Review Article |
Corresponding author: Adriano Sfriso ( sfrisoad@unive.it ) Academic editor: Lucilla Capotondi
© 2019 Adriano Sfriso, Alessandro Buosi, Michele Mistri, Cristina Munari, Piero Franzoi, Andrea Augusto Sfriso.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Sfriso A, Buosi A, Mistri M, Munari C, Franzoi P, Sfriso AA (2019) Long-term changes of the trophic status in transitional ecosystems of the northern Adriatic Sea, key parameters and future expectations: The lagoon of Venice as a study case. In: Mazzocchi MG, Capotondi L, Freppaz M, Lugliè A, Campanaro A (Eds) Italian Long-Term Ecological Research for understanding ecosystem diversity and functioning. Case studies from aquatic, terrestrial and transitional domains. Nature Conservation 34: 193-215. https://doi.org/10.3897/natureconservation.34.30473
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The determination of the trophic status of transitional ecosystems from the physico-chemical and biological point of view is one of the requirements of the European Water Framework Directive (WFD 2000/60/EC). In Italy, its determination is implemented by the Regional Agencies for Environmental Protection (ARPAs) that have activated multi-annual monitoring programs. However, as the availability of funds is increasingly scarce, the number of environmental parameters to detect environmental changes should be conveniently managed.
The high number of environmental parameters, nutrient and macrophyte datasets available for the LTER-Italia site “Venice lagoon” can be an useful tool to analyze the trophic changes over recent years and to foresee environmental evolutions. Nutrient data on a spatial basis have been available since 1948, whereas macroalgal maps date back to 1980. The aim of this paper is to highlight the changes of the trophic status of the lagoon since the middle of the 20th century by considering the concentrations of nutrients in the surface sediments and in the water column, the variation of some physico-chemical parameters and the biomass of macroalgae and also to foresee the way it will possibly evolve. In fact, after many anthropogenic impacts that in the second half of the 20th century affected the lagoon, starting from the year 2010, the ecological status is progressively improving. Nutrients show a significant reduction both in the water column and in surface sediments, and the macrophytes are represented by species of higher ecological value while the opportunistic species such as the Ulvaceae are in strong regression.
LTER-Italy network, trophic status, nutrient concentrations, waters, sediments, key parameters
Almost half of Europe’s population lives less than 50 kilometers from the sea and the resources of the coastal areas and transitional water systems (TWS) produce much of the economic wealth of the European Community (EU) (http://ec.europa.eu/environment/iczm/pdf/2000brochure_en.pdf). Urban settlements, industrial and agricultural activities, fishing, commercial traffic and tourism reduce vital space and introduce high quantities of nutrients and pollutants along the 89,000 kilometers of the European coasts, increasing eutrophication and pollution. TWS are mainly affected by anthropogenic impacts because of their shallow bottoms and closed morphology that rarely allows suitable hydrological renewal. These environments, which host habitats and species of conservation interest, are often severely degraded and require special attention. For this reason, they are monitored and have become the subject of numerous studies to understand and try to reverse the causes of their degradation.
The north-western Adriatic Sea is a closed shallow basin where various rivers flow, draining the Po plain and forming large TWS. From North to South three main lagoon systems are present: the lagoons of Marano-Grado, the lagoon of Venice and the lagoons and ponds of the Po Delta. Among them, the lagoon of Venice is the largest and most studied TWS in the Mediterranean Sea. The first biological studies of the lagoon date back to the end of the eighteenth century (
The present work investigates the way nutrient concentrations, macroalgal biomass and the environmental parameters of water column and surface sediments have changed since the middle of the last century. The aim is to explore the large dataset and highlight the most relevant parameters necessary to monitor trophic changes, in order to contribute to the institutional monitoring and environmental agencies’ achievement in obtaining significant results with reduced efforts and lower costs.
