[Elsevier Oceanography Series] Coastal Lagoon Processes Volume 60 || Chapter 9 Aquatic Primary...

Coastal Lagoon Processes edited by B. Kjerfve (Elsevier Oceanography Series, 60) 0 1994 Elsevier Science Publishers B.V. All rights reserved 243

C h a p t e r 9

Aquatic Primary Production in Coastal Lagoons

Bastiaan Knoppers

Departmento de Geoquimica, Universidade Federal Fluminense, CEP-24.210 Niter&, RJ, Brazil

Measurements of hourly, daily and annual rates of aquatic primary production in coastal lagoons are now numerous, but the mechanisms that regulate primary production are still difficult to assess. Short term dynamics in functioning and diversity in geomorphological configuration, hydrodynamics, nutrient supply, and autotrophic populations, as well as the usage of various methods in primary production measurements, are among some reasons. Mesotrophic to eutrophic choked lagoons with depths exceeding about two meters and light limitation at the bottom are commonly phytoplankton based. In shallower choked to restricted lagoons with high nutrient loading perennial macroalgae appear in succession with phytoplankton. Restricted to leaky lagoons harbor more macrophytes and species predominance is selected by a combination of depth, tidal flushing, and nutrient loading. Nutrient budgets for coastal lagoons are still lacking, but external inorganic nitrogen loading seems to supply 5-20% and sediment release 530% of primary production demand. Regenerated production is thus high and its largest fraction is maintained by nutrient recycling in the water column. In comparison to primary production yield, approximately 10-25% of carbon is accumulated in lagoon sediments. Many tropical and sub-tropical lagoons particularly those with typical dry/wet seasons are marked by seasonal shifts between autotrophic and heterotrophic metaboli m Be olding exceptions, annual primary production ranges from 200 to 500 g C m-fyear-qand is highest in tropical choked phytoplankton based lagoons and those gover ed by macr ph es. Global coastal lagoon primary production is estimated at 10 kg C year- and is similar to the contribution by upwelling areas and by a factor of four less than estuaries where primary production per unit area is similar to that in lagoons.

A P f l

Introduction

The fixation of carbon measured as the rate of photosynthesis is called primary production and its assessment has manifold implications. It is the major source of organic matter production for the marine food web and thus represents the building block for mass balance studies in aquatic systems. It is of relevance because of the debate on the role of oceanic carbon fixation as

244 Aquatic Primary Production in Coastal Lagoons

a sink to atmospheric build-up of carbon dioxide (Sarmiento and Toggweiler, 1984; Peterson and Melillo, 1985; Platt et al., 19891, and it partially serves to assess the trophic state, the potential eutrophication, and also to some extend to predict fisheries yields of shelf waters, estuaries, and lagoons (Nixon, 1982; Welsh et al., 1982).

In the last two decades, a considerable amount of information on primary production has become available for coastal lagoons. At first sight this is not apparent because in many publications lagoons are often denominated as either estuaries, bays, and or embayments. Various reviews on nutrient behavior, primary production, and fisheries yields, and also first approaches to relate primary productivity to general physical characteristics, have been presented for tropical and temperate coastal lagoons (Qasim et al., 1969; Vannucci, 1969; Qasim, 1979; Gilmartin and Revelante, 1978; Boynton et al., 1982; Nixon, 1982; Welsh et al., 1982; Vaulot and Frisoni, 1986). However, for the majority of coastal lagoons, it is still problematic to estimate total autotrophic production because many studies have focused on single populations of primary producers. Primary production in lagoons may be dominated by either phytoplankton, benthic micro- and macroalgae, macrophytes, and in specific cases algal mats, or a combination of these populations. This imposes a n array of specialists, analytical methods, and experimental designs with measurements at numerous different spatial and temporal scales. Furthermore, the lack of ordinance of productivity measurements to relevant temporal scales of governing physical and chemical processes, poses major difficulties for the comparison of data sets of the highly diverse functioning coastal lagoons. Similar problems are encountered for neritic systems (Platt and Rao, 1975; Harris, 1980; Harris, 1986; Platt et al., 1989).

Nixon (1982) came to the conclusion, that apart from some exceptions, the annual range of total primary production for coastal lagoons lies within 200 and 400 g C m-2 year', a range comparable to the one for estuaries and medium productive coastal upwelling regions (Lieth and Whitaker, 1975; Platt and Rao, 1975). In lagoons where phytoplankton production is re- duced, production is supplemented by benthic algae and/or seagrasses. The mechanisms involved in the selection and succession of primary producers and those that control the magnitude of total primary production have as yet to be described by an integrated ecological concept (Yaiiez-Arancibia et al., 1985; Yaiiez-Arancibia, 1987) and nutrient budgets are still lacking for coastal lagoons.

The Measurement of Primary Production in Coastal Lagoons

Numerous reviews have widely covered the experimental design and analytical methods, including their advantages and drawbacks, for productivity measurements in aquatic systems (Berman and Eppley, 1974; Wil-

B. Knoppers 245

liams et al., 1979; Harris, 1980; Morris, 1980b; Gieskes and Kraay, 1984; Harris, 1986; Platt et al., 1989). However, some specific problems may arise when studying primary production in coastal lagoons. These systems may be either dominated by phytoplankton, benthic macro- and microalgae, macrophytes, or even algal mats, and, in many cases, a combination of these primary producers. Each population differs in their ecophysiological and ecological response, and as such, whatever method is applied refers to a specific spatial and temporal scale and delivers a different index in primary production (Harris, 1986; Platt et al., 1989). Henceforth, in lagoons with a high diversity in primary producers a wide array of hardly comparable techniques with an enormous effort in research has to be applied (Reyes and Merino, 1991).

In such cases, the most suitable alternative for measurements of total production is the ‘Diurnal Curve’ method which simultaneously monitors dissolved oxygen and carbon dioxide evolution in situ during 24 hour cycles. The method is of particular interest, as it enables an estimation of whole system metabolism. In spite of its early introduction in the mid 50s (Odum and Hoskin, 1958; Odum et al., 1959; Odum and Wilson, 1962; Carmouze et al., 1991; Reyes and Merino, 19911, the method has not been a popular tool. Its lack of application is probably related to the large time expenditure needed in the field and modelling of correction factors for gas exchange at the water-atmosphere interface.

In mesotrophic to eutrophic phytoplankton based coastal lagoons, standard lightidark bottle incubation techniques with measurements of the evolution of dissolved oxygen or the incorporation of isotopic carbon (W) have been most common, and additional measurements of carbon dioxide evolution have been restricted to some coastal and calcifying Atoll lagoons (Park et al., 1958; Teal and Kannwisher, 1966; Sournia, 1977; Sournia et al., 1981; Carmouze, 1985; Carmouze et al., 1991). The drawbacks of these standard incubation techniques are aggravated by the dynamic functioning of coastal lagoons. Many coastal lagoons respond in a rapid manner to short term changes in meteorological forcing, riverine cycles, tides, and temperature changes, with a marked variability in vertical mixing and lateral advection of water masses, horizontal and vertical turbidity gradients, frequent resuspension of surficial sedimentary matter, and thus also short-term changes in light regime (Okuda, 1981; Kjerfve, 1986; Lara-Lara et al., 1981; Alvarez- Borrego and Alvarez-Borrego, 1982; Knoppers and Moreira, 1988). Inter- pretation of results obtained by the incubation techniques should thus include the previous history of physical events and preferentially be grouped and weighted according to their frequency of impact.

The quality of results of the ‘4c bottle technique varies in accordance to the growth rates and diversity of phytoplankton and as such also to the trophic state of the system (Harris, 1986). For example, in oligotrophic systems where phytoplankton attains maximum growth rates and diver-


sity, gross photosynthesis is given, and in eutrophic systems with lower growth rates and diversity, net photosynthesis is measured. As many coastal lagoons are characterized by seasonal shifts from mesotrophic to eutrophic conditions and from autotrophic to heterotrophic metabolism (Sournia et al., 1981; Nixon, 1982; Vaulot and Frisoni, 1986; Machado and Knoppers, 1988; Sandoval-Rojo et al., 1988), the quality of results by this technique shifts accordingly to the seasonal cycle of events.

In mesotrophic to eutrophic lagoons, the use of the dissolved oxygen incubation technique may also pose some problems. Large diurnal temperature changes and primary production rates are often encountered in these lagoons and bring about marked variability in dissolved oxygen levels with in many cases super saturation of up to 180%. These conditions result in rapid bubble formation in the incubation bottles which might be lost upon fixation. Results thus become invalid and this process may only be counteracted by extremely short incubation times, the use of micro titration techniques, or concomitant measurements of dissolved oxygen and carbon dioxide (Parket al., 1958; Teal and Kannwisher, 1966; Sournia, 1977; Sournia et al., 1981; Carmouze, 1985).

