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Hypoxia in a pristine stratified estuary (Krka, Adriatic Sea)
Marine Chemistry, 32 (1991) 347-359 Elsevier Science Publishers B.V., Amsterdam
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Hypoxia in a pristine stratified estuary (Krka, Adriatic Sea ) T. Legovi6, D. Petricioli a n d V. 7,uti6 Centerfor Marine Research, Rudjer Bo~ikovi~Institute, P.O. Box 1016, YU-41001 Zagreb (Yugoslavia) (Received February 5, 1990; revision accepted July 20, 1990)
ABSTRACT Legovi~, T., Petricioli, D. and ~uti~, V., 1991. Hypoxia in a pristine stratified estuary (Krka, Adriatic Sea). Mar. Chem., 32: 347-359. The occurrence of hypoxia in October 1988 in the Kxka estuary is described, with special reference to the Prokljan Lake. Hypoxia develops near the bottom in autumn in response to the temperature maximum that appears this time of the year. The decomposition rate of naturally present organic matter increases, creating higher biological oxygen demand. As the water column is stratified by salinity and temperature, mixing of seawater near the bottom with oxygen-supersaturated water which resides closer to the surface is very slow. When an extensive marine phytoplankton bloom appears below the halocline in the Prokljan Lake, then, because of the sinking and degradation of phytoplankton near the bottom, the dissolved oxygen concentration decreases further. The hypoxia becomes so severe that it causes massive mortality of benthic macrofauna. The decomposition of the macrofauna further decreases the dissolved oxygen concentration. The hypoxia may persist until an increase in the freshwater inflow occurs, which forces the arrival of colder marine water near the bottom via a compensating flow. In the absence of autumn rains, the hypoxia may be recorded throughout winter.
INTRODUCTION I n seas a n d l a k e s h y p o x i a o c c u r s w h e r e v e r o x y g e n c o n s u m p t i o n p r e d o m i n a t e s o v e r p r o d u c t i o n for a n e x t e n d e d p e r i o d , w h e r e m i x i n g is slow a n d w h e r e c o n t a c t w i t h t h e a t m o s p h e r e is lacking. H y p o x i a in t h e s e a h a s b e e n r e c o r d e d m a i n l y n e a r t h e b o t t o m . M o r e o f t e n t h a n in o p e n w a t e r s , h y p o x i a h a s b e e n f o u n d in s t r a t i f i e d a n d s e m i - e n c l o s e d b a y s a n d seas where, in a d d i t i o n , vertical m i x i n g n e a r t h e b o t t o m is v e r y s m a l l ( S v e r d r u p , 1938; D e u s e r , 1 9 7 5 ) . I n e s t u a r i e s , h y p o x i a is a c o n s e q u e n c e o f r a p i d d e g r a d a t i o n o f s i g n i f i c a n t q u a n t i t i e s o f o r g a n i c m a t t e r a n d , at t h e s a m e time, of small production rates by photosynthesis near the bottom. Inflow of anthropogenic organic matter and of limiting nutrients enhances phytoplank-
0304-4203/91/$03.50
© 1991 - - Elsevier Science Publishers B.V.
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ton blooms and the subsequent hypoxia (Officer et al., 1984; Justic et al., 1987 ). It is interesting, however, to see whether and to what extent hypoxia can occur in estuaries where both natural terrigenous and anthropogenic inflow of organic matter are small, and where, in addition, nutrient inflow is small. The Krka Estuary is such an example. The first report on the dissolved oxygen (O2) concentration in the Krka Estuary (Fig. 1 ) was published by Buljan ( 1969 ). The data taken on vertical profiles at 10 stations during cruises in March, June and November 1949 and December 1961 were considered. The maximum oxygen concentration was
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HYPOXIA IN A PRISTINE STRATIFIED ESTUARY
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found in March at the surface near the waterfalls, and the smallest value of 2.11 mg 02 1- l was found in December, close to the bottom in the Prokljan Lake. Buljan stated that in late autumn 'old' water appeared in the Prokljan Lake and extended up the estuary to Skradin bridge and down the estuary to Zaton. The second report on 02 concentration in the Krka Estuary was published by Buljan et al. (1980), using data that were taken during four cruises: 20-21 June, 3-5 August and 31 October-1 November 1973 and 13-15 February 1974. Maximum values were found again during the autumn cruise on the surface and the minimum value was close to the bottom. The authors noted that the oxygen concentration during the February cruise was still low in the Prokljan Lake and in the upper reach of the estuary. On the basis of seasonal cruises in the period from 1983 to 1988 (Zutir, 1984-1989 ), Gr~eti6 (1990) also hypothesized that the presence of hypoxia is caused by water that resides close to the bottom for a long time, and pointed to the dominance of decomposition processes. The purpose of this paper is to document the extent of hypoxia and to infer the sequence of events which caused the hypoxia that resulted in massive mortality of benthic macrofauna in the central part of the Krka Estuary during autumn 1988. KRKA ESTUARY
The river Krka is a karstic river that enters the Adriatic Sea. The Visovac Lake and a series of moss-covered tufa barriers and waterfalls precede the estuary and retain much of the already low sediment load. The estuary is relatively narrow, except for two wider parts: the Prokljan Lake and the area around ~ibenik harbour (Fig. 1 ). The depth gradually increases from 1-2 m below the waterfalls to 43 m near the estuary mouth. A well-defined surface brackish layer is separated from the underlying marine layer by a sharp and hence narrow halocline. The estuary is of a saltwedge type (7.uti6 and Legovir, 1987). From daily readings of the gauge near the waterfalls the flow of the Krka varies between 0.17 and 564 m 3 s -1, with the mean around 50 m 3 s- 1. Depending on the river flow, the thickness of the brackish layer has been found to vary between 0.2 and 6.3 m (Legovir, 1991 ). The exchange of freshwater in the estuary varies approximately between 6 and 20 days in spring and between 30 and 100 days in autumn. The exchange of marine water is approximately five times longer during spring and three times longer during autumn. The Krka is poor in nutrients (Buljan, 1969 ). The mean concentration of reactive phosphorus is ~ 0.1 #M (PO4) (range: < 0.01, 0.4), the mean concentration of nitrogen is ~ 18 #M (NO3) (range: 4, 45) and the mean concentration of silica is 25.8 #M (SiO4) (range: 2, 51 ) (GrSetir, 1990). How-
