(1997) In: Hawkins LE, Hutchinson S, Jensen AC, Williams JA, Sheader M (eds) The responses of marine organisms to their environments. University of Southampton, Southampton, p.143-151.

Proceedings of the

3d' European

Marine Biological Symposium. Southampton,

143

UK, September 1995

Is water column productivity in an Aegean embayment reflected to its benthic assemblages? Konstantinos Ar. Kormas, Maria Thessalou-Legaki Nicolaidou

and Artemis

Department of Zoology & Marine Biology, School of Biology, University of Athens, 15784 Panepistimiopoli, Greece

Athens,

Abstract Maliakos Gulf is a small, relatively enclosed embayment on the east coast of Greece. In the outer eastern part the average depth is 30 m and in the inner western part it does not exceed 25 m The bottom is covered mostly by soft sediments. River Spercheios meets the sea in the SW corner of the bay. Data on temperature, dissolved oxygen, salinity, depth of Secchi disc, nutrients, plant pigments, suspended particulate matter (SPM), and particulate organic carbon (POC) were collected monthly over a period of 18 months. Three water column stations and four surface stations were sampled. At the three main stations zooplankton vertical and horizontal samples were also obtained monthly. A benthic survey was carried out at 14 stations, while the benthic sampling was repeated at the three main sampling sites. Hydrographic parameters, nutrients, plant pigments and zooplankton showed a seasonal pattern. In the inner part of the gulf, closer to the river, sharper peaks were observed. According to the nutrients and plant pigment levels in the water together with the increased organic carbon in the sediment, the area is characterised as one of the most productive in the Aegean. This is reflected to the dense population of filter feeders (mussels, oysters, barnacles, thalassinids) which are found in the very shallow water around the gulf wherever hard surfaces or relatively stable sediments are available. On the contrary, the benthic fauna established on.silty sand covering the greatest part of the gulf, is poor both in species abundance and density. The individual size is also small. The assemblage does not conform to any of the classical community types of the Mediterranean. It contains elements of deep water communities and some opportunistic species. The deposit feeders dominate and only a few carnivores are present in the outer gulf. The inconsistency between the dense filter feeding community at the periphery and the restricted deposit feeding fauna in the main part of the bay, is attributed to sediment input from the river and resuspension of sediment. This makes the substratum unstable and does not allow the soft-bottom fauna to benefit from the food which reaches the bottom Keywords: pelagic production, benthic communities,

Aegean Sea.

Introduction The transfer of organic material between pelagic and benthic pools is a central topic in biological oceanography (Ambrose Jr. & Renaud, 1995). Its quality and quantity reaching the sediment surface can be assumed to be one of the major factors influencing benthic community structure (Graf, 1992). Also, there is strong evidence of changes in benthic metabolic activity associated with variations in particulate matter fluxes (Sayles et al., 1994). The organic material produced in the pelagic zone is considered as the beginning of the benthic food web in most cases. Since the phytoplankton bloom is considered as a pulsed source of organic carbon important to productivity and carbon flux in marine ecosystems (Andersson & Rudehall, 1993) and since a significant fraction of it sediments to the bottom, it is not surprising that it sometimes has a major effect on the benthos (Legendre, 1990). As reported by Buchanan (1993), the sedimented phytoplankton is rapidly incorporated into the bodies of deposit-feeders and suspension-feeders after the phytoplankton bloom. The immediate response of the benthos, defined either by direct (community structure/patterns) or indirect (ATP-biomass, organic content and/or heat-loss of the sediment etc.) measurements, is confIrmed in a number of papers (Graf et al., 1982, 1983; Graf, 1989; Smith et al., 1992; Buchanan, 1993). Another important input of organic matter to the bottom of the sea is the production of faecal pellets by zooplankton. These pellets, which are one of the few types of particles with sufficient mass and sinking speeds to be removed rapidly from surface waters, are among the major carriers for vertical transport of particulate organic matter from surface to deeper seawaters (Dellile & Razouls, 1994). Consequently, the organic matter that reaches benthic communities is governed by the type of the water column trophic web. The relationship, however, between the benthos and the pelagos is not always straightforward, especially in coastal waters. Estuaries, as an example, represent gradients in both physical, chemical and biological processes, and their function as fIlters for dissolved and particulate matter is determined by these gradients (Kamp-Nielsen, 1992). Lesser et al. (1994) suggest that regional differences in productivity between coastal and central open waters, could affect the dynamics of

