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Evaluating the coastal ecosystem status of two Western and Eastern Mediterranean islands using the seagrass Posidonia oceanica
Ecological Indicators 108 (2020) 105734
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Evaluating the coastal ecosystem status of two Western and Eastern Mediterranean islands using the seagrass Posidonia oceanica
T
A. Güreşena, , G. Pergentb, S.O. Güreşena, Y. Aktana ⁎
a b
University of Istanbul, Faculty of Aquatic Sciences, Turkey University of Corsica, Faculty of Sciences, France
ARTICLE INFO
ABSTRACT
Keywords: Posidonia oceanica Biological quality element Biotic index Ecological status Monitoring
Mediterranean seagrass Posidonia oceanica is used as a ‘biological quality element’ in the long-term monitoring programmes of the Water Framework Directive (WFD 2000/60/EC) for the evaluation of ecological status of coastal waters. Due to its low resilience to anthropogenic pressures, P. oceanica meadows have disappeared irreversibly along some of the Mediterranean coasts. The main objective of this survey, is therefore to compare the ecological status of coastal waters and P. oceanica meadows in two islands from Eastern (Gökçeada, Turkey) and Western (Corsica, France) Mediterranean Sea based on the Posidonia Biotic Index (BiPo) and the Vitality Index besides concentrating on: (i) their consistency in different environmental conditions present in the Mediterranean Sea, (ii) their effectiveness to discriminate the ecological status of coastal waters in relation to different anthropogenic pressures and (iii) their application capacity to initiate long-term data series for monitoring the evolution of the meadows in less evaluated regions (i.e. from the Eastern Mediterranean). The measurements of several descriptors of P. oceanica are interpreted based on the BiPo and the Vitality indices for 2 regions; 9 sites from Gökçeada and 15 sites from Corsica exposed to different human pressures. The mean BiPo and Vitality indices are higher in Corsica than in Gökçeada, where the values correspond to a “good” status for Corsica and a “moderate” status in Gökçeada. The application of these biotic indices showed their feasibility and comparability to assess the ecological status in different environmental conditions. Significant relationships between the scores of Anthropization index and the EQR values of the BiPo index (r = −0.745, p < 0.01) and the Vitality index (r = −0.702, p < 0.01) highlighted their efficiency to determine the seagrass degradation in the sites subjected to higher pressure levels. It can be assumed that this study initiates the development of longterm data series and also meets the essential data deficiency in less evaluated regions.
1. Introduction Changing climate conditions and recent anthropogenic pressures on coastal regions, cause irreversible regressions and habitat losses of the seagrass meadows (Ruiz et al., 2001; Duarte, 2002; Ruiz and Romero, 2003; Boudouresque et al., 2009; Waycott et al., 2009; Telesca et al., 2015). Apart from these, wastewater discharges, aquacultural, agricultural and recreational activities (Manzanera et al., 1995; Boudouresque et al., 2012) cause water quality degradation as eutrophication, harmful algal blooms, high turbidity and mucilage formation (Innamorati et al., 2001; Precali et al., 2005). Therefore, the Water Framework Directive (WFD 2000/60/EC) has been established (EC, 2000) with the aim of conserving and managing of all types of water bodies for a sustainable development. The WFD is
also concentrated on the evaluation of the coastal ecosystem status through angiosperm classification practices in a wide spatial extent in order to reach “good” ecological status for all types of waterbodies by 2020 (EC, 2000). As a common representative species of the angiosperms in the Mediterranean Sea in terms of abundance (Med-GIG, 2011), Posidonia oceanica (Linnaeus) Delile is used as a “biological quality element” in the long-term monitoring programmes implemented by the WFD (Pergent et al., 1995; Ruiz and Romero, 2003; Balestri et al., 2004; Pergent-Martini et al., 2005; Boudouresque et al., 2009; Montefalcone, 2009). Various biotic indices using P. oceanica, have been developed to assess the ecological status in general and in a wide spatial extent as much as possible (A Multivariate Index_POMI by Romero et al., 2007;
⁎ Corresponding author at: Department of Marine and Freshwater Resources and Management, Faculty of Aquatic Sciences, University of Istanbul, 34134 Istanbul, Turkey. E-mail address: [email protected] (A. Güreşen).
https://doi.org/10.1016/j.ecolind.2019.105734 Received 22 February 2019; Received in revised form 9 September 2019; Accepted 12 September 2019 1470-160X/ © 2019 Elsevier Ltd. All rights reserved.
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Fig. 1. The sites of Gökçeada and Corsica considered for the application of the BiPo and the Vitality indices.
INTERREG Posidonia Programme_POSID by Pergent et al., 2007; Valencian CS by Fernandez-Torquemada et al., 2008; Rapid Easy Index_PREI by Gobert et al., 2009; Biotic Index_BiPo by Lopez y Royo et al., 2010). In accordance with the WFD requirements, their common objectives are to obtain the descriptors of the relevant index in order to quantify the ecological quality ratio (EQR) that compares the status of a “biological quality element” both in a specific water body and in a pristine area (EC, 2000). The main objective of this survey is to compare the ecological status of coastal waters and P. oceanica meadows in two islands from the Eastern (Gökçeada, Turkey) and the Western (Corsica, France) Mediterranean Sea based on the Posidonia Biotic Index (BiPo) and the Vitality Index. The study will concentrate on: (i) the consistency of these indices in different environmental conditions present in the Mediterranean Sea, (ii) the effectiveness of these indices to discriminate the ecological status of coastal waters in relation to different anthropogenic pressures and (iii) the application capacity of these indices to initiate long-term series data for monitoring the evolution of the meadows and related environment in less evaluated regions.
The region is also affected by tourism pressures in the summer season (9 000–390 000 inhabitants). Corsica Island (42°4′8.55″N–9°4′55.82″E), one of the five largest islands of the Mediterranean Sea (8 680 km2), located in the Northwestern Basin, is characterized by extensive P. oceanica meadows (53 736 ha) and moderate human pressure with less than 350 000 inhabitants and very few industrial activities (Valette-Sansevin et al., 2015). 2.2. Evaluation of the anthropogenic pressures Anthropogenic pressures are evaluated with the combination of techniques used in various studies on the assessment of human-induced pressures on coastal ecosystems (Gobert et al., 2009; Lopez y Royo et al., 2009a; Bermejo et al., 2014; Pinedo et al., 2015). Therefore anthropization index is calculated within this study as the sum of seven pressure types: aquaculture (number, km distance from the study site), industrial development (type, km distance from the study site), agriculture (landuse), tourism (activities, hotels), fishing (activity type, number of boats), commercial port (harbour traffic, km distance from the study site) and urbanization (landuse, wastewater discharge, population density). These seven pressures in each site, are evaluated by quantifying in a 3 km radius circle through the satellite images and census data since the sites are approximately 5 km far from each other. Then they are classified from 0 (none impact) to 5 (high impact) and the final class scores for each pressure are summed up in order to determine the anthropization degree of each site that can be easily used by coastal managers (Gobert et al., 2009).
2. Material and methods 2.1. Study sites Study sites correspond to representative islands from the Eastern Basin (Gökçeada) and North-western Basin (Corsica) of the Mediterranean Sea, even if their size is rather different. Gökçeada (40°10′10.19″N–25°50′13.93″E) is the largest island of Turkey (289 km2); located in the North Aegean Sea, it has distinct hydrological characteristics comparing to Western Mediterranean Sea due to the Turkish Straits Current System. Salinity (38.8–39.0‰) in the deep reflects Levantene waters whereas; brackish waters in the surface reflect the Black Sea waters (Ignatiades, 2005; Siokou-Frangou et al., 2009). As a result, stenohaline Posidonia oceanica meadows (about 400 ha) resist to maintain a healthy life-span around Gökçeada coasts.
