Environmental variation and macrofauna response in a coastal area influenced by land runoff

Estuarine, Coastal and Shelf Science 132 (2013) 34e44

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Environmental variation and macrofauna response in a coastal area influenced by land runoff Ioanna Akoumianaki a, *, Sokratis Papaspyrou b,1, Konstantinos Ar. Kormas b, 2, Artemis Nicolaidou b a b

Institute of Oceanography, Hellenic Centre for Marine Research, Anavissos 19013, Attiki, Greece Department of Biology, University of Athens, Panepistimiopolis 15784, Athens, Greece

a r t i c l e i n f o

a b s t r a c t

Article history: Available online 5 June 2012

Macrofauna community interactions with environmental variables in the water column (salinity, temperature, turbidity, transparency, suspended particulate matter, particulate organic matter, choloroplastic pigments) and in the sediment (granulometric variables, organic carbon and pigments) were investigated in a coastal area with high land runoff due to riverine and temporary stream discharges (Greece, Aegean Sea, Maliakos Gulf). Samples were taken along a distance-depositional gradient from the river mouth to the open sea at eight stations, at times of different precipitation regime from August 2000 to May 2001. The physical variables, such as transparency and median grain size, generally increased seawards, and parallelled the depositional gradient as opposed to measures of food inputs and hydrodynamic regime. High environmental heterogeneity was observed during peak precipitation. The total number of species increased seawards and from August (122 species) to May (170 species). Maximum abundance also increased from August (4953 m
2) to May (10,220 individuals m
2), irrespective of distance from river mouth. Species belonging to different functional groups, as to recolonization, feeding, motility and substrate preferences, coexisted at all times indicating high functional diversity. Nonparametric multivariate regression showed that at times of low, rising and falling precipitation 78 e81% of community variation was explained by environmental variables, indicating that macrofauna distribution and species composition respond to food inputs and sediment characteristics. During peak land runoff the communityeenvironment relationship weakened (57% of the variability explained). The diversity of functional traits of the most abundant species indicates that the macrofauna community can absorb the impact of increased turbidity, sedimentation and current-driven dispersion. The study offers baseline information for the integrated coastal zone management in microtidal areas with high land runoff under Mediterranean-type climate conditions. During peak land runoff the communityeenvironment relationship weakened (57% of the variability explained) whilst species distribution ranges increased. The study shows that the functional diversity in the study area prior to high discharge period enable macrofauna community to absorb the impact of increased turbidity, sedimentation and current-driven dispersion. The study offers baseline information for the impact of high land runoff in microtidal areas under Mediterranean-type climate conditions. Ó 2012 Elsevier Ltd. All rights reserved.

Keywords: benthos community structure land runoff Mediterranean

1. Introduction The distribution of organisms in relation to the environmental characteristics in their habitat is of central importance in ecology.

* Corresponding author. E-mail addresses: [email protected], [email protected] (I. Akoumianaki). 1 Present address: Department of Biology, University of Cadiz, 11510 Puerto Real, Cadiz, Spain. 2 Present address: Department of Ichthyology and Aquatic Environment, University of Thessaly, 38334, N. Ionia, Volos, Greece. 0272-7714/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2012.04.009

In coastal systems environmental factors are controlled by natural processes (e.g. water mass movements, sediment deposition) and anthropogenic activities such as land resource management, urbanization and dredging. Irrespective of habitat type, important abiotic structuring factors of coastal benthic communities, include characteristics of sedimentary environment (Gray, 1974; Rhoads et al., 1985; Snelgrove and Butman, 1994; Anderson et al., 2004; Akoumianaki and Nicolaidou, 2007), sedimentary organic matter lability (Pearson and Rosenberg, 1978; Albertelli et al., 1999), water column phytodetrital concentrations (Josefson and Conley, 1997; Moodley et al., 1998), contaminant levels (Warwick et al., 1990)

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and hydrological gradients (e.g. turbidity, salinity) (McLusky, 1993). In particular, sediment discharges may adversely affect bottomdwelling organisms by smothering immobile forms or forcing mobile forms to migrate and by altering grain size distribution, thus impacting colonization during recovery (Gray et al., 1997). In addition, the fine sediments in areas with high land runoff are susceptible to water agitation and in combination with discharged particulate material can remain in suspension for variable periods of time, impacting light penetration, primary productivity and benthic surface dwelling organisms, especially filter feeders. Finally, the absorption or adsorption of land-derived contaminants in the discharged particles along with sediment displacement through resuspension and near-bottom currents, can change or even destroy benthic habitats (Thrush et al., 2004). Therefore, the identification of benthic response to the environmental variables associated with land runoff is of great importance (GESAMP, 1994). Studies in coastal areas with high riverine inputs, such as the continental shelves off major rivers, have suggested that the interaction between benthic community and sedimentary processes is dependent upon depositionaledistance gradients from the river mouth (Rhoads et al., 1985) and/or the temporal variability in water and sediment discharge rates (Rhoads et al., 1985; Aller and Aller, 1986; Aller and Stupakoff, 1996). In the Mediterranean Sea, in particular, macrofauna community structure at the Gulf of Lions was influenced by the periodicity of Rhone River flood events (SalenPicard et al., 2003) and at Alfacs Bay by the fluctuations of the Ebro River outflow (Palacin et al., 1991). The macrofauna relationship to grain size and food inputs closely followed the water mass circulation temporal pattern of the plumes of the Danube River at the northwestern Black Sea shelf (Wijsman et al., 1999) and the Po river at the northwestern Adriatic Sea (Moodley et al., 1998). Similarly, studies regarding the effect of river dilution plumes on Mediterranean benthic communities along the shelves seaward of small rivers, i.e. draining areas smaller than 104 km2, although scarce, indicate that macrofauna community is influenced by depositional gradients (Kormas et al., 1997; Albertelli et al., 1999; Akoumianaki et al., 2006). Sediment accumulation rates in the submarine beds of the small mountainous rivers of South Europe range between 3 and 6 m over the last 7000 yr (Poulos et al., 1996a). These values are about 30e200 times lower than those of major world rivers (Milliman and Syvitski, 1992) and about 5e10 times lower than those of Rhone (Radakovitch et al., 1999) and Po rivers (Frignani et al., 1996). On the other hand, temporary rivers and streams that are dominant throughout arid and semiarid regions, cover about 30% of

