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Dinoflagellate Cysts as Indicators of Cultural Eutrophication in the Oslofjord, Norway
Estuarine, Coastal and Shelf Science (1999) 48, 371–382 Article No. ecss.1999.0427, available online at http://www.idealibrary.com on
Dinoflagellate Cysts as Indicators of Cultural Eutrophication in the Oslofjord, Norway B. Dalea, T. A. Thorsena and A. Fjellsa˚b a b
Department of Geology, University of Oslo, PB 1047 Blindern, N-0316 Oslo, Norway Statoil, N-4035 Stavanger, Norway
Received 16 January 1998 and accepted in revised form 13 October 1998 Dinoflagellate cyst records were analysed from four sediment cores from the inner Oslofjord. The cores covered the pre-industrial period, and the most important period of human population growth associated with industrial development of the region, from the mid-1800s to the present, including the reported development of cultural eutrophication. Comparisons between the cyst records and the known history of eutrophication suggest cyst signals that should prove useful for tracing the development of eutrophication. The eutrophication signal consisted of a doubling of total cyst concentration, and a marked increase in one species in particular, Lingulodinium machaerophorum (from <5 to around 50% of the assemblages) with increased eutrophication. In the core considered most representative of general water quality in the inner fjord, these trends reversed back to pre-industrial levels during the 1980s and 1990s when improved sewage treatment took effect. 1999 Academic Press Keywords: eutrophication; marine pollution; sewage disposal; dinoflagellates; cysts; sedimentological tracers; fjords; Norway Coast
Introduction Eutrophication is an increase in the rate of supply of organic matter to an ecosystem (Nixon, 1995), termed cultural eutrophication when this results from human activities. Cultural eutrophication has been associated with harmful effects on marine ecosystems in different parts of the world (e.g. Nixon, 1990; Rosenberg et al., 1990; Smayda, 1990; GESAMP, 1991). However, there is no automatic threat to the marine environment from eutrophication. The full range of oligotrophic to hyperotrophic conditions is found in natural environments, determined by dynamic factors such as topography, hydrography, and climate that change naturally on time scales of tens to a few hundreds of years. Many coastal ecosystems may thus be presumed have a capacity for adapting to some degree of eutrophication. Identifying cultural eutrophication and its impact on ecosystems has proved difficult, mainly because it is a process involving changes over time. Its identification therefore requires an adequate time-series of observations. Ideally, these would include: (1) the human source of the problem (e.g. nutrients from sewage outfalls, agricultural run-off and air-borne pollution), (2) effects on the environment (e.g. levels of dissolved oxygen in the water) and (3) the ecosystem (e.g. primary productivity and benthos). In 0272–7714/99/030371+12 $30.00/0
reality, such efforts have been applied only when environmental deterioration is seen to be problematic by which time adequate observations are not available (e.g. Rydberg et al., 1990). Increased primary production produces eutrophication (Nixon, 1995), but the few long-term records suggest the need for caution in assuming a simple cause and effect relationship between increased nutrients from human activities and eutrophication (Rydberg et al., 1990, though see also Richardson & Heilmann, 1995; Hickel et al., 1993). The general lack of time-series data has prompted attempts to demonstrate marine eutrophication from present-day observations (e.g. from the benthic community (Gray, 1982)), and from chemical criteria (Abdullah & Danielsen, 1992). However, most reported cultural eutrophication is based on time-series observations of changes associated with or believed to be caused by eutrophication, including: the supply of nutrients (Rosenberg et al., 1990), oxygen concentration (Johannessen & Dahl, 1996), changes in benthic communities (Baden et al., 1990) and changes in fish communities (Hansson & Rudstam, 1990). There are few such long-term records, and there is a need to develop other methods, especially methods that may be applied retrospectively. The main approaches to retrospective evaluation suggested so far utilise the record of environmental 1999 Academic Press