2.3. Sampling design Data collection has been conducted by SCUBA diving in 2 regions: 9 sites from Gökçeada and 15 sites from Corsica, exposed to different environmental pressures (Fig. 1). In order to assess the ecological status, several descriptors of Posidonia oceanica are measured in two 2
Ecological Indicators 108 (2020) 105734
< 119 ((X/119) × 0.225) + 0.1
< 481
152–119 ((X-119)/33)x0.225) + 0.325
651–481
N/a
< 172 ((X/172) × 0.225) + 0.1 239–172 ((X-172)/67) × 0.225) + 0.325
N/a 0.05
Regressive limits recent dead matte 0.21 Sparse limits < 15% cover, % plagio N/a 0.44
31–25 ((X-25)/6) × 0.225) + 0.55
Sharp limits < 70% cover and < 70% plagio 0.66
339–239 ((X-239)/100) × 0.225) + 0.55
200–152 ((X-152)/48) × 0.225) + 0.55
812–651
> 31 ((X-31)/7) × 0.225) + 0.775
Progressive and erosive limits > 70% cover or > 70% plagio 0.89
> 339 ((X-339)/260) × 0.225) + 0.775
> 200 ((X-200/133) × 0.225) + 0.775
> 812
1
599 1
310 1
Values Supporting parameters EQR′
Values (shoots m2) EQR′
Values (cm shoot−1) EQR′
Values (mm)
Lower limit type
Shoot density
Shoot leaf surface
Or shoot length
3. Results The indices and the relevant descriptors measured, are reported for each site in Table 3. According to the BiPo index, the ecological status of Gökçeada varies between “poor” and “good” with an average value of “moderate” (EQR BiPo = 0.44 ± 0.05), while the ecological status of the Corsica varies between “moderate” and “high” with an average value of “good” (EQR BiPo = 0.67 ± 0.07). In the same way, the Vitality index measured in Gökçeada, is also lower (2.80 ± 0.28) than Corsica (3.48 ± 0.22) (Fig. 2). EQR values of the BiPo index and the Vitality index with the relevant descriptors of Posidonia oceanica, also showed significant differences between Gökçeada and Corsica (Table 4). Depths of the meadow lower limit varied significantly (t-test, p < 0.05) between the two regions where the mean depths are recorded as 24.6 ± 4.8 m and 33.3 ± 4.3 m from Gökçeada and Corsica, respectively. Subsequently the lower limit types showed differencesaccording to the Chi square test; especially progressive (12.5%) and sharp limits (20.8%) are mainly present in the sites where the seagrass vitality is evaluated in “good” status. On the other hand, sparse limits (29.2%) indicating slight deterioration and regressive limits
955
38 1 Values (m) EQR′ Lower limit depth
N/a
Good (0.775–0.550) High (1–0.775) RC
Differences of the Posidonia oceanica descriptors between Gökçeada and Corsica are tested using a t-test for independent samples when conditions of normality are met or the non-parametric Mann–Whitney U test when normality was not met. Considering the qualitative data (eg. limit type), differences between regions are tested using a Chi square (2 × N) test. Normality of distribution is analyzed using the Kolmogorov–Smirnov test, while the homogeneity of variance using the Levene’s test. Significancy of levels are tested at p < 0.01 and p < 0.05. Spearman’s rank correlation analysis is performed in order to verify the negative impacts of anthropogenic pressures on the ecological status and on the meadow vitality. Also, possible relations between the BiPo and the Vitality indices are tested using the Pearson’s correlation coefficient. A multidimensional scaling (PROXSCAL) analysis has performed to explore how each index might provide a generalization of the ecological status of coastal waters at broad scale.
X: value measured for each descriptor. RC: reference conditions. N/a: Not applicable.
N/a 0.05
< 19 ((X/19) × 0.225) + 0.1 25–19 ((X-19)/6)x0.225) + 0.325
N/a N/a 0.05
Poor (0.325–0.100) Moderate (0.550–0.325)
N/a 0.05
bathymetric zones accepted as reference depths (intermediate depth: 15 ± 1 m and the meadow lower limit) (Med-GIG, 2007). The shoot density (shoot m−2), meadow cover (%), plagiotropic growth of the rhizomes (%), rhizome elongation (mm y−1), exposure or burial of rhizomes (cm), lower limit depth (m) and type of the lower limit are measured. At both depths, shoot density (shoot m−2) is counted in 40 cm × 40 cm quadrats (Pergent et al., 2008) and 20 shoots of P. oceanica are collected randomly. Leaves are sorted according to the protocol of Giraud (1979) to measure the phenological and lepidochronological parameters (Pergent and Pergent-Martini, 1990): leaf surface (cm2 shoot−1), shoot length (mm shoot−1), coefficient A (%) and leaf production (number y−1). Measurements of four descriptors (lower limit depth, type of the lower limit, shoot density and leaf surface) are interpreted based on (i) the Ecological Quality Ratio (EQR) of the BiPo classification system (Lopez y Royo et al., 2010). The EQR value of the BiPo Index is determined by averaging EQŔ scores of the four individual descriptors shown in Table 1. Subsequently, measurements of eight descriptors (lower limit depth, type of the lower limit, shoot density, meadow cover, plagiotropic growth of the rhizomes, leaf production, exposure or burial of rhizomes and leaf surface) are interpreted based on (ii) the Vitality Index validated by the Barcelona Convention (UNEP-MAPRAC/SPA, 1999; Pergent et al., 2015). The Vitality Index is determined by averaging the metrics of the eight descriptors (max = 5, min = 1) shown in Table 2. 2.4. Data analysis
Class
Table 1 Class boundaries of the BiPo index: evaluation of Posidonia oceanica descriptors (Lopez y Royo et al., 2010).
Bad (< 0.100)
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Table 2 Assessment of the Vitality index of Posidonia oceanica based on several descriptors (Pergent et al., 2015). Descriptors
Location
High (5.0–4.5)
Good (4.4–3.5)
Moderate (3.4–2.5)
Poor (2.4–1.5)
Bad (1.4–1.0)
Lower limit depth (m) Lower limit type Leaf cover (%) Plagiotropic rhizomes (%) Leaf production (leaf number.y−1) Rhizome elongation (mm.y−1) Leaf surface (cm2.shoot−1) Density (shoot.m−2)
Lower limit Lower limit Lower limit Lower limit Lower limit Lower limit 15 ± 1 m 15 ± 1 m
> 34.2 Progressive > 35 > 70 ≥8.0 ≥8.0 > 362 > 339
34.2–30.4 Sharp high cover 35–25 70–30 7.9–7.0 7.9–6.0 361–292 339–239
30.4–26.6 Sharp low cover 25–15 < 30 6.9–6.0 5.9–4.0 291–221 238–172
26.6–22.8 Sparse 15–5 – 5.9–5.0 3.9–2.0 220–150 < 172
< 22.8 Regressive <5 – < 4.9 < 1.9 < 150 N/a
N/a: Not applicable.
(37.5%) indicating obvious deterioration, are frequent in the sites classified as “moderate” status. Regarding the siltation, which is one of the important factor affecting the meadows, exposure of rhizomes are recorded very low in Stareso (1.3 ± 1.1 cm) and Kapıkaya (1.0 ± 1.0 cm). Nine sites monitored around Gökçeada exhibit a mean Anthropization index of 2.9 with 11% of the sites classified in “good”, 78% in “moderate” and 11% in “poor” status, while 15 sites monitored around Corsica exhibit a mean Anthropization index of 1.7 with 27% of the sites classified in “high”, 60% in “good” and 13% in “moderate” status (Table 5). Significant relations are observed between the Anthropization index and the EQR values of the BiPo index (r = −0.745, p < 0.01) and the Vitality index (r = −0.702, p < 0.01) in the two regions (Gökçeada and Corsica) (Fig. 3). A significant correlation between the EQR values of the BiPo index and the Vitality index has been found in each site (r = 0.882, p < 0.01). The results of the multidimensional scaling analysis confirm the interchangeable application of the BiPo (Normalized raw
stress = 0.00012) and the Vitality (Normalized raw stress = 0.00008) indices in order to determine the ecological status of coastal waters at broad scale. The spatial segregation of each investigated site in the MDS plots for both indices is grouped due to the level of anthropization (Fig. 4). 4. Discussion The biotic indices (BiPo Index and Vitality Index) used in this study, have provided important ecological information and allowed the comparison between two Mediterranean islands (Gökçeada and Corsica). Mean EQR values of the BiPo index and the Vitality index are higher in Corsica than in Gökçeada, where the values correspond to a “good” status for Corsica and a “moderate” status in Gökçeada. Posidonia oceanica status in the western part as well as in the eastern part of the Mediterranean Sea has been investigated in previous studies using the BiPo Index (Table 6). In comparison with other sites, the mean value of Gökçeada Island (EQR = 0.44) can be compared to Catalonia Coast (mean EQR = 0.46) strongly affected by urbanization
