Lagoons are naturally formed shallow waters found in coastal areas of the oceans and separated from the main body of water by sand and patch reefs (Kjerfve 1994). They are important forms in the marine environment as they provide shelter, feeding and breeding grounds for many organisms. However, these unique formations are at risk of deterioration caused by climate change and heavy pollution due to human activities, urbanization and industrialization. These factors are responsible not only for chemical and biological deterioration, but also for changes in the microbial balance of water in these areas (Scialabba 1998; Fiandrino et al. 2003; Yetis & Selek 2015; Freeman et al. 2019; Zoppini et al. 2020).
The microbial environment of seawater is composed of naturally occurring microorganisms and is generally not considered hazardous to the health of humans and marine organisms. However, discharges from various sources, such as sewage, ship ballast, domestic and industrial effluents, can lead to the introduction of fecal-derived microorganisms that pose a threat by altering the microbial ecology of seawater (Mansilha et al. 2009; Cabral 2010). Coliforms and fecal coliforms, along with
Çardak Lagoon is an important coastal lagoon located on the southern coast of the Çanakkale Strait, the Marmara Sea, Turkey. A rich natural habitat has existed in and around the lagoon, the condition of which has deteriorated over the years and is now protected by the relevant regulations of the Ministry of Environment and Urbanization of Turkey. Before the deterioration and exposure to pollution, the lagoon supported commercial fish species, such as
The study area – Çardak Lagoon – is located on the southern coast of the Çanakkale Strait (Fig. 1). The lagoon is the third largest lagoon in the Turkish Strait system, with an area of 1.2 km2. The lagoon has a coastline of 4.3 km and an average depth of 1.3 m depth (Calıskan et al. 2011; Cataudella et al. 2015). The study area was divided into seven sampling locations (also referred to as sites), one of which was used as a reference site. The reference site was located outside the lagoon to indicate the quality of water entering the system. The coordinates and depths of the sampling locations are summarized in Table 1.
Study area
Coordinates and maximum depths of the sampling locations
Sites | Coordinates | Max depth (cm) | |
---|---|---|---|
1 | 40°22′906″N | 26°43′103″E | 150 |
2 | 40°23′053″N | 26°43′264″E | 100 |
3 | 40°23′203″N | 26°43′491″E | 150 |
4 | 40°23′345″N | 26°43′399″E | 100 |
5 | 40°23′278″N | 26°42′988″E | 180 |
6 | 40°23′236″N | 26°42′800″E | 150 |
7 (reference) | 40°22′931″N | 26°42′768″E | 100 |
Water sampling for all analyses was conducted seasonally at the selected sites between October 2018 and June 2019. Samples were collected from the surface water (10–30 cm) at each site using a 1 l sterilized amber glass bottle. The collected water samples were transported to the laboratory at 2–7°C within 4 h.
Physicochemical parameters such as temperature (°C), salinity (PSU), dissolved oxygen (mg l−1), pH and oxidation-reduction potential (ORP) were measured in situ using a YSI 650 MDS multiparameter water quality meter.
Chemical oxygen demand (COD) was determined using the open reflux method. Standard methods for the examination of water and wastewater (Eaton & Franson 2005) were used for spectrophotometric determination of nitrite (NO2−), nitrate (NO3−), ammonium (NH4+), phosphate (PO4−) and SiO2− levels (Strickland & Parsons 1972).
Microbiological analyses were performed according to the most probable number (MPN) and plate count methods (FDA 1998; APHA 2005). To count coliforms, peptone-diluted water samples were inoculated in Lauryl Sulfate Tryptose (LST) Broth (Merck) and incubated at 37°C for 20 h. Positive tubes indicating turbidity and gas production were transferred to Brilliant Green Bile Lactose (BGBL) Broth (Merck) and levels of total coliforms (TC) were determined after incubation of inoculated tubes for 36 h at 37°C. Fecal coliforms were assessed after transferring loop full samples from total coliform positive tubes into
Seasonal differences between the sampling locations in terms of bacterial levels and environmental factors were compared using one-way ANOVA. The correlation between the bacterial levels and the factors were determined using Pearson's correlation analysis in Minitab 17 (Minitab, LLC, USA). The significance level for differences between the factors was set at 0.05.
In this study, total coliform, fecal coliform,
Values of environmental parameters at seven sites in each season are presented in Table 2.