372 B. Dale et al.
change archived in bottom sediments. Walsh et al. (1981) postulated that the geochemically determined C:N atomic ratio in sediment could be used as an indicator of eutrophication. Others have used microfossils, for example, diatoms have proved useful indicators of eutrophication in freshwater (Stockner, 1972; Simola, 1977; Alhonen, 1979), and brackish waters (Riseberg, 1990), and benthic foraminifera are useful indicators of oxygen concentration in bottom sediments (Alve, 1991). These methods have limitations, and a more robust future strategy for assessing eutrophication should therefore involve the development of as many such methods as possible, and applying these collectively. Work reported here investigates for the first time the possibility of using dinoflagellate cysts in bottom sediments as indicators of cultural eutrophication. Dinoflagellate cysts are an important group of microfossils, used extensively for biostratigraphy and palaeoecology of sediments from Mesozoic to recent ages (Stover et al., 1996; Dale, 1996). They are also proving increasingly useful as indicators of short-term environmental change caused by climate and human pollution (Dale & Nordberg, 1993; Dale & Fjellsa˚, 1994; Dale, 1996; Sætre et al., 1997; Thorsen & Dale, 1997). The cysts used here are recovered by palynological methods; they are acid-resistant and therefore not subject to dissolution problems sometimes affecting diatoms and foraminifera. As the fossilised remains of one of the major groups of phytoplankton, the cysts have an obvious potential for recording both quantitative and qualitative changes induced by cultural eutrophication. Cultural eutrophication in the Oslofjord The Oslofjord is recognized as having undergone eutrophication (Mirza & Gray, 1978; Abdullah & Danielsen, 1992), which may be traced to increased nutrient loading due to human population growth in the region. The population increase started in the mid-1800s, and particularly after the early 1900s, the fjord received increasing amounts of sewage disposal. The innermost fjord adjacent to the city of Oslo was affected the most, as local sewage treatment plants were established in the 1930s. Two are of particular interest here: Bekkelaget—established in 1963 and upgraded significantly in 1976 and since 1983; and VEAS—established in 1982 for improved treatment of most of the sewage previously treated elsewhere (Figure 1). Natural conditions in the Oslofjord are particularly favourable for the development of cultural eutrophication. The inner fjord basins, Vestfjord and
Oslo Bekkelaget
Bunnefjorden Vestfjorden
59°50'
×
VEAS
Core Water depth × B88 0–100 m D90 > 100 m B95 V95 Sill
59°40' 10°30'
10°40'
F 1. Map of the inner Oslofjord showing the core locations and the major sills.
Bunnefjord (both 160 m deep), are separated from the outer fjord by a relatively narrow channel, Drøbak Sound, with a maximum sill depth of only 19·5 m (Figure 1). This severely restricts circulation, exchange and renewal of waters in the inner fjord (Gade, 1968). During winter, mixing processes provide nutrient replenishment within the euphotic zone, often leading to a spring bloom of predominantly diatoms, while in summer, pronounced stratification in the water column may develop which favours blooms of dinoflagellates and other small flagellates. Ruud (1968a) summarized the main evidence for cultural eutrophication in the Oslofjord, including high phytoplankton populations in the innermost fjord first recorded in 1917 (Gaarder & Gran, 1927) and a pronounced effect from pollution (Braarud & Bursa, 1939). In 1950–1951, the deep waters of innermost Bunnefjord were found to be completely void of oxygen, and contained H2S from the bottom up to a depth of 75 m (Beyer & Føyn, 1951). Reports from the first comprehensive research project on the Oslofjord and its pollution problem include Ruud (1968a,b), Beyer (1968) and Munthe-Kaas (1968). Since the 1960s, The Norwegian Institute of Water Research (NIVA) has monitored the effects of
Dinoflagellate cysts as indicators 373 T 1. Core collection data
Core
Position (N/E)
Water depth (m)
Sampling date
Location
B88 D90 B95 V95
5946.95 /1043.30 5937.6 /1037.5 5950.23 /1042.48 5948.91 /1032.85
150 200 100 100
April 1988 1990 September 1995 September 1995
Bunnefjord (inner) Drøbak Sound Bunnefjord (outer) Vestfjord