Table 3 Ecological status and the vitality of P. ocenica meadows within the sites (mean value ± 95% confidence interval). Lower limit
15 ± 1 m
Depth (m)
Type
Leaf cover (%)
Plagiotropic rhizomes (%)
Leaf production (number.y−1)
Rhizome elongation (mm.y−1)
Density (shoot.m−2)
Leaf surface (cm2.shoot−1)
BiPo index (Ecological status)
Vitality index (Ecological status)
Fidanlık Tepeköy Kaleköy Yıldızkoyu Kuzulimanı Güzelcekoy Yüzentaşlar İncesu Kapıkaya
28.0 28.0 25.2 23.5 29.2 30.2 17.0 22.4 17.8
± ± ± ± ± ± ± ± ±
0.6 1.2 0.6 0.8 3.0 3.3 0.4 4.3 1.8
P Sp Sp Sp Sp Sp S+ R Sp
38.0 11.3 11.7 37.4 18.4 22.2 45.0 76.7 25.0
60.3 ± 12.8 8.9 ± 0.8 27.0 ± 8.0 45.7 ± 7.8 23.0 ± 5.4 19.1 ± 6.5 18.4 ± 13.6 27.4 ± 5.7 10.5 ± 5.3
6.3 7.4 5.0 5.4 6.4 6.7 5.4 6.7 6.4
± ± ± ± ± ± ± ± ±
0.3 0.5 0.3 0.2 0.3 0.3 0.3 0.3 0.4
6.6 6.1 5.1 7.7 4.9 5.2 7.5 6.7 4.9
± ± ± ± ± ± ± ± ±
2.0 2.1 0.4 2.3 0.7 1.5 2.1 2.1 1.9
175.0 ± 15.2 154.8 ± 20.5 66.7 ± 24.1 108.4 ± 38.8 154.8 ± 16.7 103.7 ± 46.7 69.7 ± 12.5 120.8 ± 50.5 41.4 ± 15.4
246.0 247.0 217.7 195.7 235.0 218.0 214.5 238.0 164.0
± ± ± ± ± ± ± ± ±
11.9 14.0 16.8 11.6 16.6 15.2 16.1 14.1 16.9
0.62 0.46 0.43 0.41 0.47 0.44 0.41 0.37 0.32
(Good) (Moderate) (Moderate) (Moderate) (Moderate) (Moderate) (Moderate) (Moderate) (Poor)
3.8 2.9 2.3 2.9 2.5 2.6 2.9 2.8 2.5
(Good) (Moderate) (Poor) (Moderate) (Moderate) (Moderate) (Moderate) (Moderate) (Moderate)
Macinaggio Cap Sagro Toga Arinella Bravone Favone La Chiappa Lavezzi Porto Pollo La Parata Sagone Porto Stareso Ile Rousse Canari
38.0 33.0 24.3 26.9 36.1 36.9 35.3 30.3 32.2 35.3 33.2 36.5 38.6 35.8 27.4
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.1 0.3 0.4 0.3 0.1 0.2 0.1 0.1 0.2 0.2 0.1 1.3 0.3 0.2 0.8
P R R R R Sp R P R R SSSR S+
14.2 ± 9.2 5.7 ± 3.7 41.2 ± 13.2 6.8 ± 4.5 28.3 ± 12.1 7.6 ± 2.6 12.5 ± 5.9 44.0 ± 18.4 4.8 ± 2.2 1.0 ± 0.9 35.2 ± 16.0 23.5 ± 9.5 19.2 ± 4.6 22.6 ± 12.7 97.5 ± 3.5
78.5 90.9 21.3 52.1 65.1 81.4 83.4 67.2 79.3 92.5 67.7 85.8 94.5 81.5 28.5
7.2 6.9 7.0 7.6 7.0 7.0 6.9 8.1 7.6 7.9 7.8 7.0 7.0 7.1 8.1
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.7 0.5 0.8 0.6 0.6 0.8 0.6 0.7 0.7 0.7 0.6 0.6 0.7 0.7 0.6
5.2 4.0 6.2 4.3 4.7 6.2 4.2 5.2 4.0 3.5 4.9 4.9 3.7 3.8 6.3
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
1.7 1.0 1.7 0.8 1.1 1.7 0.9 1.3 1.1 0.8 0.9 1.4 0.7 1.1 1.5
368.8 307.6 268.4 260.4 308.4 322.8 318.0 241.6 351.2 211.6 448.0 298.4 240.8 258.4 376.8
307.2 304.4 253.7 352.1 171.5 188.7 195.3 312.1 215.6 244.2 106.5 288.1 276.0 139.5 387.5
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
37.7 29.8 37.5 27.9 21.6 29.6 37.8 62.4 33.1 36.0 21.2 38.7 28.3 20.9 78.3
0.95 0.69 0.49 0.61 0.59 0.66 0.61 0.82 0.60 0.55 0.65 0.80 0.69 0.49 0.83
(High) (Good) (Moderate) (Good) (Good) (Good) (Good) (High) (Good) (Good) (Good) (High) (Good) (Moderate) (High)
4.1 3.1 3.3 3.1 3.4 3.5 3.1 4.1 3.1 3.0 3.6 3.8 3.6 3.1 4.3
(Good) (Moderate) (Moderate) (Moderate) (Moderate) (Good) (Moderate) (Good) (Moderate) (Moderate) (Good) (Good) (Good) (Moderate) (Good)
± ± ± ± ± ± ± ± ±
15.1 7.9 7.2 18.1 7.0 6.8 12.4 14.3 9.4
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
12.6 12.8 13.7 19.0 12.5 8.5 17.2 17.4 13.6 10.2 11.6 15.7 8.0 14.1 11.3
P: Progressive, S+: Sharp high cover, S−: Sharp poor cover, Sp: Sparse, R: Regressive limits.
4
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
22.0 32.2 29.3 33.0 30.6 49.7 32.0 32.3 46.2 25.0 32.3 47.3 20.5 25.0 38.1
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and agriculture (Lopez y Royo et al., 2009a), while the values of Corsican sites (mean EQR = 0.67) are closer to Ischia Island (mean EQR = 0.68) and Cyprus Island (mean EQR = 0.72). The relation between the Anthropization Index and the EQR values of the BiPo Index and the Vitality Index highlighted their efficiency in showing the meadow degradation in the sites subjected to higher human pressures. In Corsica, the lowest EQR values of the BiPo index are concerned with urbanized areas (Toga and Ile Rousse) and the lowest Vitality index is recorded in the sites close to the aquaculture activities (La Parata). Conversely, pristine sites (Marine Protected Areas) as Macinaggio and Lavezzi, exhibit higher values for both indices. Concerning Canari site, the high index values could be in relation with the fact that P. oceanica meadow is actually in development, after the cessation of mining discharges since 1965 (Bernier et al., 1997; Pergent et al., 2015). The density of the permanent population is similar for both regions (38 inhabitants km−2 in Corsica and 30 inhabitants km−2 in Gökçeada); however the increase of the population (and related impact) during the summer season is much higher for Gökçeada with a increase of more than 4 000% (from 9 000 to 390 000 inhabitants, while it does not exceed 750% in Corsican. In Gökçeada, the highest values for both indices recorded in Fidanlık correspond to a pristine site with sparse human-induced pressures, while the lowest values recorded in Kapıkaya and Kaleköy, could be in relation with the uncontrolled development of tourism and agricultural activities. The mean land use is rather similar for both sites (6.4% for Gökçeada and 6.6% for Corsica), but the mean Anthropization index is higher in Gökçeada where the mean surface occupied by agriculture, is much more important (12.4%) in comparison with Corsica (less than 1%). Indeed, intensive agricultural activities are mainly observed in
Fig. 2. EQR values of the BiPo index and the Vitality index (mean value ± confidence level 95%) between two regions. Table 4 Differences of the relevant descriptors for the BiPo and the Vitality indices between Gökçeada and Corsica (t-test value is t; Mann-Whitney U test value is U; Chi-Square test value is X2). Descriptor
Test
Value
p-Value
Lower limit depth Limit type Leaf cover Plagiotropic rhizomes Rhizome elongation Rhizome baring Leaf production Foliar surface Shoot density EQR BiPo Vitality index
t-test X2 t-test t-test t-test t-test M-W-U M-W-U t-test t-test t-test
−4.586 11.5 0.769 −5.223 3.168 3.356 35.50 50.00 −8.115 −4.734 −3.752
0.00* 0.02* 0.45 0.00* 0.00* 0.03* 0.65 0.29 0.00* 0.00* 0.00*
*Significant values at p < 0.05 level.
Table 5 Type of pressures evaluated by the Anthropization index (Gobert et al., 2009). Sites
Visual Assessment of Pressures Landuse (%)
Fidanlık Tepeköy Kaleköy Yıldızkoyu Kuzulimanı Güzelcekoy Yüzentaşlar İncesu Kapıkaya Macinaggio Cap Sagro Toga Arinella Bravone Favone La Chiappa Lavezzi Porto Pollo La Parata Sagone Porto Stareso Ile Rousse Canari
U
A
0.0 0.5 15.0 15.0 16.0 7.0 1.0 0.4 3.0 0.0 7.5 25.0 28.0 0.0 2.0 1.0 0.1 1.2 3.0 7.0 0.5 7.5 15.0 1.1
6.0 0.5 30.0 30.0 0.50 12.5 9.6 0.0 22.2 0.2 0.0 0.0 8.0 1.0 0.0 0.0 0.0 0.0 0.0 1.8 0.0 0.0 0.0 0.0
Aqua-culture (km)
Industry (km)
Tourism
Fishing
Port (km)
Anthropization Index
Pressure evaluation
No No No No No No No No No No No No No 3 No No No No 500 m No No No No No
No No No No No No No No No No No No No No No No No No No No No No No 3
No No Yes Yes Yes No Yes No Yes No No Yes Yes No No Yes No No No No No Yes Yes No
No Yes Yes No Yes Yes Yes Yes Yes No No Yes Yes Yes Yes No No No No No No Yes Yes No
No No No No 1 No No No No No No 1 3 No No No No No No No No 3 2 No
0 0 7 5 5 0 4 1 4 0 0 3 6 1 0 2 0 0 4 0 0 1 3 3
None None Low Low Low None Low Low Low None None Low Low Low None Low None None Low None None Low Low Low
For industries and ports, distances from the site in km; ‘No’ when absent from the considered range. Anthropization index within an area of 3 km radius. U: urbanized, A: agricultural.
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Fig. 3. Relation between the Anthropization Index in the study sites and the EQR determined by the BiPo and Vitality index.
Fig. 4. Plots for the BiPo and the Vitality indices with the spatial segregation of each site.
