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Assessing Marine Ecosystem Response to Nutrient Inputs
PII:
Marine Pollution Bulletin Vol. 43, Nos. 7±12, pp. 175±186, 2001 Ó 2001 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0025-326X/01 $ - see front matter S0025-326X(01)00071-6
Assessing Marine Ecosystem Response to Nutrient Inputs TRIANTAFYLLOU GEORGE *, PETIHAKIS GEORGEà,1, DOUNAS COSTAS and ATHANASIOS THEODOROUà,1 Institute of Marine Biology of Crete, P.O. Box 2214, Iraklio, 71003 Crete, Greece àDepartment of Agriculture Crop and Animal Production, University of Thessaly, Pedion Areos 383 34 Volos, Greece The response of the Pagasitikos Gulf to enrichment caused by run-o fertilizers and the development and evolution of harmful algal blooms is investigated through ecosystem modelling. A standard generic complex model has been developed to describe the ecosystem processes of Pagasitikos and has been validated with in situ data. Additionally external nutrient ¯uxes have been assimilated and incorporated into the ecosystem dynamics. The investigation of spatial eects due to nutrient enrichment is investigated along a North±South transect. When externally forced the model successfully assimilates the external river inputs producing nutrient and chlorophyll-a concentrations, which are in good agreement with the in situ data. The nutrient inputs result in a more stable ecosystem at the north part of the Gulf and in the development of eutrophic conditions. The changes in the ecosystem functioning with emphasis on the nutrient cycling, the increase of primary production, and the modes of operation are investigated and discussed. Ó 2001 Elsevier Science Ltd. All rights reserved. Keywords: ecosystem disturbance; ecosystem management; mathematical models; nutrients; phytoplankton; primary production.
Introduction Pagasitikos is a semi-enclosed Gulf situated on the western part of Aegean Sea north of the island of Evia. It has a mean depth of 69 m with the deepest point located at the east part (108 m) characterizing a rather shallow water body. The area of the bay is 520 km2 with a total volume of 36 km3 . It is connected at the south with the Aegean Sea through the 5.5 km wide, narrow channel of Trikeri (Fig. 1). The system of Pagasitikos is greatly in¯uenced by human activities especially around the industrial town of Volos (population 120 000). Although in the sur*Corresponding author. Tel.: +30-81-346-860; fax: +30-81-241-882. E-mail address: [email protected] (T. George). 1 Tel.: +30-421-74312; fax: +30-421-63383.
rounding area there are no major rivers with the exception of small torrents, signi®cant quantities of polluted waters enter the system of the Gulf on a permanent or occasional basis. There are three major pollution sources, the scattered farmlands along the coastline, some rather distant sources and the domestic or industrial euents. In the greater area of Pagasitikos intensive agriculture of cereals and cotton is practized using signi®cant quantities of fertilizers rich in nitrogen, phosphate and sulphur. An important distant source of pollution is Lake Karla where during a drainage programme large quantities of water enriched in nutrients were discharged via channels into the north part of the bay. Also apart from the winter period when rainwater from the wider area of Karla washes the soil, becoming enriched with fertilizers, pesticides and particulate material pour into Pagasitikos and there are discharges of domestic and industrial sewage into the drainage channels throughout the year. Finally the sewage treatment plant of the city of Volos as well as the industrial park of the area located 5 km west from the city are important sources of pollution. The water enrichment at the north part of the bay in conjunction with the increased temperatures of the summer period results in the frequent appearance of harmful algal blooms, causing problems both to tourism and ®sheries (Friligos, 1987). Due to compensatory and buering mechanisms within the food web natural systems seem able to withstand nutrient inputs below a certain limit or critical load without any undesirable eects. However for a given food web structure there should be a certain critical level of nutrient supply where the likelihood of uncontrolled blooms should increase abruptly and nonlinearly (Ingrid et al., 1996). There have been extensive ecosystem studies in the area since 1975 (Friligos et al., 1990; Theocharis and Friligos, 1985) on a number of physicochemical (temperature, salinity, nutrients) and biological parameters (chlorophyll-a, phytoplankton, zooplankton). Also in the recent past (1998±1999) a monitoring programme was set up (Koliou-Mitsou, 1999) in an attempt to study the extent as well as the eects of the nutrient enrichment from Lake Karla. 175
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Fig. 1 Map of Pagasitikos Gulf and simulation transect.
The results of the recent research programme in Pagasitikos (Theodorou and Petihakis, 2000) show that the water mass of Pagasitikos is fairly mixed in the winter months, forming a two-layer thermocline for the rest of the year at approximately 20 m depth, with the exception of August when three layers are observed. Lowest temperatures (12.5°C) are observed during winter (February±March) reaching maximum values (27.4°C) during summer. Salinity exhibits wide ¯uctuations (32±38½) with values increasing with depth due to the in¯ow of low salinity surface waters from the Aegean Sea. In¯ows of fresh waters in the areas of Volos and Almiros are also observed occasionally. Water currents are generally small to moderate due to weak winds and renewal occurs mainly through the deepwater layer of the communication channel with Aegean Sea, in¯owing across the east part and out¯owing across the west part. This water movement is reversed at the surface layer. The dynamics of the system of Pagasitikos are highly in¯uenced both by the anthropogenic activities and the in¯ow of nutrients at the north and west parts as well as by water exchange between the Gulf and the Aegean Sea at its south part through Trikeri channel. The above, in conjunction with the formation of intense thermocline, results in the development of dierent areas within the Gulf. Thus the internal part is characterized by eutrophic conditions, which under favourable conditions 176
result in the development of the harmful algal blooms observed. The central part of Pagasitikos is an organic matter deposition zone since it includes the deep areas of the bay, which due to long strati®cation periods and the dominant anticyclonic circulation, traps all nutrients released from the sediment, developing a microbial food web. It is only when the thermocline erodes that nutrients ®nd their way up in the upper layers of the euphotic zone shifting the system into a classic food web with increased primary production. The outer bay is highly in¯uenced by the Aegean Sea creating a dilution zone with mesotrophic conditions. Thus initially a standard 1D generic complex model developed (Allen et al., 1998) to describe the ecosystem dynamics of Pagasitikos was applied and validated in the central-external (Petihakis et al., 2000b) and internal (Petihakis et al., 2000a) parts of the Gulf. The in¯uence of external nutrient inputs in the internal part of the Gulf, as depicted in the model results, is very important, causing signi®cant changes in the ecosystem functioning. An important issue when examining the eects of a natural or man-induced disturbance is the spatial distribution as well as the magnitude of change moving away from the pollutant source. The aim of this study is to describe along a transect the vertical gradients of the ecological parameters as a function of time in order to investigate the response of the ecosystem due to point source external nutrient inputs.
