Coastal Lagoons - Chapter 5 pot

Effects of Changing Environmental Conditions on Lagoon Ecology Sofia Gamito, Javier Gilabert, Concepción Marcos Diego, and Angel Pérez-Ruzafa CONTENTS 5.1 Introduction 5.2 Eutrophication Process 5.2.1 Oligotrophic State 5.2.1.1 Submerged Vegetation and Related Energy Pathways 5.2.1.2 Phytoplankton 5.2.1.3 Zooplankton 5.2.1.4 Benthic Fauna 5.2.1.5 Fish Assemblages 5.2.2 Mesotrophic State 5.2.2.1 Competition between Rooted Vegetation and Macroalgae 5.2.2.2 Microbial vs. Herbivorous Food Web 5.2.2.3 Benthic Fauna 5.2.2.4 Fish Assemblages (Pelagic/Benthic) 5.2.3 Eutrophic State 5.2.3.1 Phytoplankton 5.2.3.2 Benthic Vegetation 5.2.3.3 Benthic Fauna 5.2.3.4 Fish and Bird Assemblages 5.3 Water Renewal Rates 5.3.1 Choked Lagoons 5.3.2 Restricted Lagoons 5.3.3 Leaky Lagoons 5.3.4 Water Renewal Rate and Eutrophication 5.4 Changes in Lagoon Processes and Management of Living Resources 5.5 Remarks References 5 L1686_C05.fm Page 193 Monday, November 1, 2004 3:37 PM © 2005 by CRC Press 5.1 INTRODUCTION Coastal lagoon ecosystems are dynamic and open systems, dominated and subsi- dized by physical energies, and characterized by particular features (such as shallowness, presence of physical and ecological boundaries, and isolation) that distinguish them from other marine ecosystems. 1 Shallowness usually provides a lighted bottom, and the wind affects the entire water column, promoting resus- pension of materials, nutrients, and small organisms from the sediment to the surface layer. The large number of boundaries (between water and sediment, pelagic and benthic communities, and among lagoon, marine, freshwater, and terrestrial systems and with the atmosphere) involve the existence of intense gradients and, consequently, a high potential to do work. 1 (Figure 5.1). Because of that, coastal lagoons are usually among the marine habitats with the highest biological productivity. 2 Nutrient input from both run-off and irrigated land waters and from currents through tidal channels contribute to increase the primary pro- ductivity affecting the structure of the communities. On the one hand, due to their relatively high degree of isolation, outlets usually have a total surface of less than 20% of the barrier closing the lagoon, 3 and the water exchange between lagoons and the open sea is limited, resulting in a series of physical, chemical, and hydrodynamic boundaries. 4 On the other hand, the generated environmental stress regulates the structure of biological assemblages and leads to complex interactions among physical (light, temperature, mixing, flow), chemical (organic and inor- ganic carbon, oxygen, nutrients), and biological parameters and processes (nutri- ents uptake, predation, competition). As a consequence of high levels of biological productivity, lagoons play an important ecological role among the coastal zone ecosystems, providing a collection of habitat types for many species 5 and maintaining high levels of biological diversity. Most lagoons are subjected to human exploitation through fishing, aquaculture, tourism, and urban, industrial and agricultural developments, inducing changes that affect their ecology. Under the designation of lagoons a high diversity of environments can be found. Size can vary from a few hundred square meters to extensive areas of shallow coastal sea. The salinity range can go from nearly fresh to hyperhaline waters, with concentrations of salt reaching three times the salinity of the adjacent sea. 6 Salt balance relies on several factors such as the exchange of water with the open sea, the inputs of continental waters from rivers, watercourses and ground- water, and on the rainfall-evaporation balance. The variability of salinity can also be observed inside the lagoon both spatially and temporally. From a hydrographical point of view, most of this variability between lagoons can be summarized by a set of quantitative parameters or indexes that describe both lagoon orientation and structure, as well as spatial variability and the potential sea influence (see Chapter 6 for details). In biological terms, heterogeneity can be applied to both the structure (species composition and abundance) and functioning (productivity, trophic webs, and fluxes) of the lagoon ecosystem at a wide range of spatial and temporal scales, from biogeographic (thousands of kilometers) to regional (hundred to thousands L1686_C05.fm Page 194 Monday, November 1, 2004 3:37 PM © 2005 by CRC Press FIGURE 5.1 Diagram showing the main components and ecological relationships in a coastal lagoon. External inputs of matter and energy and intense gradients at different interfaces result in ecosystems with high le vels of biological productivity. Solar energy