Comparisons between lagoons by ecophysiological indices based upon the biomass index chlorophyll a, such as the assimilation ratio (PB) and the light harvesting efficiency, hold some caveats. Apart from the fact that these indices constantly change in accordance with species composition and physiological state of populations (Knoppers, 1982; Hecky and Kilham, 1988), they are biased in coastal lagoons by the frequent resuspension of surficial sedimentary matter that contain pigment degradation products. Studies have shown that functional chlorophyll a estimates by trichromatic equations may, in comparison to high pressure liquid chromatography (HPLC), bring about a substantial overestimation (Jacobsen, 1978 and 1980; Field- ing et al., 1988). In contrast, the often criticized monochromatic method by Lorenzen (1967) appears to provide a more suitable estimate for sedimentary chlorophyll (Fielding et al., 1988). The HPLC method with its wide spectrum of pigment analysis is undoubtedly most suitable for shallow coastal lagoons that present frequent resuspension of sedimentary matter, but i t remains a costly alternative to standard methods.

Primary production of macrophytobenthos may be assessed by a variety of methods, including in situ estimates of biomass increment and dissolved oxygen and carbon dioxide evolution by the ‘Diurnal Curve’ method, and lightldark incubations with a larger volume than those applied for phytoplankton. Measurements of microphytobenthos and benthic algal mat productivity necessitate some special methodological adaptations. In situ incubations with small light and dark acrylic domes with both the inclusion and exclu- sion of the sediment surface is one alternative, and controlled in uztro experiments with intact surface sediment samples obtained by box or piston corers, is the other (Zeitzschel and Davies, 1978; Asmus, 1985; Fielding et

B. Knoppers 241

al., 1988). Monitoring of parameter evolution during incubations may be conducted manually or via the use of continuous recording electrodes. However, care should be taken to avoid resuspension of matter by excessive stirring of the incubated overlying water which promotes excessive nutrient release from the bottom, the stirring rates in general, and prolonged incubation times which may alter redox conditions of the sedimenhwater interface. These methodological problems are aggravated by the presence of sedimentary organic rich flocculent layers, commonly found in coastal lagoons, and are similar to those encountered in studies of sediment oxygen consumption and nutrient release rates (Aller, 1980; H u m p and Martens, 1981; Nixon and Lee, 1981; Kemp et al., 1982; Balzer, 1984; Machado and Knoppers, 1988). An elegant experimental design has been introduced by Revsbeck and Ward (1984) with the application of micro-electrodes for the measurement of the vertical structure of physical and chemical parameters of surficial sediments. Primary productivity of both micro-phytobenthos and algal mats is assessed by continuous profiling over several diurnal cycles and with a vertical resolution ranging from microns to centimeters.

Physical Setting and the Primary Producers

Coastal lagoons may be classified based on their geomorphological and hydrological criteria into choked, restricted, and leaky systems (Kjerfve, 1986). Accordingly, the main feature which controls their physical functioning is the number and nature of entrance channels and as such tidal exchange. Examples of various types of coastal lagoons are presented in Fig. 9.1.

All types of autotrophic populations proliferate in coastal lagoons. Accord- ing to dominance of autotrophic populations, three types of lagoons may be distinguished. At one end of the spectrum lie the phytoplankton based systems with some seasonal contribution of micro- and macro phytobenthos in shallower depths and with or without anaerobic autotrophic bacteria depending upon stratification of the water column and stagnation and anoxia of bottom waters. The intermediate position holds the benthic macroalgal and macrophyte based systems, and at the other end of the spectrum the algal mat systems of hypersaline lagoons and lagoons with intertidal zones that are subject to prolonged exposure during dry seasons. Table 9.1 presents a compilation of some physiographic data, annual primary production, and corresponding dominance of primary producers, for a variety of choked, restricted, and leaky coastal lagoons.

Several approaches attempted to link the magnitude of primary production to simple physiographic and hydrological characteristics of lagoons and also estuaries. Included are studies on the dependance of phytoplankton doubling rates upon the tidal exchange ratio of estuaries (Ketchum, 1954),


on nutrient loading and primary production versus the dynamics of river run-off, tides, and winds, and estuarindagoon morphometry (Jaworski, 1981; Boynton et al., 19821, and also on the tidal and biogenic matter exchange with the adjacent sea (Nixon and Lee, 1981; Nixon, 1988). The overall concepts are still conflicting and there seems to be no simple link between a single physical factor and the magnitude of primary production and autotrophic biomass. Some advances were made by Welsh et al. (1982), who compared simple parameters such as size, the area to volume ratio, and tidal characteristics with total primary production for four estuaries and five choked to restricted lagoons of the southern New England coast, USA. Total production, benthic production, and the benthic to pelagic production ratio were only strongly correlated to the area to volume ratio, and the tidal exchange ratio was of less significance. However, the physical characteristics between the systems were highly diverse and they were pooled

42?42'w

N19'

86

N18"401

N18' 20'

4 7 ' W

PIo08' W

Fig. 9.1. Some typical lagoons of the world's continental coastline. Above, from left to right am top to bottom: choked Lagoa de Guarapina (Brazil), choked Lagune d'Ebri6 (Ivory Coast), restricted Laguna de TBnninos (Mexico), choked Laguna de Nichupte (NLS, MBxico). Opposite page, from left to right and top to bottom: restricted to leaky Biscayne Bay (USA), choked to restricted Bahia Falsa-San Quentin (MBxico), leaky Wadden Sea with its western (WWS) and eastern sections (EWS) and Yssel Meer and Ems-Dollard (Netherlands), choked Potter Pond (USA), and choked Peel-Harvey Estuary (Australia).

B. Knoppers

8 l o 5 0 ' W

249

0 2 4 6 8 1 0 -

-50' N

30O24' 25O 30"

10

PE

TABLE 9.1

Physiographic data, mean annual primary production and dominant plant communities in coastal lagoons. CHK= Choked, RES= Restricted, LKY= Leaky

Lagoon Type Area Mean ResidencePrimary Dominant (km') depth time production plant

(m) (weeks) (g c m-2 yr-'1 community

References

Tropical and Subtropical Cochin Backwaters, India Ebrie, Ivory Coast

Mukwe, Ghana Langebaana, S. Africa

Guarapina, Brazil

Patos, South Section, Brazil Cananeia, Brazil Saquarema, Brazil Cianaga Grande, Colombia Barra Navidad, Mexico Bojorguez, Mexico

Chautengo, Mexico El-Verde, Mexico Huizache Caimanero, Mexico

Mitla, Mexico Nichupte, Mexico

Terminos, Mexico Urias, Mexico

LKY 500 3.5 CHK 556 4.5

CHK 0.4 0.5 RES 35 3.0

CHK 6.5 1.0

CHK - 1.0 LKY - 2.5 CHK 23 1.0 CHK 423 1.6 CHK 5 1.5 CHK 2.5 1.7

CHK 36 1.0 CHK 0.5 1.0 CHK 128 0.8

CHK 36 2.0 CHK 50 2.2

RES 2500 3.5 CHK 11 0.6

- 14

- -

3

- 2 4

1-2 200

4-6

150

-

-

- 66

2 -

124 235

416 653

324 and 412

50 125 468 1555 242 489

248 521 453

551 183

228 620

phytoplankton Qasim et al. (1969) phytoplankton

phytoplankton Kwei (1977) macrophytes 54% microphytobenthos 26% phytoplankton phytoplankton Machado and Knoppers

Pages et al. (1981); Dufour (1984)

Fielding et al. (1988)

(1988); Moreira and Knoppars (1990)

phytoplankton Proena (1990) phytoplankton Tundisi (1969) phytoplankton Carmouze et al. (1991) phytoplankton Hernandez and Gocke (1990) phytoplankton Sandoval-Rojo et al. (1988) macrophytes, macroalgae and others phytoplankton Mee (1978); Mandelli (1981) phytoplankton, macrophytes Flores-Verdugo e t al. (1988) phytoplankton Arenas (1979); Moore and

phytoplankton Mee (1978) macrophytes, macroalgae

phytoplankton Day et al. (1982,1988) Phytoplankton

Reyes and Merino (1991)

Slinn (1984)

Merino et al. (1990) Reyes and Merino (1991)

RoblesJarero (1985)