Material and Methods The ecosystem processes are described by a system of three online linked mathematical models. More speci®cally the hydrodynamics are described by the Princeton Ocean Model (POM), (Blumberg and Mellor, 1978; Blumberg and Mellor, 1987; Mellor, 1991), where both formulation and numerical solutions are described in detail. The physical model contains all information speci®c to the area to be modelled, whereas the biological/chemical sub-models have been constructed to respond to the physico-chemical environment within which they are placed. The advection diusion model of the suspended in the water ecological parameters is simulated by the conservative scheme of (Lin et al., 1994). Lastly the biology is described by the European Regional Seas Ecosystem Model (ERSEM) (Baretta et al., 1995; Baretta-Bekker et al., 1995; Blackford and Radford, 1995; Broekhuizen et al., 1995; Ebenhoh et al., 1995; Petihakis et al., 2000a; Petihakis et al., 2000b; Ruardij and van Raaphost, 1995; Varela et al., 1995). A transect (a) and (b) de®ned by 22.93° longitude and 39.13° to 39.35° latitude from North to South (Fig. 1) across the Pagasitikos Gulf was selected for modelling implementation, since it includes both the area where the Karla euents are discharged and the central and external parts of the Gulf. This transect has been extracted from a three-dimensional model. The transect
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grid consists of 13 boxes along the transect with a size of 1852 m each and 12 boxes in the vertical with a dierent depth ranging from 25 to 86 m. Since ecosystem dynamics near the surface are expected to be more complicated, and thus require more accuracy, the 12 elements have a variable thickness with smaller size near the surface. The upper boxes are open to the air, while in the bottom boxes a benthic module is incorporated. In the ecological model the biological groups are grouped according to their trophic level subdivided by their size class or feeding method. In an attempt to realistically simulate the ecosystem of Pagasitikos following an extensive literature search and in situ data analysis, the food web with the trophic relations among the dierent groups was set up as shown in Fig. 2. The biological variables in the model are; phytoplankton, groups related to the microbial loop, zooplankton and benthic fauna. Biologically driven carbon dynamics are coupled to the chemical dynamics of nitrogen, phosphate, silicate and oxygen. The phytoplankton pool is described by four functional groups based on size and ecological properties. These are diatoms (silicate consumers, 20±200 l), nanophytoplankton (2±20 l), picophytoplankton (< 2 l) and dino¯agellates (> 20 l). All phytoplankton groups contain internal nutrient
pools and have dynamically varying C:N:P ratios. The nutrient uptake is controlled by the dierence between the internal nutrient pool and external nutrient concentration. Since the deep chlorophyll maximum is deeper than biomass maximum, the cell chlorophyll-a content in the model increases with depth following a prede®ned function (Triantafyllou and Petihakis, 1999). The microbial loop contains bacteria, heterotrophic ¯agellates and microzooplankton, each with dynamically varying C:N:P ratios. Bacteria act to decompose detritus and can compete for nutrients with phytoplankton. A mechanism for the phosphorus limitation of bacterial growth is included, which is very important in controlling the ecosystem in the mesotrophic and oligotrophic upper waters (Thingstad and Lignell, 1997). Bacteria are not coupled to the phytoplankton but are dispersed in the water column since dissolved organic carbon exists as a state variable and its usage is nutrient limited. Heterotrophic ¯agellates feed on bacteria and picophytoplankton, and are grazed by microzooplankton. Microzooplankton also consume diatoms and nanophytoplankton and are grazed by mesozooplankton. The benthic±pelagic coupling is described by the settling of organic detritus into the benthos and diusional nutrient ¯uxes into and out of the
Fig. 2 Simulation models and trophic web.
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sediment ± water interface after mineralization and diagenesis. Model application area, initial conditions and forcing The physical model was forced with daily wind velocity values from Anchialos airport for the period 1999 and relaxed, to the monthly mean surface temperature and salinity. It was initialized with January 1999 temperature and salinity values (Theodorou and Petihakis, 2000). The ecosystem model was initialized with in situ biogeochemical winter (January) ®eld data where available (Theodorou, 1998) while all other parameters used are the standard ERSEM v11 values (Petihakis et al., 2000a; Petihakis et al., 2000b).
The nutrient inputs were implemented in the model as an external source calculated from the dierence in nutrient concentrations in the central part of the Gulf and those measured at the mouth of Xirias River. The external nutrient quantities were assimilated in the model using a simple relaxation scheme: H d v ; 1 v vdata s dt where v; vdata are four-dimensional vectors with components concentrations of NO3 ; NH4 ; PO4 and SiO2 of the model and in situ data, respectively. H 7 m the depth in¯uenced by the external nutrient inputs and s 1 day the relaxation time.
Fig. 3 Model results and in situ measurements of central-external Gulf at 30 m depth.
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Results and Discussion Central-external Gulf The 1D model for the central-external Pagasitikos reproduces well the evolution of physico-chemical parameters at 30 m layer (Fig. 3). The increased levels of nitrate ammonia and phosphate during spring depicted by the in situ data concentrations might be attributed to the degradation of primary production and recycling of organic material as evidenced by the chlorophyll-a levels, rather than in¯ows since the increased levels are observed in the whole water column and not in the
surface layer only. According to the phytoplankton succession, maximum biomass occurs during winter with the ¯agellates being the dominant group followed by diatoms and nanoplankton. In the following months nanoplankton becomes the dominant group while all other groups exhibit signi®cant lower levels of biomass. Internal Gulf Model results depicting the seasonal variation of nutrients and primary producers in the surface layer with and without ¯ux were validated with in situ data (Fig. 4). In all four nutrient simulations the implementation of
Fig. 4 Model results with and without nutrient input ¯ux and in situ measurements of internal Gulf (Karla euents) at surface layer.