Detritus Nutrients Wind Rainfall Run-off Phytoplankton Zooplankton Pelagic fishes Benthic fishes MF mf IB MF= Macrophytobenthos mf = Microphytobenthos IB = Benthic invertebrates Pelagic system Benthic system Fisheries Migrations OPEN SEA Inputs from the open sea Human activities Dredging Pumping Coastal works L1686_C05.fm Page 195 Monday, November 1, 2004 3:37 PM © 2005 by CRC Press of kilometers, including distinct lagoons in the same area) and local (the inside of the lagoon) (Table 5.1). From both structural and functional points of view, it is possible to categorize two extreme types of lagoons, one with a stable and predictable environment and the other with frequent physical and chemical disturbances and fluctuations 1 or, according to Sanders, 7 biologically adapted lagoons and physically controlled ones, respectively. Species strategies respond to these situations according to a continuum of life-history strategies, r vs. K ( r refers to the rate of increase in the exponential population growth curve and K refers to the carrying capacity of the population in the logistic growth model). 8 The r -strategy involves increased reproductive effort through early reproduc- tion, small and numerous offspring with large dispersive capability, short life span, and small body size of adults. This provides a selective advantage in unpredictable or short-lived environments. At the other extreme, K -strategy species spend more energy on maintenance structures and adaptations, in a predictable environment, than on reproduction. Species with this kind of strategy usually are larger, long living, less abundant, and show higher biomass/reproductive ratios. The models used to simulate lagoons dynamics can work at different spatial and temporal scales depending on the process considered, the grid size used, and the quality of input data. Physical and hydrodynamic numerical models can provide quantitative descriptions in a continuum of spatial and temporal scales because of the linearity of many of the involved processes (see Chapters 3 and 6 for details). However, biological processes are complex and show nonlinear TABLE 5.1 Main Sources of Variability to Explain Differences at Hierarchical Spatial and Temporal Scales, in Coastal Lagoons Spatial Scales Main Source of Spatial Variability Temporal Scales Main Source of Temporal Variability 10 3 km Biogeographical climatic differences >10 4 years Global climatic change (ecosystem level) 10 2 –10 3 km Hydrographic features and geomorphology of lagoons (mainly isolation degree); trophic status 10 1 –10 4 years Changes in hydrographic and geomorphological features and trophic status (sucessional level) 10 − 3 –10 2 km Substrate type; confinement gradient; hydrodynamics; trophic status 10 0 –10 1 years Interannual fluctuations in populations; changes in recruitment; colonization of species and migrations; predation and competition processes (community level) 10 − 5 –10 − 3 km Vertical zonation; patchiness of species distribution and population density; microhabitat heterogeneity < 10 0 years Seasonal fluctuations of populations; predation and competition processes (population and community level) L1686_C05.fm Page 196 Monday, November 1, 2004 3:37 PM © 2005 by CRC Press relationships, and the scale of the scenarios to be modeled should be previously defined (see Chapter 2 for details). In coastal lagoons, the relevant spatial and temporal scales for management purposes mainly affect the overall lagoon ecosystem and its successional stages. At these scales, heterogeneity can be explained mainly by variations in two principal factors: water renewal rate related to isolation degree, and trophic status related to availability of nutrients. The focus of this chapter is to outline changes in the main biological features and processes in lagoons under different eutrophication states and water renewal rates that must be considered when implementing ecological modeling as a decision support tool for sustainable use and development. 5.2 EUTROPHICATION PROCESS As explained in Chapter 2, human activity is responsible for extensive modifications of many of the global element cycles, to the extent that more elements/nutrients are fixed annually by human-driven activities than by natural processes. 9 Coastal lagoons may receive nutrients from a wide range of sources such as domestic sewage, agricultural activities, industrial wastewater, and atmospheric fall-out. The process in which there is an increase in the rate of addition of nitrogen and phosphorus, considered as the two main limiting factors for primary production to a natural system, usually aquatic, is called eutrophication. Eutrophication is a process, 10 not a trophic state, meaning “an increase in the rate of supply of organic matter to an ecosystem.” 