pollution on the Oslofjord. Their main conclusion is that the inner fjord has experienced eutrophication, with a corresponding reduction of dissolved oxygen in bottom waters, though the negative effects of this seem to have been reduced as a result of improved sewage treatment from the mid 1970s onwards (summarized by Magnusson & Rygg, 1988). Supportive evidence for eutrophication of the inner fjord was also suggested by Rosenberg et al. (1987). Materials and methods The work reported here was carried out in three phases. Madsen (now Fjellsa˚) analysed a sediment core from Bunnefjord collected in 1988 (core B88, Table 1), in a first attempt to examine whether dinoflagellate cysts might provide useful signals for tracing the history of marine eutrophication (Madsen, 1990). The results were promising, and in the second phase of this work, in 1990, Dale and co-workers analysed four cores from various parts of the Oslofjord as part of a joint research project with NIVA, investigating the possibility of eutrophication in the outer fjord (Dale, 1990). Results from the outer fjord proved inconclusive, but results from a core in the Drøbak Sound, adjacent to the inner fjord (D90, Table 1), gave comparable signals to those recorded from the original core from Bunnefjord. The preliminary conclusions from these studies were included in a general assessment of the possibility of using cysts as palaeoproductivity indicators (Dale & Fjellsa˚, 1994), and in a review of cysts as environmental indicators (Dale, 1996). One important result from the Bunnefjord study was the indication that the eutrophication signal reversed towards pre-eutrophication levels in the very top of the core, possibly in response to improved water quality in the inner fjord as a result of improved sewage treatment (Dale & Fjellsa˚, 1994). In phase three of this work, therefore, Thorsen in 1995 analysed a new core from Bunnefjord (B95, Table 1) to examine whether this trend continued through the seven years since the first core was studied. He also
analysed a core from Vestfjord (V95, Table 1), geographically situated between Bunnefjord and Drøbak Sound. Together, these cores provided broad coverage of the inner fjord system, allowing us to better assess the possibility that cysts may be useful indicators of the development of eutrophication. The cores were all taken with standard gravity corers; details of core collection are given in Table 1, and the location of sites is shown in Figure 1. Core B88 was sampled as 1 cm-thick slices, taken from the top and every second cm throughout; Core D90 as 101 cm slices from 0–10 cm and 102 cm slices from 10–30 cm; Cores B95 and V95 were sampled as 1 cm slices throughout. From each slice of sediment, the outer edges were trimmed off to avoid contamination from the core barrel, leaving a sample representing about 2 cm2 from the centre. Samples were dried at 50 C, weighed and subjected to standard palynological treatment involving the digestion of minerals by cold HCl, followed by warm HF (similar to Barss & Williams, 1973). The remaining organic concentrate was gently sonified to disaggregate particles, sieved to retain the >25 ìm fraction, an aliquot portion of which was mounted in glycerine jelly on a slide, and counted for cysts using an optic microscope. The results of cyst analysis were expressed both qualitatively (% occurrence of species in the assemblage) and quantitatively (cysts/g dry sediment). The cyst nomenclature used here is the combination of biological and palynological names recommended by Dale (1983), to ease comparisons between this and earlier work. Synonyms for the three main cyst types discussed here are as follows: Peridinium faeroense (cyst first described by Dale, 1977, =Pentapharsodinium dalei Indelicato & Loeblich III 1986); Lingulodinium machaerophorum (=the cyst of Gonyaulax polyedra von Stein, 1883); and Operculodinium centrocarpum (=the cyst of Gonyaulax grindleyi Reinecke, 1967). The dating of cores for this study was based on the 210 Pb-method (Pheiffer Madsen & Sørensen, 1979). The initial dates inferred for Core B88 (in Dale & Fjellsa˚, 1994) were based on another core from the
374 B. Dale et al.
0
0
0
Cysts/g sediment
Phase
75 000 150 000
30 000
60 000
Percent 0
Cysts/g sediment
20
40
60
4 5 10
C B 3
15 A 20
Depth (cm)
25
2
30 35 40 45
1
50 55 60 L. machaerophorum O. centrocarpum P. faeroense Total cysts/g
F 2. Cyst data for Core B88, Bunnefjord: total cyst concentrations; concentration and percentage values of the three most important species; and phases of development of assemblage changes.