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external ¯uxes signi®cantly improves the model results (especially those of silicate and ammonia). Chlorophylla simulation also improves with the implementation of external nutrient ¯uxes indicating that the dierence in the chlorophyll-a levels between the central and inner parts of the Gulf might be attributed to nutrient enrichment. Transect An important characteristic of Pagasitikos is the smooth increase in depth at the northern in contrast to the high gradient observed at the south resulting in ef®cient wind mixing and transport of resuspended nutrients from the sediment into the water column, while at
the deeper parts in the south sediment nutrient releases are trapped at the 50±85 m layer for signi®cant time periods. Two model runs have been made for one year, one with nutrient inputs at the north part of the transect and one without inputs (standard run). Three months were selected for the presentation of the results: March is the month when the water column is mixed most, while during August an intense strati®cation is observed and ®nally December is characterized by signi®cant rainfalls and subsequent inputs from Lake Karla into the system of Pagasitikos. Model runs for 1999 (monthly means for ecosystem parameters) from both runs for the three months are presented and discussed.
Fig. 5 Nitrate simulations (lmol l 1 ) along the transect (a) with external inputs and (b) without external inputs for the months March, August and December.
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Nitrate enrichment is rather signi®cant only in the north part of Pagasitikos with maximum values during December (3 lmol l 1 ) producing a gradient zone of approximately 5 km (Fig. 5). High concentrations (3:3 lmol l 1 ) at the deeper parts of the transect (50±85 m) at the end of the year are possibly due to the destruction of strati®cation with the subsequent settling of organic material and increased benthic activity. In the absence of external inputs the distribution of nitrates is characterized by higher levels of nitrate in the water layers close to the bottom especially in December. Unlike nitrate, phosphate enrichment is maximum during March (0:7 lmol l 1 ), strongly aecting the shallow area at the north part (Fig. 6). Minimum levels
(0:03 lmol l 1 ) occur in the upper and middle layers of the central-external parts of the Gulf during August and December. In the model run without inputs phosphate concentrations are very low (0:01±0:22 lmol l 1 ) in all three months increasing with depth. From the chlorophyll-a results (Fig. 7) it is shown that the area with nutrient inputs close to the city of Volos produces a similar picture in all three months with maximum concentrations (5:5 lg l 1 ) at the shallower area extending to approximately 5 km. In August a tongue of 0:5 lg l 1 of chlorophyll-a is extended to the central part of the simulation area possibly due to the presence of thermocline. In the absence of nutrient inputs the levels of chlorophyll-a as produced by the
Fig. 6 Phosphate simulations (lmol l 1 ) along a transect (a) with external inputs and (b) without external inputs for the months March, August and December.
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Fig. 7 Chlorophyll-a simulations (lg l 1 ) along a transect (a) with external inputs and (b) without external inputs for the months March, August and December.
model are signi®cantly lower (0:02±1:4 lg l 1 ) with maximum values during August at 40±50 m layer due to regenerated production, designating the presence of a nitracline. High chlorophyll-a concentrations (1:2 lg l 1 ) are also produced during December in the shallow north part close to the city of Volos, which might be attributed to resuspension of nutrients and adequate light. As with chlorophyll-a total primary biomass at the shallow north part of the Gulf under the in¯uence of nutrient enrichment does not dierentiate signi®cantly between the three months exhibiting particularly high levels (270 lgC l 1 ), while the area with increased values (60±270 lgC l 1 ) extends to approximately 5 km (Fig. 182
8). Also a subsurface tongue is produced during August between 15 and 60 m. In the absence of external inputs total primary biomass is much lower with maximum levels during August and December (40 lgC l 1 ). As expected in March higher values occur in the upper layers taking advantage of the mixing of waters in contrast with August when maximum biomass is located in the 30±50 m layer close to the thermocline. December is characterized also by a subsurface maximum (50 lgC l 1 ) but also at shallower depths (20±30 m) possibly because of thermocline erosion. Under nutrient enrichment diatoms contribute approximately 2/3 of the total phytoplankton biomass followed by picoplankton and ¯agellates. The large
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Fig. 8 Total primary biomass simulations (lgC l 1 ) along the transect (a) with external inputs and (b) without external inputs for the months March, August and December.
primary producers (diatoms and ¯agellates) exhibit a signi®cant increase in biomass as expected with the addition of nutrients in contrast with the small size cells, which seem to have an upper threshold. It is suggested that nutrient enrichment causes a shift away from small phytoplanktonic groups (nano and pico plankton) with a clear advantage to bigger cells (Ingrid et al., 1996). This is possibly due to the fact that in oligotrophic waters, small cells are dominant with the majority of primary production driven by reduced nitrogen (NH4 ), and only when new nitrogen (NO3 ) arrives either as external inputs or due to water column mixing the large cells take over (Eppley and Peterson, 1979). Another reason is that the acquisition
of nutrients by large cells can be limited by molecular diusion at very low nutrient concentrations since cells with small radius can grow at higher rates (Chislholm, 1992; Thingstad, 1998). It is suggested that the total amount of chlorophyll in each size fraction has an upper limit and beyond certain thresholds chlorophyll can be added to a system only by adding a larger size class of cells, mostly diatoms (Chislholm, 1992). (Thingstad and Sakshaug, 1990) showed that in a plankton model with two parallel food chains increased nutrient supply could lead to a shift from dominance of a four-level chain (small algae ± ciliates-copepods®sh) to a shorter three-level chain (large algae ± copepods-®sh). 183
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Fig. 9 Simulations net primary production (mgC m 2 yr 1 ) along the transect with external inputs and without external inputs.