11 It is mainly identified with an increase in the input of inorganic nutrients in the ecosystem. It must be taken into account, however, that if the level of primary production, even though it is high, remains constant over time, it does not imply that eutrophication will occur because there will not be any change in the carbon supply rate. It is well known that small amounts of nutrients usually stimulate primary production. This does not automatically imply a linear increase of the whole pro- duction of the ecosystem, but it frequently produces changes in the biological structure and functioning of the whole ecosystem. This leads to the progressive replacement of seagrasses and slow-growing macroalgae by fast-growing macroal- gae and phytoplankton, with a final dominance of phytoplankton at high nutrient loads. 12,13 Competition of primary producers for nutrients is one of the responsible processes, but not the only one. Alteration in water turbidity, changes in the hydraulic conditions resulting in modifications of water residence time and a decline of grazing pressure, are also factors that promote shifts in the dominant plant communities. A comprehensive sequence of changes in major plant groups following nutrient enrich- ment in a wide range of ecosystems has been given by Harlin. 14 These changes in submerged vegetation during eutrophication appear to occur as a step process, with sudden shifts in submerged vegetation, not directly coupled to increased nutrient loading alone, but occurring due to many indirect and feedback mechanisms. 12 Changes in the primary producers’ structure affect secondary producers, as they are the basis of the trophic food web. The trophic status of a coastal lagoon, however, does not depend exclusively on the nutrient load but on the hydrodynamics, which, in L1686_C05.fm Page 197 Monday, November 1, 2004 3:37 PM © 2005 by CRC Press turn, determine the residence time of nutrients in the lagoon. For example, discharging the same amount of nutrients into a leaky lagoon with strong tidal currents will not have the same local effects as will a similar discharge into a choked lagoon with a low water exchange (see Chapter 6 for classifications of lagoons). Four successional stages can be identified in the eutrophication process: olig- otrophic, mesotrophic, eutrophic, and hypertrophic. Nixon 11 provides some ranges of carbon supply (primary production) in the ecosystem for each stage (Table 5.2). Abundant seagrasses (such as Eelgrass Zostera, Cymodocea, Posidonia, or Thalassia ) and transparent water at relatively low nutrient concentrations generally characterize the oligotrophic state of coastal lagoons. The mesotrophic state, charac- terized by moderate nutrient concentrations, is associated with the presence of benthic macroalgae at the bottom level and some higher phytoplankton concentration in the water column. At this stage, complex interactions among these primary producers (macroalgae and phytoplankton) and with primary consumers (grazers) lead, in some systems, to cycles of alternate dominance by either submerged vegetation or phy- toplankton. These cycles can be relatively stable. However, a large disturbance, with the ability to affect different parts of the ecosystem, can override the self-stabilizing capacities, causing a shift from a benthic to a planktonic dominated system. 15,16 A lagoon is considered eutrophic when high nutrient concentrations can be found in the water column. The biomass and production of phytoplankton communities that are greatly stimulated with nutrients produce highly turbid waters until the point that the phytoplankton biomass becomes dense enough to limit light access to the bottom, 17 thus preventing growth of benthic vegetation seagrasses. Benthic vegetation is then restricted to shallower areas, mostly disappearing in the deepest zones. Oxygen con- sumption from degradation of produced organic material increases, especially in the sediment, thus causing anoxic periods. The lack of oxygen and production of toxic gasses, such as hydrogen sulphide, due to the anaerobic condition in the sediment (see Chapter 4), has detrimental effects on the bottom-living fauna and in the recruit- ment of species (mainly fishes and crustaceans) that enter into the lagoon as larvae and juvenile stages. Hypereutrophy is generally considered an extreme case of eutro- phy in which the above-mentioned characteristics are heavily enhanced. An idealized sequence of the main features of the eutrophication processes is summarized in Figure 5.2 and will be described in the following sections of this chapter. TABLE 5.2 Successional Stages in Eutrophication Processes Related to