same area, dated in 1977. This is now superseded by more reliable dates obtained on material from the other three sites (though there is no marked difference between the overall timing of eutrophication inferred from these sources). For Core D90, coring was repeated immediately at the site to obtain a duplicate core that was sampled in the same way as D90 for dating. For Cores B95 and V95, duplicate samples from the same core were used for dating. Bulk sediment samples from all three cores were dated by the Danish Isotope Centre, in Copenhagen. Depth/age plots for B95 and V95 are shown in Figure 6.
Results Statistically viable assemblages of cysts recovered from all samples, included a total of 32 species. Three species, which dominated assemblages by up to 30–
60%, accounted for almost all of the variance in the data: L. machaerophorum, O. centrocarpum and P. faeroense. Their distributions in the cores is shown, together with total cyst concentrations, in Figures 2–5. Similar changes with time in both the percentage composition of these three species and the total cyst concentrations were recorded in all the cores. Core B88 from Bunnefjord (Figure 2) No samples from this core were available for dating, but estimates were inferred, particularly for the upper 20 cm, from a dated core taken nearby in 1977 by Dr Jens Skei, from NIVA (dates shown in Dale & Fjellsa˚, 1994, Figure 2). Based on comparisons with the other cores reported here, these estimated ages appear to have been too young. The cyst data suggest four distinct phases of development:
Dinoflagellate cysts as indicators 375 Cysts/g sediment Phase Cysts/g sediment 0
0
4 5
20 000 40 000
Percent 0
0
50 000 100 000
20
40
Dating 60
1980
C B
3
A
1900
10
Depth (cm)
2
15
1700
20 1 25
1500
30
35 L. machaerophorum O. centrocarpum P. faeroense Total cysts/g
F 3. Cyst data for Core B95, Bunnefjord: total cyst concentrations; concentration and percentage values of the three most important species; and phases of development of assemblage changes.
Phase 1. The lower 30 cm (58–30 cm, probably representing the 1700s to mid 1800s) contains relatively low cyst concentrations (<20 000 g 1) in the lower 15 cm, increasing to around 50 000 g 1 at 30 cm sediment depth. Assemblages are dominated by O. centrocarpum in the lower four samples and P. faeroense (between 40 and 60%) above this. Phase 2. From 30–20 cm (probably representing the mid to latest 1800s) cyst concentrations increase from around 50 000 g 1 to between 50 000 g 1 and 75 000 g 1. L. machaerophorum increases from <5% in the lower two samples to >10% in the upper sample of this phase. O. centrocarpum and P. faeroense continue to dominate at between 30% and 50%. Phase 3. From 20–4 cm (probably representing the earliest 1900 s to about 1980) cyst concentrations show three distinct pulses of increase (A, B and C in Figure 1), centered around 17 cm (up to 115 571 g 1), 11 cm (up to 115 593 g 1) and 6 cm (up to 156 042 g 1). These mainly comprise a
marked increase in L. machaerophorum (reflected by an increase from around 10% to between 30–40%), and to a lesser extent O. centrocarpum. Phase 4. The upper two samples (probably representing the 1980s up to 1988) show reduced cyst concentrations to the lowest levels recorded since the earliest phase 1 (25 000 g 1). L. machaerophorum and O. centrocarpum continue as the dominant species (about 30–40%).
Core B95 from Bunnefjord (Figure 3) The data suggest four distinct phases of development: Phase 1. The lower 19 cm (32–13 cm, representing the 1500s up to about the mid 1800s) contains relatively low cyst concentrations (25 000– 50 000 g 1), and assemblages dominated by O. centrocarpum and P. faeroense (between 30% and 55%).