The eects of the enrichment in the productivity of the system of Pagasitikos can be quanti®ed from the integrated annual net primary productivity along the transect (Fig. 9). It is shown that in the area of nutrient inputs at the north of the Gulf there is an addition of 400 gC m 2 yr 1 decreasing away from the point source (approximately 5 km) to 100 gC m 2 yr 1 . Also there is a transition zone at the central part covering a distance of about 10 km while the rest (outer part) remains unaected. An interesting feature emerging from the model result is the relation between primary production and bacteria biomass. In the case of nutrient ¯ux total primary production is signi®cantly higher (approximately 3-fold) compared to the bacterial biomass (Figs. 8 and 10). When there are no nutrient inputs bacterial biomass is three times higher than total primary biomass during March and slightly higher in the other two months. In an environment where primary production is limited by the availability of mineral nutrients this would lead to competition between phytoplankton and heterotrophic bacteria for the limiting mineral nutrient (Bratbak and Thingstad, 1985). Considering the larger surface to volume ratio and the small size of bacteria it is obvious that they are more ecient competitors for mineral nutrients although they cannot out-compete the algae completely since this would remove their source of carbon/energy substrate. In oligotrophic waters the bacterial biomass, depth integrated over the euphotic zone exceeds that of phytoplankton, although heterotrophic bacterial production is low, with population doubling times of about a week or more. Even with this slow 184
growth, bacteria consume an amount of organic carbon that is a large fraction of primary production (Azam et al., 1983). Thus it is suggested that a relatively small phytoplankton biomass must turn over much faster than the bacteria in order to feed the larger bacterial biomass (Fuhrman, 1999).
Conclusions The simulations of the ecosystem of Pagasitikos indicate that nutrient inputs at the north shallow parts close to the city of Volos result in a more stable ecosystem with small monthly variations among the various parameters due to the existence of sucient amounts of nutrients and adequate light to support primary production throughout the year. Even with rather small nutrient inputs the ecosystem of Pagasitikos responds with a signi®cant increase in the primary production with diatoms playing a major role. Although the eect of the enrichment is mostly localized close to the area of inputs (internal Pagasitikos) the whole system responds with a shift to a more classical food chain. Without nutrient inputs the pelagic system of the central-external part of the Gulf is dominated by a microbial loop characterized by the competition for nutrients between bacteria and phytoplankton with a higher heterotrophic to autotrophic biomass. Enrichment develops a more productive system with high autotrophic biomass passing more energy to higher trophic levels. The approximately 400 gC m 2 yr 1 of net primary production produced at the north part due
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Fig. 10 Bacteria simulations (lgC l 1 ) along the transect (a) with external inputs and (b) without external inputs for the months March, August and December.
to nutrient inputs can result in serious eutrophic conditions with the development of intense algal growth. Azam, F., Fenchel, T., Gray, J. G., Meyer-Reil, L. A. and Thingstad, T. (1983) The ecological role of water-column microbes in the sea. Marine Ecology Progress Series 10, 257. Allen, J.I., Blackford, J. and Radford, J. (1998) An 1-D vertically resolved modelling study of the ecosystem dynamics of the middle and southern Adriatic Sea. Journal of Marine Systems 18, 265±286. Baretta, J., Ebenhoh, W. and Ruardij, P. (1995) The European Regional Seas Ecosystem Model, a complex marine ecosystem model. Netherlands Journal of Sea Research 33, 233±246. Baretta-Bekker, J., Baretta, J. and Rasmussen, E. (1995) The microbial foodweb in the European regional Seas Ecosystem Model. Netherlands Journal of Sea Research 33 (3-4), 363±379. Blackford, J. and Radford, P. (1995) A structure and methodology for Marine Ecosystem Modelling. Netherlands Journal of Sea Research 33 (3-4), 247±260.
Blumberg, A. F. and Mellor, G. L. (1978) A coastal ocean numerical model. In Mathematical Modelling of Estuarine Physics. Proceedings of the International Symposium, pp. 203±214. Hamburg. Blumberg, A. F. and Mellor, L. (1987) A description of a threedimensional coastal ocean circulation model. In Coastal Estuarine Science, ed. N. S. Heaps. Bratbak, G. and Thingstad, T. F. (1985) Phytoplankton-bacteria interactions: an apparent paradox? Analysis of a model system with both competition and commensalism. Marine Ecology Progress Series 25, 23±30. Broekhuizen, N., Haeth, M. R., Hay, S. J. and Gurney, W. S. C. (1995) Predicting the dynamics of the North Seas mesozooplankton. Netherlands Journal of Sea Research 33 (3-4), 381±406. Chislholm, W. S. (1992) In Phytoplankton size. Primary Productivity and Biogeochemical Cycles in the Sea, eds. P. G. Falkowski and A. D. Woodhead, pp. 213±237. Plenum Press, New York. Ebenhoh, W., Kohlmeier, C. and Radford, P. J. (1995) The benthic biological sub-model in the European Regional Seas Ecosystem Model. Netherlands Journal of Sea Research 33 (3-4), 423±452.
185
Marine Pollution Bulletin Eppley, W. R. and Peterson, J. B. (1979) Particulate organic matter ¯ux and planktonic new production in the deep ocean. Nature 282, 677±680. Friligos, G. (1987) Eutrophication assessment in Greek coastal waters. Toxical and Enviromental Chemistry 15, 185±196. Friligos, N., Voutsinou-Taliadouri, F., Georgakopoulou-Grigoriadou, F., Gkotsi-Skreta, O., Barbatseas, S., Bogdanos, K., Nikolaou, B., Satsmatjis, I., Siokou, I., Fragoudaki, S., Hatzigeorgiou, E. and Psilidou, R. (1990) Oceanographic Study of Pagasitikos Gulf, National Center of Marine Research, Athens. Fuhrman, A. J. (1999) Marine viruses and their biogeochemical eects. Nature 399, 541±548. Ingrid, G. Andersen, T., Vadstein, O. (1996) Pelagic food webs and Eutrophication of Coastal Waters: impact of grazers on algal communities. Marine Pollution Bulletin 33 (1±6), 22±35. Koliou-Mitsou, A. (1999) Development of integrated policy for the sustainable management of Pagasitikos Gulf, Municipal Water Authority, Volos. Lin, S. J., Chao, W. C., Sud, Y. C. and Walker, G. K. (1994) A Class of the van Leer type transport schemes and its application to the moisture transport in a general circulation model. Monthly Weather Review 122, 1575±1593. Mellor, G. L. (1991) User's Guide for a Three-Dimensional, Primitive Equation, Numerical Ocean Model. Princeton University Press, Princeton. Petihakis, G., Triantafyllou, G. and Theodorou, A. (2000a). Enrichment of Pagasitikos Gulf by run-o fertilisers. A modelling study. Fifth International Conference on the Environmental Pollution. Thessaloniki, Greece.