Organic Carbon Supply Successional Stages Organic Carbon Supply (g C m − 2 y − 1 ) Oligotrophic <100 Mesotrophic 100–300 Eutrophic 301–500 Hypertrophic >500 Source : Nixon, S.W., Ophelia , 41, 199, 1995. With permission. L1686_C05.fm Page 198 Monday, November 1, 2004 3:37 PM © 2005 by CRC Press FIGURE 5.2 Representation of changes in the lagoon ecosystem with increasing nutrient loads. Top: In the oligotrophic state submerged aquatic vegetation is dominated by seagrasses and the planktonic food web is based on the microbial loop. At moderate nutrient loads— mesotrophic state—macroalgae outcompete seagrasses and small phytoplankton grow. At high nutrient loads, large-celled phytoplankton dominates in the water column. Light is strongly trapped becoming the limiting factor for macroalgae and benthic fauna turns to deposit feeders. Middle: Evolution of the abundance of submerged aquatic vegetation, epiphytes and phy- toplankton, with nutrient load and light reaching the bottom. (Adapted from Nienhuis, P.H., Vie Milieu , 42, 59, 1992. With permission.) Bottom: Relative changes from benthic to pelagic dominated vegetation with nutrient load and residence time of the water in the lagoon (S = seagrass; M = macroalgae; P = phytoplankton). (Adapted from Valiela, I. et al., Limnol . Oceanogr ., 42, 1105, 1997. Copyright 1997 by the American Society of Limnology and Oceanography, Inc. With permission.) Seagrass Epiphytes Macroalgae Phytoplankton Nutrient load Bottom Light Intensity Short Residence Time Long Residence Time Low High Low High Nitrogen loading rates Nitrogen loading rates S S M M P P Biomass L1686_C05.fm Page 199 Monday, November 1, 2004 3:37 PM © 2005 by CRC Press 5.2.1 O LIGOTROPHIC S TATE Oligotrophic lagoons have low levels of nutrient concentrations in the water column. The first consequence of this lack of nutrients is to restrict phytoplankton growth, keeping water at high transparency levels. Light can easily reach the bottom, and is not a limiting factor for benthic vegetation. 5.2.1.1 Submerged Vegetation and Related Energy Pathways Under oligotrophic conditions, with very low concentrations of nutrients in the water column, nutrients are mainly available at the sediment level. Therefore, the stimu- lation of growth of aquatic plants that take up nutrients from roots vs . algae that take up nutrients directly from water is enhanced. 18 Seagrass can develop within coastal lagoons for a long time (decades to centuries) based on slowly accumulating nutrient pools which are efficiently recycled. 19 This long-term development is also supported by self-stabilizing mechanisms. Seagrass influences the water transpar- ency, decreasing sediment resuspension by retention in the water-sediment interface. Benthic microalgae also contribute to keep sediment oxygenated through photosyn- thesis. Sediment mineralization (see Chapter 4) usually supplies enough nutrients to benthic micro algae to make them relatively independent of nutrient concentration in the water. 20,21 Sediment maintained at high oxygenation levels provide a suitable environment for both benthic filter feeders and detritivorous organisms. Low levels of nutrients in water, moreover, prevent the presence of epiphytes on seagrasses that can cause a detrimental effect on their growth by reducing light at the leaf level. 16,22 Benthic rooted vegetation seagrass is the main primary producer in oligotrophic lagoons, providing food to many organisms such as benthic invertebrates and fishes. However, the energy of most seagrasses becomes available to secondary producers after being fragmented and processed through the detritical pathway. 23 The process of decomposition of leaf litter usually starts with autolysis leaching out soluble materials, such as dissolved organic matter (DOM) with bacteria colonizing frag- mented material. Macrobenthic organisms, mainly debris-eating amphipods and isopods, can also tear off pieces of plant material with its attached community of microorganisms. Other macrobenthic organisms, such as herbivorous gastropods, can enhance seagrass growth and production by grazing on epiphytes. 24,25 Popula- tions of predators such as ciliates, nematodes, and some polychaetes can develop and their feces may be re-colonized by microorganisms and reingested again, thus reducing progressively the size of the debris. 26–28 Part of the dissolved organic matter is released to the water column and some is aggregated into amorphous organic particles (approximately from a few µ m to 500 µ m in diameter). 29 Many biotic and abiotic mechanisms are involved in the aggregate formation, providing a microenvironment that facilitates growth of bacteria and very small phytoplankton in nutrient-deficient waters. 