144

benthic suspension-feeding communities because of the linkage between the food resource of these communities and the hydrographic events occurring in the overlying water; these hydrographic events do affect the production and transport of particulate food to the benthos. Maliakos Gulf, the area of the present investigation, is known for the successful fisheries of oysters and clams and the culture of mussels. Its innermost part is a fish nursery ground and as such it is protected. It is one of the few such areas in the oligotrophic Aegean Sea. Despite this interest very little work has been done in the area. However, the existing data (Papathanassiou, 1992; Anagnostou & Papathanassiou, 1994; Christou et aI., 1995) point to an impoverished plankton and benthos. The present study attempts to explain the apparent controversy and to investigate the relationships between the productivity of the pelagic environment and the benthos. Materials and Methods Description of site Maliakos Gulf (Figure 1) is an enclosed embayment on the eastern coast of Greece, connected to the Aegean Sea through the Orei Channel and the Evoikos Gulf through the Knimida Channel. It covers an area of ca. 120 km2 and is divided by two headlands into two parts. The Figure I Map of study area and sampling sites. western part forms a basin with a N maximum depth of 27 m. Its southwest A. coast receives the intermittent flow of Sperchios River, becoming shallower by deposited materials. The depth of the eastern part increases progressively towards the two openings of the bay. Thus, three ecologically different areas can be distinguished. The shallow southwest area influenced by the river General survey 0 (inner compartment), the outer gulf more influenced by the Aegean (outer Regular Surface only e sampling rI Depth profiles compartment) and the intermediate middle basin (middle compartment). Three stations representative of each compartment, were selected.

Sampling and laboratory analyses Pelagic environment Water column samples: Water samples were collected monthly, from surface, 1, 5, 10 and 20 m depths (surface, 1, and 5 m in the shallow inner compartment where the depth reached only 7 m) from July 1992 to September 1993. Surface water samples were obtained from four additional stations from April 1992 to September 1993. HYDROBIOS and LIMNOS bottles were used. Samples for nutrient analyses were immediately frozen and the analyses performed within two days after sampling. Samples for pigments and particulate organic carbon were filtered a few hours after collection; the filters were frozen at -20°e. Dissolved oxygen was determined by the Winkler method (Carrit & Carpenter, 1966), salinity was measured using an "AUTOSAL 3000" salinometer and temperature was taken by a HYDROBIOS thermometer; the depth of disappearance of Secchi disc was used as a measure of transparency for every station. Nutrients - nitrate, nitrite, phosphate and silicate - were measured spectrophotometrically as described in Parsons et al. (1984). Prior to the analysis, the samples were filtered by a 200 /-lm mesh net to remove large particles and large zooplankton. Phytoplankton pigments were measured fluorimetrically after concentration of the algae onto 'Whatman' GF/C filters and extraction in 90% acetone (Parsons et aI., 1984). Suspended Particulate Matter (SPM) was measured on ashed (500°C) and preweighed 'Whatman' GF/C filters (Strickland & Parsons, 1972). Particulate Organic Carbon (POC) was assessed by filtering onto precombusted 'Whatman' GF/C filters. Carbon was then determined by wet ashing with a mixture of

-/

145 Konnas et al. Water column productivity and benthic assemblages

potassium dichromate and concentrated sulphuric acid, and measuring the decrease in extinction of the yellow dichromate solution after its reduction by the organic matter (parsons et al., 1984). Zooplankton: Horizontal hauls for zooplankton were made at each compartment at the depth of ca. 1 m on a monthly basis. A WP2 (200 flm mesh) net equipped with a HYDROBIOS flow meter was hauled for 5-10 minutes at a boat speed of 1.5 to 2 knots so that an average volume of 592 m3 was sampled. At the deeper outer and middle parts vertical hauls from the bottom (i.e. 20 m) to surface were also taken monthly. The samples were preserved in 4% formaldehyde. The specimens were allocated to main animal groups. Benthic environment A general benthic survey of the Maliakos Gulf was carried out in the winter of 1992, using a Ponnar 0.05 m2 grab. Two replicates were collected at each of fourteen stations (Figure 1). In the summer of 1993 ten replicates were collected from each of the three main stations. A small part of each sample was kept for sediment analyses. On hard or more stable soft substrata at the periphery of the gulf the density of a few dominant species was estimated using quadrats. Sediment characteristics: Grain size analysis was carried out by the pipette method as described by Buchanan (1984). Organic carbon content of the sediment was measured by the chromic acid oxidation technique described by Gaudette et al. (1974). Zoobenthos: The benthic samples were sieved on board through a 1 mm mesh sieve, stained with Rose Bengal and preserved in 4% formaldehyde. In the laboratory the samples were sorted and the animals were identified and counted. Results Pelagic environment Water column: The ranges of the environmental parameters measured in the water column are shown in Table 1. The temperature followed the expected seasonal pattern with lowest values in the winter (8.8-9.4°C) and highest in the summer months (25.6-26.0°C). The maximum and minimum values of salinity did not vary considerably between the three compartments. Dissolved oxygen concentrations fluctuated but never dropped to limiting levels. Water transparency, expressed as depth of disappearance of Secchi disc, decreased from the outer (2.5-20.0 m) to the inner gulf (1.10-4.50 m). Table I