376 B. Dale et al. Cysts/g sediment Phase Cysts/g sediment 0
0
D 5
C
10 000 20 000
Percent 0
0
30 000 60 000
20
40
Dating 60
1980 3
B 10
A
1900
Depth (cm)
2
15
20 1
25 1700
30 L. machaerophorum O. centrocarpum P. faeroense Total cysts/g
F 4. Cyst data for Core V95, Vestfjord: total cyst concentrations; concentration and percentage values of the three most important species; and phases of development of assemblage changes.
Phase 2. From 13–10 cm (representing about the mid-late 1800s) contains slightly higher cyst concentrations (just over 50 000 g 1), and shows a marked increase in L. machaerophorum (from <5% to >25%). O. centrocarpum is dominant (around 40–50%), while P. faeroense remains numerically important (around 20%).
Assemblages are dominated by O. centrocarpum and P. faeroense (between 20 and 45%).
Phase 3. From 10–4 cm (representing about 1900– 80) shows three distinct pulses of increase in cyst concentration (A, B and C in Figure 3), centered around 9 cm (up to 121 628 g 1), 7 cm (up to 102 813 g 1) and 5 cm (up to 94 938 g 1). These are mainly comprised of a marked increase in L. machaerophorum, which dominates assemblages in the middle of this phase (between 40 and 60%), together with O. centrocarpum (between 20 and 40%).
Phase 1. The lower 14 cm (28–14 cm, representing the 1700s to about the mid-1800s) contains relatively low cyst concentrations (generally between 15 000 and 30 000 g 1), and assemblages dominated by P. faeroense (between 35 and 55%) and O. centrocarpum (between 20 and 35%).
Phase 4. The upper four samples (1980s to 1995) show reduced cyst concentrations to the lowest levels recorded since Phase 1 (down to 38 250 g 1).
Core V95 from Vestfjord (Figure 4) The data suggest three phases of development:
Phase 2. From 14–10 cm (representing the mid-1800s to 1900) contains about the same cyst concentrations as Phase 1. There is a marked increase in L. machaerophorum (from <5 to >20%) in assemblages dominated by P. faeroense and O. centrocarpum, as in Phase 2 assemblages from the other cores studied.
Dinoflagellate cysts as indicators 377 Cysts/g sediment Phase Cysts/g sediment 0
15 000
3000
6000
Percent 0
0
0
7500
20
40
Dating 60
D 5 1980
C 2 B
Depth (cm)
10
A 15
20
1890
1 25
30 L. machaerophorum O. centrocarpum P. faeroense Total cysts/g
F 5. Cyst data for Core D90, Drøbak Sound: total cyst concentrations; concentration and percentage values of the three most important species; and phases of development of assemblage changes.
Phase 3. The upper nine samples (representing 1900– 95) contain increased cyst concentrations (generally between 30 000 and 60 000 g 1) in which three pulses comparable to those in cores from Bunnefjord may be distinguished (A, B and C in Figure 4), with an additional pulse (D) within the 1980s. There is a marked increase in L. machaerophorum, which dominates assemblages in the middle of this phase (between 30 and 40%), together with O. centrocarpum (20–35%) and P. faeroense (10–30%).
Phase 2. The upper 19 cm (representing 1900–90) contains generally higher cyst concentrations (mostly between 7500 and 12 500 g 1) with four distinct pulses (A, B, C, and D in Figure 5). There is a marked increase in L. machaerophorum in the lower two samples from this phase (from <5 to 40%) after which this species dominates the assemblages (around 40– 50%). O. centrocarpum remains the co-dominant species (around 30–40%). Discussion
Core D90 from Drøbak Sound (Figure 5) The data suggest two phases of development: Phase 1. The lower 11 cm (30–19 cm, representing the early to late-1800s) contains generally lower cyst concentrations (between 5000 and 7500 g 1), and assemblages heavily dominated by O. centrocarpum (around 60%), with around 15% P. faeroense and <5% L. machaerophorum.
The four cores studied here provide cyst records from the three main areas of the inner Oslofjord: the innermost Bunnefjord, the outermost Drøbak Sound and the intermediate Vestfjord (Figure 1). All these records cover the most important period of population growth associated with industrial development in the region, from the mid-1800s to the present, and they provide ample coverage of the period between the early 1900s and the 1970s, which is considered to
378 B. Dale et al. Year 2000 1975 1950 1925 1900 1875 1850 1825 1800 1775
0
Depth (cm)
4
8
Core B95 Core V95 12
F 6. Age/depth plots for and V95.