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ever, when compared with oligotrophic waters of the Adriatic Sea, the concentration of nutrients is an order of magnitude higher. The halocline is significantly enriched by dissolved and particulate surfaceactive organic matter of freshwater and marine phytoplankton origin (7.uti6 and Legovir, 1987; t~osovi6 and Vojvodir, 1989), Most of the freshwater phytoplankton that arrives via the waterfalls sinks through the halocline to the bottom in the estuarine reach preceding the Prokljan Lake and in the lake. The decomposing freshwater phytoplankton is the main nutrient source for the marine phytoplankton which develops below the halocline in the Prokljan Lake. In the lower part of the estuary, near ~ibenik, the main source of nutrients above the natural concentration comes from the outfalls of the town and the transshipment of phosphate ore (SekuliG 1990). As a result, in this part of the estuary the highest concentration of marine phytoplankton is found (Vili~i4 et al., 1989). MATERIALS AND METHODS
In situ measurements of temperature ( + 0.2 °C), salinity ( __+0.65%0) and 02 concentration (+0.1 mg 02 1-~ ) were performed, using type 53 and 58 YSI probes. Oxygen was also measured by the standard Winkler method (Strickland and Parsons, 1972 ). Samples were collected in 5-1 Niskin bottles. Oxygen measurements were performed during two intervals: October 2-7 and 18-21, 1988. Secchi depth was measured using a disk of 30 cm diameter. Underwater observations were performed by scuba divers on six transects along the bottom (see Fig, 4). Transects were from 50 to 300 m long. Living and dead benthic organisms were observed and identified. Also changes in color and visibility near the bottom have been recorded. Temperature was also measured at station E3 at 20-m depth during seasonal cruises from 1983 to 1989 (~utir, 1984-1989; Gr~.etir, 1990). RESULTS AND DISCUSSION
Hydrographic conditions During the period October 2-18, 1988, the weather over theKxka Estuary was calm. On October 2, the north wind (bora) decreased to zero and the weather then kept stable and mostly sunny. Inflow of the Krka River decreased from 10 m 3 s -~ on October 2 to 5 m 3 s -t on October 18. The exchange time of freshwater in the Proldjan Lake was ~ 2 months (Legovir, 1991 ). This was approximately six times longer than the mean of 10 days in October (based on the data for 1980-1986 ). The exchange o f marine water was ~ 6 months, which is about four times longer than the mean.
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The water column was stratified. The brackish water occupied the top 2 m and the rest of the water column was marine (Fig. 2). At station 8 on October 2, the temperature of the brackish layer ranged from 22.25°C at the surface to 24.7°C at the contact with marine water. Below this peak, temperature decreased with depth to 22 °C at 5 m and remained constant below this depth. Hence, the water column from the halocline down to 5 m was stratified by temperature. On October 2, the white Secchi disk depth was 6 m and the black disk depth was 2 m. This means that the bottom is above the euphotic depth. During the second observation interval, a sub-surface marine phytoplankton bloom occupying the central and northwestern parts of the Prokljan Lake was observed
(Legovi6 et al., 1991c). Dissolved oxygen concentration The 02 concentration is around the saturation value in the brackish layer (Fig. 2), because of photosynthesis of freshwater and some marine phyto-
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p l a n k t o n species. It increases below the halocline because o f p h o t o s y n t h e s i s o f exclusively m a r i n e p h y t o p l a n k t o n . Below 6-m depth, t h e O 2 c o n c e n t r a t i o n decreases with d e p t h f r o m 100% o f the s a t u r a t i o n value (6.9 m g 02 l - t ) to 65%. During October 18-21, a significant decrease o f 0 2 concentration with depth has been recorded n o t only in the Prokljan Lake b u t t h r o u g h o u t the estuary (Fig. 3). In the brackish layer a n d a few meters below the halocline, the 02 c o n c e n t r a t i o n is above s a t u r a t i o n value. T h e c o n c e n t r a t i o n decreases rapidly
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HYPOXIA IN A PRISTINE STRATIFIED ESTUARY
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as the bottom is approached. The largest vertical gradient is in the salt wedge near Skradin (station E2 ). This can be explained by two factors: the presence of larger quantities of organic matter (dissolved organic carbon (DOC) -~ 6 #g 1- l , particulate organic carbon (POC) = 1 gg 1-I ) and higher temperatures near the bottom. Both cause a higher decomposition rate and hence greater consumption of 02 than in the rest of the estuary. The vertical gradient of the oxygen decrease is not as large in the Prokljan Lake. However, the lake is deeper than the reach toward the waterfalls, and O2 concentration near the bottom may be higher, the same or lower, depending on the depth. Near the bottom at station 10 on 04.45, October 21, the lowest concentration, 0.41 mg 02 1- l , was recorded. In the lower estuary (40-m depth ), the bottom layer is colder and contains water rich in oxygen which came recently from the surrounding coastal sea. The bottom 30-m-thick layer is unstratified, and hence greater vertical mixing is expected. Although the inflow of nutrients to the surface layer is higher, hypoxia such as was found in the Prokljan Lake is unlikely to occur.
Scuba observations The bottom of the Prokljan Lake is mainly covered with mud and silt and in some places rocks were found with associated fouling communities. The most abundant fauna on the muddy and silty bottom of the Prokljan Lake is: bivalves (Bivalvia: Pecten jacobaeus, Flexopecten glabra, Chlamys varia, Ostrea edulis ); sea-snails (Gastropoda: Murex brandaris, M. trunculus, Aporhais pes-pelecani), brittle stars (Ophiuroidea: Amphiura texturata, Ophiothrix fragilis ) ; sea-urchins (Echinoidea: Psammechinus microtuberculatus, Paracentrotus lividus); sea-stars (Asteroidea: Astropecten spp., Marthasterias glacialis ); sea-cucumbers (Holothuroidea: Cucumaria plancii) and eight-rayed corals (Alcyonium palmatum, Veretillum sp.). In the sediment one finds some species of bivalves, ragworms (Polychaeta: Nereis spp., Aphrodite sp.), sipunculoid worms (Sipunculus nudus) and acorn worms (Enteropneusta: Balanoglossus sp. ). Most of the above organisms are detritus feeders, planktophages and bacteriophages, and the rest are predators and scavengers (Murex spp., Astropecten spp. and Marthasterias gracilis ).
