Corresponding author: Silvia Pulina ( pulinasi@uniss.it ) Academic editor: Maria Grazia Mazzocchi
© 2019 Silvia Pulina, Antonella Lugliè, Maria Antonietta Mariani, Marco Sarria, Nicola Sechi, Bachisio Mario Padedda.
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:
Pulina S, Lugliè A, Mariani MA, Sarria M, Sechi N, Padedda BM (2019) Multiannual decrement of nutrient concentrations and phytoplankton cell size in a Mediterranean reservoir. 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: 163-191. https://doi.org/10.3897/natureconservation.34.30116
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Reservoirs are primary water resources for many uses in the Mediterreanean region and need dedicated studies for understanding the complexity of their dynamics particularly vulnerable to local and global stressors. This study focused on phytoplankton variations in relation to seasonal environmental changes on a multiannual time scale (2006–2015) at a Mediterranean eutrophic reservoir (Bidighinzu Lake, Italy) belonging to the Italian, European and International Long Term Ecological Research networks. Phytoplankton cell density, volume and biomass and chlorophyll a concentrations were analysed together with meteo-climatic, hydrological, physical and chemical variables to detect trends and correlations. The period under study was also compared with previous years to assess the presence of significant differences in the environmental and planktonic compartments. Multiannual changes were more pronounced in summer than in the other seasons during the decade under study. The most conspicuous environmental changes were a significant decrease in summer nutrient concentrations in the reservoir and a simultaneous anthropic pressure reduction in the watershed. In addition, the mixing zone and euphotic zone ratio also increased. Multiannual changes in summer phytoplankton composition consisted of an increased density of smaller Bacillariophyceae and Cyanophyceae, which replaced larger species of the same phytoplankton classes. This resulted in opposite trends of total phytoplankton cell density (increasing) and mean phytoplankton cell volume (decreasing) over the study years. The nutrient decrement was statistically the strongest environmental driver of the phytoplankton changes observed in the reservoir. However, the mixing zone and the euphotic zone ratio and water temperature also significantly affected the multiannual phytoplankton variations. Therefore, we conclude that the success of small cell-sized phytoplankton in Bidighinzu Lake was most probably due to the synergic interactions of more environmental forces related to changing anthropic pressures and climate variability. Our results highlight the importance of long-term monitoring of reservoirs in the Mediterranean basin, especially in semi-arid regions where the need and scarcity of high quality water will be further exacerbated due to the global climate change.
Phytoplankton, cell size, nutrients, climate change, reservoir, LTER
In all aquatic ecosystems, phytoplankton growth depends on water temperature and on light and nutrient availability (
Different selective pressures, such as light availability, nutrient limitation, fluctuating nutrient supply or grazers, can influence the size structure in natural phytoplankton communities (
Many studies have highlighted drastic modifications in phytoplankton cell size composition and abundance in lakes related to changes in nutrient concentrations (
This work examines phytoplankton variations in relation to seasonal environmental changes on a multiannual time scale in a warm monomitic eutrophic Mediterranean reservoir (Bidighinzu Lake, Sardinia, Italy), mainly used for drinking water for 20 urban areas and about 100,000 inhabitants. In the Mediterranean area, climate conditions (such as long lasting periodic droughts) seriously restrict the water availability, especially during summer and cause strong variations in the water level of reservoirs, which in turn affect the phytoplankton abundance and composition (
Multiannual observations allow detecting meaningful ecological shifts, distinguishing significant changes from the normal patterns and the background noise and the assessment of whether ecological changes are due to human or natural causes (
Phytoplankton and environmental variables have been monitored since 1978 (
The Bidighinzu Lake is located in the northern part of Sardinia (Italy, 40°33'22"N 8°39'41"E) at an altitude of 334 m a.s.l. (Figure
Water sampling was conducted in the Bidighinzu Lake at monthly frequency from March 1988 to April 1989, from March 1994 to November 1997, from July to October 2003 and from March 2006 to October 2015 at a single station close to the deepest part of the reservoir (Figure
The water transparency was measured with a Secchi disc and the water temperature was recorded using a multi-parametric probe (Hydrolab Datasonde 5 and YSI 6600V2). Water samples (1.5 l) from the Niskin bottles were stored in cold (4 °C) and dark conditions prior to laboratory analysis for ammonium (N-NH4), nitrite (N-NO2), nitrate (N-NO3), total nitrogen (TN), reactive silica (Si-SiO4), orthophosphate (P-PO4) and total phosphorus (TP) according to
The Consiglio per la Ricerca in Agricoltura (CREA) provided daily meteorological data of rainfall and air temperature from a meteorological station nearby the Lake (about 15 km) from January 2006 to December 2015. Daily temperature values were monthly averaged and daily rainfall values were monthly cumulated. Monthly data on the climatic index WEMO (Western Mediterranean Oscillation) were provided by the Climatology Group of the University of Barcelona (Spain). This index measures the difference between the standardised atmospheric pressure recorded at Padua in northern Italy and San Fernando in south-western Spain (
The phytoplankton samples (100 ml), taken from the Niskin bottles, were immediately fixed after collection in 2% acid Lugol’s solution. Sample aliquots of 5 to 10 ml (depending on cell density) were analysed to estimate the cell density using the Utermöhl method (1958) with an inverted microscope (Zeiss, Axiovert 10). Cell counts were made at magnifications of 200× and 400× on at least 10% of the total bottom area of the sedimentation chamber. Additional non-fixed samples were observed immediately after collection to facilitate the identification of certain species. The species were identified following the taxonomic guides listed in
Mean cell volume of each species was obtained by geometrical approximations from measurement of at least 30 cells in each sample according to
Water samples (1.5 l) for measuring chlorophyll a concentrations were stored in cold (4 °C) and dark conditions before the laboratory analysis (within 24 hours), which were conducted with a spectrophotometer (50 SCAM, Varian), according to
Environmental data were depth-averaged for the entire water column, whereas phytoplankton data were depth-averaged only for the euphotic zone assuming that these organisms live and grow mainly in this water layer.
