late 1970s, macroalgal biomass production would typically start at the end of February. When the water temperature increased above 10-1TC and the photoperiod was optimal, seaweeds grew quickly and populated all the available space ISfriso & Cavolo, 1983). After initial rapid growth and dominance of Enteromorpha sp. pl., Ulva rigida C. Ag. prevailed. Large algal biomass fluctuations occurred for periods of a few days to two weeks, depending on climatic conditions, mainly wind and storms. The biomass of Ulca rigida was maximal from April to May; afterwards the biomass fluctuated and declined in summertime, usually becoming negligible in autumn and winter. Such processes always occurred under aerobic conditions (Sfriso & Cavolo, 1983). Since ten vears ago. however, this typical seasonal trend appears to have been changing. As a predominant consequence of hydrodynamical changes, a poor water exchange occurs in more extended areas, and an extraordinary growth of macroalgae is supported by hypertrophic conditions (Sfriso & Cavolo, 1983; Alberotanza & Piergallini, 1986) and anaerobic conditions are established. So tklr no integrated chemical-biological approach has been applied to study the lagoon. Some papers report systematical studies on the lagoon macroalgal species and associations (Schiffner & Vatova, 1938: Pignatti, 1962: Sfriso, 1987) and others deal with the content of nutrients ICossu eta/., 1983; 1984) in water and sediments. Study of the eutrophication in the lagoon water has so far been based mainly on the approach which emphasizes the role of the nutrient concentrations in determining phytoplankton blooms (Facco et al., 1986). However. since macroalgal biomass of many kg m - 2 (even more than 10 kg m - 2 wet weightl occupies a major part of the lagoon during the February-October period (Sfriso & Cavolo, 19831 and the phosphorus and nitrogen contents in macroalgae range from 1"34 to 3.17mgg -~ and from 17.6 to 4 3 m g g -~ tdry weight) respectively (Kornfeldt, 1982), we thought it worthwhile to study fluctuations of macroalgae and concentrations of nutrients in water and sediment.
300
.4. Sl~"so, .4. Marcomini, B. Patoni
MATERIALS AND METHODS
Sampling and analytical procedures Since macroalgal blooms had been observed in the spring-summer period (Sfriso & CavoIo. 1983: Alberotanza & Piergallini, 1986) twenty sampling sessions were carried out from April 21 to August 12, 1985, at a station 1300m 2 wide), located some hundred meters from the Lido island (Fig. 1). The sampling area is immediately south of the watershed dividing the northern basin from the central one, in a highly productive area of the Venice Lagoon. The mean water depth at the station was 0.9 m with a mean tide difference of + 3 0 c m lsee also Pirazzoli, 1974). To measure macroalga[ biomass, 4-6 adjacent spots of the bottom were isolated by a metallic cylinder (45-cm i.d.) lowered from the surface. Algae fronds trapped by the cylinder walls were cut by a stainless steel blade, collected with a landing-net and weighed wet. The mean and standard deviation of the recorded macroalgal weights were scaled to a square meter. The thickness of the macroalgae layer was measured as a percentage of height with respect to the water column. Macroalgae samples were stored in polyethylene foils, frozen at - 25-C and freeze-dried for dry weight, total phosphorus IP~,,t) and total nitrogen (Nt,,0 determinations. Three liters of water were sampled using a Kemmerer bottle at 20-30cm from the surface and filtered through Whatman G F F glass fibre filters for the analyses of chlorophyll a/Chl, a) and nutrients. Water samples were immediately frozen and stored at -25~C. Chlorophyll a was measured after acetone extraction of the total suspended matter by a fluorescence spectrophotometer (PerkinElmer MPG-44B, Norwalk, Connecticut), according to Strickland & Parsons (19721. Ammonia (NH2), nitrite (NOy), nitrate (NO3) and reactive phosphorus (RP) concentrations were determined, as soon as possible, using a Perkin-Elmer 320 or 156 spectrophotometer (Strickland & Parsons, 1972). The sum of NH2, NO 3 and N O ; is referred to as total inorganic nitrogen (TIN). Air and water temperatures, water transparency, redox potential (Eh) and pH were measured in situ with a mercury thermometer, Secchi disk and laboratory instruments adapted for field work (Orsenigo & Co., Milan, Italy), respectively. The water parameters reported were measured at 20-30cm from the surface; occasionally also the values at the bottom were monitored. Water samples for dissolved oxygen (DO) and sulfide analyses were immediately stabilized and analyzed as soon as possible by titration according to Strickland & Parsons (1972) and A P H A - A W W A - W P C F (1975). After measuring Eh and pH of the surface sediments, the 5-cm surface layer was
:l,lacroalgal biomass and nutrient concentrations m Venice Lagoon
301
sampled with a 10cm i.d. plexiglas corer, homogenized, wrapped in polyethylene foils and stored frozen at - 2 5 ° C for nutrient analyses. Total nitrogen (N,o t) was determined on freeze-dried macroalgae and sediment using a Perkin-Elmer 240B Elemental Analyzer. Inorganic (Pml and total phosphorus (P~o~)in sediment were determined by the phosphomol.vbdenum blue method (Aspila et al., 1976) before and after combustion at 550:C, respectively. Organic phosphorus (Po~g) was calculated by difference. Total phosphorus of macroalgae was determined with the same method after digestion by HCIO,~/HNO>4/1, according to Kornfeldt i 1962). All analyses were repeated at least twice.