Transect 8 (Fig. 4) (October 4; depth 9-12 m) Benthic organisms were alive. A much larger density of Pecten jacobaeus was observed than in June. However, most of the animals were lying on the surface of the sediment, whereas normally the lower shell of the organisms is buried in the sediment. This indicates that they migrated recently to this location.
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Transect 4 (October 5; depth 13 m) Most organisms were found dead. Bivalves were recently dead, except for a few oysters which were attached to the top o f 0.5-m-high boulders. Flesh was found in dead scallops, with organs present and distinguishable. Also dead
HYPOXIA IN A PRISTINE STRATIFIED ESTUARY
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were gastropods and brittle stars, except Amphiura texturata. Brittle stars were compact, which means that they had also died recently. Urchins were dead, except for some Psammechinus microtuberculatus specimens. Bristle worms and sipunculoides died recently. Sipunculoides, which were found in large numbers at this transect, must have been dead for at most 2 days, as they decompose rapidly and later cannot be seen. Sea stars, brittle stars and seacucumbers were also dead, and were compact.
Transect 7 (October 5; depth 15-16 m) All of the above organisms were found dead. The scallops contained flesh, and sipunculoides were not found. A large Marthasterias was found with flesh partially decomposed.
Transect 5 (October 19; depth 17 m) Empty shells of scallops were observed. However, no fouling on the interior side of the shells was visible yet. The organisms probably died at the same time as those that resided on transect T7. No other organisms were found.
Transect 9 (October l & depth 23-0m) Recently dead ( 1-2 days) specimens of Glossobalanus were noted at the maximum depth. These organisms live in the sediment and obtain oxygen through channels which end at the surface of the sediment. Corals and seapens whose colonies extend 20 cm above the bottom were alive (i.e. Alcyonium sp. and Veretillum sp. ). Toward the shallow part all observed organisms were alive.
Transect 6 (October 21; depth 17-0 m) This transect was ~ 300 m long and extended to the coast. The bottom at 17 m was covered with a thin organic film. Below this was a 1-cm-thick soft brownish grey mud. Deeper, the sediment was grey and more compact. Water was turbid, with visibility of 1.5 m from near the bottom to 2-3 m above the bottom. Above this layer, visibility was ~ 5 m. The macrozoobenthic organisms were dead at depths > 14 m. Only scallop shells were found, without flesh, but no fouling in the shells was detected. Frequent traces of scallops' movement were visible at depths < 15 m. Spherical aggregations of up to 200 dead brittle stars (A mphiura texturata) were found on top of protrusions that were created by benthic organisms and have dimensions of ~ 0.5 m in height and 1.3 m in diameter. Towards the top of a hill that is 12 m below the surface, some live brittle stars and urchins were found. On the hill and towards the coast at depths < 12 m the macrobenthic organisms were alive. On December 4, transect 7 was visited again. Only a few live crabs (Paguridae) and snails (Murex brandaris and M. trunculus) were found as the first invaders in the area.
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It should be pointed out that benthic mortality of the proportions described has not been recorded before and it does not seem to be a regular yearly phenomenon in the estuary. Two indications point to this conclusions, First, the m a x i m u m age of the scallops found in the Prokljan Lake was > 4 years. Second, during the subsequent year, the density of scallops was much smaller than during the 5 years monitored before the benthic mortality described above.
Origin of hypoxia Generally, the concentration of organic matter is lower in the Proldjan Lake than in the upper reach near Skradin. Temperatures near the bottom are also lower, as the Prokljan Lake is deeper. As a result, the 02 concentration near the bottom decreases to values which are, on average, slightly higher than in the upper reach. Further down, in the Sibenik area, the temperature near the bottom is even lower ( 15.5 oC at 40-m depth) and 02 concentrations are similar to those in the Prokljan Lake or somewhat higher. There are situations which may result in lower O~ concentration near the bottom of the Prokljan Lake than in the upper reach. During long periods of sunny and dry weather, phytoplankton blooms may develop in the Visovac Lake, which is located upstream from the waterfalls (Fig. 1 ). This brings larger quantities of freshwater phytoplankton through the waterfalls. The phytoplankton sinks to the halocline. Most of the sinking is compIeted from Skradin to the entrance to the Prokljan Lake (Legovi~ et al., 1991 c ). As the temperature is rather high at the lower edge of the halocline (up to 31 ~C: Legovi~ et al.. 1991 a ), decomposition is fast. Marine phytoplankton takes advantage of the nutrients released and a bloom develops in Prokljan Lake. Rapid sinking and decomposition of such a bloom may cause severe hypoxia on the bottom. One such bloom was present at the northwestern side of the Prokljan Lake during the second interval of measurements (Legovi6 et al., 199 l c). The decomposition of algae originating from this bloom increased hypoxia on the bottom of the Prokljan Lake. When 02 concentration drops below 1 mg 02 l- ' at a temperature of 22 ° C, this is followed by mortality of most of the macrozoobenthic organisms, which are either buried in the sediment or are too slow to escape. The organisms most sensitive to low 02 concentration belong to the bivalves, brittle stars and sea-cucumbers (Theede et al.. 1969 ). In nearly anoxic conditions, even organisms which are more resistant to oxygen insufficiently but which cannot move fast die (Sipunculoidea, Enteropneusta and Polycheta). When these organisms die all at once, the larger quantity of organic matter is subject to mineralization, which further decreases the 02 concentration and hence severe hypoxia may persist longer. How long it will persist depends on the appearance of the first intensive rains, which increase the discharge of the river Krka. This in turn increases the exchange rate of seawater in the Prokljan Lake through compensatory flow (Legovi6. 1991 ).