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Petihakis, G., Triantafyllou, G. and Theodorou, A. (2000b). A numerical approach to simulate nutrient dynamics and primary production of a semi-enclosed coastal ecosystem (Pagasitikos Gulf, Western Aegean, Greece). Periodicum Biologorum 102, 339±348. Ruardij, P. and van Raaphost, W. (1995) Benthic nutrient regeneration in the ERSEM ecosystem model of the North Sea. Netherlands Journal of Sea Research 33 (3-4), 453±483. Theocharis, A. and Friligos, N. (1985) Physical and chemical characteristics of Pagasitikos Gulf. Symposium on the Pollution of Enclosed Bays. The Pagasitikos Case, pp. 85±86. Volos Greece. Theodorou, A. (1998) Oceanographic study of Pagastitikos Gulf. Final Report, University of Thessaly, Volos. Theodorou, A. and Petihakis, G. (2000). Study of Pagasitikos Gulf. Final Report, University of Thessaly, Volos. Thingstad, T. F. (1998) A theoretical approach to structuring mechanisms in the pelagic food web. Hydrobiologia 363, 59±72. Thingstad, T. F. and Lignell, R. (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquatic Microbial Ecology 13, 19±27. Thingstad, T. F. and Sakshaug, E. (1990) Control of phytoplankton growth in nutrient recycling ecosystems. Theory and terminology. Marine Ecology Progress Series, 63, 261±272. Triantafyllou, G. and Petihakis, G. (1999) Ecological Modeling of The Aegean Sea. Institute of Marine Biology of Crete, Iraklion Crete. Varela, R. A., Cruzardo, A. and Gabaldon, J. E. (1995) Modelling the primary production in the North Sea using ERSEM. Netherlands Journal of Sea Research 33 (3±4), 337±361.
Marine Pollution Bulletin Vol. 43, Nos. 7±12, pp. 175±186, 2001 Ó 2001 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0025-326X/01 $ - see front matter S0025-326X(01)00071-6
Assessing Marine Ecosystem Response to Nutrient Inputs TRIANTAFYLLOU GEORGE *, PETIHAKIS GEORGEà,1, DOUNAS COSTAS and ATHANASIOS THEODOROUà,1 Institute of Marine Biology of Crete, P.O. Box 2214, Iraklio, 71003 Crete, Greece àDepartment of Agriculture Crop and Animal Production, University of Thessaly, Pedion Areos 383 34 Volos, Greece The response of the Pagasitikos Gulf to enrichment caused by run-o fertilizers and the development and evolution of harmful algal blooms is investigated through ecosystem modelling. A standard generic complex model has been developed to describe the ecosystem processes of Pagasitikos and has been validated with in situ data. Additionally external nutrient ¯uxes have been assimilated and incorporated into the ecosystem dynamics. The investigation of spatial eects due to nutrient enrichment is investigated along a North±South transect. When externally forced the model successfully assimilates the external river inputs producing nutrient and chlorophyll-a concentrations, which are in good agreement with the in situ data. The nutrient inputs result in a more stable ecosystem at the north part of the Gulf and in the development of eutrophic conditions. The changes in the ecosystem functioning with emphasis on the nutrient cycling, the increase of primary production, and the modes of operation are investigated and discussed. Ó 2001 Elsevier Science Ltd. All rights reserved. Keywords: ecosystem disturbance; ecosystem management; mathematical models; nutrients; phytoplankton; primary production.
Introduction Pagasitikos is a semi-enclosed Gulf situated on the western part of Aegean Sea north of the island of Evia. It has a mean depth of 69 m with the deepest point located at the east part (108 m) characterizing a rather shallow water body. The area of the bay is 520 km2 with a total volume of 36 km3 . It is connected at the south with the Aegean Sea through the 5.5 km wide, narrow channel of Trikeri (Fig. 1). The system of Pagasitikos is greatly in¯uenced by human activities especially around the industrial town of Volos (population 120 000). Although in the sur*Corresponding author. Tel.: +30-81-346-860; fax: +30-81-241-882. E-mail address: [email protected] (T. George). 1 Tel.: +30-421-74312; fax: +30-421-63383.
rounding area there are no major rivers with the exception of small torrents, signi®cant quantities of polluted waters enter the system of the Gulf on a permanent or occasional basis. There are three major pollution sources, the scattered farmlands along the coastline, some rather distant sources and the domestic or industrial euents. In the greater area of Pagasitikos intensive agriculture of cereals and cotton is practized using signi®cant quantities of fertilizers rich in nitrogen, phosphate and sulphur. An important distant source of pollution is Lake Karla where during a drainage programme large quantities of water enriched in nutrients were discharged via channels into the north part of the bay. Also apart from the winter period when rainwater from the wider area of Karla washes the soil, becoming enriched with fertilizers, pesticides and particulate material pour into Pagasitikos and there are discharges of domestic and industrial sewage into the drainage channels throughout the year. Finally the sewage treatment plant of the city of Volos as well as the industrial park of the area located 5 km west from the city are important sources of pollution. The water enrichment at the north part of the bay in conjunction with the increased temperatures of the summer period results in the frequent appearance of harmful algal blooms, causing problems both to tourism and ®sheries (Friligos, 1987). Due to compensatory and buering mechanisms within the food web natural systems seem able to withstand nutrient inputs below a certain limit or critical load without any undesirable eects. However for a given food web structure there should be a certain critical level of nutrient supply where the likelihood of uncontrolled blooms should increase abruptly and nonlinearly (Ingrid et al., 1996). There have been extensive ecosystem studies in the area since 1975 (Friligos et al., 1990; Theocharis and Friligos, 1985) on a number of physicochemical (temperature, salinity, nutrients) and biological parameters (chlorophyll-a, phytoplankton, zooplankton). Also in the recent past (1998±1999) a monitoring programme was set up (Koliou-Mitsou, 1999) in an attempt to study the extent as well as the eects of the nutrient enrichment from Lake Karla. 175
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Fig. 1 Map of Pagasitikos Gulf and simulation transect.