Minimum and maximum values of environmental

Part of the

parameters measured in each part of Maliakos Gulf.

34.9-37.5 4.7-7.0 1.10-4.50 0.00-0.85 0.00-1.38 0.00-43.85 0.00-30.85 0.00-71.05 0.00-0.55 0.00-0.42 0.00-0.95 0.00-1.38 0.00-1.05 35.1-37.9 8.8-25.6 9.3-25.6 4.1-7.4 2.50-20.00 4.5-7.9 16.9-434.0 48.4-431.1 0.00-3.50 1.2-429.9 POC 9.4-26.0 0.00-4.96 0.00-0.46 0.00-0.73 34.9-38.1 1.85-15.00 0.00-4.97 SPM 13,300-65,500 12,000-7,900 ChI a 10,700-8,500 (ml P-P04·3 Cc) rl) N-NOz N-N03' Secchi Temperature Oxygen Salinity disc (ppt) Si-SiOz rl) (flg (m) (flg-at r1) (flg-at (flg-at r1) (mg m·3)depth (mg rl)m·3)

All nutrients measured drop to practically zero for part of the year. The maximum concentrations of nitrates and nitrites are lower in the inner compartment (0.8 and 0.5 flg-at 1'1) and higher in the outer (1.4 and 0.7 flg-at 1'\ On the contrary, maximum phosphate values are higher in the inner compartment (1.0 flg-at 1'1) and a lot lower (0.4 flg-at 1'1) in the outer compartment. Finally, maximum concentrations of silicates are higher in the inner compartment (71.0 flg-at 1'1) and lower in the middle (30.8 flg-at 1'1). The lowest levels of SPM were similar at the three compartments (10,700 mg m-3 in the outer 13,300 mg m-3 in the inner), the highest however was a lot greater in the shallower inner

146

compartment (27,900 mg m-3 in the middle - 65,500 mg m-3 in the inner). On the other hand, the highest values of POC are similar in the three compartments while the lower values increase gradually from the outer to the inner compartment. ChI a ranged from practically 0 to almost 5 flg rl (Table 1). Temporal variations in ChI a concentrations in the three compartments of the gulf are shown in Figure 2. There is a' long period, from December to April, of phytoplankton growth. Higher values were measured in the inner and middle compartments for the greatest part of the year, with a sharp peak: in January. Zooplankton: The surface zooplankton density (Fi§ure 2b and 3) reaches a peak: in all three compartments in May. Highest density (6,104 ind. m- ) occurs in the inner station and lowest in the middle (2,872 ind. m-3). The decline is a lot sharper in the outer compartment. The dominant group is the copepods all year round. On some occasions, towards the' end of winter and in the spring, they account for more than 90% of the individuals in the sample. The second most numerically important group is the cladocerans. Their importance increases from the inner to the outer compartment where Figure 2

(a) Temporal variations of chlorophyll a concentrations and (b) temporal variations of zooplankton abundance (horizontal hauls).

5-

a

4.5 -

4~ 3.5-

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g.

o is

2-

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o--...----..J

AS

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M

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1993

_Outer

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I

their percent abundance reaches 42% in September. The larvae of quite a few benthic groups, including decapods, molluscs, polychaetes and phoronids, are abundant at certain times of the year. Their contribution to the plankton composition is more evident in the vertical hauls (Figure 3), especially in the middle compartment where they account for as much as 50% of the individuals. The copepods are again the most numerically important group but their numbers are not as high as in the horizontal hauls. Benthic environment Sediment characteristics: The sediment is nearly homogenous throughout the gulf, characterised as sandy silt, except at one station (station 14) where it is clayey silt. The percent organic carbon of the sediments ranged from 0.31 % in the inner compartment to 2.72% in the outer. Zoobenthos: The depth of the sampling stations of the general survey ranged from 7 to 39 m. From the 14 stations sampled, 93 taxa were identified, of which 51 were polychaetes, 21 crustaceans, 9 molluscs, 6 echinoderms and 6 minor phyla. The benthic fauna of Maliak:os Gulf does not conform

147 Kormas et al. Water column productivity and benthic assemblages

Figure 3

Temporal variations of most abundant zooplankton groups (vertical hauls).