The depth of the euphotic layer was calculated as Zeu = 2.5 times the Secchi disc depth (
Seasons were considered as: summer = July–September, autumn = October–December, winter = January–March and spring = April–June.
For each separate season, the non-parametric Mann-Kendall test (
All statistical analyses were performed using R 3.4.3 software (
The non-parametric Mann-Kendall test was applied to detect significant monotonic trends in the summer WEMO index over all the historical datasets.
One-way analysis of variance (ANOVA) was performed to assess significant differences in environmental (WEMO index, air temperature, rainfall, Zmix/Zeu, water temperature, Si-SiO4, P-PO4, TP, N-NO3, N-NO2, N-NH4, DIN, TN and TON) and phytoplankton (cell density and cell volume of each phytoplankton class observed) variables amongst the four continuous time cycles of samplings available (1988–1989, 1994–1997, 2003, 2006–2015). Prior to ANOVA, all data were log10(x+1) transformed to meet ANOVA assumptions: normal distribution (Kolmogorov-Smirnov test) and homogeneity of variance (Bartlett test). When significant differences in the dependent variables based on these factors were observed, the post hoc Tukey’s pairwise comparisons test was performed.
All the analyses were performed using R 3.4.3 software (
To explore the land cover and land use changes of the Bidighinzu Lake watershed (52.18 km2) over time, a spatial data processing analysis with the support of a geographic information system (GIS) was performed (
The seasonal values of environmental and phytoplankton parameters considered during the decade 2006–2015 are reported in Tables
Minimum (Min), maximum (Max) and mean values ± standard deviation (SD) of environmental variables in Bidighinzu Lake considering the decade 2006–2015 (WEMOi, Western Mediterranean Oscillation index; Zmix/Zeu, mixing depth-euphotic depth ratio; Si-SiO4, silicate; P-PO4, orthophosphate; TP, total phosphorous; N-NO3, nitrate; N-NO2, nitrite; N-NH4, ammonia; DIN, dissolved inorganic nitrogen; TN, total nitrogen; TON, total organic nitrogen). Number of observations are reported in Table
Winter | Spring | Summer | Autumn | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Min | Max | Mean±SD | Min | Max | Mean±SD | Min | Max | Mean±SD | Min | Max | Mean±SD | |
WEMOi | -2.6 | 1.6 | -0.2±1.0 | -4.3 | 1.2 | -1.4±1.4 | -2.6 | 1.1 | -1.0±0.9 | -2.7 | 1.6 | -0.6±0.9 |
Air temperature (°C) | 4.8 | 10.8 | 8.3±1.5 | 12.4 | 22.8 | 17.1±3.5 | 19.2 | 26.0 | 23.1±2.0 | 7.1 | 18.9 | 12.5±3.7 |
Rainfall (mm) | 4.0 | 104.6 | 47.8±26.8 | 0.8 | 111.0 | 47.6±31.0 | 0.0 | 101.2 | 16.4±23.4 | 2.6 | 191.6 | 59.5±41.9 |
Water temperature (°C) | 6.6 | 11.5 | 9.3±1.4 | 12.0 | 26.4 | 16.8±3.3 | 17.7 | 24.8 | 20.4±1.8 | 8.6 | 19.1 | 15.0±2.2 |
Water transparency (m) | 0.3 | 11.1 | 0.6±0.2 | 0.3 | 1.6 | 0.9±0.3 | 0.3 | 2.5 | 1.1±0.5 | 0.3 | 1.3 | 0.8±0.1 |