The results of the recent research programme in Pagasitikos (Theodorou and Petihakis, 2000) show that the water mass of Pagasitikos is fairly mixed in the winter months, forming a two-layer thermocline for the rest of the year at approximately 20 m depth, with the exception of August when three layers are observed. Lowest temperatures (12.5°C) are observed during winter (February±March) reaching maximum values (27.4°C) during summer. Salinity exhibits wide ¯uctuations (32±38½) with values increasing with depth due to the in¯ow of low salinity surface waters from the Aegean Sea. In¯ows of fresh waters in the areas of Volos and Almiros are also observed occasionally. Water currents are generally small to moderate due to weak winds and renewal occurs mainly through the deepwater layer of the communication channel with Aegean Sea, in¯owing across the east part and out¯owing across the west part. This water movement is reversed at the surface layer. The dynamics of the system of Pagasitikos are highly in¯uenced both by the anthropogenic activities and the in¯ow of nutrients at the north and west parts as well as by water exchange between the Gulf and the Aegean Sea at its south part through Trikeri channel. The above, in conjunction with the formation of intense thermocline, results in the development of dierent areas within the Gulf. Thus the internal part is characterized by eutrophic conditions, which under favourable conditions 176
result in the development of the harmful algal blooms observed. The central part of Pagasitikos is an organic matter deposition zone since it includes the deep areas of the bay, which due to long strati®cation periods and the dominant anticyclonic circulation, traps all nutrients released from the sediment, developing a microbial food web. It is only when the thermocline erodes that nutrients ®nd their way up in the upper layers of the euphotic zone shifting the system into a classic food web with increased primary production. The outer bay is highly in¯uenced by the Aegean Sea creating a dilution zone with mesotrophic conditions. Thus initially a standard 1D generic complex model developed (Allen et al., 1998) to describe the ecosystem dynamics of Pagasitikos was applied and validated in the central-external (Petihakis et al., 2000b) and internal (Petihakis et al., 2000a) parts of the Gulf. The in¯uence of external nutrient inputs in the internal part of the Gulf, as depicted in the model results, is very important, causing signi®cant changes in the ecosystem functioning. An important issue when examining the eects of a natural or man-induced disturbance is the spatial distribution as well as the magnitude of change moving away from the pollutant source. The aim of this study is to describe along a transect the vertical gradients of the ecological parameters as a function of time in order to investigate the response of the ecosystem due to point source external nutrient inputs.
Material and Methods The ecosystem processes are described by a system of three online linked mathematical models. More speci®cally the hydrodynamics are described by the Princeton Ocean Model (POM), (Blumberg and Mellor, 1978; Blumberg and Mellor, 1987; Mellor, 1991), where both formulation and numerical solutions are described in detail. The physical model contains all information speci®c to the area to be modelled, whereas the biological/chemical sub-models have been constructed to respond to the physico-chemical environment within which they are placed. The advection diusion model of the suspended in the water ecological parameters is simulated by the conservative scheme of (Lin et al., 1994). Lastly the biology is described by the European Regional Seas Ecosystem Model (ERSEM) (Baretta et al., 1995; Baretta-Bekker et al., 1995; Blackford and Radford, 1995; Broekhuizen et al., 1995; Ebenhoh et al., 1995; Petihakis et al., 2000a; Petihakis et al., 2000b; Ruardij and van Raaphost, 1995; Varela et al., 1995). A transect (a) and (b) de®ned by 22.93° longitude and 39.13° to 39.35° latitude from North to South (Fig. 1) across the Pagasitikos Gulf was selected for modelling implementation, since it includes both the area where the Karla euents are discharged and the central and external parts of the Gulf. This transect has been extracted from a three-dimensional model. The transect
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grid consists of 13 boxes along the transect with a size of 1852 m each and 12 boxes in the vertical with a dierent depth ranging from 25 to 86 m. Since ecosystem dynamics near the surface are expected to be more complicated, and thus require more accuracy, the 12 elements have a variable thickness with smaller size near the surface. The upper boxes are open to the air, while in the bottom boxes a benthic module is incorporated. In the ecological model the biological groups are grouped according to their trophic level subdivided by their size class or feeding method. In an attempt to realistically simulate the ecosystem of Pagasitikos following an extensive literature search and in situ data analysis, the food web with the trophic relations among the dierent groups was set up as shown in Fig. 2. The biological variables in the model are; phytoplankton, groups related to the microbial loop, zooplankton and benthic fauna. Biologically driven carbon dynamics are coupled to the chemical dynamics of nitrogen, phosphate, silicate and oxygen. The phytoplankton pool is described by four functional groups based on size and ecological properties. These are diatoms (silicate consumers, 20±200 l), nanophytoplankton (2±20 l), picophytoplankton (< 2 l) and dino¯agellates (> 20 l). All phytoplankton groups contain internal nutrient
pools and have dynamically varying C:N:P ratios. The nutrient uptake is controlled by the dierence between the internal nutrient pool and external nutrient concentration. Since the deep chlorophyll maximum is deeper than biomass maximum, the cell chlorophyll-a content in the model increases with depth following a prede®ned function (Triantafyllou and Petihakis, 1999). The microbial loop contains bacteria, heterotrophic ¯agellates and microzooplankton, each with dynamically varying C:N:P ratios. Bacteria act to decompose detritus and can compete for nutrients with phytoplankton. A mechanism for the phosphorus limitation of bacterial growth is included, which is very important in controlling the ecosystem in the mesotrophic and oligotrophic upper waters (Thingstad and Lignell, 1997). Bacteria are not coupled to the phytoplankton but are dispersed in the water column since dissolved organic carbon exists as a state variable and its usage is nutrient limited. Heterotrophic ¯agellates feed on bacteria and picophytoplankton, and are grazed by microzooplankton. Microzooplankton also consume diatoms and nanophytoplankton and are grazed by mesozooplankton. The benthic±pelagic coupling is described by the settling of organic detritus into the benthos and diusional nutrient ¯uxes into and out of the
Fig. 2 Simulation models and trophic web.