Apalichola Bay, USA LKY 688 370

360

phytoplankton

phytoplankton macrophytes macrophytes 54% phytoplankton 46% phytoplankton phytoplankton macrophytobenthos

Eastabrook (1973); cited in P 9

Day et al. (1973) s Madden et al. (1988) 2

Nixon and Pilson (1983)

a Roman et al. (1983)

Lower Barataria Bay, USA RES 2.0 4

Biscayne Bay, USA RES

Forleague Bay, USA LKY Harrington Sound, Bermuda CHK

576 2.0 52 221-302

93 4.8

1.5 14.6

3-12 20

196439 304

Randall and Day, 1987 Bodungen et al. (1982)

Temperate Beaufort, USA LKY Pamlico River, USA RES

Newport River, USA RES South River, USA RES North River, USA RES Cape Lookout Bight, USA LKY Alewife Cove, USA CHK

4.1 230

115 200-500

phytoplankton phytoplankton

phytoplankton phytoplankton phytoplankton phytoplankton phytoplankton 47% macrophytes 40% microphytobenthos 13% macrophytes 87% microphytobenthos 6% phytoplankton 7% -

Thayer (1991,1974) Day et al. (1978); Kuenzler et al. (1978) Fisher et al. (1982) Fisher et al. (1982) Thayer (1971) Fisher et al. (1982) Welsh et al. (1982)

- 4.2

- 40

27 25

1.0 2

1.1 1.2

-

1-2 10 - - 1

119 288 70 50 348

- 0.2

Bissel Cove, USA - 0.7 4.0 1 820 Welsh et al. (1982)

Chimnteague Bay, USA RES 3 10

0.1

180 Boynton (1974) cited in Nixon (1982) Moll (1974) cited in Nixon (1982)

Flax Pond, USA CHK 1.6 419 1 macrophytes 73% phytoplankton 13% microphytobenthos 13% phytoplankton 85% macrophytobenthos 15% phytoplankton 63% macrophytes 15% microphytobenthos 22%

Great South Bay, USA RES 240 1.6 7

1-2

455 Lively et al. (1983)

Hempstead Bay, USA RES 46.5 0.5 281 Udell et al. (1969) Welsh et al. (1982)

(continued) 6: +

N VI lu

(continuatwn)

Lagoon Type Area Mean Residence Primary Dominant (km') depth time production plant

(m) (weeks) ( g ~ m - ~ y r - ' ) community

References

Long Island Sound, USA Peconic Bay, USA Potters Pond, USA

Charlestown Pond, USA

Wadden Sea, Netherlands

Ems-Dollard, Netherlands

Mediterraneau Biguglia, France Diana, France Maguio, France Thau, France Urbino, France Edku, Egypt

Mariut, Egypt

LKY 2000 12 2 RES - - - CHK 1.4 0.7 2-3

CHK 7.9 0.9 2-3

LKY 770 3.6 1-2

LKY 480 3.0 2-4

CHK 14.5 1.5 24 CHK 5.7 6.0 6.9 CHK 31.6 1.0 14.6 CHK 75 4.5 13.4 CHK 7.9 5.0 61 CHK - 1 RES CHK - 1.0 - RES

-

209

320

316

162-213

100-200

130-400

289 183 225 204 297 475

1847

phytoplankton phytoplankton macrophytes 63% phytoplankton 37% macrophytes 74% phytoplankton 13% macrophytobenthos 13% phytoplankton microphytobenthos phytoplankton

phytoplankton phytoplankton phytoplankton phytoplankton phytoplankton phytoplankton macrophytes macrophytes phytoplankton

Riley (1956) Bruno et ul. (1982) Nowicki and Nixon (1985)

Thome-Miller and Harlin (1984)

Cade and Hegeman (1974) Cad& (1980) Cad& (1986a) and Colijn et al. (1983)

b 9 E

Vaulot and Frisoni (1986) $. 3 2.

Vaulot and Frisoni (1986) a

Aleem and Samaan (1969) g.

Vaulot and Frisoni (1986) Vaulot and Frisoni (1986) Vaulot and Frisoni (1986)

Samaan (1974) z 6 J

5-

B. Knoppers 253

together irrespective of differences in the degree of predominance of autotrophic populations.

In contrast, a strong link between primary production and the flushing rate was evidenced by Vaulot and Frisoni (1986) for five mediterranean lagoons, and between the trophic state and flushing rate by Knoppers et al. (1991) for six lagoons of Brazil. All lagoons were choked, similar in morphometry and hydrodynamics, and phytoplankton based. In both cases, the flushing rate was obtained from computations of the hydrological balance. From comparative studies in several Rhode Island lagoons, Thorne-Miller et al. (1983) suggested, that the distribution and predominance of macrophytes and macroalgae is related to the degree of enclosure and as such tidal flushing. Poorly flushed choked lagoons were characterized by the macrophytes Potamogeton sp. and Ruppia sp. and filamentous green algae, and well flushed restricted lagoons by the macrophyte Zosteru sp. and unat- tached green and red algae. In these cases, salinity represents a selection factor which is ultimately related to tidal exchange.

Figure 9.2 shows a rough attempt to relate mean annual primary production to mean residence times of water and Figs. 9.3 and 9.4 primary production to depth for phytoplankton and macrophyte based lagoons, respectively. The data are compiled in Table 9.1, and information on residence times of water were estimated, considering the tidal prism and the fresh water inflow. It is obvious that comparisons should be conducted from computations of the hydrological balance, but for some exceptions, these are still lacking for coastal lagoons. Primary production of phytoplankton based

PP a20

t so0

5

x FT-200 FTA,l50

@FT-52 0 FTw61

Rrsidrna tlmr of wahr (wrrkr)

Fig. 9.2. Primary production and the residence time of water for phytoplankton based lagoons (dots) and macrophyte based lagoons (crosses). References and data sets are found in text (Table 9.1). FT = Residence time of water in weeks.

254

c

t B : E 100-

4 300-

200- t


I 1

0 \. 0 . . Zm 14.5 . a n 4 2 : b, 0 . -- - -. - - 0 , d . . * .

0:- 0 1 2 3 4 1 6

Mean depth ( f m

Fig. 9.3. Primary production and mean depth for phytoplankton based lagoons. References and data sets are found in the text (Table 9.1). PP = Primary production.

lagoons tend towards a dampened increase with the residence time of water, whereas macrophyte based lagoons tend towards high primary production with lower residence times and a linear increase with depth in lagoons without light limitation at the bottom. The large scatter of the data probably reflect the rudimentary estimations of the residence times of water, incom- plete descriptions of the physical setting of the lagoons in works on primary production, measurements of primary production by different methods and sampling frequencies, and differences in the ecophysiological and ecological response of the populations.

Similar comparisons for lagoons dominated by macroalgae are as yet unfeasible, because estimates of their annual primary production have been scant. However, the occurrence of macroalgae is consistent in shallow choked to restricted lagoons with substantial cultural nutrient loading, such as Venice Lagoon, Italy (Sfriso et al., 19871, the NichuptB Lagoon System, Cancun, MBxico (Merino et al., 1990; Reyes and Merino, 19911, Piratininga Lagoon, Brazil (Knoppers et al., 19911, and the Peel-Harvey, Australia (Hodgkin and Birch, 1982). Algal mats prevail in hypersaline lagoons, or in those characterized by large intertidal flats subject to prolonged exposure, such as Shark Bay and Spencer Gulf, Australia (Bauld et al., 1980; Bauld, 1984), Guerrero Negro and Ojo de Liebre lagoons, Mexico (Javor and Catenholz, 19841, and the Long Island Sound flats, USA (Burk- holder et al., 19651.

B. Knoppers 255

(Q PPl847)

I200

yean dep(h(Zm)

Fig. 9.4. Primary production and mean depth for macrophyte based lagoons. References and data sets are found in text (Table 9.1). PP = Primary production.

In many tropical and sub-tropical choked lagoons subject to marked dry/wet seasons, closure and rupture of the tidal inlet, resulting from changes in river flow, is a major factor regulating levels of primary production and succession of autotrophic populations. Yaiiez-Arancibia et al. (1985) sum- marized the sequence of physical+cological events for these types of lagoons (Fig. 9.51, which are often encountered along the Pacific coast of MBxico and western Australia (Mee, 1978; Hodgkin and Birch, 1981; Mandelli, 1981; Flores-Verdugo et al., 1988; Sandoval-Rojo et al., 1988). Conditions may vary between mesohaline to hypersaline, mesotrophic to eutrophic, and nutrient and light limitation. River flow may, depending on its time scale of impact, either enhance photosynthesis by nutrient input or suppress by light limitation due to an increase in turbidity (Randall and Day, 1987).