Table 6 Evaluation of BiPo index in different regions of the Mediterranean Sea. Site
Location
EQR BiPo
Status
Reference
Mataro Montroig Lacco Ameno Scarrupata Calvi (3 sites) Nisia Cape Greco Limassol 15 sites 9 sites
Catalonia (Spain) Catalonia (Spain) Ischia island (Italy) Ischia island (Italy) Corsica Cyprus Cyprus Cyprus Corsica Gökçeada
0.552 0.359 0.588 0.778 0.750–0.849 0.744 0.768 0.663 0.49–0.95 0.32–0.62
Good Moderate Good High Good to High Good Good Good Good to High Moderate to Good
Lopez y Royo et al., 2009a Lopez y Royo et al., 2009a Lopez y Royo et al., 2009a Lopez y Royo et al., 2009a Lopez y Royo et al., 2011 Pergent-Martini et al., 2013 Pergent-Martini et al., 2013 Pergent-Martini et al., 2013 This study This study
Kapıkaya and Kaleköy where the meadow vitality is minimum. In these sites, oxydation processes due to the mineralization of organic matters, initiate the formation of anoxic conditions in the sediment. As a result, toxic substances due to the high activity of anaerobic bacteria, affect
ion absorbtion by the plant (Hemminga, 1998; Delgado et al., 1999). Also in 2009–2011 period, extensive mucilageous layers on the benthic system were observed due to the eutrophic conditions and the opportunistic phytoplankton blooms prevailing in these sites (Aktan and 6
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Gümüşoglu, 2010; Güreşen and Aktan, 2014). Actually, eutrophication is well known to be one of the main pressures affecting seagrass meadows (Short and Wyllie-Echeverria, 1996; Delgado et al., 1999; Bianchi and Morri, 2000). Therefore, specific attention should be paid for these sites classified at the “borderline” values (moderate/poor) in order to minimize the possible stress factors through monitoring programmes. The biotic indices used in this study, have verified their reliability and feasibility in different environmental conditions of two Mediterranean islands, as also proved by other researches (Lopez y Royo et al., 2009b, 2011; Bermejo et al., 2014). They also confirm their interchangeable application to assess adequately the ecological status of P. oceanica meadows everywhere in the Mediterranean basin (Gobert et al., 2009; Lopez y Royo et al., 2011). It is obvious that the application of the biotic indices in this study, cannot effectively contributes to the construction of long-term data series, but initiates its development. Therefore, further cost-effective applications at the Mediterranean scale could be beneficial for monitoring the evolution of P. oceanica meadows as functional ecosystem services (Cullen-Unsworth and Unsworth, 2013; Vassallo et al., 2013). In conclusion, this study responding to the legislative obligations, provides a functional tool in terms of the land use planning and management implementations and meets the essential data deficiency in less evaluated regions (e.g. Turkey, Libya).
the ecological status of Mediterranean French coastal waters as required by the Water Framework Directive using the Posidonia oceanica Rapid Easy Index: PREI. Mar. Pollut. Bull. 58, 1727–1733. Güreşen, A., Aktan, Y., 2014. Seasonal and vertical variations of phytoplankton composition in Marine Park of Gökçeada Island in the North Aegean Sea. J. Black Sea/ Mediterranean Environ. 20 (3), 200–212. Hemminga, M.A., 1998. The root/rhizome system of seagrasses: an asset and a burden. J. Sea Res. 39, 183–196. Ignatiades, L., 2005. Scaling the trophic status of the Aegean Sea, Eastern Mediterranean. J. Sea Res. 54, 51–57. Innamorati, M., Nuccio, C., Massi, L., Mori, G., Melley, A., 2001. Mucilages and climatic changes in the Tyrrhenian Sea, Aquatic conservation. Marine Freshw. Ecosystems 11, 289–298. Lopez y Royo, C., Silvestri, C., Pergent, G., Casazza, G., 2009. Assessing human-induced pressures on coastal areas with publicly available data. J. Environ. Manage. 90, 1494–1501. Lopez y Royo, C., Silvestri, M., Salivas-Decaux, G., Pergent, G., Casazza, G., 2009. Application of an angiosperm-based classification system (BiPo) to Mediterranean coastal waters using spatial analysis and data on metal contamination of plants in identifying sources of pressure. Hydrobiologia. https://doi.org/10.1007/s10750009-9880-z. Lopez y Royo, C., Casazza, G., Pergent-Martini, C., Pergent, G., 2010. A biotic index using the seagrass Posidonia oceanica (BiPo) to evaluate ecological status of coastal waters. Ecol. Ind. 10, 380–389. Lopez y Royo, C., Pergent, G., Alcoverro, T., Buia, M.C., Casazza, G., Martínez-Crego, B., Pérez, M., Silvestre, F., Romero, J., 2011. The seagrass Posidonia oceanica as indicator of coastal water quality. Experimental intercalibration of classification systems. Ecol. Ind. 11 (2), 557–563. Manzanera, M., Peres, M., Romero, J., 1995. Seagrass mortality due to oversedimentation: an experimental approach. Int conf Mediterranean coastal environment, MEDCOAST 95, Terragona, Spain, 24-27 Oct 1995, 123–129. Med-GIG, 2007. WFD Intercalibration technical report for coastal and transitional waters in the Mediterranean ecoregion. In: WFD Intercalibration technical report–Part 3: coastal and transitional waters. EU-JRC, Ispra 342 pp. Available from: http://circa. europa.eu/Public/irc/jrc/jrc_eewai/library. Med-GIG, 2011. WFD Intercalibration technical report for coastal and transitional waters in the Mediterranean ecoregion. In: WFD Intercalibration Phase 2: Milestone 5 report: Coastal Waters, Marine Angiosperms. EU-JRC, 22 pp. Montefalcone, M., 2009. Ecosystem health assessment using the seagrass Posidonia oceanica: a review. Ecol. Indic. 9, 595–604. Pergent, G., Pergent-Martini, C., Casalta, B., Lopez Y Royo, C., Mimault, B., SalivasDecaux, M., Short, F., 2007. Comparison of three seagrass monitoring systems: SeagrassNet, “Posidonia” programme andRSP. Proceedings of the third Mediterranean symposium on marine vegetation (Marseilles, 27-29 March 2007). C. Pergent-Martini, S. El Asmi, C. Le Ravallec ed., RAC/SPA publ., Tunis, 141–150. Pergent, G., Leonardini, R., Lopez y Royo, C., Mimault, B., Pergent-Martini, C., 2008. Mise en oeuvre d’un Réseau de Surveillance Posidonies le long du littoral de la Corse – Rapport de synthe‘se 2004-2008. Contrat office de l’Environnement de la Corse et GIS Posidonie centre de Corse, GIS Posidonie Publ., Corte, 1–273. Pergent, G., Pergent-Martini, C., 1990. Some applications of lepidochronological analysis in the seagrass Posidonia oceanica. Botanica Marina 33, 299–310. Pergent, G., Pergent-Martini, C., Boudouresque, C.F., 1995. The use of the meadow of Posidonia oceanica as a biological indicator of the water quality in the Mediterranean Sea: state of the knowledge. Mesogee, Bulletin du Muséum d’Histoire Naturelle de Marseille 54, 3–27. Pergent, G., Pergent-Martini, C., Bein, A., Dedeken, M., Oberti, P., Orsini, A., Santucci, J.F., Short, F., 2015. Dynamic of Posidonia oceanica seagrass meadows in the northwestern Mediterranean: could climate change be to blame. C.R. Biol. 338 (7), 484–493. Pergent-Martini, C., Bonacorsi, M., Bein, A., Braschi, J., Kremmer, L., Pergent, G., 2013. Mapping of coastlines of the Republic of Cyprus – Progress report, April 2013. Agreement GIS Posidonie & AP Marine Environmental Consultancy Ltd, Ref n°1115, GIS Posidonie Publ., Corte, 1–38. Pergent-Martini, C., Leoni, V., Pasqualini, V., Ardizzone, G.D., Balestri, E., Bedini, R., Belluscio, A., Belsher, T., Borg, J., Boudouresque, C.F., Boumaza, S., Bouquegneau, J.M., Buia, M.C., Calvo, S., Cebrian, J., Charbonnel, E., Cinelli, F., Cossu, A., Di Maida, G., Dural, B., Francour, P., Gobert, S., Lepoint, G., Meinesz, A., Molenaar, H., Mansour, H.M., Panayotidis, P., Peirano, A., Pergent, G., Piazzi, L., Pirrotta, M., Relini, G., Romero, J., Sanchez-Lizaso, J.L., Semroud, R., Shembri, P., Shili, A., Tomasello, A., Velimirov, B., 2005. Descriptors of Posidonia oceanica meadows: use and application. Ecol. Ind. 5, 213–230. Pinedo, S., Jordana, E., Ballesteros, E., 2015. A critical analysis on the response of macroinvertebrate communities along disturbance gradients: description of MEDOCC (MEDiterranean OCCidental) index. Mar. Ecol. 36 (2), 141–154. Precali, R., Giani, M., Marini, M., Grilli, F., Ferrari, C.R., Pecar, O., Paschini, E., 2005. Mucilaginous aggregates in the Northern Adriatic in the period 1999–2002: typology and distribution. Sci. Total Environ. 353, 10–23. Romero, J., Martínez-Crego, B., Alcoverro, T., Pérez, M., 2007. A multivariate index based on the seagrass Posidonia oceanica (POMI) to assess the ecological status of coastal waters under the water framework directive (WFD). Mar. Pollut. Bull. 55, 196–204. Ruiz, M., Perez, M., Romero, J., 2001. Effects of fish farm loadings on seagrass (Posidonia oceanica) distribution, growth and photosynthesis. Mar. Pollut. Bull. 42 (9), 749–760. Ruiz, J.M., Romero, J., 2003. Effects of disturbances caused by coastal constructions on spatial structure, growth dynamics and photosynthesis of the seagrass Posidonia oceanica. Mar. Pollut. Bull. 46, 1523–1533. Short, F.T., Wyllie-Echeverria, S., 1996. Natural and human induced disturbance of