Summary of environmental data by season
Temp. | Sal. | pH | O2* | COD* | ORP | PO4-P* | TP* | NO2+N3* | NH4* | TN* | SiO2* | ||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Oct. 18 | Min. | 13.25 | 20.74 | 7.85 | 6.40 | < 40.00 | 70.30 | < 0.01 | 0.015 | 0.014 | < 0.01 | 0.20 | 0.03 |
Max | 16.89 | 20.81 | 8.35 | 9.51 | 277.00 | 91.00 | < 0.01 | 0.195 | 0.195 | < 0.01 | 0.99 | 0.55 | |
Mean | 14.77 | 20.78 | 8.14 | 8.08 | 197.83 | 80.41 | < 0.01 | 0.019 | 0.129 | < 0.01 | 0.61 | 0.34 | |
SD | 1.15 | 0.02 | 0.17 | 1.13 | 84.92 | 7.78 | n.a. | 0.004 | 0.061 | n.a. | 0.32 | 0.19 | |
Feb. 19 | Min. | 7.57 | 22.74 | 7.78 | 6.33 | 125.00 | −87.60 | < 0.01 | 0.016 | 0.060 | < 0.01 | 0.10 | 0.25 |
Max | 8.72 | 23.47 | 8.27 | 8.95 | 296.00 | −74.50 | < 0.01 | 0.025 | 0.120 | < 0.01 | 0.40 | 0.60 | |
Mean | 7.99 | 24.40 | 8.16 | 7.46 | 178.86 | −83.37 | < 0.01 | 0.018 | 0.086 | < 0.01 | 0.23 | 0.39 | |
SD | 0.44 | 0.62 | 0.17 | 0.91 | 59.18 | 4.34 | n.a. | 0.004 | 0.024 | n.a. | 0.11 | 0.14 | |
Apr. 19 | Min. | 13.7 | 22.14 | 8.04 | 5.90 | < 40.00 | −99.80 | < 0.01 | 0.020 | 0.025 | < 0.01 | 0.20 | 0.05 |
Max | 17.3 | 22.78 | 8.45 | 8.20 | 95.00 | −78.70 | 0.030 | 0.070 | 0.085 | < 0.01 | 0.60 | 0.25 | |
Mean | 15.5 | 22.54 | 8.31 | 6.48 | 80.75 | −92.24 | 0.025 | 0.040 | 0.059 | < 0.01 | 0.44 | 0.17 | |
SD | 1.44 | 0.22 | 0.14 | 0.82 | 28.54 | 7.51 | 0.006 | 0.021 | 0.021 | n.a. | 0.18 | 0.06 | |
June 19 | Min. | 24.07 | 20.17 | 8.12 | 7.21 | < 40.00 | −111.0 | < 0.01 | 0.040 | 0.015 | < 0.01 | 0.15 | 0.17 |
Max | 27.34 | 22.17 | 8.56 | 8.47 | 106.00 | −88.00 | 0.030 | 0.170 | 0.045 | < 0.01 | 0.33 | 1.50 | |
Mean | 25.67 | 21.04 | 8.30 | 7.84 | 74.00 | −100.61 | 0.023 | 0.097 | 0.029 | < 0.01 | 0.21 | 0.83 | |
SD | 1.13 | 0.75 | 0.15 | 0.45 | 24.52 | 8.54 | 0.005 | 0.059 | 0.010 | n.a. | 0.06 | 0.63 |
– mg l−1; n.a. – not applicable; St. – sites; Temp. – temperature (°C); Sal. – salinity (PSU); COD – chemical oxygen demand; ORP (mV) – oxidation-reduction potential; TP – total phosphate; TN – total nitrogen; SD – standard deviation
Levels of bioindicator microorganisms and their threshold levels are presented by site and season in Figure 2.
Summary graphs of bioindicator bacteria levels with their national and international threshold levels by season and location
The levels of detectable total coliform bacteria fluctuated during the study between 1.85 and 4.04 log10 cfu 100 ml−1. The highest levels of coliforms were detected at site 3 in the summer season. The level of total coliforms determined in samples collected from site 3 in October 2018 was higher than the hitherto applied national threshold value (4.0 log10 cfu 100 ml−1) for bathing water (Anonymous 2006). The minimum and maximum detectable levels of fecal coliforms were in the range of 1.47–4.04 log10 cfu 100 ml−1. The highest level of fecal coliforms was also found in samples collected from site 3 in October 2018. The national threshold level for fecal coliforms (3.03 log10 cfu 100 ml−1) was also exceeded in these samples (Anonymous 2006). The minimum and maximum detectable
Changes in bioindicator bacteria and environmental factor levels at the sampling sites and their correlations with all parameters in the autumn season are summarized in Figure 3.
(A) Changes in total coliform (TC), fecal coliform (FC),
The primary factors affecting the survival of bacterial cells in seawater columns, such as temperature, salinity, pH and O2, were determined in the range of 13.2–16.9°C, 20.7–20.9 PSU, 7.85–8.36 and 6.40–9.51 mg l−1, respectively. The lowest oxygen level (6.40 mg l−1) was determined at site 3, which was characterized by the highest bacterial levels. The correlation between O2 and bacterial levels, and between temperature (for site 7) and TC and FC were significant (
Changes in bioindicator bacteria and environmental factor levels at the sampling sites and their correlations with all parameters in the winter season are summarized in Figure 4.
(A) Changes in total coliform (TC), fecal coliform (FC),
Values of physiochemical parameters – temperature, salinity, pH and O2 – were in the following ranges: 7.57–8.72°C, 22.85–24.40 PSU, 7.78–8.27 and 6.33–8.95 mg l−1, respectively. Differences between the parameters at the sampling sites and the correlation between the parameters and microorganism levels were insignificant in the winter season (
Changes in bioindicator bacteria and environmental factor levels at the sampling sites and their correlations with all parameters in the spring season are summarized in Figure 5.