Zmix/Zeu | 1.8 | 26.7 | 14.3±6.4 | 0.3 | 22.8 | 5.1±5.7 | 0.2 | 20 | 4.1±4.0 | 3.3 | 26.7 | 10.4±5.1 |
Si-SiO4 (mg l-1) | 0.7 | 9.5 | 6.1±2.0 | 0.0 | 9.2 | 4.8±1.8 | 0.2 | 62.0 | 5.1±10.0 | 0.1 | 7.1 | 2.6±0.8 |
P-PO4 (mg m-3) | 13.0 | 164.2 | 84.1±33.5 | 5.0 | 159.7 | 70.7±35.1 | 24.8 | 343.0 | 130.1±62.2 | 31.9 | 243.0 | 96.2±75.3 |
TP (mg m-3) | 83.5 | 355.1 | 183.7±70.2 | 61.0 | 399.4 | 170.1±75.0 | 79.8 | 457.9 | 246.9±79.6 | 68.9 | 396.3 | 190.9±89.1 |
N-NO3 (mg m-3) | 328.8 | 1295.6 | 878.5±361.0 | 16.2 | 684.4 | 231.3±199.1 | 6.7 | 126.7 | 38.3±21.3 | 24.0 | 1435.3 | 344.3±97.5 |
N-NO2 (mg m-3) | 11.7 | 60.4 | 22.1±5.4 | 29.0 | 720.6 | 13.0±7.3 | 2.6 | 37.4 | 666.4±402.8 | 3.3 | 47.6 | 16.7±8.1 |
N-NH4 (mg m-3) | 25.4 | 648.0 | 111.1±180.0 | 2.9 | 37.0 | 171.9±171.0 | 40.0 | 1736.4 | 620.4±404.1 | 22.3 | 939.9 | 427.4±250.5 |
DIN (mg m-3) | 504.9 | 1386.6 | 1011.6±295.5 | 63.0 | 803.6 | 416.3±182.4 | 73.2 | 1778.3 | 7.6±8.2 | 53.1 | 1977.0 | 788.4±229.0 |
TN (mg m-3) | 1839.2 | 4049.2 | 2703.9±653.5 | 1171.7 | 3519.1 | 2114.2±596.6 | 1212.0 | 4658.7 | 2431.0±925.8 | 442.0 | 4131.8 | 2347.4±848.6 |
TON (mg m-3) | 1004.0 | 3238.8 | 1692.3±584.1 | 858.1 | 3086.0 | 1697.9±588.6 | 344.5 | 4284.1 | 1766.1±985.6 | 146.2 | 3411.4 | 1572.2±872.8 |
Minimum (Min), maximum (Max) and mean values ± standard deviation (SD) of phytoplankton variables in Bidighinzu Lake considering the decade 2006–2015. Number of observations are reported in Table
Winter | Spring | Summer | Autumn | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Min | Max | Mean±SD | Min | Max | Mean±SD | Min | Max | Mean±SD | Min | Max | Mean±SD | |
Total cell density (103 cells l-1) | 448 | 52970 | 10298±13641 | 3068 | 515428 | 86784±133223 | 2633 | 1570361 | 203256±308627 | 1542 | 803909 | 149885±217932 |
Bacillariophyceae | 56 | 2613 | 720±757 | 14 | 6300 | 594±1259 | 41 | 15128 | 3224±3493 | 216 | 6926 | 2530±2171 |
Chlorophyceae | 78 | 4026 | 1123±1169 | 759 | 68065 | 9957±12968 | 324 | 36047 | 5657±7989 | 267 | 32226 | 9736±9146 |
Chrysophyceae | 0 | 383 | 55±94 | 0 | 70 | 13±20 | 0 | 705 | 55±137 | 0 | 1344 | 127±298 |
Conjugatophyceae | 0 | 35 | 7±10 | 0 | 62 | 8±15 | 0 | 336 | 42±75 | 2 | 1429 | 213±422 |
Cryptophyceae | 0 | 24693 | 3706±6394 | 5 | 4143 | 972±1120 | 9 | 2299 | 498±571 | 39 | 9884 | 1465±2179 |
Cyanophyceae | 0 | 27783 | 4618±8417 | 0 | 513989 | 75209±133927 | 1020 | 1562687 | 193740±308718 | 696 | 780464 | 135650±216116 |
Dinophyceae | 0 | 81 | 11±24 | 0 | 58 | 4±11 | 0 | 148 | 15±27 | 0 | 56 | 12±16 |
Euglenophyceae | 0 | 276 | 57±77 | 0 | 158 | 27±36 | 0 | 130 | 23±28 | 0 | 1528 | 153±325 |
Mean cell volume (µm3) | 0.52 | 25.68 | 6.95±6.64 | 0.06 | 18.44 | 1.97±3.57 | 0.03 | 34.67 | 3.12±6.58 | 0.09 | 14.80 | 2.40±3.87 |
Bacillariophyceae | 3.12 | 256.49 | 66.59±91.78 | 1.54 | 941.19 | 169.59±228.36 | 0.13 | 120.96 | 20.08±29.79 | 1.48 | 70.09 | 1.48±70.09 |