Acknowledgements This work is supported by Scientific Research Projects Coordination Unit of Istanbul University-Project numbers: FDK-2016-21299 and FHZ2016-22153 and Scientific and Technological Research Council of Turkey-Project number: 115Y486. Also, we would like to thank to the reviewers and to the editor for their valuable comments on the manuscript. References Aktan, Y., Gümüşoglu, A., 2010. Another threat on Posidonia oceanica beds: Mucilage effect in Gökçeada Island, North Aegean Sea, Turkey. Proceedings of the 4. Mediterranean Symposium on Marine Vegetation, RAC/SPA, 2-4 December 2010, Tunis, 251 pp. Balestri, E., Benedetti-Cecchi, L., Lardicci, C., 2004. Variability in patterns of growth and morphology of Posidonia oceanica meadows exposed to urban and industrial waste: contrasts with two reference locations. J. Exp. Mar. Biol. Ecol. 308, 1–21. Bermejo, R., Mangialajo, L., Vergara, J.J., Hernandez, I., 2014. Comparison of two indices based on macrophyte assemblages to assess the ecological status of coastal waters in the transition between the Atlantic and Mediterranean ecoregions. J. Appl. Phycol. 26, 1899–1909. Bernier, P., Guidi, J.B., Boanttcher, M.E., 1997. Coastal progradation and very early diagenesis of ultramafic sands as a result of rubble discharge from asbestos excavations (northern Corsica, western Mediterranean). Mar. Geol. 144, 163–175. Bianchi, C.N., Morri, C., 2000. Marine biodiversity of the Mediterrannean Sea: Situation, problems and prospects for future research. Mar. Pollut. Bull. 40 (5), 367–376. Boudouresque, C.F., Bernard, G., Pergent, G., Shili, A., Verlaque, M., 2009. Regression of Mediterranean seagrasses caused by natural processes and anthropogenic disturbances and stress: a critical review. Bot. Mar. 52, 395–418. Boudouresque, C.F., Bernard, G., Bonhomme, P., Charbonnel, E., Diviacco, G., Meinesz, A., Pergent, G., Pergent-Martini, C., Ruitton, S., Tunesi, L., 2012. Protection and conservation of Posidonia oceanica meadows. RAMOGE and RAC/SPA Publisher, Tunis, pp. 1–202. Cullen-Unsworth, L.A., Unsworth, R., 2013. Seagrass meadows, ecosystem services, and sustainability. Environment 55, 14–28. Delgado, O., Ruiz, J., Perez, M., Romero, J., Ballesteros, E., 1999. Effects of fish farming on seagrass (Posidonia oceanica) in a Mediterranean bay: seagrass decline after organic loading cessation. Oceanol. Acta 22 (1), 109–117. Duarte, C.M., 2002. The future of seagrass meadows. Environ. Conserv. 29 (2), 192–206. EC, 2000. DIRECTIVE 2000/60/EC of the European parliament and of the council, of 23 October 2000, establishing a framework for Community action in the field of water policy. Official Journal of the European Communities, G.U.C.E. 22/12/2000, L 327. Fernandez-Torquemada, Y., Diaz-Valdes, M., Colilla, F., Luna, B., Sanchez-Lizaso, J.L., et al., 2008. Descriptors from Posidonia oceanica (L.) Delile meadows in coastal waters of Valencia, Spain, in the context of the EU Water Framework Directive. ICES J. Mar. Sci. 65, 1492–1497. Giraud, G., 1979. Sur une methode de mesure et de comptage des structures foliaires de Posidonia oceanica (Linnaeus) Delile. Bulletin du Museum d’Histoire Naturelle de Marseille 39, 33–39. Gobert, S., Sartoretto, S., Rico-Raimondino, V., Andral, B., Chery, A., 2009. Assessment of
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A. Güreşen, et al. seagrasses. Environ. Conserv. 23, 17–27. Siokou-Frangou, I., Zervoudakı, S., Chrıstou, E.D., Zervakıs, V., Georgopulos, D., 2009. Variability of mesozooplankton spatial distribution in the North Aegean Sea, as ınfluenced by the Black Sea Waters outflow. J. Mar. Syst. 78, 557–575. Telesca, L., Belluscio, A., Criscoli, A., Ardizzone, G., Apostolaki, E.T., Fraschetti, S., Gristina, M., Knittweis, L., Martin, C.S., Pergent, G., Alagna, A., Badalamenti, F., Garofalo, G., Gerakaris, V., Louise Pace, M., Pergent-Martini, C., Salomidi, M., 2015. Seagrass meadows (Posidonia oceanica) distribution and trajectories of change. Sci. Rep. 5 (12505), 1–14. UNEP-MAP-RAC/SPA, 1999. Action plan for the conservation of marine vegetation in the Mediterranean Sea, CAR/ASP Publ., Tunis.
Valette-Sansevin, A., Alami, S., Bonacorsi, M., Damier, E., Pergent, G., Pergent-Martini, C., 2015. Continuous mapping of the main habitats of the Corsican littoral. In: Proceedings of the Twelfth International Conference on the Mediterranean Coastal Environment – MEDCOAST 2015, Bulgaria, MEDCOAST Mediterranean Coastal Foundation, Turkey, 1, 263–269. Vassallo, P., Paoli, C., Rovere, A., Montefalcone, M., Morri, C., Bianchi, C.N., 2013. The value of the seagrass Posidonia oceanica: a natural capital assessment. Mar. Pollut. Bull. 75, 157–167. Waycott, M., Duarte, C.M., Carruthers, T.J.B., et al., 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc. Natl. Acad. Sci. U.S.A. 106, 12377–12381.
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Evaluating the coastal ecosystem status of two Western and Eastern Mediterranean islands using the seagrass Posidonia oceanica
T
A. Güreşena, , G. Pergentb, S.O. Güreşena, Y. Aktana ⁎
a b
University of Istanbul, Faculty of Aquatic Sciences, Turkey University of Corsica, Faculty of Sciences, France
ARTICLE INFO
ABSTRACT
Keywords: Posidonia oceanica Biological quality element Biotic index Ecological status Monitoring
Mediterranean seagrass Posidonia oceanica is used as a ‘biological quality element’ in the long-term monitoring programmes of the Water Framework Directive (WFD 2000/60/EC) for the evaluation of ecological status of coastal waters. Due to its low resilience to anthropogenic pressures, P. oceanica meadows have disappeared irreversibly along some of the Mediterranean coasts. The main objective of this survey, is therefore to compare the ecological status of coastal waters and P. oceanica meadows in two islands from Eastern (Gökçeada, Turkey) and Western (Corsica, France) Mediterranean Sea based on the Posidonia Biotic Index (BiPo) and the Vitality Index besides concentrating on: (i) their consistency in different environmental conditions present in the Mediterranean Sea, (ii) their effectiveness to discriminate the ecological status of coastal waters in relation to different anthropogenic pressures and (iii) their application capacity to initiate long-term data series for monitoring the evolution of the meadows in less evaluated regions (i.e. from the Eastern Mediterranean). The measurements of several descriptors of P. oceanica are interpreted based on the BiPo and the Vitality indices for 2 regions; 9 sites from Gökçeada and 15 sites from Corsica exposed to different human pressures. The mean BiPo and Vitality indices are higher in Corsica than in Gökçeada, where the values correspond to a “good” status for Corsica and a “moderate” status in Gökçeada. The application of these biotic indices showed their feasibility and comparability to assess the ecological status in different environmental conditions. Significant relationships between the scores of Anthropization index and the EQR values of the BiPo index (r = −0.745, p < 0.01) and the Vitality index (r = −0.702, p < 0.01) highlighted their efficiency to determine the seagrass degradation in the sites subjected to higher pressure levels. It can be assumed that this study initiates the development of longterm data series and also meets the essential data deficiency in less evaluated regions.