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As a consequence, the layer near the bottom is partially renewed with marine water that has a higher concentration of oxygen and is colder. Episodes of strong bora wind will also cause more intensive horizontal and vertical transport within the marine layer (Legovid et al., 1991b). This will result in 02 enrichment near the bottom. Why does the most intensive benthic hypoxia occur in autumn? Particulate organic matter which is brought in by the river or is generated in the water column sinks to the bottom. It is well known that the decomposition rate increases exponentially with temperature (Rudnick and Oviatt, 1986). It appears that the temperature near the bottom is highest in autumn (Fig. 5 ). In addition, during summer and autumn the marine layer is horizontally stratified by temperature, which means that vertical mixing is slower than during the rest of the year. What is so special about the hypoxia in autumn of 1988, i.e. why does such hypoxia not appear every year? Here we shall not enter into long-term arguments (Justi6 et al., 1987), as our data reach back only 5 years. Hence, our discussion will focus only on year-to-year differences. In comparison with several earlier years, autumn 1988 was very dry. As a consequence, the river flow was low and the brackish layer was thin. Because of the thin brackish layer and sunny weather, a higher light intensity was available to phytoplankton in the marine layer. Hence, if given enough nutrients, marine plankton is able to develop denser blooms. Although the Krka discharge was smaller, the inflow of phytoplankton from the freshwater Visovac Lake was higher as it developed denser blooms because of the stagnant water. When the concentration of marine phytoplankion is larger than usual in 20 32 n tU a 18
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the Prokljan Lake, its sinking and decomposition cause higher oxygen demand near the bottom. As the residence time of marine water in the Prokljan Lake is longer than average, renewal with the more oxygen-rich and colder water from the sea is slower, and hence hypoxia is m o r e intensive and persists longer. CONCLUSIONS In general, we expect lower 02 concentration near the b o t t o m in the salt wedge toward the waterfalls than in the Prokljan Lake. To a smaller extent, the hypoxia also appears in front of ~ibenik. A severe hypoxia may develop in the Prokljan Lake during autumn following a marine phytoplankton bloom. The decomposition o f such a b l o o m m a y drive the 02 concentration practically to zero at depths > 10-15 m, causing massive mortality o f benthic macrofauna. The hypoxia m a y persist until the Krka river flow increases and water on the b o t t o m is renewed by the compensatory flow o f colder and oxygen-richer water. Extensive hypoxia followed by massive benthic mortality in the Prokljan Lake is expected in future during very dry autumns or an increase in anthropogenic nutrient load, ACKNOWLEDGEMENTS The authors would like to thank G. Kugpili6 for participation in the measurement programme and M. Petricioli for underwater observations. This research has been supported by the N S F of Croatia, Yugoslavia, the Commission of the European Communities, Directorate General for Science Research and D e v e l o p m e n t (project 1 CI-0333-YU), the National Park Krka and U N E P / F A O (Mediterranean Action Plan).
REFERENCES Buljan, M., 1969. Some hydrographic properties of Krka and Zrmanja estuaries (in SerboCroatian). Kr~ Jugoslavije, JAZU, 6: 303-331. Buljan, M., Stojanovski, L. and Vukadin, I., 1980. Chemical properties of water in Krka estuary with an accent on pollution (in Serbo-Croatian). Hidrografski Godi~njak 1967-77, Split, 97-122. (~osovir, B. and Vojvodir, V., 1989. Adsorption behaviour of hydrophobic fraction of organic matter in natural waters. Mar. Chem., 28:183-198. Deuser, W.G., 1975. Reducing environments. In: J.P. Riley and G. Skirrow (Editors), Chemical Oceanography, Vol. 2. Academic Press, London, pp. 1-37. Gr~etir, Z., 1990. Basic hydrologic and chemical properties of Krka estuary (in Serbo-Croatian ). Ph.D. Dissertation, Institute Rudjer Bo]kovir, Zagreb, 162 pp. JustiC D., Legovir, T. and Rottini-Sandrini, L., 1987. Trends in the oxygen content 1911-1984
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and occurrence of benthic mortality in the Northern Adriatic Sea. Estuarine Coastal Shelf Sci., 25: 435-445. Legovir, T., 1991. Exchange of water in a stratified estuary with an application to Krka (Adriatic Sea). Mar. Chem., 32: 121-135. Legovir, T., Gr'2etir, Z. and Zuti~, V., 1991 a. Subsurface temperature maximum in a stratified estuary. Mar. Chem., 32: 163-170. Legovir, T., Grietir, Z. and Smir~ir, A., 1991b. Effects of wind on a stratified estuary. Mar. Chem., 32: 153-161. Legovir, T., Vili~ir, D., Petricioli, D. and ,~,utir, V., 1991 c. Subsurface Gonyaulaxpolyedra bloom in a stratified estuary. Mar. Chem., 32: 361-374. Officer, C.B., Biggs, R.B., Taft, J.L., Cronin, L.E., Tyler, M.A. and Boynton, W.R., 1984. Chesapeake Bay anoxia: origin, development and significance. Science, 223: 22-27. Rudnick, D.T. and Oviatt, C.A., 1986. Seasonal lags between organic carbon deposition and mineralization in marine sediments. J. Mar. Res., 44:815-837. Sekulir, B., 1990. Estimation of anthropogenic sources of pollution in the Krka estuary. In: National Park Krka, State of Research and Problems of Ecosystem Protection (in Serbocroatian). Croatian Ecological Society, Zagreb (in press). Strickland, J.D.H. and Parsons, T.R., 1972. A Practical Handbook of Seawater Analysis. Fish. Res. Bd. Can. Bull., 167, 310 pp. Sverdrup, H.U., 1938. On the explanation of the oxygen minima and maxima in the oceans. J. Cons. Perm. Int. Explor. Mer, 13: 163-172. Theede, H., Ponat, A., Horoki, K. and Schliper, C., 1969. Studies on the resistance of marine bottom invertebrates to oxygen-deficiency and hydrogen sulphide. Mar. Biol., 2: 325-337. Vili~ir, D., Legovi~, T. and Zuti~, V., 1989. Vertical distribution ofphytoplankton in a stratified estuary. Aquatic Sci., 51: 32-46. Zutir, V. (Coordinator), 1984-1989. Long-term research and pollution monitoring of the Krka estuary and Kornati Archipelago. MED POL Phase II. Annual Reports. Rudjer Bogkovi6 Institute, Zagreb. Zutir, V. and Legovir, T., 1987. A film of organic matter at the freshwater/seawater interface of an estuary. Nature, 328:612-614.