Chlorophyceae | 0.14 | 29.04 | 7.43±8.48 | 0.04 | 24.06 | 2.12±4.79 | 0.11 | 14.98 | 3.05±3.33 | 0.22 | 26.35 | 2.87±5.58 |
Chrysophyceae | 0.11 | 2590.58 | 219.07±659.78 | 3.89 | 1469.34 | 270.71±407.10 | 4.10 | 1012.90 | 165.82±211.08 | 1.14 | 769.60 | 146.41±213.10 |
Conjugatophyceae | 4.37 | 3306.90 | 542.12±826.55 | 73.73 | 12708.87 | 1367.56±3076.65 | 4.35 | 4772.39 | 475.39±824.45 | 0.56 | 3164.18 | 477.99±760.72 |
Cryptophyceae | 0.12 | 178.12 | 22.07±47.11 | 0.04 | 61.57 | 9.02±15.50 | 0.70 | 209.54 | 15.39±36.20 | 0.26 | 44.28 | 9.61±12.64 |
Cyanophyceae | 0.00 | 5.22 | 0.43±1.33 | 0.00 | 0.14 | 0.02±0.03 | 0.00 | 0.27 | 0.02±0.05 | 0.00 | 0.08 | 0.02±0.02 |
Dinophyceae | 9.80 | 3834.09 | 637.89±1299.79 | 0.68 | 103248.12 | 14703.87±28210.65 | 73.333 | 172092.97 | 17474.80±35443.87 | 31.92 | 32951.37 | 5757.98±9131.45 |
Euglenophyceae | 28.88 | 2283.72 | 414.01±574.54 | 43.14 | 4971.75 | 557.40±1035.71 | 1.89 | 2870.58 | 471.52±658.84 | 3.79 | 338.55 | 117.14±11.23 |
Total cell biomass (mg l-1) | 0.20 | 9.19 | 3.46±2.51 | 0.28 | 29.86 | 3.87±5.57 | 2.14 | 68.86 | 13.12±13.43 | 0.65 | 21.60 | 9.18±5.90 |
Bacillariophyceae | 0.08 | 7.54 | 2.39±2.57 | 0.03 | 24.95 | 1.52±4.58 | 0.05 | 65.43 | 6.78±11.70 | 0.49 | 16.99 | 3.42±3.47 |
Chlorophyceae | 0.01 | 0.69 | 0.18±0.19 | 0.12 | 10.89 | 1.60±2.11 | 0.04 | 3.67 | 1.11±1.05 | 0.06 | 9.88 | 2.47±2.73 |
Chrysophyceae | 0.00 | 0.04 | 0.01±0.01 | 0.00 | 0.04 | 0.01±0.01 | 0.00 | 2.39 | 0.13±0.47 | 0.00 | 1.39 | 0.10±0.30 |
Conjugatophyceae | 0.00 | 0.09 | 0.01±0.02 | 0.00 | 0.11 | 0.01±0.02 | 0.00 | 0.45 | 0.06±0.10 | 0.00 | 1.51 | 0.20±0.38 |
Cryptophyceae | 0.00 | 2.58 | 0.61±0.82 | 0.00 | 0.76 | 0.19±0.19 | 0.00 | 2.12 | 0.16±0.36 | 0.00 | 4.33 | 0.59±0.96 |
Cyanophyceae | 0.00 | 0.16 | 0.02±0.04 | 0.00 | 5.55 | 0.46±1.15 | 0.01 | 21.22 | 3.99±5.85 | 0.00 | 13.22 | 1.32±3.43 |
Dinophyceae | 0.00 | 0.23 | 0.02±0.06 | 0.00 | 0.25 | 0.02±0.06 | 0.00 | 7.34 | 0.68±1.40 | 0.00 | 4.81 | 0.70±1.27 |
Euglenophyceae | 0.00 | 0.14 | 0.20±0.31 | 0.00 | 0.57 | 0.07±0.11 | 0.00 | 0.20 | 0.04±0.04 | 0.00 | 4.79 | 0.38±1.02 |
Chlorophyll a (mg m-3) | 2.16 | 33.90 | 13.86±8.85 | 2.15 | 40.70 | 10.52±8.64 | 3.40 | 150.54 | 20.50±28.88 | 2.81 | 58.61 | 22.04±14.13 |
The Mann-Kendall test revealed no significant multiannual trends in the meteo-climatic variables considered nor in the water temperature and transparency during the study decade (Table
Results of the Mann-Kendall test for detection of long-term trends (2006–2015) in the environmental parameters (WEMOi, Western Mediterranean Oscillation index; Zmix/Zeu, mixing zone and euphotic zone ratio; Si-SiO4, silicate; P-PO4, orthophosphate; TP, total phosphorous; N-NO3, nitrate; N-NO2, nitrite; N-NH4, ammonia; DIN, dissolved inorganic nitrogen; TN, total nitrogen; TON, total organic nitrogen) in Bidighinzu Lake. Significant trends are in bold (S = Kendall score, it indicates the trend direction; p = significance; n = number of observations).