Outer

::I ~ oD ;::

100 40 J 20

AS

Il~

0

N

1993 DJ

FM

AM

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J

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0

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to any of the classical community types described for the Mediterranean (Peres, 1967). It contains elements of deep water communities, such as Stemaspis scutata, Nephthys hystricis and Oncnezoma steenstrupi. Some species characteristic of disturbed environments such as Lumbrineris latreilli, Corbulla gibba and Thyasira flexuosa are also present but not in high densities. The erratic appearance of species is reflected in the dendrogram in Figure 4. Similarities between stations are very low and no discrete groups are formed. In general the benthic fauna is poor, in both numbers of species and individuals (Table 2). In the winter the lowest number of species (4 species) was observed in the inner compartment and the highest (14 species) in the middle compartment. In the summer, the numbers of species increased considerably and ranged from 45 in the inner to 59 in the outer compartment indicating some recruitment. The number of individuals did not show such drastic increase between winter and summer. They ranged between 180 to 320 ind. m-2 in the winter and 343 to 597 ind. m-2 in the summer. The density of individual species usually does not exceed 40 ind. m-2• The greatest species abundance observed is 460 ind. m-2 of the juvenile echinoderm Amphiurafiliformis, 140 ind. m-2 of the sipunculid Oncnezoma steenstrupi and 100 ind. m-2 of the polychaete Sternaspis scutata and the echinoderm Echinocardium cordatum. On the contrary, a dense filter feeding fauna is established on hard substrata. Some density measurements showed that the mussel Mytilus galloprovincialis reach densities of up to 3,139 ind. m-2 (mean density 1,247 ind. m-2) and the barnacle Chthamalus stellatus 2,667 ind. m-2. Newly settled barnacles show 100% coverage with densities of 62,000 ind. m-2. Finally the filter

148

Figure 4

u
P:: g:: If.i :>-<

j~ I

f-o c:r:: p:) :>-< :::> c:r:: Cl)

Clustering of survey stations using Bray-Curtis indices of similarity of the benthic fauna.

50. 40. 7 11 10 16 20 21 14 4 518 328O. 60. 30. 70. 80. 22

100. 10. 20. 90.

feeding decapod Upogebia pusilla, found on more stable intertidal soft substrata has an average density of 32 ind. m-2.• The feeding strategies of the soft bottom fauna are shown in Table 3. The deposit feeders dominate making up to 97.1 % of the biomass at the inner compartment, while the filter feeders are practically missing. The carnivores range from 2.87% in the inner compartment to 19.40% in the middle. Discussion Nutrients in Maliakos Gulf reach concentrations which are higher than those observed in the open Aegean Sea as well as in semi-enclosed naturally enriched bays ~Table 4). The mean annual concentrations of phosphates (0.28 Ilg-at rl) and nitrates (0.65 Ilg-at r ) are within the limits given by Ignatiades et al. (1992) for mesotrophic areas (0.14-0.68 Ilg-atl-l for phosphates and 0.65-1.19 Ilg-at r1 for nitrates). Psillidou-Giouranovits et al. (1993) also consider Maliakos as an enriched area, at least as far as nitrates and silicates are concerned. The observed ChI a concentrations in Maliakos are also higher than in other areas (Table 4). They are even higher than those observed by Christou et al. (1995) in Maliakos a year earlier. This may be due to the fact that the present survey extended further inward in the gulf and as it is shown, the concentrations of ChI a increase from the outer to the inner part of the gulf. The timing of the ChI a peak agrees on two occasions. The observed zooplankton abundance was also higher in the present study (6,104 ind. m-3 as opposed to 1336 ind. m-3 a year earlier (Christou et al., 1995)). It is possible that the more frequent sampling, allowed detection of the zooplankton peak which was proved to be very short lived. It seems that the pelagic component of the Maliakos ecosystem is relatively rich and well organised, with the phytoplankton bloom occurring at the end of winter/beginning of spring, followed by a peak in the zooplankton. The zoobenthic community on the contrary, in the largest part of the bay covered by soft sediment, is not well developed. No typical communities, of those described for the Mediterranean (peres, 1967) were observed. Despite the uniform sediment characteristics (Table 2), the similarities of the fauna between the stations, as shown by the classification analysis, is very low. The number of species in Maliakos, especially in the winter, is smaller compared with other areas of similar sediment characteristics (Table 5). More pronounced is the difference in the density of the fauna, which is a lot lower. The only other comparable site is a station in Amvrakikos Gulf which, like Maliakos, receives considerable riverine inputs. It seems therefore, that there is no direct relationship between the productivity in the water column and that of the benthic fauna. This is also obvious when examining the gradients within the gulf.