In choked multiple basin lagoons with a single access to the sea at its exterior basin (Lankford, 1976; Kjerfve, 1986), spatial variability in functioning is a marked feature. Depending on the geomorphological configuration of the basins, the width of interconnecting channels and depth of sills between individual basins, differences in salinity, residence times of water, structure of the water column (i.e homogeneous or stratified), light and nutrient limitation, and primary production levels and species assemblages, are encountered (Mee, 1978; Nixon, 1982; Thorne-Miller et al., 1983; Dufour, 1984; Knoppers et al., 1984; Carmouze and Caumette, 1985; Ode- brecht, 1988; Reyes and Merino, 1991).


i I

2.5-

y. i !

i

2.4.

S I5 A 34PPM S > 35 PPM S 4 I I PPM E > P * R + F E+F< P * R

R

A S 0 N D E F M A M J J A m

Fig. 9.5. A conceptual model of seasonal stages ofthe hydrological cycle, nutnents, and primary production for tropical to sub-tropical lagoons with typical drybet seasons of the Pacific Coast of Mexico. S = Salinity, P = precipitation, E = evaporation, R = river Mow, F = flux of water by percolation through the sand barrier, T = tidal exchange, F" = orthophosphate, N = total inorganic nitrogen, Prim.Prod. = primary production. Adapted from YAiiez-Arancibia et al . (1985).

Nutrient Sources and Sinks

Information on the short temporal and seasonal behavior of nutrients has been reviewed by Nixon (1982), estimations of external nutrient supply, internal recycling, and accumulation are relatively scant, and complete nutrient budgets are non-existent for coastal lagoons.

Nutrients are imported to coastal lagoons via the atmosphere, rivers, direct land run-off, groundwater seepage, and the sea, and exported via tidal exchange, sediment accumulation, and denitrification. An additional source is nitrogen fixation by certain species of cyanobacteria, which can counteract some of the loss by denitrification. Internal sources are pelagic and benthic nutrient regeneration.

The relative importance of a nutrient source varies considerably between lagoons. Choked coastal lagoons with well developed drainage basins in the humid tropics and temperate regions receive their major external nutrient supply from rivers, the remaining outside sources may play a secondary role (Jaworski, 1981; Mandelli, 1981; Boynton et al., 1982). Examples of such lagoons are the Peel-Harvey estuary, Western Australia (McComb et al., 19811, Guarapina Lagoon, Brazil (Moreira and Knoppers, 19901, Ebrie Lagoon, Ivory Coast (Dufour, 1984), and the Backwaters of Cochin, India (Qasim, 1979). In restricted to leaky lagoons such as along some sections of

B. Knoppers 257

the eastern coast of USA (Thayer, 1974; Fisher et al., 1982; Roman et al., 1983; Nixon and Pilson, 1983) and the northern European coast (Cadee, 1986a; Baretta and Ruardij, 1988), riverine and marine sources are both of importance. In contrast, choked, restricted, and leaky lagoons of arid regions as found along the Pacific coast of MBxico (Gilmartin and Relevante, 1978), and southwestern Australia (Hodgkin and Lenanton, 19811, the major fraction of new nutrients is supplied by the sea and the atmosphere. Of particular interest are those lagoons that lie in regions of coastal upwelling. A well studied example is San Quentin Bay, MBxico, (Lara-Lara et al., 1980; Farfan and Alvarez-Borrego, 1983), which receives new nutrients during intrusion of upwelled water.

Nutrient Supply by Atmosphere and Groundwater

In general, little is known on the supply of nutrients by the atmosphere and groundwater seepage to coastal lagoons. Direct estimates of atmospheric input have been made for some estuaries and lagoons, but input is so variable making generalizations unfeasible. Nitrogen input from the atmosphere compared to total nitrogen supply from other sources to the Rhode Island Ponds and also Buttermilk Bay, USA, range between 4 and 9% (Nixon and Pilson, 1983; Lee and Olsen, 1985; Valiella and Costa, 1988). In regions subject to acid rain deposition, nutrient input is expected to be higher.

Lee (1977) studied groundwater seepage velocities at Beaufort, North Carolina, and observed a decrease with distance from shore and an inverse trend with water elevation. Changes in pore water conductivity and hydrau- lic pressure have been shown to be responsible for variability in seepage velocities in Great South Bay, New York (Bokuniewicz, 1980). In some lagoons such as TBrminos lagoon, Mdxico (Stevenson et al., 1988), some of the Rhode Island ponds, Massachusetts (Lee and Olsen, 1985), and Butter- milk Bay (Valiela and Costa, 19881, water seepage supplies a considerable fraction of nutrients, and may surpass stream and direct run-off input. However, this large contribution is also due to groundwater contamination by domestic discharge. In Potters Pond, Rhode Island, low inorganic phosphate and high N/P ratios in the water column are influenced by a high input of nitrate and low phosphate from groundwater (Nowicki and Nixon, 1985).

Riverine Input

Some examples of total areal inorganic nitrogen loading and its percentage contribution to the demand of primary production are presented in Table 9.2. In cases where information is available, the contribution by the atmosphere, groundwater seepage, and tidal exchange are included in the

TABLE 9.2 Dissolved inorganic nitrogen (DIN) load, nitrogen demand by primary production and percentage supply to demand of primary production in coastal lagoons. Major external DIN sources a re given as: R = river, S = sewage, P = precipitation, M = marine, GW = ground water. Asterisk (*) refers t o a mean value obtained from a given range in the literature.

Lagoons Main DINload Demand by primary Demand References sources (mmol N m-' yr production supplied

(mol N m-' year-') (%)

Harrington Sound, Bermuda Charlestown Pond, USA

Ninigret Pond, USA

Potter Pond, USA

Pamlico Sound, USA Long Island Sound, USA Apalichola Bay, USA Barataria Bay, USA Laguna de Terminos, Mexico Lagoa Guarapina, Brazil

Lagoa Urussanga, Brazil Lagoa Fora, Brazil

Lagune Mauguio, France Lagune Thau, France Ems-Dollard, Netherlands Lagune d'Ebri, Ivory Coast

136 561

340

7 10

860 400 560 570 20 313

26 156

291 582 414 410

3.86 3.12

2.98

3.18

4.41* 2.58 4.53 4.53 2.87 5.18

5.89 5.73

2.57 2.84 3.77* 2.97

4 18

11

22

20 15 12 12 1 6

<1 3

11 20 11 14

~

Bodungen et al. (1982) Nowicki and Nixon (1985); Lee and Olsen (1985) Nixon and Pilson (1985); Thorne-Miller et al. (1983) Lee and Olsen (1985); Thorne-Miller et al. (1983) Davies et al. (1978); Nixon and Pilson (1983) Nixon and Pilson (1983); Riley (1959) Nixon and Pilson (1983) Day et al. (1978); Nixon and Pilson (1983) Day et al. (1988); Stevenson et al. (1988) Moreira and Knoppers (1990); Knoppers et al. (1990) Costa-Moreira (1989); Carmouze et al. (1991) Carmouze et al. (1991); Knoppers et al. (1991) Vaulot and Frisoni (1986) Vaulot and Frisoni (1986;) Baretta and Ruardij (1988); Cad& (1980) Dufour and Slephoukha (1981); Dufour (1984)

B. Knoppers 259

overall computations of nitrogen areal loading. The data show, that apart from few exceptions where cultural eutrophication is marked, fresh water nitrogen supplies between 5 and 20% of the areal primary production demand. Considering that most of the examples are from humid regions, the overall areal nitrogen loading in relation to primary production demand is lower than expected. However, dissolved and particulate organic matter, after its oxidation, may in comparison, also be a substantial source of new nutrients (Smith and Mackenzie, 1987), but its contribution to coastal lagoons demands more studies. It follows, that the major nutrient fraction which sustains primary production in coastal lagoons comes from the autochthonous decomposition of organic matter.

Autochthonous Supply

Lagoon studies on sediment nutrient release to the water column are not always complemented with studies on primary production. A compilation of sediment release rates of total inorganic nitrogen and orthophosphate and their percentage contribution to the demand of primary production is given in Table 9.3. Although data are scarce, total inorganic nitrogen supply seems to sustain 10-30% of primary production demand and orthophosphate 3-30%. Beholding some exceptions, such as Forleague Bay, Colorado Lagoon and Guarapina Lagoon, N:P release ratios agree fairly well with the demand according to the Redfield ratio of phytoplankton (Table 9.3). The contribution by the dissolved organic fraction has been noted to be of significant importance in shallow water sediments (Nixon et al., 1976; Teague et al., 1988).