35

the total land surface (Thornes, 1977). Such streams are very common in Mediterranean catchments and the majority of them fall dry during summer. Temporary rivers are linked to the problem of water stress in several aspects, including water scarcity during summer and the creation of runoff and pollution pulses during the rainy period that create flush floods, which carry high loads of sediments, solutes and pollutants (Thornes, 1977). All the aforementioned characteristics of sediment yields and spatial distribution of small mountainous rivers and temporary streams raise the concern about their impact on coastal ecosystems. In this study, we investigated the relationship between macrofauna community interactions with environmental variables in a coastal area with freshwater discharges from a small mountainous river and several temporary streams (Maliakos Gulf, Aegean Sea, Greece). Maliakos is a shallow semi-enclosed gulf that receives in its innermost part sediments and freshwater from River Spercheios, spreading as buoyant plumes in an offshore direction (Poulos et al., 1996b). As a result, a depositional gradient exists with consistently finer sediments, denser benthic nepheloid layer and a lower salinity in the surface nepheloid layer from the outer Maliakos towards the mouth of River Spercheios. Sediments discharged by several temporary streams also enter this coastal system forming temporary fans along the coastline. The environmental variables chosen in the present study are those that can be recorded on spatial and temporal scales in relation to the fluctuations of land runoff and that are likely to be related to macrofauna species distribution. The aim of the study is to explore how freshwater and sediments discharged by temporary streams influence 1) food inputs to benthos and substrate characteristics, 2) macrofauna species diversity, abundance and composition and 3) the relationship between macrofauna community and environmental variables along the seaward depositional gradient. 2. Material and methods 2.1. Study area Maliakos Gulf (38 450 N; 22 310 E), is aligned in an eastewest direction and covers ca 200 km2. It is separated by two headlands to inner-west and outer-east Maliakos and communicates with the Aegean Sea through the outer part (Fig. 1). Maximum depth is 20 m in the inner gulf and 50 m in the outer. Approximately 1,140,080 m3 of sediments are annually exported to Maliakos Gulf from River Spercheios, a major Greek river, that drains an area of 1664 km2 characterized by high elevations and steep slopes (Poulos et al.,

Fig. 1. Study site and sampling stations showing Spercheios River mouth and the temporary streams along the north coast of Maliakos Gulf.

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1996b). These riverine sediments are mainly deposited in the delta front of the inner part of the gulf at a rate of 0.04 km2/yr (Zamani and Maroukian, 1980). The River Spercheios has a mean annual water discharge of 62 m3/s, varying between 110 m3/s (in January) and 22 m3/s (in August) (Therianos, 1974). Flood events are common and may exceed 800 m3/s (Zamani and Maroukian, 1979). A number of temporary streams discharge along the north coast. Zamani and Maroukian (1980) have mentioned the presence of a weak coastal current flowing from east to west, along the northern part of the gulf. Wind direction (from the west and the northwest) and the tidal movements (tidal range: 1 m) enable an anticlockwise water mass circulation pattern in the gulf that allows the homogenization of the water column throughout the year and the fast turnover of the water masses (Kormas et al., 2003). This results in an average seawater salinity in the inner Maliakos close to that of the open sea which is above 38 (Kormas et al., 2003), although annual freshwater inputs through River Spercheios exceed 500  106 m3 (Data from the Greek Ministry of the Environment, Constructions and Public Works). Due to the fine sediment and the bottom currents a bottom nepheloid layer was observed regularly by divers from the bottom to approximately 1 m above it. A detailed description of the conditions in the delta front area is given by Akoumianaki and Nicolaidou (2007). 2.2. Collection and processing of samples Samples were collected at eight stations, four in the inner (S1eS4) and four in the outer (S5eS8) part of Maliakos Gulf (Fig. 1), on four occasions covering the seasonal range of precipitation conditions: low in August 2000 (A), rising in November 2000 (N), peak in February 2001 (F), and falling in May 2001 (M). All stations were set at a depth of 20 m except for station S1 which was at 12.5 m. With respect to the distance-depositional gradient from the river mouth to outer Maliakos Gulf, stations S1, S2, S3 and S4 in inner Maliakos were set at a distance of 2, 2, 5, and 10 km away from the mouth of River Spercheios, respectively, while stations S5, S6, S7 and S8 in outer Maliakos were set at a distance of 13, 15, 18 and 15 km away from the river mouth, respectively (Fig. 1). All distances were measured with a GPS as the boat moved to the sampling stations from the river mouth. Vertical profiles of salinity (in Practical Salinity Units), temperature ( C) and turbidity (Tu) in the water column were obtained using a Seabird CTD while transparency depth (m) (Secchi) was measured with a 20 cm Secchi disk. Transparency was used as a proxy of light penetration enabling photosynthesis in the water column whereas turbidity accounted for the amount of sediment particles entrained in the river plume. Seawater samples for the analyses of suspended material and chloroplastic pigments were taken at the surface and the bottom nepheloid layers (SNL and BNL, respectively) and were filtered within 3 h after sampling on GF/F filters. Triplicate quantitative benthic samples were taken by means of a Ponar grab (sampling area: 0.05 m2, penetration depth: 15 cm). A cut-off syringe core subsample (2.9 cm inner diameter, 8 cm length) was taken from each grab for the determination of sediment biochemical parameters, i.e. total organic carbon (TOC), and chloroplastic pigments at the top 2 cm (0e2 cm sediment depth) in November 2000 and February 2001 and May 2001. The August samples were destroyed due to freezer malfunction in the summer. Particle size analysis was based on subsamples taken from a fourth grab sample at each station. All filters and sediment core subsamples were immediately stored frozen at
22  C for subsequent laboratory analyses. Sediment biochemical parameters were measured using freeze-dried homogenized aliquots. The concentrations of suspended particulate material (SPM) and particulate organic material (POM) were