The lagoon of Venice (https://deims.org/f7d94927-17be-4d3d-9810-e3c9bc91829c) is a polyhedric shallow water body located in the northern Adriatic Sea which has a water surface of ca. 432 km2 and a mean depth of ca. 1.2 m (Fig.
Information on data collected before 1980 is reported in the cited papers whereas the surveys carried out by our research team, sampling procedures and analytical methods are summarized in the following pages.
Data on nutrients, macroalgal biomass and environmental parameters of the water column have been collected in the whole central lagoon since 1987 (34 sites). Monitoring surveys were carried out in 1993 (34 sites), 1998 (52 sites), 2003 (65 sites), 2011 (45 sites) and 2014 (34 sites). Data of ammonium concentration were also reported for the whole lagoon in 2011 (118 sites).
Thirty-four sites in early summer 1987, 1993, 1998 and 2003, and 31 sites in 2011 were monitored by collecting the 5 cm surface sediment top layer for phosphorus, total nitrogen analyses and determination of the sediment density.
At each site, dissolved oxygen was measured with a portable instrument (Oxi 196 oximeter, Wissenschaftlich-Technische Werkstätten GmbH, Weilheim, Germany). Oxygen concentrations were reported as percentage of saturation (%DO) taking into account water temperature and salinity. Water transparency was measured with the Secchi disk. Transparency measurements were reported as a percentage of water column visibility because the waters are shallow (0.5–2.5 m) and the tidal excursion is relatively high (0.5–1 m). A value corresponding to 100% means that the bottom was visible, 50% means that the disk disappeared half way to the bottom. pH and Eh were measured with a portable pH-meter (pH 25) of the CRISON Instruments (Barcelona, Spain).
Six water column samples were collected with a home-made cylindrical sampler (length: 1.50 cm, diameter: 4 cm) which was repeatedly plunged into the water and poured to a tank. Sub-samples of 0.1–1.0 L were filtered through GF/F Whatman glass fiber filters (porosity: 0.7 mm). Filters and water samples were stored frozen at -18 °C for chlorophyll-a (Chl-a) analyses (
At each site three sediment cores (first 5 cm top layer) were collected with a Plexiglas corer (i.d. 10 cm) and carefully mixed together. Sub-samples were retained to determine density and nutrient (total nitrogen and total, inorganic and organic phosphorus) concentrations. Density was obtained as g cm-3 of wet and dry sediment according to
Total nitrogen (TN) concentrations were obtained by a Flash 2000 CHNS Analyser (Thermo Fisher Scientific spa), sediment freezing, lyophilization and pulverization. Inorganic (Pinorg) and total phosphorus (Ptot) were, respectively, determined before and after combustion at 550 °C for two hrs, with dissolution in 1N HCl and spectrophotometric measurements according to
The macroalgal biomass was sampled between late May and July, which is the period when it is most abundant. At each site, biomass samples were collected with a 71×71 cm square frame or with a rake when the biomass was low (3–6 replicates) according to
Data of different datasets of the whole central lagoon have been compared and means, standard deviations, maximum and minimum values have been determined. The Shapiro-Wilk test differentiated non-normal data, and then Friedman one-way ANOVA values (p <0.05) and Spearman’s non-parametric coefficients have also been calculated. The basic statistics and correlation analyses of the data collected in the 5 periods were carried out both separately (1987, 1993, 1998, 2003, 2011) and by considering the whole data set (1987–2011). The total information has been summarized in a table reporting the number of significant (p<0.05) correlations per single parameter and period. The principal component analysis (PCA) has been applied to log-transformed data to visualize the variance and the association between parameters of both single and total periods, and to explore the scores with a loading >0.7, which is the generalized standard used for this statistical analysis. Total data are visualized in a bi-plot, whereas the loadings >0.7 of the single variables of each period are reported in Table
The similarities and differences between the stations during the 5 sampling periods have been investigated by analyzing the same data in a transposed matrix and bi-plotting the results. The stations are grouped according to their ecological characteristics and comparisons between the separated or overlapped periods highlight their differences.