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Hypoxia in a pristine stratified estuary (Krka, Adriatic Sea ) T. Legovi6, D. Petricioli a n d V. 7,uti6 Centerfor Marine Research, Rudjer Bo~ikovi~Institute, P.O. Box 1016, YU-41001 Zagreb (Yugoslavia) (Received February 5, 1990; revision accepted July 20, 1990)
ABSTRACT Legovi~, T., Petricioli, D. and ~uti~, V., 1991. Hypoxia in a pristine stratified estuary (Krka, Adriatic Sea). Mar. Chem., 32: 347-359. The occurrence of hypoxia in October 1988 in the Kxka estuary is described, with special reference to the Prokljan Lake. Hypoxia develops near the bottom in autumn in response to the temperature maximum that appears this time of the year. The decomposition rate of naturally present organic matter increases, creating higher biological oxygen demand. As the water column is stratified by salinity and temperature, mixing of seawater near the bottom with oxygen-supersaturated water which resides closer to the surface is very slow. When an extensive marine phytoplankton bloom appears below the halocline in the Prokljan Lake, then, because of the sinking and degradation of phytoplankton near the bottom, the dissolved oxygen concentration decreases further. The hypoxia becomes so severe that it causes massive mortality of benthic macrofauna. The decomposition of the macrofauna further decreases the dissolved oxygen concentration. The hypoxia may persist until an increase in the freshwater inflow occurs, which forces the arrival of colder marine water near the bottom via a compensating flow. In the absence of autumn rains, the hypoxia may be recorded throughout winter.
INTRODUCTION I n seas a n d l a k e s h y p o x i a o c c u r s w h e r e v e r o x y g e n c o n s u m p t i o n p r e d o m i n a t e s o v e r p r o d u c t i o n for a n e x t e n d e d p e r i o d , w h e r e m i x i n g is slow a n d w h e r e c o n t a c t w i t h t h e a t m o s p h e r e is lacking. H y p o x i a in t h e s e a h a s b e e n r e c o r d e d m a i n l y n e a r t h e b o t t o m . M o r e o f t e n t h a n in o p e n w a t e r s , h y p o x i a h a s b e e n f o u n d in s t r a t i f i e d a n d s e m i - e n c l o s e d b a y s a n d seas where, in a d d i t i o n , vertical m i x i n g n e a r t h e b o t t o m is v e r y s m a l l ( S v e r d r u p , 1938; D e u s e r , 1 9 7 5 ) . I n e s t u a r i e s , h y p o x i a is a c o n s e q u e n c e o f r a p i d d e g r a d a t i o n o f s i g n i f i c a n t q u a n t i t i e s o f o r g a n i c m a t t e r a n d , at t h e s a m e time, of small production rates by photosynthesis near the bottom. Inflow of anthropogenic organic matter and of limiting nutrients enhances phytoplank-
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ton blooms and the subsequent hypoxia (Officer et al., 1984; Justic et al., 1987 ). It is interesting, however, to see whether and to what extent hypoxia can occur in estuaries where both natural terrigenous and anthropogenic inflow of organic matter are small, and where, in addition, nutrient inflow is small. The Krka Estuary is such an example. The first report on the dissolved oxygen (O2) concentration in the Krka Estuary (Fig. 1 ) was published by Buljan ( 1969 ). The data taken on vertical profiles at 10 stations during cruises in March, June and November 1949 and December 1961 were considered. The maximum oxygen concentration was
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found in March at the surface near the waterfalls, and the smallest value of 2.11 mg 02 1- l was found in December, close to the bottom in the Prokljan Lake. Buljan stated that in late autumn 'old' water appeared in the Prokljan Lake and extended up the estuary to Skradin bridge and down the estuary to Zaton. The second report on 02 concentration in the Krka Estuary was published by Buljan et al. (1980), using data that were taken during four cruises: 20-21 June, 3-5 August and 31 October-1 November 1973 and 13-15 February 1974. Maximum values were found again during the autumn cruise on the surface and the minimum value was close to the bottom. The authors noted that the oxygen concentration during the February cruise was still low in the Prokljan Lake and in the upper reach of the estuary. On the basis of seasonal cruises in the period from 1983 to 1988 (Zutir, 1984-1989 ), Gr~eti6 (1990) also hypothesized that the presence of hypoxia is caused by water that resides close to the bottom for a long time, and pointed to the dominance of decomposition processes. The purpose of this paper is to document the extent of hypoxia and to infer the sequence of events which caused the hypoxia that resulted in massive mortality of benthic macrofauna in the central part of the Krka Estuary during autumn 1988. KRKA ESTUARY
The river Krka is a karstic river that enters the Adriatic Sea. The Visovac Lake and a series of moss-covered tufa barriers and waterfalls precede the estuary and retain much of the already low sediment load. The estuary is relatively narrow, except for two wider parts: the Prokljan Lake and the area around ~ibenik harbour (Fig. 1 ). The depth gradually increases from 1-2 m below the waterfalls to 43 m near the estuary mouth. A well-defined surface brackish layer is separated from the underlying marine layer by a sharp and hence narrow halocline. The estuary is of a saltwedge type (7.uti6 and Legovir, 1987). From daily readings of the gauge near the waterfalls the flow of the Krka varies between 0.17 and 564 m 3 s -1, with the mean around 50 m 3 s- 1. Depending on the river flow, the thickness of the brackish layer has been found to vary between 0.2 and 6.3 m (Legovir, 1991 ). The exchange of freshwater in the estuary varies approximately between 6 and 20 days in spring and between 30 and 100 days in autumn. The exchange of marine water is approximately five times longer during spring and three times longer during autumn. The Krka is poor in nutrients (Buljan, 1969 ). The mean concentration of reactive phosphorus is ~ 0.1 #M (PO4) (range: < 0.01, 0.4), the mean concentration of nitrogen is ~ 18 #M (NO3) (range: 4, 45) and the mean concentration of silica is 25.8 #M (SiO4) (range: 2, 51 ) (GrSetir, 1990). How-