1. Introduction Changing climate conditions and recent anthropogenic pressures on coastal regions, cause irreversible regressions and habitat losses of the seagrass meadows (Ruiz et al., 2001; Duarte, 2002; Ruiz and Romero, 2003; Boudouresque et al., 2009; Waycott et al., 2009; Telesca et al., 2015). Apart from these, wastewater discharges, aquacultural, agricultural and recreational activities (Manzanera et al., 1995; Boudouresque et al., 2012) cause water quality degradation as eutrophication, harmful algal blooms, high turbidity and mucilage formation (Innamorati et al., 2001; Precali et al., 2005). Therefore, the Water Framework Directive (WFD 2000/60/EC) has been established (EC, 2000) with the aim of conserving and managing of all types of water bodies for a sustainable development. The WFD is
also concentrated on the evaluation of the coastal ecosystem status through angiosperm classification practices in a wide spatial extent in order to reach “good” ecological status for all types of waterbodies by 2020 (EC, 2000). As a common representative species of the angiosperms in the Mediterranean Sea in terms of abundance (Med-GIG, 2011), Posidonia oceanica (Linnaeus) Delile is used as a “biological quality element” in the long-term monitoring programmes implemented by the WFD (Pergent et al., 1995; Ruiz and Romero, 2003; Balestri et al., 2004; Pergent-Martini et al., 2005; Boudouresque et al., 2009; Montefalcone, 2009). Various biotic indices using P. oceanica, have been developed to assess the ecological status in general and in a wide spatial extent as much as possible (A Multivariate Index_POMI by Romero et al., 2007;
⁎ Corresponding author at: Department of Marine and Freshwater Resources and Management, Faculty of Aquatic Sciences, University of Istanbul, 34134 Istanbul, Turkey. E-mail address: [email protected] (A. Güreşen).
https://doi.org/10.1016/j.ecolind.2019.105734 Received 22 February 2019; Received in revised form 9 September 2019; Accepted 12 September 2019 1470-160X/ © 2019 Elsevier Ltd. All rights reserved.
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Fig. 1. The sites of Gökçeada and Corsica considered for the application of the BiPo and the Vitality indices.
INTERREG Posidonia Programme_POSID by Pergent et al., 2007; Valencian CS by Fernandez-Torquemada et al., 2008; Rapid Easy Index_PREI by Gobert et al., 2009; Biotic Index_BiPo by Lopez y Royo et al., 2010). In accordance with the WFD requirements, their common objectives are to obtain the descriptors of the relevant index in order to quantify the ecological quality ratio (EQR) that compares the status of a “biological quality element” both in a specific water body and in a pristine area (EC, 2000). The main objective of this survey is to compare the ecological status of coastal waters and P. oceanica meadows in two islands from the Eastern (Gökçeada, Turkey) and the Western (Corsica, France) Mediterranean Sea based on the Posidonia Biotic Index (BiPo) and the Vitality Index. The study will concentrate on: (i) the consistency of these indices in different environmental conditions present in the Mediterranean Sea, (ii) the effectiveness of these indices to discriminate the ecological status of coastal waters in relation to different anthropogenic pressures and (iii) the application capacity of these indices to initiate long-term series data for monitoring the evolution of the meadows and related environment in less evaluated regions.
The region is also affected by tourism pressures in the summer season (9 000–390 000 inhabitants). Corsica Island (42°4′8.55″N–9°4′55.82″E), one of the five largest islands of the Mediterranean Sea (8 680 km2), located in the Northwestern Basin, is characterized by extensive P. oceanica meadows (53 736 ha) and moderate human pressure with less than 350 000 inhabitants and very few industrial activities (Valette-Sansevin et al., 2015). 2.2. Evaluation of the anthropogenic pressures Anthropogenic pressures are evaluated with the combination of techniques used in various studies on the assessment of human-induced pressures on coastal ecosystems (Gobert et al., 2009; Lopez y Royo et al., 2009a; Bermejo et al., 2014; Pinedo et al., 2015). Therefore anthropization index is calculated within this study as the sum of seven pressure types: aquaculture (number, km distance from the study site), industrial development (type, km distance from the study site), agriculture (landuse), tourism (activities, hotels), fishing (activity type, number of boats), commercial port (harbour traffic, km distance from the study site) and urbanization (landuse, wastewater discharge, population density). These seven pressures in each site, are evaluated by quantifying in a 3 km radius circle through the satellite images and census data since the sites are approximately 5 km far from each other. Then they are classified from 0 (none impact) to 5 (high impact) and the final class scores for each pressure are summed up in order to determine the anthropization degree of each site that can be easily used by coastal managers (Gobert et al., 2009).
2. Material and methods 2.1. Study sites Study sites correspond to representative islands from the Eastern Basin (Gökçeada) and North-western Basin (Corsica) of the Mediterranean Sea, even if their size is rather different. Gökçeada (40°10′10.19″N–25°50′13.93″E) is the largest island of Turkey (289 km2); located in the North Aegean Sea, it has distinct hydrological characteristics comparing to Western Mediterranean Sea due to the Turkish Straits Current System. Salinity (38.8–39.0‰) in the deep reflects Levantene waters whereas; brackish waters in the surface reflect the Black Sea waters (Ignatiades, 2005; Siokou-Frangou et al., 2009). As a result, stenohaline Posidonia oceanica meadows (about 400 ha) resist to maintain a healthy life-span around Gökçeada coasts.
2.3. Sampling design Data collection has been conducted by SCUBA diving in 2 regions: 9 sites from Gökçeada and 15 sites from Corsica, exposed to different environmental pressures (Fig. 1). In order to assess the ecological status, several descriptors of Posidonia oceanica are measured in two 2
Ecological Indicators 108 (2020) 105734
< 119 ((X/119) × 0.225) + 0.1
< 481
152–119 ((X-119)/33)x0.225) + 0.325
651–481
N/a
< 172 ((X/172) × 0.225) + 0.1 239–172 ((X-172)/67) × 0.225) + 0.325
N/a 0.05
Regressive limits recent dead matte 0.21 Sparse limits < 15% cover, % plagio N/a 0.44
31–25 ((X-25)/6) × 0.225) + 0.55
Sharp limits < 70% cover and < 70% plagio 0.66
339–239 ((X-239)/100) × 0.225) + 0.55
200–152 ((X-152)/48) × 0.225) + 0.55
812–651
> 31 ((X-31)/7) × 0.225) + 0.775
Progressive and erosive limits > 70% cover or > 70% plagio 0.89
> 339 ((X-339)/260) × 0.225) + 0.775
> 200 ((X-200/133) × 0.225) + 0.775
> 812
1
599 1
310 1
Values Supporting parameters EQR′
Values (shoots m2) EQR′
Values (cm shoot−1) EQR′
Values (mm)
Lower limit type
Shoot density
Shoot leaf surface
Or shoot length
3. Results The indices and the relevant descriptors measured, are reported for each site in Table 3. According to the BiPo index, the ecological status of Gökçeada varies between “poor” and “good” with an average value of “moderate” (EQR BiPo = 0.44 ± 0.05), while the ecological status of the Corsica varies between “moderate” and “high” with an average value of “good” (EQR BiPo = 0.67 ± 0.07). In the same way, the Vitality index measured in Gökçeada, is also lower (2.80 ± 0.28) than Corsica (3.48 ± 0.22) (Fig. 2). EQR values of the BiPo index and the Vitality index with the relevant descriptors of Posidonia oceanica, also showed significant differences between Gökçeada and Corsica (Table 4). Depths of the meadow lower limit varied significantly (t-test, p < 0.05) between the two regions where the mean depths are recorded as 24.6 ± 4.8 m and 33.3 ± 4.3 m from Gökçeada and Corsica, respectively. Subsequently the lower limit types showed differencesaccording to the Chi square test; especially progressive (12.5%) and sharp limits (20.8%) are mainly present in the sites where the seagrass vitality is evaluated in “good” status. On the other hand, sparse limits (29.2%) indicating slight deterioration and regressive limits
955
38 1 Values (m) EQR′ Lower limit depth
N/a
Good (0.775–0.550) High (1–0.775) RC
Differences of the Posidonia oceanica descriptors between Gökçeada and Corsica are tested using a t-test for independent samples when conditions of normality are met or the non-parametric Mann–Whitney U test when normality was not met. Considering the qualitative data (eg. limit type), differences between regions are tested using a Chi square (2 × N) test. Normality of distribution is analyzed using the Kolmogorov–Smirnov test, while the homogeneity of variance using the Levene’s test. Significancy of levels are tested at p < 0.01 and p < 0.05. Spearman’s rank correlation analysis is performed in order to verify the negative impacts of anthropogenic pressures on the ecological status and on the meadow vitality. Also, possible relations between the BiPo and the Vitality indices are tested using the Pearson’s correlation coefficient. A multidimensional scaling (PROXSCAL) analysis has performed to explore how each index might provide a generalization of the ecological status of coastal waters at broad scale.
X: value measured for each descriptor. RC: reference conditions. N/a: Not applicable.