analysed as in Parsons et al. (1984). Chlorophyll a and its degradation products, i.e. phaeopigments (Phaeo), from filters (Chl aw) and sediment (Chl a) samples were extracted with 90% acetone and determined fluorometrically according to Yentsch and Menzel (1963). Then, the sum of chlorophyll a and phaeopigments were used to calculate chloroplastic pigments equivalent in the water column (CPEw) and the sediment (CPE). TOC was estimated as in Nelson and Sommers (1975). Median grain size (md), sorting coefficient (s) and skewness (sk) were determined according to Buchannan (1984). Environmental variables were used as measures of food inputs in the water column and sediment (i.e. POM, CPEw/ POM, Chl aw, Chl a/CPE and TOC), suspended load (i.e. SPM, Tu and Secchi), and deposition and hydrodynamics (i.e. md, s and sk) (Gao and Collins, 1994). Following syringe core subsampling, the remainder of the sediment from each grab replicate (area: 0.047 m2) was sieved through a 0.5 mm mesh and the residue was immediately fixed in 4% formaldehyde. The organisms retained were sorted enumerated and identified to species level. The species from all major taxa were classified to functional groups according to their food acquisition mode, i.e. surface (S) or subsurface (B) deposit feeders, suspension feeders (F), omnivorous (O) and carnivorous (C) feeders, using the ecological literature for families, genera or species (e.g. Woodin, 1976; Fauchald and Jumars, 1979; Levinton, 1982; Holdich and Jones, 1983; Kamermans, 1994). The species were also classified, following Rhoads et al. (1978), in (1). first-order opportunistic species (Group 1 colonizers), i.e. pioneering species in highly disturbed sediments, (2). second-order opportunistic species (Group 2 colonizers), i.e. species that reach high abundances in slightly to highly disturbed sediments and (3) equilibrium species (Group 3 colonizers), that may also appear early and maintain constant and persistent but relatively low populations under undisturbed conditions. Additional information for the present classification was taken from the review by Borja et al. (2000). 2.3. Statistical analyses The relations of environmental variables with community structure were analysed based on replicates at each station (n ¼ 3). To account for the structure of the sedimentary environment, variables measured in both the water (i.e. SPM, POM, Chl aw, Secchi, Tu, CPEw/POM) and the surface sediments (i.e. md, sk, s, TOC, Chl a/ CPE) were used in multivariate analyses. The Pearson product moment correlation coefficients were also calculated between distance from the mouth of River Spercheios and macrofauna community variables, i.e total number of individuals, numbers of species per grab sample (0.05 m2) and dominant species densities (per m2), to explore macrofauna response to the depositional gradient. Community structure was assessed using macrofauna species that exceeded 1 individual 0.05 m2 at each sampling time. Non-metric multidimensional scaling (nMDS) was carried out to visualize patterns in environmental and species variables at each sampling time. Then, projection biplots were drawn onto to environmental and community MDS axes to examine their Pearson correlation relationship with environmental and species variables, respectively. The relationship between the aforementioned set of environmental variables and the community assemblage was investigated using non-parametric multivariate multiple regression (DISTLM) (McArdle and Anderson, 2001) and visualized using distance-based redundancy analysis (db-RDA) (Legendre and Anderson, 1999), after removing environmental variables that highly correlated (r > 0.8) with other variables. Species variables were square root transformed to retain information regarding relative abundances but to reduce differences in scale among them (Clarke and Green, 1988). Euclidean and BrayeCurtis (Bray and

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37

SPM was highest in February, exceeding 30 mg l
1 along the north coast (S3, S4, S5, S6) while high POM levels (up to 29 mg l
1) were also observed in February near the outflow of temporary streams (Table 1). Strong correlations of POM in the BNL with SPM (r ¼ 0.9) and Secchi (r ¼
0.8) were observed in May and weaker correlations were found in February (r < j0.5j). Contribution of POM to SPM in the BNL increased from 40% in August to 80% in November and February along the north coast and then decreased to less than 23% in May. Chl a values in the BNL were lowest in August (minimum in S4 ¼ 0.1 mg l
1) and highest in May (maximum in S8 ¼ 1.6 mg l
1). CPEw/POM was generally lower than 30% in inner Maliakos and lower than 10% in outer Maliakos except for May when it ranged between 7 and 97%. Significant correlations among water column variables in the BNL and the distance from the river mouth were only detected for Tu (
0.7 < r <
0.5, p < 0.05) and Chl aw (
0.63 < r <
0.5, from August to February and r ¼ 0.87, May, p < 0.05). POM correlated

Curtis, 1957) dissimilarities were calculated between all pairs of environmental and species observations, respectively. All multivariate analyses were obtained using Primer 6 for Windows (Clarke and Gorley, 2006) and Permanovaþ for Primer (Anderson et al., 2008). 3. Results 3.1. Environmental structure The physical and chemical properties of the water column in the SNL and BNL as well as the sediment characteristics of the area studied are given in Table 1. Temperature in the BNL peaked in August as would be expected and salinity in May. Gradual seaward decreases of BNL Tu and increases in Secchi were observed at all sampling times. Temperature, salinity and turbidity values in the SNL were positively and significantly correlated with values in the BNL (0.5 < R < 0.9, p < 0.05).

Table 1 Water column and sediment characteristics at all sampling times and stations. Variable abbreviations and measurement units as in Material and Methods. Water column

Sediment

Station Turbidity

Temperature ( C)

Salinity (psu)

Time

SNL

BNL

SNL

BNL

3.7 3.4 4.4 28.3

25.9 17.5 12.2 20.5

25.9 17.8 13.4 19.0

36.5 36.2 36.8 34.6

36.5 36.7 37.1 36.9

1.8 1.1 2.4 2.3 2.9 4.9 125.5 132.4

26.1 17.2 13.2 20.5

24.9 17.5 13.4 15.9

36.1 36.3 36.4 36.5

S1 A N F M S2 A N F M

SNL 3.3 2.4 3.4 34.7

BNL

Secchi (m) SPM (mg l
1)

POM (mg l
1)

Chl aw (mg l
1)

Phaeo (mg l
1)

SNL

BNL

SNL

md (mm) s (phi) sk (phi)