Data were processed by Statistica software, Release 10 (StatSoft Inc. Tulsa, USA) provided by an academic license.
The first detailed distribution of macroalgae over the whole lagoon took place in 1980 and was replicated in 2003 (
Trends of the mean, standard deviation, maximum, minimum and median values of the macroalgal biomass, Chl-a, dissolved oxygen, pH and water transparency in the central lagoon of Venice.
The environmental parameters mainly affected by the presence of macroalgae (i.e. the concentration of dissolved oxygen, pH and water transparency) showed a strongly related trend to the biomass variation (Fig.
Changes of nutrient concentrations in the surface sediments of the Venice lagoon are reported in Table
Nitrogen and phosphorus changes in surface sediment top layer (5 cm) in the whole lagoon.
1948–2011 | ||||||||||
Sediment thickness | Phosphorus | Nitrogen | ||||||||
cm | Mean | SD | Max | Mean | SD | Max | ||||
µg g-1 | mg g-1 | |||||||||
Perin 1974 | 1948–49 | 30 | 24 | ± | 16 | 50 | 1.00 | ± | 0.86 | 1.96 |
Perin 1974 | 1968–73 | 30 | 164 | ± | 79 | 250 | 1.86 | ± | 2.20 | 3.56 |
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1983 | 20 | 454 | ± | 126 | 682 | 1.33 | ± | 0.59 | 2.74 |
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1987–88 | 20 | 339 | ± | 215 | 1102 | 1.33 | ± | 0.89 | 4.80 |
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1987 | 5 | 386 | ± | 96 | 720 | 1.21 | ± | 0.60 | 3.00 |
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1993 | 5 | 361 | ± | 80 | 682 | 1.14 | ± | 0.48 | 2.62 |
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1998 | 5 | 375 | ± | 65 | 541 | 0.93 | ± | 0.48 | 1.37 |
Facca et al. 2009 | 2003 | 5 | 358 | ± | 99 | 635 | 0.71 | ± | 0.36 | 1.48 |
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2011 | 5 | 367 | ± | 114 | 896 | 0.69 | ± | 0.75 | 2.89 |
Total Nitrogen (Ntot) exhibited a mean value of 1.00±0.86 mg g-1 in 1948–49, increasing up to 1.86±2.20 mg g-1 in the period 1968–73, followed by a progressive decrease to 0.69 µg g-1 in 2011. The maximum value was recorded in the period 1968–73 by
Some more detailed information is available for the central basin of the Venice lagoon where the same operators monitored the surface sediment top layer (5 cm) of 31–34 stations in successive late spring-early summer periods, characterized by different scenarios (1987: presence of high algal biomass; 1993: sharp reduction of macroalgal biomass; 1998: intense Manila clam (Tapes philippinarum Adams and Reeve) harvesting; 2003: the highest Manila clam harvesting; 2011: sharp reduction of clam stocks (from ca. 40,000 tonnes in 2010 to ca. 2000 tonnes in 2012) and decrease of clam fishing activities).
During the period between 1987 and 2011 the mean concentrations of Ptot per volume unit (µg cm-3 of sediment) did not change significantly, except for the maximum value of 720 µg cm-3 in 1987, then progressively decreased to 473 µg cm-3 (-34%) in 2011 (Table
Changes of Total Phosphorus, Organic Phosphorus and Total Nitrogen in the central lagoon.