N/a 0.05
< 19 ((X/19) × 0.225) + 0.1 25–19 ((X-19)/6)x0.225) + 0.325
N/a N/a 0.05
Poor (0.325–0.100) Moderate (0.550–0.325)
N/a 0.05
bathymetric zones accepted as reference depths (intermediate depth: 15 ± 1 m and the meadow lower limit) (Med-GIG, 2007). The shoot density (shoot m−2), meadow cover (%), plagiotropic growth of the rhizomes (%), rhizome elongation (mm y−1), exposure or burial of rhizomes (cm), lower limit depth (m) and type of the lower limit are measured. At both depths, shoot density (shoot m−2) is counted in 40 cm × 40 cm quadrats (Pergent et al., 2008) and 20 shoots of P. oceanica are collected randomly. Leaves are sorted according to the protocol of Giraud (1979) to measure the phenological and lepidochronological parameters (Pergent and Pergent-Martini, 1990): leaf surface (cm2 shoot−1), shoot length (mm shoot−1), coefficient A (%) and leaf production (number y−1). Measurements of four descriptors (lower limit depth, type of the lower limit, shoot density and leaf surface) are interpreted based on (i) the Ecological Quality Ratio (EQR) of the BiPo classification system (Lopez y Royo et al., 2010). The EQR value of the BiPo Index is determined by averaging EQŔ scores of the four individual descriptors shown in Table 1. Subsequently, measurements of eight descriptors (lower limit depth, type of the lower limit, shoot density, meadow cover, plagiotropic growth of the rhizomes, leaf production, exposure or burial of rhizomes and leaf surface) are interpreted based on (ii) the Vitality Index validated by the Barcelona Convention (UNEP-MAPRAC/SPA, 1999; Pergent et al., 2015). The Vitality Index is determined by averaging the metrics of the eight descriptors (max = 5, min = 1) shown in Table 2. 2.4. Data analysis
Class
Table 1 Class boundaries of the BiPo index: evaluation of Posidonia oceanica descriptors (Lopez y Royo et al., 2010).
Bad (< 0.100)
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Table 2 Assessment of the Vitality index of Posidonia oceanica based on several descriptors (Pergent et al., 2015). Descriptors
Location
High (5.0–4.5)
Good (4.4–3.5)
Moderate (3.4–2.5)
Poor (2.4–1.5)
Bad (1.4–1.0)
Lower limit depth (m) Lower limit type Leaf cover (%) Plagiotropic rhizomes (%) Leaf production (leaf number.y−1) Rhizome elongation (mm.y−1) Leaf surface (cm2.shoot−1) Density (shoot.m−2)
Lower limit Lower limit Lower limit Lower limit Lower limit Lower limit 15 ± 1 m 15 ± 1 m
> 34.2 Progressive > 35 > 70 ≥8.0 ≥8.0 > 362 > 339
34.2–30.4 Sharp high cover 35–25 70–30 7.9–7.0 7.9–6.0 361–292 339–239
30.4–26.6 Sharp low cover 25–15 < 30 6.9–6.0 5.9–4.0 291–221 238–172
26.6–22.8 Sparse 15–5 – 5.9–5.0 3.9–2.0 220–150 < 172
< 22.8 Regressive <5 – < 4.9 < 1.9 < 150 N/a
N/a: Not applicable.
(37.5%) indicating obvious deterioration, are frequent in the sites classified as “moderate” status. Regarding the siltation, which is one of the important factor affecting the meadows, exposure of rhizomes are recorded very low in Stareso (1.3 ± 1.1 cm) and Kapıkaya (1.0 ± 1.0 cm). Nine sites monitored around Gökçeada exhibit a mean Anthropization index of 2.9 with 11% of the sites classified in “good”, 78% in “moderate” and 11% in “poor” status, while 15 sites monitored around Corsica exhibit a mean Anthropization index of 1.7 with 27% of the sites classified in “high”, 60% in “good” and 13% in “moderate” status (Table 5). Significant relations are observed between the Anthropization index and the EQR values of the BiPo index (r = −0.745, p < 0.01) and the Vitality index (r = −0.702, p < 0.01) in the two regions (Gökçeada and Corsica) (Fig. 3). A significant correlation between the EQR values of the BiPo index and the Vitality index has been found in each site (r = 0.882, p < 0.01). The results of the multidimensional scaling analysis confirm the interchangeable application of the BiPo (Normalized raw
stress = 0.00012) and the Vitality (Normalized raw stress = 0.00008) indices in order to determine the ecological status of coastal waters at broad scale. The spatial segregation of each investigated site in the MDS plots for both indices is grouped due to the level of anthropization (Fig. 4). 4. Discussion The biotic indices (BiPo Index and Vitality Index) used in this study, have provided important ecological information and allowed the comparison between two Mediterranean islands (Gökçeada and Corsica). Mean EQR values of the BiPo index and the Vitality index are higher in Corsica than in Gökçeada, where the values correspond to a “good” status for Corsica and a “moderate” status in Gökçeada. Posidonia oceanica status in the western part as well as in the eastern part of the Mediterranean Sea has been investigated in previous studies using the BiPo Index (Table 6). In comparison with other sites, the mean value of Gökçeada Island (EQR = 0.44) can be compared to Catalonia Coast (mean EQR = 0.46) strongly affected by urbanization
Table 3 Ecological status and the vitality of P. ocenica meadows within the sites (mean value ± 95% confidence interval). Lower limit
15 ± 1 m
Depth (m)
Type
Leaf cover (%)
Plagiotropic rhizomes (%)
Leaf production (number.y−1)
Rhizome elongation (mm.y−1)
Density (shoot.m−2)
Leaf surface (cm2.shoot−1)
BiPo index (Ecological status)
Vitality index (Ecological status)
Fidanlık Tepeköy Kaleköy Yıldızkoyu Kuzulimanı Güzelcekoy Yüzentaşlar İncesu Kapıkaya
28.0 28.0 25.2 23.5 29.2 30.2 17.0 22.4 17.8
± ± ± ± ± ± ± ± ±
0.6 1.2 0.6 0.8 3.0 3.3 0.4 4.3 1.8
P Sp Sp Sp Sp Sp S+ R Sp
38.0 11.3 11.7 37.4 18.4 22.2 45.0 76.7 25.0
60.3 ± 12.8 8.9 ± 0.8 27.0 ± 8.0 45.7 ± 7.8 23.0 ± 5.4 19.1 ± 6.5 18.4 ± 13.6 27.4 ± 5.7 10.5 ± 5.3
6.3 7.4 5.0 5.4 6.4 6.7 5.4 6.7 6.4
± ± ± ± ± ± ± ± ±
0.3 0.5 0.3 0.2 0.3 0.3 0.3 0.3 0.4
6.6 6.1 5.1 7.7 4.9 5.2 7.5 6.7 4.9
± ± ± ± ± ± ± ± ±
2.0 2.1 0.4 2.3 0.7 1.5 2.1 2.1 1.9
175.0 ± 15.2 154.8 ± 20.5 66.7 ± 24.1 108.4 ± 38.8 154.8 ± 16.7 103.7 ± 46.7 69.7 ± 12.5 120.8 ± 50.5 41.4 ± 15.4
246.0 247.0 217.7 195.7 235.0 218.0 214.5 238.0 164.0
± ± ± ± ± ± ± ± ±
11.9 14.0 16.8 11.6 16.6 15.2 16.1 14.1 16.9
0.62 0.46 0.43 0.41 0.47 0.44 0.41 0.37 0.32
(Good) (Moderate) (Moderate) (Moderate) (Moderate) (Moderate) (Moderate) (Moderate) (Poor)
3.8 2.9 2.3 2.9 2.5 2.6 2.9 2.8 2.5
(Good) (Moderate) (Poor) (Moderate) (Moderate) (Moderate) (Moderate) (Moderate) (Moderate)
Macinaggio Cap Sagro Toga Arinella Bravone Favone La Chiappa Lavezzi Porto Pollo La Parata Sagone Porto Stareso Ile Rousse Canari
38.0 33.0 24.3 26.9 36.1 36.9 35.3 30.3 32.2 35.3 33.2 36.5 38.6 35.8 27.4
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.1 0.3 0.4 0.3 0.1 0.2 0.1 0.1 0.2 0.2 0.1 1.3 0.3 0.2 0.8
P R R R R Sp R P R R SSSR S+
14.2 ± 9.2 5.7 ± 3.7 41.2 ± 13.2 6.8 ± 4.5 28.3 ± 12.1 7.6 ± 2.6 12.5 ± 5.9 44.0 ± 18.4 4.8 ± 2.2 1.0 ± 0.9 35.2 ± 16.0 23.5 ± 9.5 19.2 ± 4.6 22.6 ± 12.7 97.5 ± 3.5
78.5 90.9 21.3 52.1 65.1 81.4 83.4 67.2 79.3 92.5 67.7 85.8 94.5 81.5 28.5
7.2 6.9 7.0 7.6 7.0 7.0 6.9 8.1 7.6 7.9 7.8 7.0 7.0 7.1 8.1
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
0.7 0.5 0.8 0.6 0.6 0.8 0.6 0.7 0.7 0.7 0.6 0.6 0.7 0.7 0.6
5.2 4.0 6.2 4.3 4.7 6.2 4.2 5.2 4.0 3.5 4.9 4.9 3.7 3.8 6.3
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
1.7 1.0 1.7 0.8 1.1 1.7 0.9 1.3 1.1 0.8 0.9 1.4 0.7 1.1 1.5
368.8 307.6 268.4 260.4 308.4 322.8 318.0 241.6 351.2 211.6 448.0 298.4 240.8 258.4 376.8
307.2 304.4 253.7 352.1 171.5 188.7 195.3 312.1 215.6 244.2 106.5 288.1 276.0 139.5 387.5
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
37.7 29.8 37.5 27.9 21.6 29.6 37.8 62.4 33.1 36.0 21.2 38.7 28.3 20.9 78.3
0.95 0.69 0.49 0.61 0.59 0.66 0.61 0.82 0.60 0.55 0.65 0.80 0.69 0.49 0.83
(High) (Good) (Moderate) (Good) (Good) (Good) (Good) (High) (Good) (Good) (Good) (High) (Good) (Moderate) (High)
4.1 3.1 3.3 3.1 3.4 3.5 3.1 4.1 3.1 3.0 3.6 3.8 3.6 3.1 4.3
(Good) (Moderate) (Moderate) (Moderate) (Moderate) (Good) (Moderate) (Good) (Moderate) (Moderate) (Good) (Good) (Good) (Moderate) (Good)
± ± ± ± ± ± ± ± ±
15.1 7.9 7.2 18.1 7.0 6.8 12.4 14.3 9.4
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
12.6 12.8 13.7 19.0 12.5 8.5 17.2 17.4 13.6 10.2 11.6 15.7 8.0 14.1 11.3
P: Progressive, S+: Sharp high cover, S−: Sharp poor cover, Sp: Sparse, R: Regressive limits.