210
Pb datings of cores B95
have produced the most extensive cultural eutrophication. This allows us to compare the cyst records in the sediments with the known history of cultural eutrophication, to test for any consistent changes that may be utilized as signals for tracing the development of eutrophication. The eutrophication signal New results, here, support the main conclusion presented by Dale and Fjellsa˚ (1994) and Dale (1996) that the cyst record in the inner Oslofjord does provide a eutrophication signal. The signal comprises a combination of increased total cyst concentrations and a proportional increase in L. machaerophorum. The three cores from Bunnefjord and Vestfjord contain records from before the mid-1800s, prior to the human population increase accompanying industrial development in the region (Phase 1). These data provide pre-industrial background values for comparison with subsequent changes. In all three records, total cyst concentrations increased to about double their pre-industrial values during the period of exten-
sive cultural eutrophication (phase 3, 1900–80). A similar increase is also implied for the same period in the record from Drøbak, although the core did not recover pre-industrial sediments. That overall cyst concentrations increased with the development of eutrophication is not surprising. Though only about 10% of the over 2000 known dinoflagellate species may produce acid-resistant cysts (Dale, 1996), the results here suggest that the increase in primary producers during eutrophication included also the cystforming dinoflagellates. The extent to which cyst production reflects total productivity is presently unknown, but in the meantime the data suggest a useful signal that may be applied to show relative changes. In all four cores, a massive increase in L. machaerophorum accounts for much of the increased total cyst concentration associated with eutrophication in Phase 3. This is also a proportional increase, which elevates L. machaerophorum from a minor element of the pre-industrial assemblages (<5%) to the dominant species during eutrophication (around 40–50%). In Bunnefjord and Vestfjord, the increase in L. machaerophorum seems to have begun in the mid-to late-1800s (Phase 2). The suggested importance of L. machaerophorum to the eutrophication signal was surprising (Dale, 1996). Prior to work reported here, this species was established in the literature as an indicator of lower salinities, largely due to observed increases associated with present-day river estuaries along the French coast (Morzadec-Kerfourn, 1977). Recent work has revealed high amounts of this species in shelf sediments from nutrient-enriched waters associated with upwelling off California (Santa Barbara Basin) and NW Africa (Dale, unpublished work). This, together with its association with eutrophication here, strongly suggests an alternative explanation: that increased amounts in estuaries reflected increased nutrient loads from the rivers, rather than lower salinities. Interpreting the eutrophication signal While the main elements of the eutrophication signal are shown by all four cyst records, there are differences in details that most likely reflect local environmental differences between the various sites. Core B95 contains the best record for comparison with the other cores studied—including a particularly comprehensive record of the environmental recovery from the 1970s to 1995, from a location well suited to record the positive effects of relocating much of the city’s sewage treatment to VEAS in the outer Vestfjord in 1982 (Figure 1). In contrast, cores B88 and D90 contain less record from the recovery period (by about
Dinoflagellate cysts as indicators 379
7 and 5 years, respectively), while the waters at the sites of cores V95 and D90 may well have received local increases in nutrient levels from the new VEAS treatment plant after 1982. Core B95 shows the most robust eutrophication signal, details of which may be interpreted, to some extent, based on the known ecological requirements of the main species involved. Pre-industrial assemblages are characterized by co-dominance of approximately equal amounts of O. centrocarpum and P. faeroense (around 40%), with very little L. machaerophorum (<5%). Such assemblages are typically found today in the relatively unpolluted outer Oslofjord (Bakken, 1983), and similar locations from the southern Norwegian coast (Dale, unpublished records), implying the presence of similar conditions in the preindustrial inner fjord. Little is known regarding the ecological requirements of P. faeroense, but it is a colder water species found regularly in the Spring plankton of Oslofjord (Dale, 1977). The actual amounts