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sediment ± water interface after mineralization and diagenesis. Model application area, initial conditions and forcing The physical model was forced with daily wind velocity values from Anchialos airport for the period 1999 and relaxed, to the monthly mean surface temperature and salinity. It was initialized with January 1999 temperature and salinity values (Theodorou and Petihakis, 2000). The ecosystem model was initialized with in situ biogeochemical winter (January) ®eld data where available (Theodorou, 1998) while all other parameters used are the standard ERSEM v11 values (Petihakis et al., 2000a; Petihakis et al., 2000b).
The nutrient inputs were implemented in the model as an external source calculated from the dierence in nutrient concentrations in the central part of the Gulf and those measured at the mouth of Xirias River. The external nutrient quantities were assimilated in the model using a simple relaxation scheme: H d v ; 1 v vdata s dt where v; vdata are four-dimensional vectors with components concentrations of NO3 ; NH4 ; PO4 and SiO2 of the model and in situ data, respectively. H 7 m the depth in¯uenced by the external nutrient inputs and s 1 day the relaxation time.
Fig. 3 Model results and in situ measurements of central-external Gulf at 30 m depth.
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Results and Discussion Central-external Gulf The 1D model for the central-external Pagasitikos reproduces well the evolution of physico-chemical parameters at 30 m layer (Fig. 3). The increased levels of nitrate ammonia and phosphate during spring depicted by the in situ data concentrations might be attributed to the degradation of primary production and recycling of organic material as evidenced by the chlorophyll-a levels, rather than in¯ows since the increased levels are observed in the whole water column and not in the
surface layer only. According to the phytoplankton succession, maximum biomass occurs during winter with the ¯agellates being the dominant group followed by diatoms and nanoplankton. In the following months nanoplankton becomes the dominant group while all other groups exhibit signi®cant lower levels of biomass. Internal Gulf Model results depicting the seasonal variation of nutrients and primary producers in the surface layer with and without ¯ux were validated with in situ data (Fig. 4). In all four nutrient simulations the implementation of
Fig. 4 Model results with and without nutrient input ¯ux and in situ measurements of internal Gulf (Karla euents) at surface layer.
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external ¯uxes signi®cantly improves the model results (especially those of silicate and ammonia). Chlorophylla simulation also improves with the implementation of external nutrient ¯uxes indicating that the dierence in the chlorophyll-a levels between the central and inner parts of the Gulf might be attributed to nutrient enrichment. Transect An important characteristic of Pagasitikos is the smooth increase in depth at the northern in contrast to the high gradient observed at the south resulting in ef®cient wind mixing and transport of resuspended nutrients from the sediment into the water column, while at
the deeper parts in the south sediment nutrient releases are trapped at the 50±85 m layer for signi®cant time periods. Two model runs have been made for one year, one with nutrient inputs at the north part of the transect and one without inputs (standard run). Three months were selected for the presentation of the results: March is the month when the water column is mixed most, while during August an intense strati®cation is observed and ®nally December is characterized by signi®cant rainfalls and subsequent inputs from Lake Karla into the system of Pagasitikos. Model runs for 1999 (monthly means for ecosystem parameters) from both runs for the three months are presented and discussed.
Fig. 5 Nitrate simulations (lmol l 1 ) along the transect (a) with external inputs and (b) without external inputs for the months March, August and December.
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Nitrate enrichment is rather signi®cant only in the north part of Pagasitikos with maximum values during December (3 lmol l 1 ) producing a gradient zone of approximately 5 km (Fig. 5). High concentrations (3:3 lmol l 1 ) at the deeper parts of the transect (50±85 m) at the end of the year are possibly due to the destruction of strati®cation with the subsequent settling of organic material and increased benthic activity. In the absence of external inputs the distribution of nitrates is characterized by higher levels of nitrate in the water layers close to the bottom especially in December. Unlike nitrate, phosphate enrichment is maximum during March (0:7 lmol l 1 ), strongly aecting the shallow area at the north part (Fig. 6). Minimum levels
(0:03 lmol l 1 ) occur in the upper and middle layers of the central-external parts of the Gulf during August and December. In the model run without inputs phosphate concentrations are very low (0:01±0:22 lmol l 1 ) in all three months increasing with depth. From the chlorophyll-a results (Fig. 7) it is shown that the area with nutrient inputs close to the city of Volos produces a similar picture in all three months with maximum concentrations (5:5 lg l 1 ) at the shallower area extending to approximately 5 km. In August a tongue of 0:5 lg l 1 of chlorophyll-a is extended to the central part of the simulation area possibly due to the presence of thermocline. In the absence of nutrient inputs the levels of chlorophyll-a as produced by the
Fig. 6 Phosphate simulations (lmol l 1 ) along a transect (a) with external inputs and (b) without external inputs for the months March, August and December.
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Fig. 7 Chlorophyll-a simulations (lg l 1 ) along a transect (a) with external inputs and (b) without external inputs for the months March, August and December.
model are signi®cantly lower (0:02±1:4 lg l 1 ) with maximum values during August at 40±50 m layer due to regenerated production, designating the presence of a nitracline. High chlorophyll-a concentrations (1:2 lg l 1 ) are also produced during December in the shallow north part close to the city of Volos, which might be attributed to resuspension of nutrients and adequate light. As with chlorophyll-a total primary biomass at the shallow north part of the Gulf under the in¯uence of nutrient enrichment does not dierentiate signi®cantly between the three months exhibiting particularly high levels (270 lgC l 1 ), while the area with increased values (60±270 lgC l 1 ) extends to approximately 5 km (Fig. 182
8). Also a subsurface tongue is produced during August between 15 and 60 m. In the absence of external inputs total primary biomass is much lower with maximum levels during August and December (40 lgC l 1 ). As expected in March higher values occur in the upper layers taking advantage of the mixing of waters in contrast with August when maximum biomass is located in the 30±50 m layer close to the thermocline. December is characterized also by a subsurface maximum (50 lgC l 1 ) but also at shallower depths (20±30 m) possibly because of thermocline erosion. Under nutrient enrichment diatoms contribute approximately 2/3 of the total phytoplankton biomass followed by picoplankton and ¯agellates. The large
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Fig. 8 Total primary biomass simulations (lgC l 1 ) along the transect (a) with external inputs and (b) without external inputs for the months March, August and December.