(A) Changes in total coliform (TC), fecal coliform (FC),
The values of temperature, salinity, pH and O2 were determined as 13.70–17.30°C, 22.14–22.78 PSU, 8.04–8.45 and 5.90–8.20 mg l−1, respectively. With the exception of the O2 level at site 7 (
Changes in bioindicator bacteria and environmental factor levels at the sampling sites and their correlations with all parameters in the autumn season are summarized in Figure 6.
(A) Changes in total coliform (TC), fecal coliform (FC),
The values of temperature, salinity, pH and O2 were determined as 24.07–27.34°C, 20.17–22.17 PSU, 8.12–8.56 and 7.50–8.47 mg l−1, respectively. Differences between environmental parameters at each site and their correlations with microorganism levels were insignificant (
Summer recreational activities in the study area continue through October, provided temperatures are favorable (Fig. 3). Sites 1, 3 and 5 are located at the shoreline of the lagoon. Therefore, the effects of potential discharges from the shore were observed during the study period, especially at sites 1 and 3. The detection of fecal coliforms and
Elevated bacterial contamination was still observed in the winter season at sites 1 through 5. However, fecal contamination was not determined in samples from sites 6 and 7. As previously mentioned, site 7 was the reference site located outside the lagoon. Therefore, the absence of any bacteria may be related to lower temperatures, varied salinity and pH, precipitation, water flows, reduced recreational activity, and marine traffic in the harbor. On the other hand, the continued fecal contamination inside the lagoon may indicate that sewage discharge is an intense and persistent problem in the winter season, despite reduced temperatures. This situation is most likely related to flushing and upwelling effects of both stormwater runoffs and wind effects that may play an important role in transporting additional bacteria into the lagoon. In addition, resuspension of settled bacterial cells from sediment to water may also help these bacteria to maintain prolonged survival via suspended particles (An et al. 2002; Medema et al. 2003; Servais et al. 2007; Hong et al. 2010). Furthermore, the transmission of fecal contamination at sites 1 and 3 during winter sampling is thought to be related to human-induced coliforms, because fecal streptococci were not detected at these sites, even though they are more resistant to environmental changes (Sinton et al. 1993; Rodriguez & Cunha, 2017). Among the chemical quality indicators, the levels of total phosphate and total nitrogen, which were at higher levels at sites 1 and 3 compared to other sites, indicated that domestic discharge may be concentrated in this part of the lagoon. Moreover, it was observed that a potential discharge may be an important factor in changing the water quality in the winter season, despite the evenly distributed precipitation and stormwater runoff flowing into the lagoon.
In the presented study, the spring was the season with the lowest fecal contamination at all sites except sites 3 and 7. Bioindicator bacteria were not found in samples collected at sites 5 and 6 that are located inside the lagoon and away from sites 1, 3 and 7. Salinity and pH were highly negatively correlated with all bacterial groups in the spring season. The observed negative correlations of pH and salinity with all bacterial groups can be explained by the negative synergic effect of increased surface evaporation and lack of precipitation as a consequence of elevated temperature in the summer season. While the differences in temperature between the seasons were significant (
Lagoons are important ecosystems due to their unique formation in coastal areas. Important studies were conducted in the Mediterranean aimed at monitoring the pollution of these unique systems. Bacterial levels in lagoons can vary from region to region due to climate differences, environmental factors dependent on geographical conditions, discharges, and other uncontrolled factors. In this study, however, coliform levels were similar to those reported by Zafiri et al. (2009) who determined the minimum and maximum levels in Koutavos Lagoon (Kefalonia, Greece) between winter and summer months as 2.0 and 2.65 log10 cfu 100 ml−1, respectively. Furthermore, our results were slightly different from the findings of another study conducted at Bizerte Lagoon (Tunisia) in the Southern Mediterranean, where coliform levels in lagoon water from autumn to summer ranged from 1.0 to 2.0 log10 cfu ml−1 (Boukef et al. 2012). In both of these studies, bacterial levels in lagoon water were affected mainly by environmental factors. In our study, summer was the season most exposed to bacterial pollution. A similar finding was reported by Avramidis et al. (2017), who emphasized that bacterial levels (4.08–4.30 log10 cfu 100 ml−1) increased during warmer months due to the lack of precipitation, but were not correlated with months owing to the presence of contamination sources in the lagoon.
Lagoons are important coastal areas as they provide refuge, breeding and feeding habitats for many marine species. Çardak Lagoon, one of the most important lagoons in the Turkish Strait system, has experienced chemical and bacterial pollution in recent years. In this study, bacterial contamination levels were determined seasonally and the results were related and correlated with environmental factors. It was concluded that the pollution in the lagoon originates mainly from potential human-induced discharges in and/or around the lagoon. Moreover, the pollution varied seasonally depending on changes in environmental parameters, which showed significant correlations. The results show that bacterial pollution in the lagoon is at elevated levels compared with the national and international threshold values, and if it continues at this rate, more severe deterioration of the lagoon is inevitable. For this reason, it is important that lagoons facing pollution problems, such as Çardak Lagoon, are closely monitored to protect their ecosystems and surrounding environment.