RESULTS AND DISCUSSION The sampling was carried out from the end of April through mid-August, when macroalgal biomass became negligible {i.e. <0"01 kgm-:). Figure 2 shows the seasonal change in the chemical-physical parameters in water and surficial sediment. Dissolved oxygen (DO) content, pH and,:Eh of water appear to follow similar trends. Dissolved oxygen showed three minima: 2.3, 0-5 and 0 . 0 m g l - ' , corresponding to 46, 10, and 0% of saturation, on May 19, June 2 and July 20. In such anoxic conditions macroalgal biomass and chemical-physical parameters had comparable variations. During this period pH and Eh in water, from the average values of 85 and 300mV, measured under aerobic conditions !(DO% > 100), dropped to about 7 and 0mV, respectively, and water transparency decreased to 40% of the depth. Similarly, pH and Eh in surficiaI sediment decreased from about 7.5 and - 5 0 m V to 68 and - 1 7 0 m V , respectively, between April 21 and May 19, when conditions were aerobic. In Figs 3a, 3b and 4, the biomass, the fluctuations and the vertical distribution of the macroalgae are graphically represented. The dominant species (almost 100%) was Ulva rigida C. Ag. The precision of the biomass measures (standard deviation, SD) reported in Fig. 3a, reflected the pattern of macroalgal dispersion on the sediment surface, which was never homogeneous. In fact, macroalgae began to grow progressively from new plants or from fronds accumulated by currents in depressions of the lagoon floor. At the beginning of the productive period, macroalgae were irregularly distributed on the lagoon sediment., and biomass estimates had high SD. After the second anoxia, macroalgae were distributed more uniformly, because they grew from fronds almost equally spaced, and the SD was lower. Standard deviation was also low at the end of April when macroalgae were sampled after a wind storm, which improved the uniform distribution over the bottom. The biomass of UIt'a ranged between 6 and 9 kg m - -" before the
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first occurrence ofanoxia (May 19) and was undetectable after the anoxia of July 20. The highest biomass was measured in the last ten days of April, when Ulva fronds, some up to 2-3 m 2 in size, were almost equally distributed through the water column (Fig. 4). Oxygen bubbles were very abundant and helped to lift Uh'a toward the surface. The sudden drop of biomass before May 19 was due to a storm which dispersed the algal fronds located 30-40cm above the bottom. Conditions of oxygen supersaturation were re-established after this meteorological perturbation, and Uh'a grew again through May l l, then decreased till the second anoxia, on June 2. Macroalgal biomass grew again in mid-June up to 6.8kgm--', and decreased very sharply to 0 . 0 k g m -2 during the third anoxia on July 20. Afterwards, for 20days, no seaweeds were observed. In Fig. 3b the macroalgal biomass daily growth or degradation rate per square meter is given. Due to the short time between the first and second anoxia a continuot, s macroalgal biomass decomposition, with a mean rate up to 7 0 0 g m - 2 d a y - t , was observed from mid-May through the first ten days of June. The third anoxia reached a mean macroalgal degradation rate of 1000 g m - 2 day - t. Between June and July, macroalgal biomass increased up to 6 k g m -2 (Fig. 3a) and highly productive periods labove 2 5 0 g m -2 day- t) alternated with low reductions in biomass (O-50gm- 2 day- t). The results reported in Figs 2, 3 and 4 can be interpreted as follows. When water temperature exceeded 20'~C and a macroalgal bloom filled the water column, dramatically decreasing the already poor water exchange, the dissolved oxygen, produced in s i t . by photosynthetic processes, was inadequate to support night respiration. Then, anoxic conditions were