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ever, when compared with oligotrophic waters of the Adriatic Sea, the concentration of nutrients is an order of magnitude higher. The halocline is significantly enriched by dissolved and particulate surfaceactive organic matter of freshwater and marine phytoplankton origin (7.uti6 and Legovir, 1987; t~osovi6 and Vojvodir, 1989), Most of the freshwater phytoplankton that arrives via the waterfalls sinks through the halocline to the bottom in the estuarine reach preceding the Prokljan Lake and in the lake. The decomposing freshwater phytoplankton is the main nutrient source for the marine phytoplankton which develops below the halocline in the Prokljan Lake. In the lower part of the estuary, near ~ibenik, the main source of nutrients above the natural concentration comes from the outfalls of the town and the transshipment of phosphate ore (SekuliG 1990). As a result, in this part of the estuary the highest concentration of marine phytoplankton is found (Vili~i4 et al., 1989). MATERIALS AND METHODS
In situ measurements of temperature ( + 0.2 °C), salinity ( __+0.65%0) and 02 concentration (+0.1 mg 02 1-~ ) were performed, using type 53 and 58 YSI probes. Oxygen was also measured by the standard Winkler method (Strickland and Parsons, 1972 ). Samples were collected in 5-1 Niskin bottles. Oxygen measurements were performed during two intervals: October 2-7 and 18-21, 1988. Secchi depth was measured using a disk of 30 cm diameter. Underwater observations were performed by scuba divers on six transects along the bottom (see Fig, 4). Transects were from 50 to 300 m long. Living and dead benthic organisms were observed and identified. Also changes in color and visibility near the bottom have been recorded. Temperature was also measured at station E3 at 20-m depth during seasonal cruises from 1983 to 1989 (~utir, 1984-1989; Gr~.etir, 1990). RESULTS AND DISCUSSION
Hydrographic conditions During the period October 2-18, 1988, the weather over theKxka Estuary was calm. On October 2, the north wind (bora) decreased to zero and the weather then kept stable and mostly sunny. Inflow of the Krka River decreased from 10 m 3 s -~ on October 2 to 5 m 3 s -t on October 18. The exchange time of freshwater in the Proldjan Lake was ~ 2 months (Legovir, 1991 ). This was approximately six times longer than the mean of 10 days in October (based on the data for 1980-1986 ). The exchange o f marine water was ~ 6 months, which is about four times longer than the mean.
HYPOXIAIN A PRISTINESTRATIFIEDESTUARY
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The water column was stratified. The brackish water occupied the top 2 m and the rest of the water column was marine (Fig. 2). At station 8 on October 2, the temperature of the brackish layer ranged from 22.25°C at the surface to 24.7°C at the contact with marine water. Below this peak, temperature decreased with depth to 22 °C at 5 m and remained constant below this depth. Hence, the water column from the halocline down to 5 m was stratified by temperature. On October 2, the white Secchi disk depth was 6 m and the black disk depth was 2 m. This means that the bottom is above the euphotic depth. During the second observation interval, a sub-surface marine phytoplankton bloom occupying the central and northwestern parts of the Prokljan Lake was observed
(Legovi6 et al., 1991c). Dissolved oxygen concentration The 02 concentration is around the saturation value in the brackish layer (Fig. 2), because of photosynthesis of freshwater and some marine phyto-
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p l a n k t o n species. It increases below the halocline because o f p h o t o s y n t h e s i s o f exclusively m a r i n e p h y t o p l a n k t o n . Below 6-m depth, t h e O 2 c o n c e n t r a t i o n decreases with d e p t h f r o m 100% o f the s a t u r a t i o n value (6.9 m g 02 l - t ) to 65%. During October 18-21, a significant decrease o f 0 2 concentration with depth has been recorded n o t only in the Prokljan Lake b u t t h r o u g h o u t the estuary (Fig. 3). In the brackish layer a n d a few meters below the halocline, the 02 c o n c e n t r a t i o n is above s a t u r a t i o n value. T h e c o n c e n t r a t i o n decreases rapidly
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HYPOXIA IN A PRISTINE STRATIFIED ESTUARY
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as the bottom is approached. The largest vertical gradient is in the salt wedge near Skradin (station E2 ). This can be explained by two factors: the presence of larger quantities of organic matter (dissolved organic carbon (DOC) -~ 6 #g 1- l , particulate organic carbon (POC) = 1 gg 1-I ) and higher temperatures near the bottom. Both cause a higher decomposition rate and hence greater consumption of 02 than in the rest of the estuary. The vertical gradient of the oxygen decrease is not as large in the Prokljan Lake. However, the lake is deeper than the reach toward the waterfalls, and O2 concentration near the bottom may be higher, the same or lower, depending on the depth. Near the bottom at station 10 on 04.45, October 21, the lowest concentration, 0.41 mg 02 1- l , was recorded. In the lower estuary (40-m depth ), the bottom layer is colder and contains water rich in oxygen which came recently from the surrounding coastal sea. The bottom 30-m-thick layer is unstratified, and hence greater vertical mixing is expected. Although the inflow of nutrients to the surface layer is higher, hypoxia such as was found in the Prokljan Lake is unlikely to occur.
Scuba observations The bottom of the Prokljan Lake is mainly covered with mud and silt and in some places rocks were found with associated fouling communities. The most abundant fauna on the muddy and silty bottom of the Prokljan Lake is: bivalves (Bivalvia: Pecten jacobaeus, Flexopecten glabra, Chlamys varia, Ostrea edulis ); sea-snails (Gastropoda: Murex brandaris, M. trunculus, Aporhais pes-pelecani), brittle stars (Ophiuroidea: Amphiura texturata, Ophiothrix fragilis ) ; sea-urchins (Echinoidea: Psammechinus microtuberculatus, Paracentrotus lividus); sea-stars (Asteroidea: Astropecten spp., Marthasterias glacialis ); sea-cucumbers (Holothuroidea: Cucumaria plancii) and eight-rayed corals (Alcyonium palmatum, Veretillum sp.). In the sediment one finds some species of bivalves, ragworms (Polychaeta: Nereis spp., Aphrodite sp.), sipunculoid worms (Sipunculus nudus) and acorn worms (Enteropneusta: Balanoglossus sp. ). Most of the above organisms are detritus feeders, planktophages and bacteriophages, and the rest are predators and scavengers (Murex spp., Astropecten spp. and Marthasterias gracilis ).