149 Konnas et al.

Water column productivity and benthic assemblages

Productivity, expressed as ChI a and zooplankton abundance in the water column, is higher in the inner than the outer stations while organic carbon in the sediment and abundance of the benthic fauna is higher in the outer stations .. Table 2

Sediment characteristics,numbers of species and numbers of individuals m·2 (min-max) in Maliakos Gulf.

II

45 240 320 59 343 597 180 550 14 4 Winter 0.31 1.21 Summer 87.68 Winter 2.72 56 92.27 99.59 72.62 72.60 78.72 % No. Fines of ind. % No.organic of species C m-2 Part of the gulf

Table 3

Percentages of the different feeding types in Maliakos Gulf

Part of the gulf Outer Middle Inner Table 4

Carnivores 13.04% 19.40% 2.87%

Deposit feeders 85.88% 80.60% 97.13%

Filter feeders 1.08% 0.00% 0.00%

0.04-4.00 0.70-2.70 0.10-2.05 0.08-2.18 0.00-71.05 0.00-1.05 0.05-0.09 2.02-8.45 0.01-0.07 0.02-0.74 0.04-0.18 0.06-1.01 0.08-3.97 0.03-0.76 0.02-0.45 150-600 0.01-0.61 0.00-0.73 0.03-1.32 0.10-2.96 0.00-4.96 0.00-1.38 0.04-1.43 1.57-20.00 0.01-0.16 0.04-0.84 ChI. a studr Author 1-6,104 461-2,596 NCMR, 162-1,322 N-N03' a values measured in Maliakos Gulf with those of other areas. Comparison of1991 and cWorophyll Friligos Zooplankton Karydis et al., 1987 p-P04·3 N-N02 Papathanassiou, &nutrients Gotsi, 1992 1987 (ind. m-3) Present Si-Si02 (Ilg-at (Ilg r1) rl) r1) rl)

Area

Table 5

Comparison of % fines in sediments, numbers of species and numbers of individuals m·2 measured in Maliakos Gulf with those of other areas.

99.7 11199 95.5 22-50 244-796 11-63 180-597 4-59 13-22 18 8 studr Author 1993 72.60-99.59 71.2-96.6 83.0 38-62 8-39 Nicolaidou et aI., 1983 No. % Area No. Fines of individuals of27 Maliakos m-2 392-2,035 Zenetos etspecies al., 1991 1014-2,183 Papathanassiou & Zenetos, Anagnostou & Papathanassiou, 1994 Present Depth

Nevertheless, there is a response of benthic organisms to pulses from the pelagic, as can be seen by the large number of larvae of benthic animals in the plankton following the peaks of phytoplankton. Thus, the small increase of ChI a in the autumn (October) is followed in the middle and outer compartments by an increased number of phoronid and polychaete larvae. The latter become the most abundant group accounting for 46% of the individuals. White & Roman (1992) attributed the dominance of polychaete larvae in the plankton to the settlement of a local diatom bloom which triggered the release of gametes by adult worms. Similarly, the ChI a increase in the winter is followed by the appearance of bivalve and decapod larvae in the plankton. The extended phytoplankton production, the high zooplankton abundance and its time lag from the phytoplankton maximum suggest (Legendre & Rassoulzadegan, 1995) that the dominant trophic web in Maliakos is either the herbivorous or the multivorous. Both of them supply the water column not only with dead phytoplankton cells but also with fast sinking zooplankton faecal pellets. Increased organic matter in the sediment is reflected to the increased concentrations of organic carbon. Thus, food should not be considered as a limiting factor. Most benthic animals are deposit feeders and the amount of organic carbon in the sediment would be sufficient to support a dense fauna. In the outer compartment in particular, the percent organic carbon in the sediment is remarkably high for a non