SNL

BNL

SNL

BNL

BNL

3.1 3.4 2.7 2.7

8.5 5.0 16.9 37.6

8.6 6.8 13.7 39.6

1.7 0.4 0.4 6.8

1.5 0.6 0.4 6.8

0.8 0.7 0.7 1.1

0.7 0.6 0.8 0.4

3.5 2.9 0.3 0.3

2.4 2.7 0.4 0.1

12 6 6 11

1.11 0.32 1.01 0.91

0.18 0.00
0.21 0.33

36.3 36.6 37.3 37.9

7.3 5.0 4.0 2.5

8.0 15.3 6.7 11.9

6.0 6.0 6.0 13.6

1.9 1.6 1.2 2.3

0.9 0.2 5.2 3.5

0.3 0.6 1.0 0.3

0.3 0.5 1.0 0.7

>0.1 2.5 0.2 >0.1

>0.1 2.7 0.4 0.1

13 12 11 12

1.43 1.41 1.21 1.36


0.03 0.00 0.02 0.05

S3 A N F M

13.0 2.0 1.5 1.5

2.5 3.4 4.4 7.8

27.4 17.8 12.9 19.7

25.1 18.0 13.3 15.9

36.4 36.8 36.8 37.0

36.3 36.9 37.1 37.8

11.0 4.5 9.0 8.0

3.5 7.1 31.5 6.9

4.1 7.8 33.6 7.3

1.0 1.5 27.7 1.5

2.7 1.3 9.3 1.3

0.5 1.2 0.5 0.3

0.3 0.8 0.9 0.9

>0.1 0.3 0.1 0.1

0.6 0.2 0.2 0.2

5 14 25 60

3.28 1.89 3.66 2.96

0.11
0.12
0.34 0.25

S4 A N F M

1.0 1.5 2.0 1.5

2.3 2.8 4.2 3.9

26.1 17.7 12.9 20.4

23.9 18.0 13.4 16.1

36.1 36.7 36.9 36.0

36.5 36.8 37.3 38.0

12.0 5.2 6.0 8.0

6.2 3.7 30.6 17.2

5.0 9.3 33.6 9.3

0.9 1.3 4.7 6.1

2.4 5.3 2.0 2.0

0.3 1.1 0.9 0.3

0.1 0.6 0.7 1.0

>0.1 0.3 0.2 >0.1

>0.1 0.2 0.2 0.2

17 15 14 17

2.38 1.70 2.21 3.51


0.68 0.09 0.02
0.47

S5 A N F M

0.8 1.9 1.5 2.0

0.9 2.0 1.9 4.4

25.6 17.7 12.2 19.4

23.5 17.9 13.3 16.4

36.3 36.7 36.7 37.1

36.5 36.7 37.2 37.9

14.0 7.0 8.7 9.0

5.6 5.0 30.9 13.2

6.0 10.5 34.8 8.7

1.7 1.8 3.1 1.9

1.0 1.8 29.2 1.6

0.2 0.7 0.7 0.4

0.2 0.8 0.6 1.1

>0.1 0.3 0.2 0.1

>0.1 0.2 0.2 0.2

16 16 16 25

2.85 1.76 2.19 3.51


0.75 0.03 0.20
0.47

S6 A N F M

0.9 1.5 1.5 2.0

1.4 2.0 1.9 2.4

25.6 17.7 12.3 19.8

24.2 17.7 13.3 16.2

35.8 36.7 36.4 37.1

36.6 36.7 37.2 37.6

14.0 6.8 8.0 9.0

5.5 4.7 35.5 17.2

3.2 6.0 32.1 11.6

3.6 0.3 8.3 9.1

1.3 2.9 4.3 0.1

0.3 0.6 0.7 0.2

0.2 0.4 0.5 1.1

0.5 0.2 0.2 0.1

>0.1 0.1 0.1 0.2

27 16 287 62

3.10 1.82 2.72 3.23


0.59
0.15 0.30
0.25

S7 A N F M

0.5 0.7 1.5 1.5

0.9 2.4 0.9 2.4

25.0 17.9 11.8 19.4

23.5 17.9 13.2 16.3

36.1 36.7 36.3 37.1

36.5 36.9 37.2 37.6

16.0 9.2 5.0 10.0

7.3 3.7 3.3 7.6

6.4 5.5 4.5 10.7

2.4 0.9 0.4 1.2

1.5 2.2 0.6 2.0

0.3 0.4 0.3 0.3

0.4 0.2 0.4 1.6

>0.1 0.1 0.1 >0.1

>0.1 0.1 0.2 0.3

257 111 469 129

2.92 2.21 3.22 2.55

0.31 0.26 0.50 0.14

S8 A N F M

0.9 1.5 2.0 2.0

1.3 1.3 2.5 3.4

25.9 17.8 12.3 19.1

23.5 17.7 12.7 17.1

36.0 36.7 36.8 37.1

36.8 36.7 37.1 37.5

11.0 4.0 4.0 8.5

4.9 4.9 8.0 15.3

2.3 5.8 6.4 7.5

1.5 0.7 2.9 0.2

0.8 0.9 2.9 1.7

0.1 0.6 0.5 0.4

0.2 0.6 1.0 1.5

0.2 0.2 0.1 0.1

0.3 0.2 0.3 0.2

33 18 14 14

3.25 1.08 1.50 1.37


0.47 0.31
0.14 0.03

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with distance only in May and November (r ¼ 0.8 and r ¼
0.6, p < 0.05, respectively). Finally, Tu positively correlated with Chl aw in August and February (r ¼ 0.65, and r ¼ 0.96, p < 0.05, respectively). The submarine depositions of Maliakos Gulf were generally characterized by poorly sorted (s > 1) clayey silts to sandy silts. Median grain size (md) ranged from 5 to 60 mm in inner Maliakos, and between 16 and 469 mm in outer Maliakos. Sediment skewness (sk) varied from
0.75 (coarsely skewed) to 0.5 (fine skewed) (Table 1). Md and sk were significantly correlated to distance (r > j0.6j); in the case of sk the correlation was negative in August and May. TOC levels varied between 0.4% and 2.2%, usually exceeding 0.8% in the inner part (Fig. 2). Chl a concentrations ranged from 0.7 (S2, May) to 3.4 (S1, May) mg g
1 and were considerably enhanced in May at most stations apart from S2 and S3 (Fig. 2). TOC was weakly associated to distance (r ¼ 0.5, p < 0.05) in February while there was no trend in Chl a distribution. MDS plots based on environmental variables mainly in the BNL and the sediment indicated considerable temporal variation in the environmental spatial patterns (Fig. 3). In August, all stations except for S7 are grouped together on the basis of a smaller Md, while other variables were not correlated to this ordering. In November there was still an environmental gradient from the innermost to the outermost stations driven by changes in s, and the highly intercorrelated variables md, sk, Secchi and CPEw/POM (Fig. 3). However, stations S3, S4, S5, S6 and S8 form a separate cluster on the basis of higher SPM, POM, Chl aw and lower TOC and Chl a/CPE. In February the granulometric gradient is not obvious and the separation of stations is based mainly on characteristics of the water column and TOC. The outermost stations S7 and S8 are grouped together with the inner station S2. Finally, in May the grouping suggests a higher hydrodynamic regime along the north coast of Maliakos Gulf (i.e. increase of s at S3, S4, S5, S7) while in the inner station S2 the turbidity remains high.