Transect 8 (Fig. 4) (October 4; depth 9-12 m) Benthic organisms were alive. A much larger density of Pecten jacobaeus was observed than in June. However, most of the animals were lying on the surface of the sediment, whereas normally the lower shell of the organisms is buried in the sediment. This indicates that they migrated recently to this location.
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Transect 4 (October 5; depth 13 m) Most organisms were found dead. Bivalves were recently dead, except for a few oysters which were attached to the top o f 0.5-m-high boulders. Flesh was found in dead scallops, with organs present and distinguishable. Also dead
HYPOXIA IN A PRISTINE STRATIFIED ESTUARY
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were gastropods and brittle stars, except Amphiura texturata. Brittle stars were compact, which means that they had also died recently. Urchins were dead, except for some Psammechinus microtuberculatus specimens. Bristle worms and sipunculoides died recently. Sipunculoides, which were found in large numbers at this transect, must have been dead for at most 2 days, as they decompose rapidly and later cannot be seen. Sea stars, brittle stars and seacucumbers were also dead, and were compact.
Transect 7 (October 5; depth 15-16 m) All of the above organisms were found dead. The scallops contained flesh, and sipunculoides were not found. A large Marthasterias was found with flesh partially decomposed.
Transect 5 (October 19; depth 17 m) Empty shells of scallops were observed. However, no fouling on the interior side of the shells was visible yet. The organisms probably died at the same time as those that resided on transect T7. No other organisms were found.
Transect 9 (October l & depth 23-0m) Recently dead ( 1-2 days) specimens of Glossobalanus were noted at the maximum depth. These organisms live in the sediment and obtain oxygen through channels which end at the surface of the sediment. Corals and seapens whose colonies extend 20 cm above the bottom were alive (i.e. Alcyonium sp. and Veretillum sp. ). Toward the shallow part all observed organisms were alive.
Transect 6 (October 21; depth 17-0 m) This transect was ~ 300 m long and extended to the coast. The bottom at 17 m was covered with a thin organic film. Below this was a 1-cm-thick soft brownish grey mud. Deeper, the sediment was grey and more compact. Water was turbid, with visibility of 1.5 m from near the bottom to 2-3 m above the bottom. Above this layer, visibility was ~ 5 m. The macrozoobenthic organisms were dead at depths > 14 m. Only scallop shells were found, without flesh, but no fouling in the shells was detected. Frequent traces of scallops' movement were visible at depths < 15 m. Spherical aggregations of up to 200 dead brittle stars (A mphiura texturata) were found on top of protrusions that were created by benthic organisms and have dimensions of ~ 0.5 m in height and 1.3 m in diameter. Towards the top of a hill that is 12 m below the surface, some live brittle stars and urchins were found. On the hill and towards the coast at depths < 12 m the macrobenthic organisms were alive. On December 4, transect 7 was visited again. Only a few live crabs (Paguridae) and snails (Murex brandaris and M. trunculus) were found as the first invaders in the area.
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It should be pointed out that benthic mortality of the proportions described has not been recorded before and it does not seem to be a regular yearly phenomenon in the estuary. Two indications point to this conclusions, First, the m a x i m u m age of the scallops found in the Prokljan Lake was > 4 years. Second, during the subsequent year, the density of scallops was much smaller than during the 5 years monitored before the benthic mortality described above.
Origin of hypoxia Generally, the concentration of organic matter is lower in the Proldjan Lake than in the upper reach near Skradin. Temperatures near the bottom are also lower, as the Prokljan Lake is deeper. As a result, the 02 concentration near the bottom decreases to values which are, on average, slightly higher than in the upper reach. Further down, in the Sibenik area, the temperature near the bottom is even lower ( 15.5 oC at 40-m depth) and 02 concentrations are similar to those in the Prokljan Lake or somewhat higher. There are situations which may result in lower O~ concentration near the bottom of the Prokljan Lake than in the upper reach. During long periods of sunny and dry weather, phytoplankton blooms may develop in the Visovac Lake, which is located upstream from the waterfalls (Fig. 1 ). This brings larger quantities of freshwater phytoplankton through the waterfalls. The phytoplankton sinks to the halocline. Most of the sinking is compIeted from Skradin to the entrance to the Prokljan Lake (Legovi~ et al., 1991 c ). As the temperature is rather high at the lower edge of the halocline (up to 31 ~C: Legovi~ et al.. 1991 a ), decomposition is fast. Marine phytoplankton takes advantage of the nutrients released and a bloom develops in Prokljan Lake. Rapid sinking and decomposition of such a bloom may cause severe hypoxia on the bottom. One such bloom was present at the northwestern side of the Prokljan Lake during the second interval of measurements (Legovi6 et al., 199 l c). The decomposition of algae originating from this bloom increased hypoxia on the bottom of the Prokljan Lake. When 02 concentration drops below 1 mg 02 l- ' at a temperature of 22 ° C, this is followed by mortality of most of the macrozoobenthic organisms, which are either buried in the sediment or are too slow to escape. The organisms most sensitive to low 02 concentration belong to the bivalves, brittle stars and sea-cucumbers (Theede et al.. 1969 ). In nearly anoxic conditions, even organisms which are more resistant to oxygen insufficiently but which cannot move fast die (Sipunculoidea, Enteropneusta and Polycheta). When these organisms die all at once, the larger quantity of organic matter is subject to mineralization, which further decreases the 02 concentration and hence severe hypoxia may persist longer. How long it will persist depends on the appearance of the first intensive rains, which increase the discharge of the river Krka. This in turn increases the exchange rate of seawater in the Prokljan Lake through compensatory flow (Legovi6. 1991 ).