?,Iacroalgal biomass and nutrient concentrations in Venice Lagoon
305
established and macroalgal biomass started to decompose. Hydrogen sulfide concentrations in water were in the range 1-8-9-6 mg 1 - Las S-" -. Before the 1980s, when the circulation of tidal waters was more active and supplied oxygen adequately, anoxic conditions were prevented, even if macroalgal blooms produced large amounts of biomass. The anoxic conditions of July 20 lasted some days and killed all the macrofauna, except chironomid larvae (Chironomus salinarius Kieff: Ceretti et al., 1985). This species has an anaerobic metabolism enabling its survival, ~vhile its predators die off. In August 1985 swarms of such Diptera invaded Venice, hindering railway and airport activities. Seaweeds were again sampled after 20 days. Some Cladophorae species, typical of the summer season (Sfriso, 1987) were sampled, but Ult'a was no longer present. The graphs of Fig. 5 show nutrient and chlorophyll a concentrations in water. The trends in the inorganic nitrogen compounds (Fig. 5a-e) were similar, in that maximum concentrations occurred after the first, second and, possibly, third anoxic events. A m m o n i a reached values above 14~g-at litre-t and nitrite and nitrate concentrations were concurrently detected above 06 and 3.5lLg-at litre-~. Two maxima of nitrate concentrations (Fig. 5c) had also been detected before the first anoxia. These may be attributable to the fluctuations of macroalgae biomass during oxic periods (Fig. 3b), which led to release of nitrogen as NO;- (Fig. 5c). Reactive phosphorus IFig. 5e) also increased, during the three anoxic periods, to 2.7. 1.9 and l81~g-at litre -t. In Fig. 5, the appearance of concentration maxima in the profile is closely related to the different biodegradation of nitrogen and phosphorus organic compounds. Since the phosphorus regeneration is faster (Golterman, 1973) the reactive phosphorus peak appeared immediately, as soon as anoxic conditions ,,,,ere established. Nitrogen concentrations increased later. Figure 5fshows the seasonal change of phytoplankton. Before the anoxia of May 19, phytoplankton was constantly below 511g litre-t of Chl a. A phytoplanktonic bloom (Chl. a above 100 llg litre - ~ occurred only after this first anoxic period, when the decomposing algal biomass released a large quantity of nutrients. Phytoplankton continued to bloom during the second anoxia of June 2. Chl. a concentrations decreased until the next macroalgal growth period and a slight increase was only detected after the anoxia of July 20{Ch1. a: from 21 to 10.1 l~g litre- ~. The low RP and TIN values recorded in water samples collected on June 2 were strictly related to concurrent occurrences of abnormal phytoplankton bloom, which delayed the TIN and RP maxima for two weeks. After the extra nutrients in ~'ater were depleted, phytoplankton Chl. a concentrations decreased to 2-2 and 5-2 l~g litre - ' on June 2 and July 20, respectively.