Winter | Spring | Summer | Autumn | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
S | p | n | S | p | n | S | p | n | S | p | n | |
WEMOi | 33 | 0.568 | 30 | 40 | 0.486 | 30 | -34 | 0.556 | 30 | 15 | 0.802 | 30 |
Air Temperature | 27 | 0.566 | 26 | 24 | 0.649 | 28 | -6 | 0.912 | 26 | 20 | 0.657 | 25 |
Rainfall | 38 | 0.440 | 27 | 20 | 0.721 | 29 | 53 | 0.303 | 28 | 20 | 0.707 | 28 |
Water Temperature | -17 | 0.544 | 24 | 2 | 0.986 | 30 | 52 | 0.469 | 35 | 21 | 0.620 | 24 |
Water Transparency | -21 | 0.444 | 24 | 62 | 0.274 | 30 | -19 | 0.797 | 35 | 45 | 0.271 | 24 |
Zmix/Zeu | 9 | 0.715 | 24 | 2 | 0.985 | 30 | 181 | 0.007 | 35 | 16 | 0.671 | 24 |
Si-SiO4 | -50 | 0.063 | 24 | 100 | 0.077 | 30 | -141 | 0.047 | 35 | -65 | 0.112 | 24 |
P-PO4 | -10 | 0.773 | 24 | 17 | 0.775 | 30 | -62 | 0.386 | 35 | -16 | 0.710 | 24 |
TP | -14 | 0.621 | 24 | -27 | 0.643 | 30 | -175 | 0.013 | 35 | -39 | 0.346 | 24 |
N-NO2 | -23 | 0.404 | 24 | -50 | 0.382 | 30 | 132 | 0.063 | 35 | 83 | 0.042 | 24 |
N-NO3 | 12 | 0.677 | 24 | -53 | 0.353 | 30 | 73 | 0.306 | 35 | 27 | 0.519 | 24 |
N-NH4 | -56 | 0.037 | 24 | -67 | 0.239 | 30 | -159 | 0.025 | 35 | -33 | 0.427 | 24 |
DIN | 10 | 0.733 | 24 | -157 | 0.005 | 30 | -161 | 0.023 | 35 | 35 | 0.399 | 24 |
TN | -6 | 0.850 | 24 | 103 | 0.069 | 30 | 113 | 0.112 | 35 | 63 | 0.124 | 24 |
TON | 32 | 0.163 | 24 | 128 | 0.027 | 30 | 221 | 0.040 | 35 | 113 | 0.031 | 24 |
Multiannual (2006–2015) variation of dissolved inorganic nitrogen (DIN) (upper panel) and of the contribution of nitrate (N-NO3), nitrite (N-NO2) and ammonium (N-NH4) to DIN (lower panel) in Bidighinzu Lake in summer. Each black dot represents a single sample and each column represents the mean value.
A significant increasing trend resulted for total phytoplankton cell density in summer during the study decade (Table
Multiannual (2006–2015) variation of total cell density (upper panel) and mean cell volume (lower panel) of the whole phytoplankton community in Bidighinzu Lake in summer. Each black dot represents a single sample and each column represents the mean value.
Multiannual (2006–2015) variation of the percentage contribution of all phytoplankton classes to the total cell density (upper panel) and mean cell volume (lower panel) of the whole phytoplankton community in Bidighinzu Lake in summer. BAC = Bacillariophyceae, CHL = Chlorophyceae, CHR = Chrysophyceae, CON = Conjugatophyceae, CRY = Cryptophyceae, CYA = Cyanophyceae, DIN = Dinophyceae, EUG = Euglenophyceae.
Multiannual (2006–2015) variation of total cell density (upper panels) and mean cell volume (lower panels) of Bacillariophyceae (A and B) and Cyanophyceae (C and D) in Bidighinzu Lake in summer. Each black dot represents a sample and each column represents the mean value.
Results of the Mann-Kendall test for detection of long-term trends (2006–2015) in the phytoplankton variables in Bidighinzu Lake. Significant trends are in bold (S = Kendall score, it indicates the trend direction; p = significance; n = number of observations).
Winter | Spring | Summer | Autumn | |||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
S | p | n | S | p | n | S | p | n | S | p | n | |
Total cell density | 24 | 0.300 | 24 | 106 | 0.065 | 30 | 175 | 0.009 | 34 | 43 | 0.236 | 24 |
Bacillariophyceae | 30 | 0.192 | 24 | -142 | 0.008 | 30 | 249 | 0.000 | 34 | 81 | 0.024 | 24 |
Chlorophyceae | 4 | 0.892 | 24 | 12 | 0.836 | 30 | -85 | 0.213 | 34 | -65 | 0.071 | 24 |
Chrysophyceae | 22 | 0.344 | 24 | 23 | 0.677 | 30 | 201 | 0.003 | 34 | 51 | 0.058 | 24 |
Cryptophyceae | -2 | 0.964 | 24 | 62 | 0.252 | 30 | 47 | 0.495 | 34 | -49 | 0.176 | 24 |
Conjugatophyceae | -1 | 1 | 24 | -140 | 0.007 | 30 | -212 | 0.002 | 34 | -99 | 0.006 | 24 |
Cyanophyceae | 60 | 0.008 | 24 | 130 | 0.015 | 30 | 167 | 0.014 | 34 | 65 | 0.071 | 24 |