4
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
22.0 32.2 29.3 33.0 30.6 49.7 32.0 32.3 46.2 25.0 32.3 47.3 20.5 25.0 38.1
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and agriculture (Lopez y Royo et al., 2009a), while the values of Corsican sites (mean EQR = 0.67) are closer to Ischia Island (mean EQR = 0.68) and Cyprus Island (mean EQR = 0.72). The relation between the Anthropization Index and the EQR values of the BiPo Index and the Vitality Index highlighted their efficiency in showing the meadow degradation in the sites subjected to higher human pressures. In Corsica, the lowest EQR values of the BiPo index are concerned with urbanized areas (Toga and Ile Rousse) and the lowest Vitality index is recorded in the sites close to the aquaculture activities (La Parata). Conversely, pristine sites (Marine Protected Areas) as Macinaggio and Lavezzi, exhibit higher values for both indices. Concerning Canari site, the high index values could be in relation with the fact that P. oceanica meadow is actually in development, after the cessation of mining discharges since 1965 (Bernier et al., 1997; Pergent et al., 2015). The density of the permanent population is similar for both regions (38 inhabitants km−2 in Corsica and 30 inhabitants km−2 in Gökçeada); however the increase of the population (and related impact) during the summer season is much higher for Gökçeada with a increase of more than 4 000% (from 9 000 to 390 000 inhabitants, while it does not exceed 750% in Corsican. In Gökçeada, the highest values for both indices recorded in Fidanlık correspond to a pristine site with sparse human-induced pressures, while the lowest values recorded in Kapıkaya and Kaleköy, could be in relation with the uncontrolled development of tourism and agricultural activities. The mean land use is rather similar for both sites (6.4% for Gökçeada and 6.6% for Corsica), but the mean Anthropization index is higher in Gökçeada where the mean surface occupied by agriculture, is much more important (12.4%) in comparison with Corsica (less than 1%). Indeed, intensive agricultural activities are mainly observed in
Fig. 2. EQR values of the BiPo index and the Vitality index (mean value ± confidence level 95%) between two regions. Table 4 Differences of the relevant descriptors for the BiPo and the Vitality indices between Gökçeada and Corsica (t-test value is t; Mann-Whitney U test value is U; Chi-Square test value is X2). Descriptor
Test
Value
p-Value
Lower limit depth Limit type Leaf cover Plagiotropic rhizomes Rhizome elongation Rhizome baring Leaf production Foliar surface Shoot density EQR BiPo Vitality index
t-test X2 t-test t-test t-test t-test M-W-U M-W-U t-test t-test t-test
−4.586 11.5 0.769 −5.223 3.168 3.356 35.50 50.00 −8.115 −4.734 −3.752
0.00* 0.02* 0.45 0.00* 0.00* 0.03* 0.65 0.29 0.00* 0.00* 0.00*
*Significant values at p < 0.05 level.
Table 5 Type of pressures evaluated by the Anthropization index (Gobert et al., 2009). Sites
Visual Assessment of Pressures Landuse (%)
Fidanlık Tepeköy Kaleköy Yıldızkoyu Kuzulimanı Güzelcekoy Yüzentaşlar İncesu Kapıkaya Macinaggio Cap Sagro Toga Arinella Bravone Favone La Chiappa Lavezzi Porto Pollo La Parata Sagone Porto Stareso Ile Rousse Canari
U
A
0.0 0.5 15.0 15.0 16.0 7.0 1.0 0.4 3.0 0.0 7.5 25.0 28.0 0.0 2.0 1.0 0.1 1.2 3.0 7.0 0.5 7.5 15.0 1.1
6.0 0.5 30.0 30.0 0.50 12.5 9.6 0.0 22.2 0.2 0.0 0.0 8.0 1.0 0.0 0.0 0.0 0.0 0.0 1.8 0.0 0.0 0.0 0.0
Aqua-culture (km)
Industry (km)
Tourism
Fishing
Port (km)
Anthropization Index
Pressure evaluation
No No No No No No No No No No No No No 3 No No No No 500 m No No No No No
No No No No No No No No No No No No No No No No No No No No No No No 3
No No Yes Yes Yes No Yes No Yes No No Yes Yes No No Yes No No No No No Yes Yes No
No Yes Yes No Yes Yes Yes Yes Yes No No Yes Yes Yes Yes No No No No No No Yes Yes No
No No No No 1 No No No No No No 1 3 No No No No No No No No 3 2 No
0 0 7 5 5 0 4 1 4 0 0 3 6 1 0 2 0 0 4 0 0 1 3 3
None None Low Low Low None Low Low Low None None Low Low Low None Low None None Low None None Low Low Low
For industries and ports, distances from the site in km; ‘No’ when absent from the considered range. Anthropization index within an area of 3 km radius. U: urbanized, A: agricultural.
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Fig. 3. Relation between the Anthropization Index in the study sites and the EQR determined by the BiPo and Vitality index.
Fig. 4. Plots for the BiPo and the Vitality indices with the spatial segregation of each site.
Table 6 Evaluation of BiPo index in different regions of the Mediterranean Sea. Site
Location
EQR BiPo
Status
Reference
Mataro Montroig Lacco Ameno Scarrupata Calvi (3 sites) Nisia Cape Greco Limassol 15 sites 9 sites
Catalonia (Spain) Catalonia (Spain) Ischia island (Italy) Ischia island (Italy) Corsica Cyprus Cyprus Cyprus Corsica Gökçeada
0.552 0.359 0.588 0.778 0.750–0.849 0.744 0.768 0.663 0.49–0.95 0.32–0.62
Good Moderate Good High Good to High Good Good Good Good to High Moderate to Good
Lopez y Royo et al., 2009a Lopez y Royo et al., 2009a Lopez y Royo et al., 2009a Lopez y Royo et al., 2009a Lopez y Royo et al., 2011 Pergent-Martini et al., 2013 Pergent-Martini et al., 2013 Pergent-Martini et al., 2013 This study This study
Kapıkaya and Kaleköy where the meadow vitality is minimum. In these sites, oxydation processes due to the mineralization of organic matters, initiate the formation of anoxic conditions in the sediment. As a result, toxic substances due to the high activity of anaerobic bacteria, affect
ion absorbtion by the plant (Hemminga, 1998; Delgado et al., 1999). Also in 2009–2011 period, extensive mucilageous layers on the benthic system were observed due to the eutrophic conditions and the opportunistic phytoplankton blooms prevailing in these sites (Aktan and 6
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Gümüşoglu, 2010; Güreşen and Aktan, 2014). Actually, eutrophication is well known to be one of the main pressures affecting seagrass meadows (Short and Wyllie-Echeverria, 1996; Delgado et al., 1999; Bianchi and Morri, 2000). Therefore, specific attention should be paid for these sites classified at the “borderline” values (moderate/poor) in order to minimize the possible stress factors through monitoring programmes. The biotic indices used in this study, have verified their reliability and feasibility in different environmental conditions of two Mediterranean islands, as also proved by other researches (Lopez y Royo et al., 2009b, 2011; Bermejo et al., 2014). They also confirm their interchangeable application to assess adequately the ecological status of P. oceanica meadows everywhere in the Mediterranean basin (Gobert et al., 2009; Lopez y Royo et al., 2011). It is obvious that the application of the biotic indices in this study, cannot effectively contributes to the construction of long-term data series, but initiates its development. Therefore, further cost-effective applications at the Mediterranean scale could be beneficial for monitoring the evolution of P. oceanica meadows as functional ecosystem services (Cullen-Unsworth and Unsworth, 2013; Vassallo et al., 2013). In conclusion, this study responding to the legislative obligations, provides a functional tool in terms of the land use planning and management implementations and meets the essential data deficiency in less evaluated regions (e.g. Turkey, Libya).
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