3.2. Macrofauna community Average macrofaunal density varied between 71  4 (S2, November) and 511  20 (S3, May) individuals per grab sample (i.e. per 0.05 m2) (Fig. 4a). Average numbers of species per ponar grab sample ranged from 15  6 (S2, August) to 70  6 (S3, May) (Fig. 4a). Abundance response to the distance-depositional gradient was variable during the course of the study, with significant positive correlations in August (r ¼ 0.4, p < 0.05) and November (r ¼ 0.73, p < 0.05) and significant negative correlation in May (r ¼
081, p < 0.05), while no relation between abundance and distance from the river mouth was detected in February. Species richness response was generally consistent, with high positive correlations between the number of species and the distance from the river mouth (0.60 < r < 0.75, p < 0.05) at all times except for May (r ¼ 0.20, p > 0.05). Mollusca (August and November) and crustaceans (February and May) in the inner and polychaetes in the outer Maliakos stations comprised the most abundant major taxa (Fig. 4b). In terms of species numbers, polychaetes counted by far the highest numbers per grab sample, followed by mollusca in the majority of the stations (Fig. 4b). Strong correlations (r > 0.85, p < 0.001) were detected between the abundance and the number of species of polychaetes in November and May and of molluscs in November (Fig. 4b). Of the 218 species recorded on the whole, 122 were present in August, 110 in November, 154 in February and 170 in May. The dominant species i.e. those exceeding 200 individuals m
2, or approximately 35%, at any station, included species that displayed sporadic or spatially and temporally variable distribution and species with a consistent response to the distance-depositional gradient (Table 2). The latter comprised the bivalve Corbula gibba and the polychaete Nephtys hystricis, that were negatively associated (
0.43 < r <
0.80, p < 0.05) with distance from the river mouth at all times, as well as the species Diplocirrus glaucus, and

Fig. 2. Variation in the composition of organic matter in the sediment surface, i.e. (0e2) cm, at the eight stations along Maliakos Gulf in November 2000, February 2001 and May 2001 (a) Total Organic Carbon (TOC) concentrations. (b) Concentrations of Chlorophyll a (Chl a), phaeopigments (phaeo) and of chloroplastic pigments equivalent (CPE). The ratio of chlorophyll a to CPE (Chl a/CPE) is also presented.

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39

Fig. 3. Projection biplots of the environmental variables onto the non-metric MDS ordination plots based on Euclidean dissimilarities between all pairs of environmental observations. Vectors indicate direction and magnitude of Pearson correlation coefficient between the variable and the MDS axes. Variables with small projection are not shown. Variable abbreviations as in Table 1.

Thyasira flexuosa, that positively responded (0.44 < r < 0.82, p < 0.05) to the seaward depositional gradient (Table 2). The MDS plots demonstrated a clear separation between the innermost (S1 and S2) and the outermost stations (S6 and S7) at all sampling times (Fig. 5). Stations S3 and S4 tended to cluster together and apart from S1 and S2 while S8 was ordered closer to inner than outer Maliakos stations during rising, peak and falling discharge periods. As shown by the MDS biplots, the species that were negatively correlated with the distance from the river mouth, such as the suspension feeding C. gibba, Lepton nitidum, Mysella

bidentata and Turitella communis, the deposit feeding Nucula turgida and the carnivorous N. hystricis (Table 2), displayed particularly high abundances at stations S1 and S2 (Fig. 5). On the other hand, the majority of the species that positively responded to distance and thus characterized outer Maliakos community, such as the deposit feeders D. glaucus, Paralacydonia paradoxa, Spiophanes bombyx and the predatory Hyalinoecia brementi, Lumbrineris latreilli and Tubulanus polymorphus (Table 2), were consistently associated with S7 (Fig. 5). However, outer Maliakos’ species, expanded their distribution establishing sizeable populations at the inner part of

Fig. 4. Relation between abundance and species richness at each sampling time. (a) Total abundance versus total species richness at each station. (b) Number of individuals versus number of species per grab of major taxa, i.e. Polychaeta (POL), Mollusca (MOL), Crustacea (CRU), Echinoderma (ECH) and Miscellanea (MIS) at inner (open symbols) and outer (closed symbols) Maliakos.

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Table 2 List of the most abundant species i.e. exceeding 200 individuals m
2 in at least one of the stations at each sampling time. Functional classification, average abundance  CV% (coefficient of variation) and Pearson correlation coefficients (r) among species and distance from Spercheios River mouth are given. Feeding mode: S ¼ surface deposit feeder; B ¼ subsurface deposit feeder; Su ¼ suspension feeder; O ¼ omnivorous; C ¼ carnivorous. Colonization pattern (sensu Rhoads et al., 1978): Group 1 (G1) ¼ first order opportunists; Group 2 (G2) ¼ second order opportunists; Group 3 (G3) ¼ equilibrium species. Only significant relationships are presented. *p < 0.05, **p < 0.01, ***p < 0.001. Species

Feeding/colonization

Ampelisca sp. Amphiura chiajei Apseudes latreilli Corbula gibba Diplocirrus glaucus Ditrupa arietina Hyala vitrea Eudorella nana Hyalinoecia brementi Lanice conchylega Leptocheirus maryae Lepton nititdum Levinsenia gracilis Lumbrineris latreilli Magelona minuta Mysella bidentata Nephtys hystricis Nucula turgida Onchnesoma steenstrupi Paralacydonia paradoxa Phoronis psamophila Pseudoleiocapitella fauveli Spiophanes bombyx Sternaspis scutata Terebellides stroemi Thyasira flexuosa Tubificoides sp. Tubulanus polymorphus Turitella communis