Reports on pelagic nutrient remineralization and its contribution for the sustenance of regenerated production are almost absent for coastal lagoons. Only indirect estimates can be computed. Considering that 5-20% of primary production is supported by external inorganic nitrogen sources (Table 9.2) and 10-30% by sediment release (Table 9.31, the largest fraction must be supplied by remineralization in the water column or supplemented in some cases by nitrogen fixation and it seems that this is a major feature characterizing coastal lagoons.

Nitrogen Fixation

The only lagoon for which both data on planktonic nitrogen fixation and freshwater nitrogen input is available, is the Peel-Harvey, Australia. Nitro- gen fixation by the Cyanobacterium Nodularia spumigena amounted to 17% of total nitrogen input to the lagoon (Huber, 1986). Although eutrophic lagoons often have cyanobacteria, few measurements on nitrogen fixation

N

0 m TABLE 9.3

Sediment release rates of dissolved inorganic phosphate (DIP) and nitrogen (DIN) and their contribution to the demand by primary production in some lagoons. Values of Forleague Bay include the dissolved organic fraction.

Lagoon DIP DIN Primary production demand References (pmol m-' d-') (mmol m-' d-') supplied in %O by

DIP DIN

Potter Pond, USA Long Island Sound, USA

South River, USA Neuse River, USA

Forleague Bay, USA (upper)

Forleague Bay, USA (lower)

Colorado Lagoon, USA Hamngton Sound, Bermuda

Guarapina, Brazil

Kanehoe Bay, USA

Maribago Reef, Phillipines

Bowling Green Bay, Aust.

16.7

38-120

150

340

408

720

548

88

175

12

23-63

-23-28

1.23

0.46-1.50

2.71

5.38

-13.3

13.0

4.66

2.11

0.98

1.18 -

4.15-0.9

4

8-27

24

31

156

106

13

25

3 -

14

7-2 1

27

31

120

-

20

9

21 -

Nowicki and Nixon (1985)

Aller (1980b)

Fisher et al. (1982b)

Fisher et al. (1982b)

Randall and Day (1987); Teague et

Randall and Day (1987); Teague et al. (1988)

al. (1988) b

8

Murphy and Kremer (1985) T

9

c.

Bodungen et al. (1982) 2. Machado,l989; Machado and 4

z Knoppers (1988)

E Smith (1979) g.

Balzer et al. (1985)

Ullman and Sandstroem (1987) 5. 3

B. Knoppers 261

and observations on species having heterocysts have been reported. The fact that nitrogenase activity has been detected in Oscillatoria species lacking heterocysts (Mee et al., 1984) and for other picoplanktonic cyanobacteria, suggest significant phytoplankton nitrogen fixation in coastal lagoons.

A review by Howarth et al. (1988) demonstrates, that nitrogen fixation in seagrass beds and phytoplankton and algal mat based lagoons (Bautista and Pearl, 1985) attain significant rates rangingfrom 0.1 to 5 mol m-2year1. Nitrogen fixation by heterotrophic bacteria is considerable at seagrass rhizospheres and in organic rich sediments with or without macrophytes and by autotrophic heterocyst cyanobacteria under more stable physical conditions with low turbulence and mixing, stratified water columns, and on surficial sediments (Carr and Whitton, 1982). There is evidence, that nitrogen fixation by epiphytes may supplement nitrogen to seagrasses during inorganic nitrogen depletion in El Verde Lagoon, M6xico (Flores- Verdugo et al., 1988).

Nutrient Loss by Denitrification

Denitrification rates of surficial sediments in estuarine and coastal waters may attain 50-250 pmol N m-2 h-l and molecular nitrogen fluxes may yield 15-70% of total nitrogen flux. The loss of nitrogen via denitrification may exceed input via nitrogen fixation in various systems and seems to be highest in sediments of eutrophic waters (Seitzinger, 1988). The major source is nitrate from nitrification in sediments but nitrate may also be made available from ground water seepage. Denitrification is a major process responsible for nitrogen limitation in estuaries and coastal waters, and as such probably also in coastal lagoons. In lagoons with considerable nitrogen fixation, nitrogen loss by denitrification could to a certain extend be counteracted.

Nutrient Loss by Accumulation in Sediments

The process of accumulation of matter in coastal lagoons deserves some special attention as it not only represents a considerable loss of biogenic elements from the pelagic benthic cycle but also the mechanism that de- scribes the role of coastal lagoons as efficient traps in the transfer of matter between land and sea. A variety of factors make a comparison of accumulation rates between coastal lagoons problematic. The computation is conducted by quantification of changes in the sedimentary record of bulk properties as a function of the time of impact of natural or catastrophic events andor the sedimentary record of various radioisotopes such as 137Cs, 21Tb, and W, and necessitates information on sediment composition, density, and porosity (Lerman, 1988). Large spatial variations in sedimentation rates and sediment composition, and sediment resuspension by tidal ex-


change and winds, and bioturbation, bring about many caveats in computations (Benninger et al., 1979; Aller, 1980; Sharma et al., 1986). Furthermore, in cases where computations of accumulation rates are feasible, comple- mentary data on primary production are usually lacking.

The data compiled in Table 9.4 have to be considered as a tentative approach to elucidate the relationship between primary production and accumulation of carbon in some coastal lagoons. The element carbon has been chosen instead of nitrogen as a reference, because it is the more accessible in the literature. Data on accumulation rates in Table 9.4 were either taken directly from the literature or from own computations. For Venice Lagoon, references on total annual primary production are not available, except for the work on phytoplankton production by Vatova (1969) and on the seasonal dry weight cycle of macroalgae by Sfriso et al. (1987). In contrast, Barataria Bay estimates of both accumulation rates and primary production represent a rough mean because of the large spatial variation of both processes. It seems that carbon accumulation rates attain

TABLE 9.4

Sedimentation, carbon accumulation, and primary production rates in some lagoons. Refer- ences are for data on sedimentation rates and in some cases carbon accumulation rates. References for primary production see Table 9.1. Range of data demonstrate the spatial variation in the systems.

Lagoon Sedimentation Accumulation Primary Accumulation to References rate rate production primary (cm yr-I) (g C m-' yr-') (g C m-2 yr-') production ratio

Barataria Bay, USA Long Island Sound, USA Guarapina, Brazil

Venice, Italy

Marsdiep, Wadden Sea Ems, Wadden Sea Kiel Bight, Germany Narragansett Bay, USA

0.7-1.3

0.3 0.2-0.6

0.1-0.3

0.3-0.7

0.9-1.1

0.1-0.3

0.15

mean 170

mean 26

30-90

8-47

34

80-100

7-55

6-14

360

209

324

147

150

300

158

3 10

0.47

0.12

0.09-0.27

0.05-0.32

0.22

0.26-0.33

0.04-0.34

0.02-0.05

Hatton et al. (1982)

Berner (1978); in Aller (1980) Patchineelam et al. (1988); Barros (1986) Donazollo et al. (1982); Pavoni et al . (1987) Cadee (1978, 1980)

Cade6 (1980, 1986)

Balzer et al. (1986)

Nixon and Pilson (1983)

B. Knoppers 263

a range between 10 and 25% of primary production and burial rates tend to increase with primary production. Autochthonous produced matter represents in many cases the principle source for accumulation as reflected by some examples on the total organic carbon isotopic (l2P3C ratio) composition of surface sediments for some lagoons (Table 9.5).

TABLE 9.5 Total organic carbon isotopic ('%/13C) composition in surficial sediments of some lagoons. PPL = Phytoplankton; MAP = Macrophytobenthos.