Total Phosphorus | ||||||
1987 | 1993 | 1998 | 2003 | 2011 | changes | |
µg/cm³ | ||||||
site N° | 34 | 34 | 34 | 34 | 31 | % |
Mean | 386 | 361 | 375 | 358 | 383 | ≈ |
SD | 96 | 80 | 65 | 99 | 50 | |
Min | 227 | 184 | 257 | 201 | 281 | |
Max | 720 | 682 | 541 | 635 | 473 | -34 |
Organic Phosphorus | ||||||
1987 | 1993 | 1998 | 2003 | 2011 | changes | |
µg/cm³ | ||||||
site N° | 34 | 34 | 34 | 34 | 31 | % |
Mean | 104 | 67 | 59 | 53 | 62 | -40 |
SD | 42 | 28 | 31 | 53 | 24 | |
Min | 49 | 27 | 16 | 2 | 13 | |
Max | 246 | 210 | 167 | 150 | 113 | -54 |
Total Nitrogen | ||||||
1987 | 1993 | 1998 | 2003 | 2011 | changes | |
mg/cm³ | ||||||
site N° | 34 | 34 | 34 | 34 | 31 | % |
Mean | 1.21 | 1.14 | 0.93 | 0.71 | 0.35 | -71 |
SD | 0.60 | 0.48 | 0.48 | 0.36 | 0.48 | |
Min | 0.22 | 0.33 | 0.10 | 0.09 | 0.04 | |
Max | 3.00 | 2.62 | 1.37 | 1.48 | 0.48 | -84 |
In the same period (1987–2011), the mean Ntot concentration decreased from 1.21 to 0.35 mg cm-3 (ca. -71.1%, one-way ANOVA: p<0.001) whereas the peak concentration lowered by 32%, from 3.00 to 2.05 mg cm-3, although the lowest value was recorded in 1998 with 1.37 mg cm-3.
Figs
Maps of the organic phosphorus distributions in the 5 cm surface top layer of the central lagoon basin in 1987, 1993, 1998, 2003 and 2011.
Maps of the total nitrogen distributions in the 5 cm surface top layer of the central lagoon basin in 1987, 1993, 1998, 2003 and 2011.
A significant decrease was also observed for the concentrations of nutrients in the water column Fig.
Distribution of ammonium in the water column in the central lagoon from 1962 to 1986 (from
Map of ammonium distribution obtained for the whole lagoon by sampling 118 sites in spring and in autumn 2011.
By considering the whole central lagoon, information on the nutrient concentrations in the water column has been available since 1987. The mean concentration of reactive phosphorus (RP) decreased from 0.76 µM in 1987 (34 sites) to 0.19 µM in 2011 (45 sites), slowly increasing to 0.24 µM in 2014 (34 sites, Fig.
The Spearman non-parametric correlation matrices of data collected in the central lagoon were determined by considering both the whole period: 1987–2011 and the years 1987, 1993, 1998, 2003, 2011, separately. On the whole, the highest number of significant (p<0.05) direct or inverse correlations was shown by RP (13 out of 18), salinity, Chl-a and nitrite (12 out of 18) and pH (11 out of 18) Tables
Spearman non-parametric coefficients for the total period 1987–2011 in the central lagoon.