30 Both environments, plant debris and amorphous organic particles, can be colonized by bacteria, making them available to larger consumers that are not effective in capturing free bacteria. Initial colonization of plant debris by bacteria is subsequently completed by a community of protozoa and ciliates feeding on them even though bacteria also can be released to the water column. L1686_C05.fm Page 200 Monday, November 1, 2004 3:37 PM © 2005 by CRC Press Bacteria in the water column are the base of the so-called microbial loop. 31 They can be effectively grazed by heterotrophic flagellates and ciliates and then by other zooplankton that in turn provide available food for larger pelagic organisms such as fish larvae and juveniles. Although the energetic transfer efficiency of the microbial loop is relatively low, because many trophic steps are involved, it remains as one of the most characteristic food web structure in the pelagic environment of oligotrophic lagoons 32 based on recycled nutrients. 5.2.1.2 Phytoplankton Photosynthesis, the process allowing phytoplankton cells to grow, is regulated by the adaptation of cells to varying environmental conditions at a certain range of space and time scales (see last row in Table 5.1). The main environmental variables affecting the physiological state of the algae are light, temperature, and nutrient concentrations. Others, such as salinity, can be determinant for the presence of certain species. The adaptative response of phytoplankton cells varies widely, depending on their ecophysiology and on the environmental conditions of the area where they have been growing. For a specific lagoon habitat, some phytoplankton species would find better con- ditions to grow on the basis of their ability to compete for resources at characteristic ranges. As mentioned above, light is not usually a problem for phytoplankton in oligotrophic waters, but lack of nutrients may constitute a serious limitation. Phy- toplankton takes up nutrients from the water following the carrier-mediated transport of Michaelis-Menten kinetics, in which nutrient uptake ( V ) is a hyperbolic function of substrate concentration ( S ), with the half-saturation constant K s equivalent to the concentration necessary to achieve half of the maximum rate of uptake ( V max ): 33 V = V max S /( K s + S ) (5.1) K s can vary, depending on temperature, light, and V max , making this parameter characteristic for species from different areas, either oceanic or coastal (see Chapter 4, Section 4.1.5 for details). If algal cells are under steady-state conditions of nutrient limitation, then the Michaelis-Menten expression can be assumed to reflect the growth kinetics in the form 33 µ = µ max S /( K s + S ) (5.2) where µ and µ max are the growth rate and maximum growth rate, respectively, and K s is now the half-saturation constant for growth which is very similar to the half- saturation constant for nutrient uptake (Figure 5.3). The steady-state condition of nutrient limitation assumed by this kinetics is not generally fulfilled in oligotrophic waters as phytoplankton cells can store nutrients in internal pools to be used when they are scarce. This phenomenon, known as luxury uptake , was described by Droop 34–36 in his model for intracellular content of the limiting nutrient: µ = µ max [1-( Q o / Q )] (5.3) L1686_C05.fm Page 201 Monday, November 1, 2004 3:37 PM © 2005 by CRC Press where Q is the nutrient content per cell ( Q = uptake rate/cell division rate) and Q o is the minimal nutrient content allowing cell division. Growth rate is thus dependent on cell nutrient content which, at the same time, depends on the adaptation of cells to nutrient concentration in water (Figure 5.4). Implications for the luxury uptake of nutrients by phytoplankton are relevant in nutrient-limited water, as nutrients are not homogeneously distributed in the water column. Zooplankton, or excretion of other organisms, creates small patches of recycled nutrients that phytoplankton can go through, taking up and storing them, 37 thus providing the chance to grow even at very low nutrient concentration in the water. FIGURE 5.3 Relation between phytoplankton growth rate and nutrient concentration. Phytoplankton takes up nutrients from the water following the Michaelis-Menten kinetics (V = V max S/(K s + S)). Different lines show kinetics with different K s and V max . FIGURE 5.4 Luxury uptake: Growth rate is dependent on cell nutrient content which, at the same time, depends on the adaptation of cells to nutrient concentration in water. Growth rate Nutrient concentration Nutrient content per cell Growth rate L1686_C05.fm Page 202 Monday, November 1, 2004 3:37 PM © 2005 by CRC Press [...]