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HYPOXIA IN A PRISTINE STRATIFIED ESTUARY
As a consequence, the layer near the bottom is partially renewed with marine water that has a higher concentration of oxygen and is colder. Episodes of strong bora wind will also cause more intensive horizontal and vertical transport within the marine layer (Legovid et al., 1991b). This will result in 02 enrichment near the bottom. Why does the most intensive benthic hypoxia occur in autumn? Particulate organic matter which is brought in by the river or is generated in the water column sinks to the bottom. It is well known that the decomposition rate increases exponentially with temperature (Rudnick and Oviatt, 1986). It appears that the temperature near the bottom is highest in autumn (Fig. 5 ). In addition, during summer and autumn the marine layer is horizontally stratified by temperature, which means that vertical mixing is slower than during the rest of the year. What is so special about the hypoxia in autumn of 1988, i.e. why does such hypoxia not appear every year? Here we shall not enter into long-term arguments (Justi6 et al., 1987), as our data reach back only 5 years. Hence, our discussion will focus only on year-to-year differences. In comparison with several earlier years, autumn 1988 was very dry. As a consequence, the river flow was low and the brackish layer was thin. Because of the thin brackish layer and sunny weather, a higher light intensity was available to phytoplankton in the marine layer. Hence, if given enough nutrients, marine plankton is able to develop denser blooms. Although the Krka discharge was smaller, the inflow of phytoplankton from the freshwater Visovac Lake was higher as it developed denser blooms because of the stagnant water. When the concentration of marine phytoplankion is larger than usual in 20 32 n tU a 18
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358
r LEGOVI{~ETAL.
the Prokljan Lake, its sinking and decomposition cause higher oxygen demand near the bottom. As the residence time of marine water in the Prokljan Lake is longer than average, renewal with the more oxygen-rich and colder water from the sea is slower, and hence hypoxia is m o r e intensive and persists longer. CONCLUSIONS In general, we expect lower 02 concentration near the b o t t o m in the salt wedge toward the waterfalls than in the Prokljan Lake. To a smaller extent, the hypoxia also appears in front of ~ibenik. A severe hypoxia may develop in the Prokljan Lake during autumn following a marine phytoplankton bloom. The decomposition o f such a b l o o m m a y drive the 02 concentration practically to zero at depths > 10-15 m, causing massive mortality o f benthic macrofauna. The hypoxia m a y persist until the Krka river flow increases and water on the b o t t o m is renewed by the compensatory flow o f colder and oxygen-richer water. Extensive hypoxia followed by massive benthic mortality in the Prokljan Lake is expected in future during very dry autumns or an increase in anthropogenic nutrient load, ACKNOWLEDGEMENTS The authors would like to thank G. Kugpili6 for participation in the measurement programme and M. Petricioli for underwater observations. This research has been supported by the N S F of Croatia, Yugoslavia, the Commission of the European Communities, Directorate General for Science Research and D e v e l o p m e n t (project 1 CI-0333-YU), the National Park Krka and U N E P / F A O (Mediterranean Action Plan).
REFERENCES Buljan, M., 1969. Some hydrographic properties of Krka and Zrmanja estuaries (in SerboCroatian). Kr~ Jugoslavije, JAZU, 6: 303-331. Buljan, M., Stojanovski, L. and Vukadin, I., 1980. Chemical properties of water in Krka estuary with an accent on pollution (in Serbo-Croatian). Hidrografski Godi~njak 1967-77, Split, 97-122. (~osovir, B. and Vojvodir, V., 1989. Adsorption behaviour of hydrophobic fraction of organic matter in natural waters. Mar. Chem., 28:183-198. Deuser, W.G., 1975. Reducing environments. In: J.P. Riley and G. Skirrow (Editors), Chemical Oceanography, Vol. 2. Academic Press, London, pp. 1-37. Gr~etir, Z., 1990. Basic hydrologic and chemical properties of Krka estuary (in Serbo-Croatian ). Ph.D. Dissertation, Institute Rudjer Bo]kovir, Zagreb, 162 pp. JustiC D., Legovir, T. and Rottini-Sandrini, L., 1987. Trends in the oxygen content 1911-1984
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and occurrence of benthic mortality in the Northern Adriatic Sea. Estuarine Coastal Shelf Sci., 25: 435-445. Legovir, T., 1991. Exchange of water in a stratified estuary with an application to Krka (Adriatic Sea). Mar. Chem., 32: 121-135. Legovir, T., Gr'2etir, Z. and Zuti~, V., 1991 a. Subsurface temperature maximum in a stratified estuary. Mar. Chem., 32: 163-170. Legovir, T., Grietir, Z. and Smir~ir, A., 1991b. Effects of wind on a stratified estuary. Mar. Chem., 32: 153-161. Legovir, T., Vili~ir, D., Petricioli, D. and ,~,utir, V., 1991 c. Subsurface Gonyaulaxpolyedra bloom in a stratified estuary. Mar. Chem., 32: 361-374. Officer, C.B., Biggs, R.B., Taft, J.L., Cronin, L.E., Tyler, M.A. and Boynton, W.R., 1984. Chesapeake Bay anoxia: origin, development and significance. Science, 223: 22-27. Rudnick, D.T. and Oviatt, C.A., 1986. Seasonal lags between organic carbon deposition and mineralization in marine sediments. J. Mar. Res., 44:815-837. Sekulir, B., 1990. Estimation of anthropogenic sources of pollution in the Krka estuary. In: National Park Krka, State of Research and Problems of Ecosystem Protection (in Serbocroatian). Croatian Ecological Society, Zagreb (in press). Strickland, J.D.H. and Parsons, T.R., 1972. A Practical Handbook of Seawater Analysis. Fish. Res. Bd. Can. Bull., 167, 310 pp. Sverdrup, H.U., 1938. On the explanation of the oxygen minima and maxima in the oceans. J. Cons. Perm. Int. Explor. Mer, 13: 163-172. Theede, H., Ponat, A., Horoki, K. and Schliper, C., 1969. Studies on the resistance of marine bottom invertebrates to oxygen-deficiency and hydrogen sulphide. Mar. Biol., 2: 325-337. Vili~ir, D., Legovi~, T. and Zuti~, V., 1989. Vertical distribution ofphytoplankton in a stratified estuary. Aquatic Sci., 51: 32-46. Zutir, V. (Coordinator), 1984-1989. Long-term research and pollution monitoring of the Krka estuary and Kornati Archipelago. MED POL Phase II. Annual Reports. Rudjer Bogkovi6 Institute, Zagreb. Zutir, V. and Legovir, T., 1987. A film of organic matter at the freshwater/seawater interface of an estuary. Nature, 328:612-614.