Su/G2 S or Su/G3 S or Su/G2 Su/G2 S/G3 Su/G3 C/G2 S or Su/G3 O/G3 Su/G3 Su/G2 Su/G3 B/G2 O/G2 or 3 S/G3 Su/G2 C/G3 B/G3 B/G3 B/G3 Su/G3 B/G2 S/G2 B/G2 S/G3 B/G2 B/G1 or G2 C/G3 Su/G3

No of individuals m
2  CV% A 208 48 123 58 46 68 220 3 36 0 154 105 57 134 61 283 93 48 6 97 48 81 16 58 85 79 0 98 38

N         

67 181 68 63 97 167 81 151 275

               

191 212 136 91 108 83 63 134 283 277 90 108 266 85 71 129

 86  101

252 12 109 55 59 22 196 0 29 0 244 18 20 183 48 211 53 72 2 0 83 64 13 45 47 132 65 84 65

Pearson correlation coefficient, rp F

      

86 85 94 97 115 283 94

 265         

88 122 125 116 112 50 94 103 185

        

71 103 122 60 65 76 271 91 122

the gulf in February. This resulted in a less clear separation between outer and inner stations as clearly shown by the MDS biplot of February. Crustaceans, such as Apseudes latreilli and tube building amphipods (e.g. Leptocheirus maryae and Ampelisca sp.), the carnivorous gastropod Hyala vitrea and the deposit feeders T. flexuosa, Terebellides stroemi and Magelona minuta (Table 2) were ubiquitous at the study site and their contribution to macrofauna community spatial changes depended on time (Fig. 5). Species found associated with different stations at each sampling time included Iphinoe serrata, L. maryae, Clymenura sp., M. minuta, Aricidea claudia (Fig. 5). The species Ditrupa arietina and Lanice conchylega appeared to have very high abundance at only one station, i.e. S3 or S4 (Fig. 5). Certain species, including Ampelisca sp., Levinsenia gracilis and Pseudoleiocapitella fauveli, exhibited significantly higher abundances at the outer part of the gulf in August and/or November but peaked at one of inner Maliakos stations in May (Table 2, Fig. 5). Among the dominant taxa there was only one Group-1 species (i.e. Tubificoides sp.) (Table 2). 3.3. Macrofaunaeenvironment relationship The db-RDA plots showed time-dependent patterns similar to those in the MDS plots (Figs. 3 and 5). In August, the first 2 db-RDA axes explained 49.6% of the variability in the species data and 61.16% of the relationship between the species and the environmental variables (Fig. 6). The separation in community structure between inner and outer Maliakos was based on differences in Tu that increased riverwards, and md and Secchi that increased seawards. Within inner Maliakos there were observed changes in community structure along gradients of SPM, Chl aw and POM from S1 and S2 towards S3 and S4 (Fig. 6).

214 30 99 93 52 1 304 69 5 76 506 53 60 89 52 185 69 91 36 14 56 10 78 117 93 133 7 40 48

M                             

50 256 103 59 127 283 54 201 283 279 175 179 85 93 125 93 100 92 254 145 81 80 229 57 152 57 177 105 105

478 8 186 281 38 6 183 21 4 8 1369 105 352 297 123 282 105 74 76 45 242 61 10 128 144 159 19 63 44

A                             

77 130 83 98 86 222 110 143 198 283 72 211 100 88 58 67 70 99 183 198 200 100 94 80 93 60 136 27 103

N

F 0.65** 0.43*

M 0.80***


0.77** 0.74*


0.77* 0.54*


0.69**
0.64* 0.57*


0.71***


0.69**


0.57*

0.52*

0.54*

0.57* 0.60* 0.47*
0.54*
0.60*
0.48*

0.63* 0.46*
0.50*
0.88**

0.52* 0.76** 0.53* 0.69* 0.56* 0.96***
0.48*

0.82** 0.76** 0.77* 0.39* 0.50* 0.66*
0.67*


0.43* 0.72*

0.55*


0.62*
0.65* 0.85**
0.55*
0.78*
0.67* 0.54* 0.71*
0.52* 0.44* 0.37*
0.44* 0.42*
0.40*

0.63*


0.80** 0.53* 0.55*
0.67* 0.64*

0.67**


0.41*

In November, the first 2 db-RDA axes explained 55.51% of the variability in the species data and 71.46% of the relationship between the species and the environmental variables (Fig. 6). At this time, the assemblage at S7 was ordered separately from the assemblages at the remainder of the stations along a gradient of increasing md, Secchi depth and Chl a/CPE and decreasing Chl aw towards S7 (Fig. 6). In parallel, the assemblages at S1 and S2 were ordered separately from that at S3eS6 on the basis of inward increasing gradients of Tu and CPEw/POM and outward increase in Chl aw, SPM, and POM. In February, the first 2 db-RDA axes explained 31.8% of the variability in the species data and 44.6% of the relationship between the species and the environmental variables (Fig. 6). This coincided with a reduced explanatory power of the species variation by the environmental variables (Table 3b). The biplot shows that macrofauna responds to an inward increase of Tu, resulting in the separation of the assemblage at S1, S2 and S8 from the assemblages at the remainder of the gulf. In May, the first 2 db-RDA axes explained 51.54% of the variability in the species data and 64.58% of the relationship between the species and the environmental variables (Fig. 6). In the biplot macrofauna assemblages were aligned along a seaward increase of Secchi and Chl a/CPE, the latter variable found to be redundant, and thus not included as an explanatory variable in the model, as it had similar to Secchi influence upon macrofauna spatial structure. Non parametric multivariate regression showed that 7e9 environmental variables together explained 56.5 (February)e 81.1% in August (Table 3). When environmental variables were considered individually, md explained considerable part of the variation in the species data at all times although transparency (Secchi) was more important in August and May. TOC was highly correlated with POM in November (r ¼
0.9) and CPEw/POM in

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41

Fig. 5. Projection biplots of the species onto the non-metric MDS ordination plots based on BrayeCurtis dissimilarities between all pairs of square root transformed taxa abundances in August and November 2000 and in February and May 2001. Vectors indicate direction and magnitude of Pearson correlation coefficient between the species variable and the MDS axes. Only species with high projection are shown at each sampling time.