Parameters | Temperature | pH | Eh | O2 | Salinity | Transparency | Chl-a | Macroalgae | RP | Ammonium | Nitrite | Nitrate | DIN | Density | P tot | P inorg | P org | TN |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Temperature | 1.00 | |||||||||||||||||
pH | -0.20 | 1.00 | ||||||||||||||||
Eh | 0.10 | 0.26 | 1.00 | |||||||||||||||
O2 | -0.14 | 0.63 | 0.41 | 1.00 | ||||||||||||||
Salinity | -0.15 | 0.12 | -0.19 | -0.07 | 1.00 | |||||||||||||
Transparency | -0.09 | 0.37 | 0.08 | 0.33 | 0.40 | 1.00 | ||||||||||||
Chl-a | 0.15 | 0.07 | 0.39 | 0.23 | -0.56 | -0.27 | 1.00 | |||||||||||
Macroalgae | -0.05 | 0.34 | 0.12 | 0.35 | 0.15 | 0.29 | -0.14 | 1.00 | ||||||||||
RP | 0.05 | 0.36 | 0.37 | 0.22 | -0.45 | -0.06 | 0.43 | -0.11 | 1.00 | |||||||||
Ammonium | -0.08 | 0.16 | -0.06 | -0.11 | -0.15 | -0.03 | 0.15 | -0.25 | 0.32 | 1.00 | ||||||||
Nitrite | 0.14 | -0.23 | 0.05 | -0.30 | -0.42 | -0.23 | 0.31 | -0.41 | 0.40 | 0.45 | 1.00 | |||||||
Nitrate | 0.25 | -0.25 | 0.24 | -0.15 | -0.39 | -0.11 | 0.35 | -0.27 | 0.45 | 0.22 | 0.75 | 1.00 | ||||||
DIN | 0.16 | -0.12 | 0.15 | -0.19 | -0.37 | -0.11 | 0.35 | -0.34 | 0.47 | 0.69 | 0.80 | 0.84 | 1.00 | |||||
Density | -0.02 | -0.06 | -0.12 | -0.07 | 0.44 | 0.27 | -0.27 | 0.04 | -0.25 | -0.07 | -0.18 | -0.04 | -0.07 | 1.00 | ||||
P tot | 0.02 | 0.09 | 0.03 | 0.03 | -0.42 | -0.34 | 0.21 | 0.00 | 0.22 | 0.09 | 0.06 | -0.07 | -0.04 | -0.44 | 1.00 | |||
P inorg | 0.03 | -0.11 | -0.08 | -0.15 | -0.29 | -0.40 | 0.08 | -0.18 | 0.11 | 0.09 | 0.14 | -0.04 | -0.01 | -0.28 | 0.87 | 1.00 | ||
P org | 0.00 | 0.32 | 0.14 | 0.27 | -0.41 | -0.15 | 0.32 | 0.23 | 0.32 | 0.13 | 0.01 | -0.05 | 0.00 | -0.56 | 0.66 | 0.28 | 1.00 | |
TN | 0.03 | 0.27 | 0.37 | 0.34 | -0.27 | 0.05 | 0.41 | 0.06 | 0.32 | 0.11 | 0.17 | 0.06 | 0.11 | -0.44 | 0.32 | 0.12 | 0.52 | 1.00 |
1997–2011 | 1987 | 1993 | 1998 | 2003 | 2011 | |
RP | 13 | 6 | 8 | 1 | 12 | 5 |
Salinity | 12 | 7 | 9 | 12 | 9 | 6 |
Nitrite | 12 | 8 | 4 | 6 | 11 | 6 |
Chl-a | 12 | 2 | 8 | 6 | 10 | 1 |
pH | 11 | 4 | 7 | 5 | 13 | 7 |
Porg (Sed) | 10 | 7 | 9 | 7 | 12 | 4 |
O2 | 10 | 7 | 9 | 4 | 11 | 2 |
Nitrate | 10 | 4 | 5 | 4 | 9 | 5 |
TN | 10 | 2 | 5 | 7 | 6 | 2 |
DIN | 9 | 7 | 6 | 7 | 9 | 7 |
Transparency | 9 | 3 | 6 | 8 | 13 | 4 |
Density (Sed) | 9 | 4 | 8 | 7 | 7 | 4 |
Macroalgae | 9 | 7 | 1 | 0 | 6 | 2 |
Ptot (Sed) | 8 | 7 | 8 | 8 | 9 | 2 |
Eh | 7 | 1 | 2 | 5 | 0 | 1 |
Ammonium | 6 | 3 | 2 | 8 | 15 | 1 |
Pinorg (Sed) | 6 | 5 | 5 | 10 | 8 | 1 |
Temperature | 3 | 9 | 0 | 5 | 0 | 0 |
The principal component analysis highlighted the parameters with the highest variance (Table
Periods | Salinity | Nitrate | Transparency | Nitrite | pH | P org | RP | temperature | Chl-a | TN | O2 | Ammonium | Eh | Density | Macroalgae | P inorg |
1987–2011 | 0.61 | 0.64 | 0.35 | 0.70 | 0.69 | 0.74 | 0.71 | 0.35 | 0.54 | 0.66 | 0.72 | 0.34 | 0.41 | 0.60 | 0.65 | 0.37 |
1987 | 0.75 | 0.38 | 0.63 | 0.62 | 0.76 | 0.73 | 0.65 | 0.85 | 0.46 | 0.31 | 0.74 | 0.46 | 0.43 | 0.59 | 0.62 | 0.54 |
1993 | 0.90 | 0.71 | 0.74 | 0.78 | 0.64 | 0.61 | 0.74 | 0.22 | 0.85 | 0.57 | 0.75 | 0.52 | 0.45 | 0.55 | 0.22 | 0.60 |