Lagoon S'3C%~ of Sediment Source Material References

Alvarado, Mexico -21.8 Carmen y Machona, Mexico -23.0 to -29.2

Madre, Mexico -21.1 to-23.9

Tamiahua, Mexico -20.5

Terminos, Mexico -19.0 to -22.5

Lower Barataria Bay, USA -22.7

Barataria Bay, USA -13.3 to -26.3

Narragansett Bay, USA -21.7

Guarapina, Brazil -19.1 to 20.3

PPL MAP Sewage PPL Mangrove PPL PPL PPL MAP C3 ta C4 plants PPL PPL

Botello and Macko (1982)





DeLaune and Lindau (1987)

DeLaune and Lindau (1987)

Gearing et al. (1984)

Erlenkeuser and Knoppers (unpublished data)

New Versus Regenerated Production

New nutrients introduced to the system from external sources sustain the fraction of new primary production (PneW) of total primary production (PJ and nutrients supplied by internal cycling maintain the fraction of regenerated production, i.e Preg (Dugdale and Goering, 1969, Eppley and Peterson, 1979; Platt et al., 1989). The contribution of new production to total production is described by the f ratio which attains values of 0.14 for oceans, 0.2 for upwelling areas, and 0.17 for coastal zones in general. Platt et al. (19891, indicated that the f ratio for the latter two systems is still too low. Within the general context of the coastal zone, organic matter after its oxidation, may be the major source supplying new nutrients (Smith and Mackenzie, 1987). If this is the case, the fresh water inorganic nitrogen supply which satisfies 5-20% of areal primary production in coastal lagoons (Table 9.21, is too low a range to estimate an f ratio for coastal lagoons. More information on the contribution by nitrogen fmation, precipitation, groundwater seepage, etc., is needed. Assuming that the range for carbon accumulation is within


10-25% of primary production for some lagoons and primarily originates from autochthonous production (Tables 9.4 and 9.5) a n f ratio could be suggested. A further alternative to estimate P,,, could be based upon the external phosphorus supply instead of nitrogen, as suggested by Smith (1988) for open ocean atolls and reef lagoons. However, many coastal lagoons are subject to cultural eutrophication with excessive phosphorous loading in relation to nitrogen, and as such are being driven towards nitrogen limitation.

Autotrophic Versus Heterotrophic Metabolism

Smith (1988) detected a trend towards a balance between autotrophism and heterotrophism for tropical reef and open ocean atoll lagoons. A similar trend for coastal lagoons in general has as yet not been reported, although lagoons are either balanced or tend towards slight heterotrophism. Reyes and Merino (1991) presented a compilation of ten lagoons studied by the ‘Diurnal Curve’ method containing primary producers ranging from phytoplankton, benthic macroalgae, to macrophytes. With the exception of some lagoons dominated by Thalassia spp. flats, the majority were, on a n annual basis, balanced to slightly autotrophic. Other observations were obtained for various lagoons of the Mexican coast such as Chautengo (Mee, 19781, T6rminos (Day et al., 19821, El Verde (Flores-Verdugo, 19851, Estero de Urias (Robles-Jarero, 19851, and Barra de Navidad (Sandoval-Rojo et al., 1988), in Colombia for La Cienaga Grande de Santa Marta (Hernandez and Gocke, 19901, and of the southeastern Brazilian coast for Saquarema (Car- mouze et d . , 1991). Some presented a balanced metabolism others slight autotrophism or heterotrophism.

It is the seasonal shift between autotrophic and heterotrophic metabolism that characterizes many coastal lagoons. This becomes particularly evident in choked lagoons of the tropical and sub-tropical zones. High peaks of respiration have been reported during the dry seasons and attributed to the accumulation of organic material during the wet season (Sandoval-Rojo et al., 1988; Hernandez and Gocke, 1990; Carmouze et al., 1991), and dystro- phy accompanied by mass mortality of algae and also fish kills may, at some stage of the seasonal cycle, be a characteristic interannual reoccurring event (Bouti6re et al., 1982; Hodgkin and Birch, 1986).

Case Studies on Primary Production

It was the intention in the preceding sections to present some mechanisms responsible for primary production control. Some links have been established and it has become obvious that although budgetary assertions are useful as a subsidy to establish a n overall ecological concept for lagoons, they are at present limited by information. The drive to maintain a holistic

B. Knoppers 265

approach to coastal lagoons is often confronted by reductionism because each lagoon is, in spite of regional commonalities, rather specific in its functioning and human impact. In order to demonstrate their high diversity, some exemplary case studies are presented in accordance to geographi- cal location, geomorphological configuration, predominance of autotrophic populations, and particularly the history of human impact.

Phytoplankton Based Lagoons

Typical examples of phytoplankton based lagoons are numerous (Table 9.1). They may harbor other primary producers during some stage of the annual cycle, but their contribution to total areal production is insignificant in comparison to phytoplankton. Tropical and subtropical choked lagoons with a dampened seasonality in precipitation usually present a unimodel pattern in primary production with highest rates in late summer (Nixon, 1982), others with marked dry/wet seasons a uni- to bimodal pattern (Yaiiez-Arancibia et al., 1985, Fig. 9.5), and temperate choked to leaky lagoons a bimodal pattern with light limited production in winter (Nixon, 1982, Cade6 and Hegeman, 1977).

A Choked Lagoon: Lagoa de Guarapina, Brazil

Guarapina lagoon is an example of a typical small sub-tropical shallow choked mesohaline eutrophic phytoplankton based lagoon (Fig. 9.1, Table 9.1) with a humid climate (Kjerfve et al., 1990). It lies approximately 50 km east of the city of Rio de Janeiro, and eutrophication is quasi-natural (Knoppers et al., 1990).

Annual phytoplankton primary production (W technique) amounts to 412 g C m-2 year ' and net primary production (oxygen technique) to 324 g C m-2 year', and follows a typical unimodal pattern with highest rates in summer and autumn and lowest in winter and spring (Fig. 9.6, Machado and Knoppers, 1988; Moreira and Knoppers, 1990). Phytoplankton succession is a marked feature with dinoflagellates (Gyrnnodiurn sp. and Proro- centrum minimum) during winter and cyanobacteria (Oscillatoria minima and Synecochoccus sp.) in summer. Minor banks of the macroalga Clado- phora uagabunda proliferate sporadically between winter and the end of summer. Pelagic remineralization accounts for the largest nutrient source and probably also nitrogen fixation for the sustenance of the summer biomass increment by cyanophytes. The Tripton carbon to phytoplankton carbon ratio (TC:PPC ratio) is 3:l during winter-spring and reverses in summer-autumn suggesting that suspended detritus is a n important stock for autochthonous nutrient remineralization in early summer (Knoppers and Moreira, 1990). An elevation of the trophic state of the lagoon is being counteracted by control of tidal exchange through periodic dredging of the


I60

4 200. \ A, '4 \

O A ' S ' O ' N ' D ' J ' F ' Y ' A ' M ' J ' J

1988 1988

Fig. 9.6. Annual cycle of primary production (dots) and chlorophyll a (crosses) in the subtropical choked Lagoa de Guarapina (Brazil). Modified from Moreira and Knoppers (1990).

tidal inlet, open since 1951. Sediment profiles on the composition of isotopic carbon ('2C/l3c) suggest, that prior to the permanent breach of the tidal inlet, a higher fraction of land derived plant material accumulated in the lagoon.

A Choked Multiple Basin Lagoon: Ebrib, Ivory Coast, Africa

Ebri6 Lagoon is a typical example of an elongated mesotrophic to eutrophic multiple basin choked phytoplankton based system, with a single outlet to the sea (Fig. 9.1). The lagoon is marked by a large regional gradient in precipitation, freshwater and nutrient inflow, salinity, residence times of water, nitrogen to phosphorous limitation, primary production, phytoplankton species assemblages, and anthropogenic impact. Nutrient loading via domestic discharge from Abidjan is extensive (Dufour and Slepoukha, 1981; Dufour, 1982). P limitation occurs in the areas bordered by forests, minor N limitation in the Savannah bordered areas, and clear N limitation in the estuarine-oceanic part.

The mean net phytoplanktonic production amounts to 235 g C m-2 yea r ' (Dufour, personal communication) and highest primary production rates and phytoplankton biomass were observed during the wetter periods (Fig. 9.7). Diatoms and Cyanophytes are the main populations. As the major section of the lagoon is mesotrophic to eutrophic, primary production is often light limited in the central deeper areas which are characterized by sporadic stratification and anoxia (Pages et al., 1981; Carmouze and Caumette, 1985). Cyanophytes may proliferate upon the halocline and filter out nutrients supplied from below. Species composition and the structure of the food web exhibit marked spatial variability, with 80% of the phytoplankton biomass being consumed by herbivores in the interior sections, and 25% in the exterior parts (Dufour, personal communication). The exterior section is subject to severe cultural eutrophication, but dilution effects by tidal exchange have managed to prolong an elevation of the trophic state. The lagoon is slightly autotrophic.

B. Knoppers 267

" J F M A M J d t M S O N D

Fig. 9.7. Annual cycle of primary production in the tropical choked Lagune d'Ebrie (Ivory Coast). Polluted area is situated close to Abidjan City and the rural area refers to a central section of the lagoon. Adapted from Pages et al. (1981) and Dufour and Slephoukha (1982).