Dinophyceae | 38 | 0.074 | 24 | 76 | 0.139 | 30 | -68 | 0.318 | 34 | 12 | 0.744 | 24 |
Euglenophyceae | 24 | 0.300 | 24 | 39 | 0.476 | 30 | -10 | 0.894 | 34 | -29 | 0.430 | 24 |
Mean cell volume | -18 | 0.444 | 24 | -105 | 0.063 | 30 | -129 | 0.030 | 34 | -9 | 0.821 | 24 |
Bacillariophyceae | -18 | 0.444 | 24 | 168 | 0.002 | 30 | -197 | 0.004 | 34 | -29 | 0.430 | 24 |
Chlorophyceae | 8 | 0.753 | 24 | 14 | 0.807 | 30 | 51 | 0.458 | 34 | 43 | 0.236 | 24 |
Chrysophyceae | 7 | 0.766 | 24 | 5 | 0.910 | 30 | -128 | 0.049 | 34 | 22 | 0.526 | 24 |
Cryptophyceae | 17 | 0.428 | 24 | 34 | 0.536 | 30 | -47 | 0.406 | 34 | 87 | 0.015 | 24 |
Conjugatophyceae | 25 | 0.235 | 24 | 46 | 0.064 | 30 | 112 | 0.072 | 34 | 129 | 0.000 | 24 |
Cyanophyceae | -29 | 0.166 | 24 | -142 | 0.005 | 30 | -195 | 0.004 | 34 | -71 | 0.048 | 24 |
Dinophyceae | -8 | 0.465 | 24 | 26 | 0.260 | 30 | 37 | 0.453 | 34 | 18 | 0.244 | 24 |
Euglenophyceae | -3 | 0.921 | 24 | -41 | 0.378 | 30 | -7 | 0.915 | 34 | 22 | 0.526 | 24 |
Total cell biomass | 16 | 0.599 | 24 | 23 | 0.695 | 30 | 89 | 0.192 | 34 | 17 | 0.691 | 24 |
Bacillariophyceae | 24 | 0.420 | 24 | -141 | 0.012 | 30 | 141 | 0.038 | 34 | 89 | 0.029 | 24 |
Chlorophyceae | -6 | 0.861 | 24 | 21 | 0.721 | 30 | -85 | 0.213 | 34 | -53 | 0.197 | 24 |
Chrysophyceae | 6 | 0.861 | 24 | 30 | 0.602 | 30 | 121 | 0.075 | 34 | 111 | 0.006 | 24 |
Cryptophyceae | -18 | 0.551 | 24 | 107 | 0.059 | 30 | 49 | 0.477 | 34 | -25 | 0.551 | 24 |
Conjugatophyceae | 2 | 0.972 | 24 | -143 | 0.009 | 30 | -166 | 0.014 | 34 | -53 | 0.197 | 24 |
Cyanophyceae | 20 | 0.505 | 24 | 67 | 0.239 | 30 | 13 | 0.859 | 34 | 25 | 0.551 | 24 |
Dinophyceae | 28 | 0.323 | 24 | 89 | 0.101 | 30 | -64 | 0.348 | 34 | 28 | 0.486 | 24 |
Euglenophyceae | 16 | 0.599 | 24 | -8 | 0.900 | 30 | -19 | 0.790 | 34 | -7 | 0.882 | 24 |
Chlorophyll a | 4 | 0.892 | 24 | 15 | 0.803 | 30 | 9 | 0.909 | 34 | -139 | 0.100 | 24 |
Considering the mean cell volume of the whole summer phytoplankton community, a multiannual decreasing trend was detected in the total assemblage, with a strong decrement in Bacillariophyceae and Cyanophyceae (Table
No significant multiannual trends were observed for total phytoplankton biomass and chlorophyll a (Table
Opposite significant trends were observed for the Cyanophyceae Chroococcales and Bacillariophyceae Centrales: cell density increased (Mann-Kendall test: S = 197, p = 0.004, n = 34 and S = 253, p < 0.001, n = 34, respectively) while their cell volume decreased (Mann-Kendall test: S = -179, p = 0.008, n = 34 and S = -205, p = 0.002, n = 34, respectively). In addition, a multiannual decrement in summer was detected for the Cyanophyceae Nostocales only in cell density (Mann-Kendall test: S = -102, p = 0.040, n = 34; Suppl. materials
Chroococcales were mainly represented by Aphanocapsa sp., Merismopedia sp. and Chroococcus sp. (mean cell volume of 0.76 µm3, 1.12 µm3 and 77.15 µm3, respectively) at the beginning of the study decade and by Aphanothece sp., Aphanocapsa spp. and Merismopedia tenuissima Lemmermann (mean cell volume of 1.30 µm3, 0.44 µm3 and 0.54 µm3, respectively) at the end. Amongst Nostocales, Dolichospermum flos-aquae (Brébisson ex Bornet & Flahault) P. Wacklin, L. Hoffmann & J. Komárek (mean cell volume of 73 µm3) and Dolichospermum spiroides (Klebhan) Wacklin, L. Hoffmann & Komárek (mean cell volume of 519 µm3) determined the highest cell density values at the beginning and at the end of the considered period, respectively. Centrales were mainly represented by Cyclotella spp. and Aulacoseira granulata (Ehrenberg) Simonsen (mean cell volume of 1035 µm3 and 982 µm3, respectively) at the beginning of the study and by A. granulata and Aulacoseira granulata var. angustissima (Otto Müller) Simonsen (mean cell volume of 608 µm3 and 180 µm3, respectively) during the last years.