Fig. 6. Distance-based redundancy analysis (db-RDA) ordination plot for the fitted model of Maliakos Gulf macrofauna community data (based on BrayeCurtis after square root transformation of abundances) versus environmental variables at each sampling time. Variable abbreviations as in Table 1.

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Table 3 Results of non-parametric multiple regression of multivariate species data on individual environmental variables for (a) each variable taken individually (ignoring other variables) and (b) overall best solutions, where the smallest value of Akaike’s Criterion (AIC) was found after fitting all of the possible models. %Var: percentage of variance in species data explained by that variable or the model. SS: Sums of Squares. RSS: Residual Sums of Squares. Variable abbreviations as in Table 1. Variable

Var (%)

Pseudo-F

August

Var (%)

Pseudo-F

November

(a) Variables 1.SPM 2.POM 3.Chl aw 4.Secchi 5.Tu 6.md 7.sk

considered 8.98 8.78 12.61 29.54 13.49 26.29 8.06

individually 2.15* 2.12 3.17** 9.22*** 3.43** 7.85** 1.93

Total SS (trace): 39020 AIC

Variable

Var (%)

RSS

(b) Overall best solutions 153.46 81.1 7374

1.SPM 2.POM 3.Chl aw 4.Secchi 5.Tu 6.CPEw/POM 7.md 8.sk 9.Chl a/CPE

Variable

Var (%)

Pseudo-F

February 2.46* 3.90** 5.75** 4.74** 1.79 6.43*** 9.90*** 2.39* 0.39

10.06 15.08 20.72 17.72 7.53 22.63 31.05 9.83 1.76

Total SS (trace): 35063

Variable

Var (%)

Pseudo-F

12.88 17.88 13.50 15.12 16.09 11.64 3.79 16.79

3.25** 4.78*** 3.43** 3.92** 4.22** 2.89** 0.86 4.44***

May

1.Secchi 2.POM 3.Tu 4.CPEw/POM 5.md 6.s 7.Chl a/CPE

10.49 6.49 19.58 11.14 19.44 11.52 12.57

2.58** 1.53 5.36*** 2.76** 5.31*** 2.86** 3.16**

Total SS (trace): 39818

1.SPM 2.Secchi 3.CPEw/POM 4.md 5.s 6.sk 7.TOC 8.Chl a/CPE

Total SS (trace): 30550

Variables

AIC

Var (%)

RSS

Variables

AIC

Var (%)

RSS

Variables

AIC

Var (%)

RSS

Variables

All

156.9

77.68

7828

All

169.3

56.50

17303

2e5, 7

149.2

79.81

6169

1e6

February (r ¼ 0.8) and was thus omitted from the analyses at these sampling times. 4. Discussion 4.1. Environmental changes along the depositional gradient The present study shows that only during the period of low precipitation, and hence low land runoff, the environment of Maliakos Gulf is structured according to the distance-depositional gradient from the river mouth to outer Maliakos. Of the variables studied only turbidity and Chlorophyll a in the BNL and md in the sediment correlated with distance from the river mouth at all seasons, higher turbidity and lower md always occurring in the inner Maliakos stations. This is in accordance with the seaward distance-clay mineral depositional gradient from the river mouth to outer Maliakos described by Poulos et al. (1996b). Other environmental variables, such as estimates of organic inputs in the BNL and the sediment, varied spatially within each part of the Gulf without displaying any consistent trend along the distance-depositional gradient during the course of the study. This can be attributed to the temporal variability of freshwater and sediment runoff from both the river and the streams driven by rainfall. Indeed, during rising and peak precipitation high SPM and POM in the north coast were observed near the outflow of temporary streams. In contrast, during the period of falling precipitation, when snow melt-down induces high freshwater discharges from Spercheios river but does not affect outflow from temporary streams, POM increased towards the river mouth. On the other hand, the variable grain size distributions in the sediment (sk and s, Table 1) suggest the stirring effect of water agitation on sediment. This is also supported by the high turbidity in the BNL, which not always correlated significantly with turbidity in the SNL. However, even though resuspended organic material evidently contributes to POM concentrations in the BNL, the temporal variation of POM, indicates that land runoff rather than resuspension control POM spatial distribution. The lack of correlation between organic inputs and the distancedepositional gradient could be also attributed to the function of the phytoplankton community as a filter of fine suspended material discharged by rivers through the formation of flocs between fine particles and the phytoplankton cells (Ayukai and Wolanski, 1997). This mechanism speeds up the sedimentation, and thus the removal of phaeopigments from the water column, allowing for

their incorporation to the sediment phaeopigment pool which is readily available to benthic decomposers and deposit feeders. Therefore, the low CPEw/POM observed in May in inner Maliakos as opposed to the high levels in outer Maliakos can be also attributed to the river rather than stream sediment discharges. That said, Chl aw varied at a lower range of levels than in other coastal areas without freshwater discharges in the Eastern Mediterranean (Stergiou et al., 1997) but at a similar range with delta front areas in the Mediterranean (Cruzado et al., 2002; Bernardi Aubry et al., 2004). In general, our results agree with those from previous studies in Maliakos Gulf (Christou et al., 1995; Kormas et al., 2003). 4.2. Macrofauna response to depositional gradient Changes in the species abundance and composition of macrofauna community along Maliakos gulf were related (up to 81.1%) with the spatially heterogeneous environmental variables measured in the present study. This strong link indicates that these environmental variables are among those driving the greatest differences in the spatial distribution of macrobenthos in this coastal environment characterized by high land runoff. Great similarities in speciesegenus composition were observed between Maliakos Gulf fauna and the subtidal communities off Po river mouth (Ambrogi et al., 1990; Moodley et al., 1998) and in the Gulf of Lions off Rnone river (Salen-Picard et al., 2003), the coastal terrigenous mud community (VTC) considered by Peres (1967), as well as the communities at the world’s major subaqueous deltaic systems (Rhoads et al., 1985; Alongi et al., 1992; Aller and Stupakoff, 1996). This similarity implies that regardless of the size of the catchment area and the amount of land runoff, the benthic macrofauna in depositional areas responds similarly to sediment instability and land inputs. A conceptual model by Rhoads et al. (1985) predicts that macrobenthic diversity and abundance increase along depositional gradients from the delta front to plume areas with the gradual increase in food inputs, due to higher light penetration in the water column. Accordingly, in Maliakos Gulf, the explanatory power of variables such as transparency, turbidity and of estimates of organic inputs in suspended load, such as CPEw/POM, was high. Besides, numbers of species and individuals always positively correlated with distance from the river during low and rising precipitation. These results indicate that macrofauna community in Maliakos responds to turbidity and food input gradients. However, these