1998 | 0.70 | 0.83 | 0.83 | 0.63 | 0.67 | 0.76 | 0.34 | 0.77 | 0.74 | 0.69 | 0.55 | 0.64 | 0.84 | 0.81 | 0.55 | 0.60 |
2003 | 0.77 | 0.76 | 0.77 | 0.88 | 0.87 | 0.84 | 0.90 | 0.35 | 0.66 | 0.75 | 0.65 | 0.94 | 0.20 | 0.63 | 0.30 | 0.62 |
2011 | 0.76 | 0.78 | 0.72 | 0.86 | 0.73 | 0.62 | 0.60 | 0.20 | 0.51 | 0.74 | 0.56 | 0.49 | 0.56 | 0.65 | 0.76 | 0.55 |
Total single years | 3.88 | 3.46 | 3.69 | 3.77 | 3.67 | 3.56 | 3.23 | 2.39 | 3.22 | 3.06 | 3.25 | 3.05 | 2.48 | 3.23 | 2.45 | 2.91 |
The bi-plot of the first two PCA components of the transposed matrix highlights the similarities/dissimilarities between the stations of the different sampling periods (Fig.
The lagoon of Venice is one of the most studied transitional environments of the Mediterranean Sea and the high number of available datasets enables us to understand environmental changes over the years and foresee its evolution. The trophic parameters and primary producers linked to their change have been studied assiduously since the early ’80s, although for some of them, data have been available since the late ‘40s. Actually, since the 2nd post-war industrial development frequent changes of the environmental scenarios have witnessed the effect of different anthropogenic activities. Between the ’60s and ’80s, a significant increase of eutrophication was recorded (
This paper was prepared in the framework of the LTER-Italy network in order to analyze a part of the great amount of data collected in the Venice lagoon. The long-term analysis of the trophic status since the middle of the 20th century made it possible to highlight both the evolution of this environment and the parameters related to the observed changes. The lagoon eutrophication increased markedly from the 2nd post-war period until the end of the ‘80s, when high nutrient amounts were released into the environment (dissolved in the water column and accumulated in the surface sediments), triggering macroalgal blooms and favoring hyper-dystrophic conditions. The parameters which are related to the primary production (%DO, pH, water transparency, RP, Porg) showed the highest changes. In the following years, different environmental scenarios have occurred but the latest data show that the lagoon environment is improving and, without other additional anthropogenic pressures, it should keep a positive trend for at least 10 years or longer. Results highlight that the trophic status of a transitional environment, from the physico-chemical point of view, can be easily detected by measuring some driver parameters such as RP and nitrites. They are the most sensitive nutrients to the environmental changes, easy to analyze and low-cost. The analysis of these two parameters together with the measurement of pH and the oxygen concentration can support macrophyte assemblages for the assessment of the ecological status according to the WFD (2000/60/EC) and provide an exhaustive method for the determination of the trophic status of a transitional water system.
The authors thank the ARPA Veneto that funded the most recent monitoring of the whole lagoon (