The results of the RDAs showed that, in summer, all environmental variables accounted for 57.8% and 53.8% of the variation in the 2006–2015 phytoplankton total cell density and volume, respectively. These results were confirmed when the years 2010 (exceptional peak of the total phytoplankton density) and 2015 (breaking of stratification due to the activation of the aeration system) were excluded from the analysis.
DIN (F = 4.21, p = 0.004), N-NH4 (F = 3.97, p = 0.002) and TP (F = 3.18, p = 0.007) were significant environmental variables, which provided a greater explanation for the variability in summer total phytoplankton cell densitiy, followed by Zmix/Zeu (F = 2.62, p = 0.029) (Figure
Results of Redundancy Analysis on the relationships between environmental explanatory variables (vectors) and phytoplankton variables (responses), considering (A) the total phytoplankton cell density and (B) the mean phytoplankton cell volume data during the decade 2006–2015 in Bidighinzu Lake in summer. Eigenvalues of the first two axes are indicated by λ1 and λ2. Asterisks indicate statistical significance (*p < 0.05; **p < 0.01; ***p < 0.001) of environmental variables. WEMOi, Western Mediterranean Oscillation index; AirTem, air temperature; Rain, rainfall; Zmix/Zeu, mixing zone and euphotic zone ratio; WatTem, water temperature; Si-SiO4, silicate; P-PO4, orthophosphate; TP, total phosphorous; N-NO3, nitrate; N-NO2, nitrite; N-NH4, ammonia; DIN, dissolved inorganic nitrogen; TN, total nitrogen; TON, total organic nitrogen; Bac, Bacillariophyceae; Chl, Chlorophyceae; Chr, Chrysophyceae; Con, Conjugatophyceae; Cry, Cryptophyceae; Cya, Cyanophyceae; Dino, Dinophyceae; Eug, Euglenophyceae; TotDens, total phytoplankton density; MeanVol, mean cell volume of the whole phytoplankton community.
TP (F = 3.34, p = 0.004), DIN (F = 2.82, p = 0.007) and N-NH4 (F = 3.18, p = 0.009), followed by water temperature (F = 3.52, p = 0.027), provided a greater explanation for the variability in summer mean phytoplankton cell volume (Figure
A significant decreasing trend (Mann-Kendall test: S = -949, p < 0.001, n = 84) was observed for the WEMO index in summer during the period 1988–2015. One-way ANOVA highlighted significant differences in the WEMO index, TP and P–PO4 amongst the four time-cycles of samplings (i.e. 1988–1989, 1994–1997, 2003, 2006–2015; Table
Results of the one-way ANOVA (F-test and p-value) to assess significant differences in selected environmental and phytoplankton variables amongst sampling year cycles (1988–1989, 1994–1997, 2003, 2006–2015) in summer in Bidighinzu Lake (WEMOi, Western Mediterranean Oscillation index; Zmix/Zeu, mixing zone-euphotic zone ratio; Si-SiO4, silicate; P-PO4, orthophosphate; TP, total phosphorous; N-NO3, nitrate; N-NO2, nitrite; N-NH4, ammonia; DIN, dissolved inorganic nitrogen; TN, total nitrogen; TON, total organic nitrogen, ns = not significant).
F | p | F | p | F | p | |||
WEMOi | 7.83 | *** | Total cell density | 1.76 | ns | Mean cell volume | 3.60 | * |
Water Temperature | 1.03 | ns | Bacillariophyceae | 10.92 | *** | Bacillariophyceae | 77.56 | *** |
Water Transparency | 1.32 | ns | Chlorophyceae | 11.27 | *** | Chlorophyceae | 406 | *** |
Zmix/Zeu | 1.24 | ns | Chrysophyceae | 13.35 | *** | Chrysophyceae | 0.15 | ns |
Si-SiO4 | 2.26 | ns | Cryptophyceae | 20.45 | *** | Cryptophyceae | 46.96 | *** |
P-PO4 | 9.44 | *** | Conjugatophyceae | 9.44 | *** | Conjugatophyceae | 0.89 | ns |
TP | 7.33 | *** | Cyanophyceae | 2.01 | ns | Cyanophyceae | 123.3 | *** |
N-NO2 | 0.55 | ns | Dinophyceae | 9.47 | *** | Dinophyceae | 9.43 | *** |
N-NO3 | 1.45 | ns | Euglenophyceae | 6.02 | ** | Euglenophyceae | 3.91 | * |
N-NH4 | 0.25 | ns | ||||||
DIN | 0.33 | ns | ||||||
TN | 2.21 | ns | ||||||
TON | 1.17 | ns |
Variation of the Western Mediterranean Oscillation index (WEMOi), total phosphorous (TP), mean cell volume of the whole phytoplankton community (Total phytoplankton) and mean Cyanophyceae volume during the four time cycles of samplings (A = 1988–1989, B = 1994–1997, C = 2003, D = 2006–2015) in summer in Bidighinzu Lake. The lowest, second lowest, middle, second highest and highest lines in the box plots represent the 10th percentile, 25th percentile, median, 75th percentile and 90th percentile, respectively. Means are represented by black dots.