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gradients, as already explained, are not related to the distancedeposition gradient from the river mouth when precipitationdriven land runoff from temporary streams and non-point sources is at its peak. The conceptual model by Rhoads et al. (1985) also predicts macrofauna increase with the gradual reduction in intensity of resuspension- and sedimentation-driven disturbance. In Maliakos Gulf the influence of the depositional gradient upon the community is evidenced by the high explanatory power of md. Thus, negative correlations between species abundance and distance reflect tolerance to the sediment instability characterizing fine sediments. The functional responses of the species in the inner Maliakos and in stations near the river mouth included high motility, subsurface dwelling, tube building and the ability to benefit from the fine sediment inputs. For example, the low motility Group 2 species C. gibba and M. bidentata, persistently abundant near the river mouth, are common in estuarine areas with high organic inputs and hydrodynamic regime because, despite the sediment instability, they benefit from the high amount of organic material associated with the suspended fine sediments (Jensen, 1990; Zenetos et al., 1991; Rosenberg, 1995). In addition, the increased food inputs during peak precipitation can explain the increase of tube-building, suspension feeding Group 2 species, such as Ampelisca sp. and L. maryae, in February. This, in turn, resulted in high macrofauna abundance despite the high sedimentation. At the same time, highly motile, carnivorous species consistently negatively correlated to the distancedeposition gradient, suggesting an ability to benefit from food sources not directly related to land inputs. However, the lack of correlation between abundance and the distance from river mouth and the wider distribution of the dominant species, as evidenced by the high % coefficient of variation (Table 2), during peak and falling precipitation, point to the stirring effect of high hydrodynamism. This mechanism, by inducing the passive transport of small surface-dwelling benthic individuals, was considered responsible for the mosaic distribution of macrofauna in inner Maliakos during the period of peak riverine discharges which coincides with high wind-induced hydrodynamic regime (Akoumianaki and Nicolaidou, 2007). Similarly, in the present study, the high explanatory power of skewness and sorting coefficient indicates that macrofauna structure is influenced by sediment resuspension and currentdriven transport of species. This in combination with the high food inputs to benthos, in the form of terrigenous and phytodetrital material, can also explain the increase in the total number of species in February and May. 4.3. Macrofauna response to land runoff The investigation of macrofaunaeenvironment relationship in Maliakos Gulf shows that during low precipitation as well as during rising and falling precipitation periods, as in November and May, macrofauna adapts to the sedimentation- and resuspension-driven disturbance. In this case, macrofauna species composition is shaped by food inputs and grain size whilst abundance and diversity parallel distance-depositional gradients. However, when land runoff increases up to the extent that through sedimentation it either limits the distribution of filter and surface deposit feeders or increases the susceptibility to resuspension and transport, as during peak precipitation, then the community-environment link weakens. In parallel, species numbers and individuals and, their distribution ranges, increase. This, in combination with the importance of s and sk and the lack of a dominant functional type, point to the importance of the functional diversity of macrofauna community prior to the high discharge and of the species pool in the surrounding area.

43

That said, the macrofauna species of Maliakos Gulf belong to a variety of functional groups, with respect to their colonization and motility pattern, trophic mode and grain size preference, indicating high functional diversity. This allows macrofauna community to maintain total species numbers and abundance within a range of high maximum values despite the environmental fluctuations and the sedimentation-driven disturbance. Macrofauna can thus take advantage of the terrigenous inputs and absorb the effects of increased turbidity and resuspension, given that these impacts remain seasonally predictable, and not detrimental (Slobodkin and Sanders, 1969). It is thus expected that community resilience, i.e. the ability for recovery from environmental change and disturbance, will explain an increasing proportion of the observed variation of the population when physical variability is too rapid or extreme, as long as it is not detrimental. Such detrimental effects might be caused by floods and the discharge of terrigenous particles contaminated with high concentrations of pollutants (GESAMP, 1994). 5. Conclusions A depositional gradient from the river mouth to the plume area of River Spercheios is evidenced by the occurrence of consistently fine sediments, high turbidity and low transparency near the river as opposed to the plume area. However, the runoff from temporary streams during the rainy period results in a patchy sedimentary and near bottom environment owing to a mosaic of processes: fine terrigenous particulate material inputs all along the coast; fast sedimentation of phytoplanktonic-particulate material flocs and sediment resuspension, especially near discharge sites; and fine sediment transport by near bottom currents. The macrofauna distribution and species composition respond to the patchiness in food inputs and substrate characteristics as indicated by the strong link between benthic community and the environment during low, rising and falling precipitation. However, during peak land runoff, and hence peak sedimentation-driven disturbance, the communityeenvironment relationship is considerably weaker. The functional traits of the most abundant species, including a high diversity of feeding modes, fast recolonisation ability, a variety of grain size preferences and dwelling modes in the sediment, suggest that the macrofauna community of Maliakos can absorb the impact of increased turbidity, sedimentation and current-driven dispersion and thus benefit from the increased phytodetrital and terrigenous organic inputs. The diverse functional response during peak land runoff is maintained through the transport and relocation of species not only within Maliakos but also by colonisation of tube-building second stage opportunistic species from neighbouring coastal areas through hydrodynamic processes. Acknowledgements This research was supported by the doctoral special funding of the University of Crete and received supplementary funding by the project of the Hellenic Ministry of the Environment, Physical Planning and Public Works for a baseline study in view of the construction of Maliakos Gulf underwater junction. References Akoumianaki, I., Nicolaidou, A., 2007. Spatial variability and dynamics of macrobenthos in a Mediterranean delta front area: the role of physical processes. Journal of Sea Research 57, 47e64. Akoumianaki, I., Papaspyrou, S., Nicolaidou, A., 2006. Dynamics of macrofauna body size in a deltaic environment. Marine Ecology Progress Series 321, 55e66.

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