primary producers (diatoms and ¯agellates) exhibit a signi®cant increase in biomass as expected with the addition of nutrients in contrast with the small size cells, which seem to have an upper threshold. It is suggested that nutrient enrichment causes a shift away from small phytoplanktonic groups (nano and pico plankton) with a clear advantage to bigger cells (Ingrid et al., 1996). This is possibly due to the fact that in oligotrophic waters, small cells are dominant with the majority of primary production driven by reduced nitrogen (NH4 ), and only when new nitrogen (NO3 ) arrives either as external inputs or due to water column mixing the large cells take over (Eppley and Peterson, 1979). Another reason is that the acquisition
of nutrients by large cells can be limited by molecular diusion at very low nutrient concentrations since cells with small radius can grow at higher rates (Chislholm, 1992; Thingstad, 1998). It is suggested that the total amount of chlorophyll in each size fraction has an upper limit and beyond certain thresholds chlorophyll can be added to a system only by adding a larger size class of cells, mostly diatoms (Chislholm, 1992). (Thingstad and Sakshaug, 1990) showed that in a plankton model with two parallel food chains increased nutrient supply could lead to a shift from dominance of a four-level chain (small algae ± ciliates-copepods®sh) to a shorter three-level chain (large algae ± copepods-®sh). 183
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Fig. 9 Simulations net primary production (mgC m 2 yr 1 ) along the transect with external inputs and without external inputs.
The eects of the enrichment in the productivity of the system of Pagasitikos can be quanti®ed from the integrated annual net primary productivity along the transect (Fig. 9). It is shown that in the area of nutrient inputs at the north of the Gulf there is an addition of 400 gC m 2 yr 1 decreasing away from the point source (approximately 5 km) to 100 gC m 2 yr 1 . Also there is a transition zone at the central part covering a distance of about 10 km while the rest (outer part) remains unaected. An interesting feature emerging from the model result is the relation between primary production and bacteria biomass. In the case of nutrient ¯ux total primary production is signi®cantly higher (approximately 3-fold) compared to the bacterial biomass (Figs. 8 and 10). When there are no nutrient inputs bacterial biomass is three times higher than total primary biomass during March and slightly higher in the other two months. In an environment where primary production is limited by the availability of mineral nutrients this would lead to competition between phytoplankton and heterotrophic bacteria for the limiting mineral nutrient (Bratbak and Thingstad, 1985). Considering the larger surface to volume ratio and the small size of bacteria it is obvious that they are more ecient competitors for mineral nutrients although they cannot out-compete the algae completely since this would remove their source of carbon/energy substrate. In oligotrophic waters the bacterial biomass, depth integrated over the euphotic zone exceeds that of phytoplankton, although heterotrophic bacterial production is low, with population doubling times of about a week or more. Even with this slow 184
growth, bacteria consume an amount of organic carbon that is a large fraction of primary production (Azam et al., 1983). Thus it is suggested that a relatively small phytoplankton biomass must turn over much faster than the bacteria in order to feed the larger bacterial biomass (Fuhrman, 1999).
Conclusions The simulations of the ecosystem of Pagasitikos indicate that nutrient inputs at the north shallow parts close to the city of Volos result in a more stable ecosystem with small monthly variations among the various parameters due to the existence of sucient amounts of nutrients and adequate light to support primary production throughout the year. Even with rather small nutrient inputs the ecosystem of Pagasitikos responds with a signi®cant increase in the primary production with diatoms playing a major role. Although the eect of the enrichment is mostly localized close to the area of inputs (internal Pagasitikos) the whole system responds with a shift to a more classical food chain. Without nutrient inputs the pelagic system of the central-external part of the Gulf is dominated by a microbial loop characterized by the competition for nutrients between bacteria and phytoplankton with a higher heterotrophic to autotrophic biomass. Enrichment develops a more productive system with high autotrophic biomass passing more energy to higher trophic levels. The approximately 400 gC m 2 yr 1 of net primary production produced at the north part due
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Fig. 10 Bacteria simulations (lgC l 1 ) along the transect (a) with external inputs and (b) without external inputs for the months March, August and December.
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Petihakis, G., Triantafyllou, G. and Theodorou, A. (2000b). A numerical approach to simulate nutrient dynamics and primary production of a semi-enclosed coastal ecosystem (Pagasitikos Gulf, Western Aegean, Greece). Periodicum Biologorum 102, 339±348. Ruardij, P. and van Raaphost, W. (1995) Benthic nutrient regeneration in the ERSEM ecosystem model of the North Sea. Netherlands Journal of Sea Research 33 (3-4), 453±483. Theocharis, A. and Friligos, N. (1985) Physical and chemical characteristics of Pagasitikos Gulf. Symposium on the Pollution of Enclosed Bays. The Pagasitikos Case, pp. 85±86. Volos Greece. Theodorou, A. (1998) Oceanographic study of Pagastitikos Gulf. Final Report, University of Thessaly, Volos. Theodorou, A. and Petihakis, G. (2000). Study of Pagasitikos Gulf. Final Report, University of Thessaly, Volos. Thingstad, T. F. (1998) A theoretical approach to structuring mechanisms in the pelagic food web. Hydrobiologia 363, 59±72. Thingstad, T. F. and Lignell, R. (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquatic Microbial Ecology 13, 19±27. Thingstad, T. F. and Sakshaug, E. (1990) Control of phytoplankton growth in nutrient recycling ecosystems. Theory and terminology. Marine Ecology Progress Series, 63, 261±272. Triantafyllou, G. and Petihakis, G. (1999) Ecological Modeling of The Aegean Sea. Institute of Marine Biology of Crete, Iraklion Crete. Varela, R. A., Cruzardo, A. and Gabaldon, J. E. (1995) Modelling the primary production in the North Sea using ERSEM. Netherlands Journal of Sea Research 33 (3±4), 337±361.