Significant variations in land cover and land use have been assessed in the Bidighinzu Lake’s watershed during the last 20 years. The GIS analyses of CORINE maps for the time series 1990, 2000 and 2012, highlighted a decrement in Agricultural Area of about 7.2% from 1990 (32.59 km2) to 2000 (30.25 km2) and of a further 16.8% from 2000 to 2012 (25.17 km2), with a total decrement of about 23% from 1990 to 2012. On the other hand, Natural and semi-Natural Areas increased by about 14.6% from 1990 (16.63 km2) to 2000 (19.06 km2) and by a further 25.3% from 2000 to 2012 (23.89 km2), with a total increment of about 44% from 1990 to 2012. A noteworthy variation in Urban Area was also assessed with an increase of about 2.5% from 1990 (1.61 km2) to 2000 (1.65 km2) and of a further 4.8% from 2000 to 2012 (1.73 km2), with a total increment of about 7.5% from 1990 to 2012.
This work showed that, during the decade 2006–2015, significant multiannual changes occurred in both environmental and phytoplankton variables in Bidighizu Lake, more in summer than during the other seasons. Our results confirmed those reported from other LTER studies in Sardinian reservoirs (
We observed strong decreases in summer concentrations of various nutrients, i.e. Si-SiO4, TP, DIN and N-NH4 and a significant but weaker increment of TON values during the decade 2006–2015 in Bidighizu Lake. It has been previously documented that the phosphorous reduction in summer has been on-going since 1978, immediately after the application of recovery actions for the reservoir and it was most likely favoured by the diversion of urban and industrial wastes being initiated in 1987 (
Explaining how the dissolved nitrogen forms vary in lakes is not straightforward as they depend upon variations in natural and pollutant sources and a variety of physical, biological and metabolic features of the lake (
Relevant changes in summer multiannual phytoplankton dynamics were observed simultaneously to the summer nutrient reduction in Bidighinze Lake during the decade 2006–2015. The total phytoplankton cell density increased significantly, whereas the mean cell volume of the whole phytoplankton community decreased significantly. Consequently, it is not surprising that the total phytoplankton biomass and chlorophyll a concentration did not show any significant trend in the same period. The phytoplankton classes that contributed more to total density in the analysed decade remained mainly Cyanophyceae, followed by Chlorophyceae and Bacillariophyceae as observed in the previous years (
Statistical analysis revealed a strong relationship between the interannual patterns of algal nutrients and of total cell density and mean cell volume of the whole phytoplankton community at the Bidighinzu Lake in summer. Specifically, the summer TP and DIN (mainly N-NH4) reduction affected, significantly and negatively, the summer total cell density. On the other hand, summer TP and DIN reduction significantly influenced the summer mean cell volume in a positive way. The decrement in phytoplankton size at lower nutrient concentrations was observed elsewhere, such as in another eutrophic Sardinian reservoir (Temo Lake,
In the hypertrophic Lake Arancio (Sicily, Italy), as well as in many other Sicilian reservoirs, nutrients have never been observed to play an important role in determining the structure of the phytoplankton community (
The strong size reduction of marine phytoplankton under increasing ocean warming has also been well documented, although without univocal evidence (
A significant multiannual decreasing trend in nutrient concentrations was detected in summer in the Bidighinzu Lake simultaneously with reduced anthropic pressure in its watershed. These environmental changes significantly affected the phytoplankton community of this Mediterranean reservoir, favouring a strong increment in the density of smaller Bacillariophyceae and Cyanophyceae taxa. This increment led to a significant multiannual increasing trend in total phytoplankton cell density and a strong multiannual decrease in mean phytoplankton cell volume. In addition, the variations of Zmix/Zeu and of water temperature in summer favoured smaller phytoplankton taxa, although their role in structuring phytoplankton communities was statistically weaker compared to that of nutrients. We can not rule out that the consumer pressure may also have acted on the phytoplankton community of Bidighinzu Lake, as observed in other environments (
This work confirms the importance of acquiring long-term ecological data in studies on phytoplankton to understand the temporal evolution of aquatic ecosystems in relation to natural and anthropogenic forces. The affirmation of smaller phytoplankton cells in Bidighinzu Lake suggests a shift of the system towards a less energy-efficient trophic web based on smaller and lower-quality prey for grazing zooplankton and planktivorous fish. The ecological changes we observed in the reservoir were most probably due to the complex and synergic interactions between the investigated environmental variables related to changing anthropic pressures and climate variability. Considering the need and scarcity of high quality water in semi-arid regions and the paucity of studies on Mediterranean reservoirs, our findings provide useful information for our understanding of these crucial ecosystems and for their management and conservation, thus adding greater value to the LTER-Italy network.
The authors thank all the colleagues of the Aquatic Ecology group of the University of Sassari for chemical, physical and nutrient analyses. The authors are also grateful to the Subject Editor of the present Special Issue, Dr. Maria Grazia Mazzocchi, for her precious and scrupulous revision of this article.