... or from adults from the open coastal sea REFERENCES 1 UNESCO, Coastal lagoons research, present and future UNESCO Technical Papers in Marine Science, 33, 1981, pp 51 –79 2 Alongi, D.M., Coastal Ecosystem Processes, CRC Press, Boca Raton, FL, 1998, p 188 3 Bird, E.C.F., Changes on barriers and spits enclosing coastal lagoons, Oceanol Acta, N.S.P 45, 1982 4 UNESCO, Coastal lagoons survey UNESCO Technical... M.F., and Sand-Jensen, K., Size-dependent nitrogen uptake in micro- and macroalgae, Mar Ecol Prog Ser., 118, 247, 19 95 40 Legendre, L and Rassoulzadegan, F., Plankton and nutrient dynamics in marine waters, Ophelia, 41, 153 , 19 95 41 Thingstad, T.F., A theoretical approach to structuring mechanisms in the pelagic food chain, Arch Hydrobiol., 363, 59 , 1998 © 20 05 by CRC Press L1686_C 05. fm Page 2 25 Monday,... previously, coastal lagoons are more productive than other ecosystems in terms of fisheries yield.120 They are important in the life cycles of many © 20 05 by CRC Press L1686_C 05. fm Page 218 Monday, November 1, 2004 3:37 PM coastal fishes, allowing a high standing stock Three main groups of fishes may occur in coastal lagoons: 1 Sedentary species—Those that spend their entire life cycle within coastal lagoons. .. macrophytes on fish-zooplankton-phytoplankton interaction: large-scale enclosure experiments in a shallow eutrophic lake, Freshwat Biol., 33, 255 , 19 95 43 Sieburth, J McN., Sea Microbes, Oxford University Press, New York, 1979, chap.1 44 Lehman, J.T., Interacting growth and loss rates: the balance of top-down and bottomup controls in plankton communities, Limnol Oceanogr., 36, 154 6, 1991 45 Landry, M.R.,... 118 Kjerfve, B and Magill, K.E., Geographic and hydrographic characteristics of shallow coastal lagoons, Mar Geol 88, 187, 1989 119 Kjerfve, B., Coastal lagoons, in Coastal Lagoon Processes, Kjerfve, B., Ed., Elsevier, Amsterdam, 1994, chap.1 ˜ 120 Pauly, D and Yá nez-Arancibia, A., Fisheries in coastal lagoons, in Coastal Lagoon Processes, Kjerfve, B., Ed., Elsevier, Amsterdam, 1994, chap 13 121 Fonseca,... indirectly by feeding on detritus and microorganisms .51 ,52 Increased transport due to ventilation © 20 05 by CRC Press L1686_C 05. fm Page 2 05 Monday, November 1, 2004 3:37 PM of burrow water usually enhances reaction rates and solute fluxes whereas reworking during burrowing is responsible for displacement of organic particles.8 5. 2.1 .5 Fish Assemblages Oligotrophic lagoons also have extensive areas of sandy and... Confinement α-hypersaline β-hypersaline FIGURE 5. 10 Diagram showing the possible classification of coastal lagoons and lagoon water bodies in function of the three main parameters (ionic composition of salts, salinity, and confinement) that affect biological communities (Redrawn from Pérez-Ruzafa, A and Marcos, C., Rapp Comm Int Mer Mediter., 33, 100, 1992 With permission.) © 20 05 by CRC Press L1686_C 05. fm Page... 1998 57 Gurney, W.S.C and Nisbet, R.M., Ecological Dynamics, Oxford University Press, Oxford, U.K., 1998, p 204 58 Baretta-Bekker, J.G., Baretta, J.W and Rasmussen, E.K., The microbial food web in the European regional seas ecosystem model, Neth J Sea Res., 33, 363, 19 95 59 Blindow, I., Long- and short-term dynamics of submerged macrophytes on two shallow eutrophic lakes, Freshwat Biol., 28, 15, 1992... advantage over seagrass, allowing them to spread extensively on the lagoon bottom .59 Seagrasses and slow-growing macroalgae have nutrient contents much lower than those of phytoplankton.60,61 It has been estimated that nitrogen and phosphorus requirements of phytoplankton and macroalgae are about 5 0- and 100-fold higher, and 8- and 1 . 5- fold higher, respectively, than those of seagrasses.12 Occasionally water... B., Aquatic primary production in coastal lagoons, in Coastal Lagoon Processes, Kjerfve, B., Ed., Elsevier, Amsterdam, 1994, chap 9 23 Newell, R.C., The energetics of detritus utilisation in coastal lagoons and nearshore waters, Oceanol Acta, 4, 347, 1982 24 Cattaneo, A., Grazing on epiphytes, Limnol Oceanogr., 28, 124, 1983 25 Orth, R.J and van Montfrans, J., Epiphyte-seagrass relationships with an . (Pelagic/Benthic) 5. 2.3 Eutrophic State 5. 2.3.1 Phytoplankton 5. 2.3.2 Benthic Vegetation 5. 2.3.3 Benthic Fauna 5. 2.3.4 Fish and Bird Assemblages 5. 3 Water Renewal Rates 5. 3.1 Choked Lagoons 5. 3.2 Restricted Lagoons 5. 3.3. Pérez-Ruzafa CONTENTS 5. 1 Introduction 5. 2 Eutrophication Process 5. 2.1 Oligotrophic State 5. 2.1.1 Submerged Vegetation and Related Energy Pathways 5. 2.1.2 Phytoplankton 5. 2.1.3 Zooplankton 5. 2.1.4. Restricted Lagoons 5. 3.3 Leaky Lagoons 5. 3.4 Water Renewal Rate and Eutrophication 5. 4 Changes in Lagoon Processes and Management of Living Resources 5. 5 Remarks References 5 L1686_C 05. fm Page 193