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Macroalgal biomass and nutrient concentrations in ['enice Lagoon
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The amount of nutrients released into water, due to macroalgal decomposition, decreased drastically from the first to the third anoxia. The nutrient profiles in Fig. 5 show no apparent relationship with the amounts of macroalgal biomass decomposed (Fig. 3a) in the same periods. Vertical distribution of macroatgae during the three anoxia was very different (Fig. 4). In May, when macroalgae started to decompose, they occupied all the water column; therefore a high nutrient release in water was observed, The over-abundance of nutrients triggered a phytoplanktonic bloom which reduced water transparency {Fig. 2) and inhibited the growth of the macroalgae. A stratification in the water column occurred with a surficial, layer of phytoplankton superimposed on a macroalgae bed in contact with the sediment, greatly reducing the growth rate of macroalgae (Fig. 3). When the second and third anoxic periods occurred, macroalgae were bound to the bottom and a very small nutrient release to the water was observed. If we take into account the percentage of dry matter in the wet fronds of Uh,a rigida (Table 1), and the related phosphorus and nitrogen concentrations, we can estimate the amount of nutrients recycled by macroalgal decomposition. A kilogram of wet UIL'arigida corresponds to an average dry weight of 126g, and to 0-31 and 3.49g of phosphorus and nitrogen respectively. Therefore, considering the average water depth at the sampling site {0.9 m), each kilogram of decomposed Ult'a, can release (per square meter) 034 mg litre- t phosphorus and 3'88 mg litre- ~ nitrogen, i.e. about 11 and 277 llg-at litre- t respectively. These values are about 10 and 50 times higher than the mean nutrient concentrations detected in water at the beginning of field samplings (Fig. 5). Since the nutrient concentrations found in water were much lower, compared to the amounts of decomposed macrolagae, storage in sediments was implicated. The concentrations of P~., Por~, P,ot and Nto~ in the surficial sediment, and the N:P atomic ratios calculated in water and sediment are reported in Fig. 6. All the measures had standard deviations within 5%. During the investigation period P~, remained practically unchanged at about TABLE I Values of Nutrients F o u n d in U/ca r~ida
Dry weight (%) P,,,dmg g - J ) N,,,,{mg g - t) N : P atomic ratio
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Macroalgal biomass and nutrient concentrations in Venice Lagoon
309
0-3 me~-,,- L, whereas Po,~ ranged from below 0-1 me, g - t . at the beeinnin~,_ of the samplings, to above 0"3 mg g- t after the anoxic periods. Consequently, P,o, ranged from 0-368 to 0"679 m g g - t . Total nitrogen, which is mainly organic nitrogen (Keeney et al., 1970: Kemp & Mudrochova, 19721, increased from below 1.3 mg g- t to above 3 mg gAn accumulation of nutrients in sediment started at the beginning of the biomass fluctuations under aerobic conditions and continued until macroalgal biomass completely disappeared at the end of July (Fig. 3). Because of macroalgal stratification in the water column, some of the macroalgae lying near the bottom decomposed continuously, even under aerobic conditions. This steady-decomposition state supported a continuous increase of nutrient concentrations in sediment favoured by the poor vertical water mixing and temperature differences. Occasionally a surface-to-bottom temperature difference up to 2~C was measured. The nutrients released by anaerobic macroalgal decomposition accumulated in surficial sediment at a faster rate (Fig. 6). Chiaudani et al. (1983), have recently reviewed the literature on the N:P ratios in different Italian coastal waters. According to them, when the ratio decreases below 4.5, nitrogen is the limiting factor in the algal growth, whereas for N:P ratios higher than 7, phosphorus becomes the limiting factor. Tile N:P atomic ratios found in water and sediments are plotted in Fig. 6. In the periods preceding the first and third anoxia, the N:P ratio in water decreased to 2-0 and 0-7, respectively, indicating nitrogen as a possible growth-limiting factor (see also Ryther and Dunstan, 1971; Goldman et al., 1973: Keeney, 1973 and Rosenberg, 1975). In fact, macroalgae grew by taking up nutrients from the water and simultaneously decayed at the surface sediments. This led to a decrease in the N : P ratio in water and an increase in the ratio in the surficial sediment, where it progressively approached the values measured in UIt'a (Table 1). During anoxias, both water and sediment N : P ratios became even closer to macroalgae values. Water N : P ratios more suitable for algal growth were observed some days after the anoxic conditions when, in fact, macroalgal growth re-commenced.
CONCLUSIONS in extended shallow water areas of the Venice Lagoon, under aerobic conditions, nutrients in water were assimilated almost completely by macroalgae during their spring and summer growth periods. When there was an imbalance in the production and consumption of oxygen, anoxic conditions occurred and large amounts of nutrients were released by the decomposition of macroalgae. The concentrations of nutrients in water
310
A. Sfriso. A. .~,larcomini. B. Pavoni
depended on the vertical distribution of the macroalgae in the water column. Most of the nutrients regenerated were accumulated in the sediments. Nutrients released in water were mostly depleted by phytoplankton, whose blooms were triggered by macroalgal decomposition. During the same spring-summer period, phytoplankton blooms were regulated by macroalgal biomass fluctuations, in hypertrophic lagoon areas with similar macroalgae crops.
A C K N O W L E D G E M ENTS The authors express their thanks to Jane Frankenfield Zanin of the I S D G M - C N R , Venice, for her suggestions in revising the manuscript. The research was supported by the Italian National Research Council (CNR) under Grants Nos 84.00175.03 and 86.01727.03.
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