A Restricted Lagoon: Laguna de Te'rminos, Mbxico

Over the last two decades Laguna de TBrminos has been subject to intensive ecological research (Yaiiez-Arancibia and Day, 1988). It is the largest restricted Mexican lagoon and it is connected to the Gulf of MBxico by two tidal inlets (Fig. 9.1). The system is polyhaline, its tropical humid climate is characterized by typical dry/wet seasons, and turbidity due to resuspension of matter is relatively high.

Mangrove swamps fringe the lagoon and the north and southeastern sections of the littoral zone harbor seagrass beds dominated by Thalassia testudinum, and also Syringodium filiforme and Halodule haubertii. Pro- ductivity of the Thalassia beds is highest during the spring dry season (Moore and Wetzel, 1988). Their growth is light limited below approximately 1 m depth, which explains its lack of further proliferation towards the deeper sections of the lagoon (Kemp et al., 1988). The primary production on a per unit area basis is approximately 4% of phytoplankton primary production which attains 219 g C m-2 year ' (Day et al., 1982; Moore and Wetzel, 1988). Phytoplankton primary production rates are higher in nearshore waters close to seagrass beds, mangroves, and river mouths, as a consequence of stimulatory effects by higher nutrient levels and humic substances (Day et al., 1982; Hopkinson et al., 988). Seasonal variability in primary production is inversely related to nutrient N:P ratios, with highest rates during the wet season and lowest in the dry season (Botello and Mandelli, 1975; Day et al., 1988). The lagoon seems to tend towards slight heterotrophism in shallow areas, but in all, presents a balanced metabolism. Cultural eutrophication is at its onset, but is minimized by tidal exchange and the large volume of the lagoon.


A Leaky Lagoon: The Wadden Sea, Netherlands

The Dutch Wadden Sea forms part of the European Wadden Sea which extends over approximately 600 km along the Dutch, German, and Danish coasts. It is a n example of a temperate shallow leaky tidal flat lagoon consisting of a series of tidal basins protected by a string of barrier islands from the North Sea (Fig. 9.1). The most impacted areas are the Marsdiep in the west, separated from the Ijsselmeer by a large dam in 1932, and the Ems-Dollard in the east, subject to cultural eutrophication by nutrient loading from agricultural and domestic run-off via the Ems river. Monitor- ing of phytoplankton and benthic microflora production, carbon dynamics and ecological modelling has been extensive (CadBe and Hegeman, 1974 and 1977; Cadee, l980,1984,1986a, 198613,1986~; Dankers et al., 1984; Postma, 1985; Vosjan, 1987; Baretta and Ruardij, 1988).

The water column of the lagoon is constantly mixed, shallow sediments are frequently resuspended by mesoscale tidal action, and primary production is limited by light due to turbidity in deeper sections and during winter. The mean annual range of phytoplankton primary production, established over a period of twelve years in Marsdiep and the central section, varies from 145 to 200 g C m-2 year ' and in the Ems-Dollard from 200 to 300 g C

-2 - I 1.8- 0C.m.d

ID- b

Q8Q 0 J F M A Y J J A S O N D

Fig. 9.8. Annual cycles of primary production of (a) phytoplankton and (b) microphytobenthos in the temperate leaky Western Dutch Wadden Sea. On an areal basis, phytoplankton primary production is the main component of total production. Adapted from Cadee and Hegeman (1977) and Cadee (1980).

B. Knoppers 269

m-2year-l. In the inner mud flat regions microphytobenthos accounts for an interannual range between 58 and 177 g C m-2 yea+ (Cadbe, 1980). The contribution of macrophytes by Zostera spp. is negligibly small with 5-26 g C m-2 year ' (Goedheer, 1977; in Cadbe, 1980). The seasonal cycle of phytoplankton primary production differs considerably from microphytobenthos (Fig. 9.8). The former tends towards a bimodal pattern with a spring and autumn bloom and several intermediate minor blooms during summer, whereas the latter follows a unimodal pattern with its peak in summer. In spring diatoms bloom, followed by predominance of the flagellate Phaeocys- tis pouchetii, and flagellates and diatoms alternate towards winter. Inter- annual seasonal patterns and spring bloom species composition vary to a great extend as a function of changes in the spring onset of favorable light conditions and water column stability (Cadke, 1986). The menace of cultural eutrophication in both the Wadden sea and the North Sea is now of large debate by recent occurrences of the Haptophycea species Phaeocystis sp. and Chrysochromulina sp. with mass blooms causing nuisance effects for the tourist and mussel industry.

Macrophyte Based Lagoons

Macrophyte based lagoons have been well studied (Table 9.1). In many cases, macroalgae are entangled with macrophytes during a period of the seasonal cycle, posing problems in estimating total primary production. Epiphytic communities often thrive upon the macrophytes and may be an important component of primary production.

Choked Lagoons: The Rhode Island Salt Ponds, USA

The Rhode Island salt ponds, northeastern USA (Fig. 9.1, Table 9.11, include Charlestown-Ninigret-Green Hill, Trustom, Potter, and Point Ju- dith Ponds and are examples of temperate shallow choked to restricted polyhaline lagoons (Lee and Olsen, 1985). The dominating freshwater nutrient source is given by groundwater seepage to all ponds.

The larger ponds exhibit an average annual primary production of around 300 g C m-2 year ' with seagrasses, mainly Zostera spp., accounting for an average of 50%, macro- and microalgae 40%, and phytoplankton 10% of total production. The ponds marked by larger tidal exchange, such as Ninigret and Point Judith, are predominated by Zostera sp. banks and entangled macroalgae and the more closed ponds including Green Hill and Trustom, by Ruppia sp. and Potamogeton spp. and various filamentous macroalgal banks. The seagrasses follow a typical unimodal seasonal pattern in biomass development in contrast to the more dampened mode of the macroalgae, as reflected by an example for Ninigret Pond (Fig. 9.9). In this pond, a


Fig. 9.9. Annual biomass cycle of the macrophyte Zosteru marina and macroalgae in the temperate choked Ninigret Pond (USA). Adapted from Thorne-Miller et al. (1983).

sequence of changes occurred since its permanent opening in the fifties. Previously, macrophyte species of Potamogeton sp. and Ruppia sp. were predominant thereafter, gradual replacement by Zostera sp. occurred. It is postulated that Zostera sp. growth was favored by light availability from an increase in transparency, by higher salinity, and enhanced nutrient exchange from intensive lateral advection of water (Thorne-Miller et al., 1983; Thorne-Miller and Harlin, 1984). A shift from Chlorophytes to Rhodophytes was also observed as marine influence augmented. Cultural eutrophication seems to have promoted macroalgae, but the impact by breachway opening, as manifested in changes of residence times of water and salinity, remains the more obvious reason for species composition changes and maintenance of macrophytes (Lee and Olsen, 1985).

A Choked Lagoon: Nichupte-Bojorguez Lagoon, Cancun, Mkxico

Nichupte-Bojorguez lagoon (Fig. 9.11, Cancun, Yucatan Peninsula, Mexico, is a multiple basin choked system with a sub-humid climate (Merino et al., 1990). In its natural state, it was dominated by a Thalassia testudinum community and oligotrophic waters (J6rdan et al., 1978) but, over the last two decades, cultural eutrophication has particularly affected the subsys- tem of Bojorguez. Spatial variation in sewage discharge has promoted community diversity and gradual substitution of the Thalassia sp. beds. Ruppia maritima-Halodule wrightii epiphyte communities thrive close to sewage discharge areas, Lyngbia sp. and Oscillatoria sp. cyanophytic algae are distributed in deeper areas over organic rich sediments, and Thalassia testudinum is found in less affected regions (Reyes and Merino, 1991). Macroalgae of the genus Chaetomorpha and Acetabularia also proliferate in

B. Knoppers 271

the lagoon. Despite cultural eutrophication, annual mean autotrophic and heterotrophic metabolism is still balanced for the entire lagoon (Reyes and Merino, 1991). The Ruppia-Halodule community is predominantly autotrophic, and the benthic algae and seagrass beds shift seasonally between autotrophic and heterotrophic metabolism.

Macroalgal-based Lagoons

Macroalgal-based lagoons have received little attention. Some well studied examples are the Peel-Harvey, western Australia (Hodgkin and Lenan- ton, 1981), Venice Lagoon, Italy (Sfriso et al., 19871, and also Lakes Edku, Mariut, and Menzalah, Egypt (Aleem and Samaan, 19691, which also harbor macrophytes. However, reports on lagoons with macroalgae as the sole primary producer are absent, because the majority of dominant species are perennial. The functioning of algal banks resembles phytoplankton based systems with stratified water columns and algal mats, the only difference being the magnitude of vertical scale. Algal banks are characterized by marked vertical gradients of physical and chemical properties at a decime- ter to centimeter scale. The top layer is oxic and represents the site of primary production and consecutive lower layers become more oxygen depleted and are sites of remineralization of matter produced at the top. The vertical density structure is usually induced by temperature as a consequence of light attenuation by the dense algal top layer. Primary production is to a large extend driven by internal recycling of nutrients which are transported to the surface by diffusion, sporadic lateral advection, and activity of micro- and macrofauna.