150

anthropogenic ally affected area. Lower concentrations of organic carbon in the sediment of the inner gulf, despite the higher production in the overlying water, may be attributed to its dilution by the increased quantities of inorganic material introduced by the river. The more frequent resuspension by wave action due to the shallowness of the area, may contribute to the loss of organic matter from the sediment. The possibility that the organic matter is not all in a form available to the organisms should also be taken into consideration. As part of it may be terrigenous contributed by the river, especially in the inner compartment, a large proportion of it may not be labile. This is something which needs further investigation. Another factor affecting the benthos is recruitment. Larvae of benthic invertebrates formed a large proportion of the zooplankton. Some settlement did occur, as shown by the slightly increased number of species and specimens in the summer. However, this recruitment was not extensive. Furthermore, there is no information concerning the survival of the recruits. A factor related to the above is the instability of the substratum. The extremely fine sediment of the gulf is readily put into resuspension by water movement especially in the inner compartment where the depth is small. It is possible that sedimentation of river imported particles together with resuspension create an environment hostile to settling larvae, juveniles and even to adults. Some evidence is given by Zenetos (1995) who, dealing with the palaeoecology of the gulf, mentions the burial in situ of populations of the gastropod Turritella communis. The populations of animals on hard substrata do not face such problems, thus they may become quite dense utilising the organic production in the water. On the contrary, the stress imposed by the instability of the bottom does not allow the soft bottom fauna to take advantage of the available food. References Ambrose Jr., W.G. & Renaud, P.E., 1995. Benthic response to water column productivity patterns: Evidence for benthic-pelagic coupling in the Northeast Water Polynya. J. geoph. Res. l00(C3): 4411-4421. Anagnostou, Ch. & Papathanassiou, E., 1994. Study for the detection of pollution in Maliakos Gulf in relation to its potential for fish farming and fisheries development. Technical report. National Center for Marine Research, Athens. [in Greek] Andersson, A.. & Rudehiill, A., 1993. Proportion of plankton biomass in particulate organic carbon in the northern Baltic Sea. Mar. Eco/. Prog. Ser. 95: 133-139. Buchanan, J.B., 1984. Sediment analysis. In N.A Holme & AD. McIntyre (eds): Methods for the study of marine benthas. Blackwell Scientific Publications. pp. 41-65. Buchanan, J.B., 1993. Evidence ofbenthic pelagic coupling at a station off the Northumberland coast. J. Exp. Mar. Bio/. Eco/. 172: 1-10. Camt, D.E. & Carpenter, J.H., 1966. Comparison and evaluation of currently employed modifications of the Winkler method for determining dissolved oxygen in seawater; A NASCO Report. J. mar. Res. 24: 286-318. Christou, E.D., Pagou, K., Christianidis, S. & Papathanasiou, E., 1995. Temporal and spatial variability of plankton communities in a shallow embayment of the Eastern Mediterranean. In A. Eleftheriou, A.D. Ansell & C.J. Smith (eds): Biology and ecology of shallow coastal waters. Olsen & Olsen. pp. 3-10. Delil1e, D. & Razouls, S., 1994. Community structures of heterotrophic bacteria of copepod faecal pellets. J. Plankton Res. 16(6): 603-615. Friligos, N. & Gotsis-Skretas, 0., 1987. Relationships of phytoplankton with certain environmental factors in the South Euboikos Gulf (Greece). P.S.z.N./.: Marine Ecology 8(1): 59-73. Gaudette, H.E., Flight, W.R., Toner, L. & Folger, D.W., 1974. An inexpensive titration method for the determination of organic carbon in recent sediments. J. sed. Petrol. 44(1): 249-253. Graf, G., 1989. Benthic pelagic coupling in a deep-sea bcnthic community. Nature 341: 437-439. Graf, G., 1992. Benthic-pelagic coupling: A benthic view. Oceanogr. mar. Bio/. annu. Rev. 30: 149-190. Graf, G., Bengtsson, W., Diesner, U., Schulz, R. & Theede, H., 1982. Benthic response to sedimentation of a spring phytoplankton bloom: processes and budget. Mar. Bio/. 67: 201-208 Graf, G., Schulz, R., Peinert. R. & Meyer-Reil, L.A., 1983. Benthic response to sedimentation events during autumn to spring at a shallow-water station in the Western Kiel Bight. Mar. Bio/. 77: 235-246. Ignatiades, L., Karydis, M. & Vounatsou, P., 1992. A possible method for evaluating oligotrophy and eutrophication based on nutrient concentration scales. Mar. Pollut. Bull. 24(5): 238-243. Kamp-Nielsen, 457-470.

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along an estuarine

eutrophication

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