A Choked Lagoon: The Peel-Harvey, Western Australia

The Peel-Harvey system consists of two interconnected basins and a single tidal channel to the sea (Fig. 9.1). It is subject to a subtropical dry/wet climate (Hodgkin and Birch, 1982).

Since the sixties, severe cultural eutrophication, in the form of excessive nutrient loading (especially phosphorus) from fertilizer usage in the drainage basins, induced a sequence of changes of the local flora and fauna. Initially, this was manifested by massive nuisance growth of the benthic macroalgae Cladophoru spp. which dominated the picture for several years. Thereafter, faster decomposing species such as Chaetomorpha spp., Entero- morpha spp., and Ulua spp. emerged, and lately continuous excessive blooms of phytoplankton diatom and dinoflagellate populations and of the nitrogen fixing cyanophyte Nodularia spumigena are common (Hodgkin and Birch, 1986).

Succession between these diverse autotrophic populations is related to the seasonal shift between allochthonous and autochthonous phosphorus


Fig. 9.10. The successional pattern between phytoplankton (pelagic chlorophyll) and the macroalga Cladophora sp. (biomass in dry weight) in the subtropical choked Peel-Harvey Estuary (Australia). Adapted from Birch and Gabrielson (1984).

supply, residence times of water, and salinity (Hodgkin and Birch, 1982, 1986; Birch and Gabrielson, 1984). Phytoplankton diatom blooms thrive on new nutrients from riverine input during the wet season, the Nodularia blooms take over after collapse and decomposition of the diatom blooms and are enhanced by nutrient supply from the bottom at the onset of the dry season. After decomposition of the cyanophyte blooms, phytoplankton and benthic macroalgae are sustained by nutrients from pelagic and benthic remineralization, until the wet season begins (Gordon et al., 1981b; McComb et al . , 1981; Hodgkin and Birch, 1982; Birch et al., 1983; Hodgkin and Birch, 1986; McComb and Lukatelich, 1986). The characteristic pattern of succession between pelagic and benthic primary producers is given in Fig. 9.10. The effects of mass blooms are nuisance odor during decomposition, deoxy- genation of the sediments, and fish kills, especially after collapse of the cyanophyte populations. Management options for the system have been forwarded, the most obvious are diminishment of the allochthonous nutrient load, especially phosphorus, and augmentation of tidal exchange (Hodgkin and Birch, 1982,1986).

A Restricted Lagoon: Venice, Italy

Venice Lagoon is a shallow restricted Mediterranean lagoon with ample tidal exchange. Human impact is given by constant dredging of accessory channels and substantial effluent discharge from the City of Venice (Pavoni et al., 1987; Sfriso et al., 1987). Vatova (1961) established an annual phytoplankton primary production of 147 g C m-2 year', but lately, massive proliferations of benthic macroalgae and succession by phytoplankton has become a common interannual reoccurring feature (Sfriso et al., 1987). After collapse of preceding macroalgae, the sediment is enriched with biogenic

B. Knoppers 273

= I

W A M J J A S O N D J F W A Y 1985 we6

Fig. 9.11. Annual cycle of macroalgal biomass (a), pelagic chlorophj I), and surface sediment content of total nitrogen and phosphorus (c) in the mediterranean leaky Laguna di Venezia (Italy). Adapted from Sfriso et al. (1987).

matter, and subsequent decomposition supplies regenerated nutrients for the sustenance of a phytoplankton bloom (Sfriso et al., 1987; Fig. 9.11). Although the successional pattern resembles the one described for the Peel-Harvey system, phytoplankton succession with the absence of cyanophyte blooms is less dynamic, probably due to larger tidal exchange.

Arid Choked to Leaky Lagoons: Algal Mat Based Systems

Algal mats are benthic microbial communities which colonize a variety of habitats ranging from inland salt lakes, coastal lagoons with marked dry/ wet seasons, and subtidal, intertidal, and supratidal zones of arid to semi- arid eury- to hypersaline regions (Krumbein, 1981; Bauld, 1984). They are often referred to as organo-sedimentary structures built by microbial activity and sediment deposition. The microbial communities usually consist of cyanobacteria and photosynthetic green and purple bacteria, and may also harbor diatoms. Depending on population composition, they may be mor- phologically distinguished into smooth, tufted, pustular, gelatinous mats (Bauld, 1984). The different populations thrive in a vertically laminated


sequence of microlayers with diatoms and cyanobacteria at the surface followed by photosynthetic and heterotrophic bacteria respectively, and with or without intermittent inorganic microlayer deposits. As a consequence of the different physiological features of the populations and lami- nation, the mats reflect extreme vertical stratification of physicochemical properties. Their study is of particular interest to elucidate the processes involved in stromatolite formation, and as such, the evolution of photosynthesis on Earth and probable formation of associated sulfide mineral deposits, and also paleoecological reconstruction of environments (Bauld, 1984).

Exemplary studies on microbial mat primary production have been conducted in Solar Lake, Gulf of Aqaba (Cohen et al., 1977a,b,c, and 1980), a small hypersaline closed lagoon fed by seawater seepage through a barrier which separates it from the sea, in Shark Bay and Spencer Gulf, Australia, within secluded intertidal zones (Bauld et al., 1980; Bauld, 19841, Long Island Sound intertidal flats (Burkholder et al., 19651, and Laguna Guer- rero Negro and Ojo de Liebre, M6xico (Javor and Castenholz, 1984). Annual estimates of primary production are absent but daily areal rates of algal mats are substantial and comparable or may surpass phytoplankton, macroalgal, and macrophyte communities of other lagoons. Estimates for Shark Bay ranged from 0.09 to 0.48 g C m-2 d-’ and for Spencer Gulf 0.2 to 3.1 g C m-2 d-1. Extreme values were recorded in Solar Lake with 5.12 g C m-2 d-1 and in Long Island Sound with 4.45-8.1 g C m-2 d-l. This suggests the presence of high accretion rates of organic matter in these lagoons. How- ever, the largest fraction of the photosynthetically produced organic matter is rapidly remineralized at the expense of sulfate reduction by sulfate-re- ducing bacteria, which usually occurs immediately below the surface. Both processes seem to be closely correlated and sulfate reduction is supposed to be the dominant terminal microbiological process in many mats (Skyrring and Chambers, 1980). Light is the main factor regulating the vertical sequence of primary producers. Each microbial layer selectively absorbs certain wavelengths of light until the onset of limitation in deeper layers (Javor and Castenholz, 1986). Salinity and desiccation are also governing features. Algal mat based lagoons of arid and semi-arid regions have been less subject to human impact.

Global Lagoon Primary Production

The contribution of coastal lagoon primary production to global primary production is unknown and may, at present, only be induced from a tentative estimate. Barrier coasts usually backed by lagoons amount to 13.1% or 32,068 km of the world’s combined continental coastline (Leont’yev and Nikiforov, 1965; Cromwell, 1971). Nixon (1982) established a median area of 78 km2 for 97 lagoons, which corresponds to a median width of approxi-

B. Knoppers 275

mately 10 km. The total coastal lagoon area should thus amount to approximately 320,000 km2. Considering a mean annual primary production of 300 g C m-2 as being a plausible estimate for coastal lagoons, total coastal lagoon production amounts to 10" kg C year'. Global coastal lagoon production attains levels close to those estimated for upwelling regions and by a factor of four less than for estuaries where primary production per unit area is similar to that in lagoons (Table 9.6). In comparison, total coastal lagoon production does not seem impressive, but their world coverage, enclosure, and recycling and accumulation potential of matter, indicates that they play a substantial role as efficient filters and modificators in the transfer of matter between land and sea, and as such within the terrestrial-marine link of the global carbon cycle.

TABLE 9.6 Net areal primary production and total production of coastal lagoons in comparison to other marine systems of the world. System data were compiled from Lieth and Whitaker (1975), Platt and Rao (1975) and Platt et al. (1989). The lagoon estimate is from this study.

System Area Net production Total production (lo4 km2) (g c m-2 year-') kg C year-')

Ocean 332 125 Upwelling 0.4 500 Shelf 33 183 Estuaries 1.4 300 Lagoons 0.3 300

41.5 0.2 4.1 0.4 0.1

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