of this species show very little variation throughout core B95 (generally between 10 000 and 20 000 g 1), strongly implying that it was not particularly affected by eutrophication. The first response to eutrophication (in Phase 2) is signalled by an increase in cyst concentration involving first O. centrocarpum, followed by L. machaerophorum. The main response (Phase 3) is a major increase in L. machaerophorum centred around peak B in Figure 3, and bracketed by two major increases in O. centrocarpum centered around peaks A and C. Both of these are bloom species (i.e. capable of forming large populations under certain conditions), with cosmopolitan distributions (Grindley & Nel, 1970; Lewis & Hallet, 1997). O. centrocarpum is the most cosmopolitan cyst type known, found in a wide variety of brackish to fully marine environments in polar to equatorial regions globally. Peak occurrences of O. centrocarpum, here, are considered indicative of an opportunistic reponse to changing environment, as in previous studies (Dale, 1985, 1996; Thorsen et al., 1995); the first peak (A) signals a change to marked eutrophication, the second (C) the change back to more normal levels. L. machaerophorum is the cyst of Gonyaulax polyedra, the known ecology of which is summarized by Lewis and Hallet (1997). L. machaerophorum is restricted to waters with summer temperatures above about 10 C, and its biogeographical boundary on the Norwegian coast occurs just North of Trondheim (Dale, 1996). It is thus probably restricted to summer plankton in the Oslofjord. The inner Oslofjord is considered to be nutrient limited (Paasche & Erga, 1988), with the amount of nutrients remaining or recycled after the
spring bloom being one of the main factors determining the extent of summer blooms. We suggest that the massive increase of L. machaerophorum accompanying eutrophication (phase 3), here, reflects elevated nutrient levels from pollution that, particularly in late summer, allowed more extensive blooms of this species than otherwise would have been sustained. This would also explain why the main cyst-producing species in the Spring plankton, P. faeroense, was seemingly unaffected by eutrophication—since Spring plankton would not have typically experienced nutrient limitation prior to eutrophication, and therefore would not have responded to the subsequently increased nutrient levels. The reversal back to preindustrial levels of L. machaerophorum, and the reestablishment of co-dominance of O. centrocarpum and P. faeroense in Phase 4, most likely reflect the general improvement of water quality in the inner fjord after the mid-1970s noted by NIVA, and particularly the improved sewage treatment at Bekkelaget after 1976. Differences between the B95 record and those from the other three cores suggest possible effects from local environments. The less complete record from B88 shows a reversal to pre-industrial levels of cyst concentrations in Phase 4, but percentage values of L. machaerophorum remain high. At this site, both maximum cyst concentrations and highest percentage values of L. machaerophorum appear to occur later than in B95 and V95. This may reflect a greater influence of local run-off from land in this long, narrow arm of the fjord. The lack of signal reversal in the upper parts of cores V95 and D90 may well be due to locally increased nutrient levels from the VEAS sewage treatment plant, from the 1980s to the present day, in effect counterbalancing the overall improvement in water quality. Most of the effluent is thought to mix with outflowing waters from the inner fjord that would be expected to affect site D90, but some probably impinges on the nearby V95 site. Fertilisation from VEAS since the early 1980s may also account for the peaks of cyst production (D in Figures 4 and 5) recorded at these two sites, but not from the innermost fjord. Comparison with other cyst signals Two other studies of cyst records from polluted fjords are particularly appropriate to compare with the eutrophication signal described here. Sætre et al. (1997) demonstrated cyst signals from a southern Norwegian fjord (Frierfjord) heavily polluted by industrial waste and sewage effluent. In contrast to the eutrophication signal, here, with increasing pollution,
380 B. Dale et al.
they showed decreasing cyst concentrations (possibly reflecting reduced production, at least of dinoflagellates), and a shift towards more heterotrophic species (possibly reflecting reduced light penetration in the euphotic zone, or increased production of prey for the heterotrophs). While the overall conclusion must be that pollution (especially toxic industrial waste) showed a negative effect on the cyst signal, a weaker eutrophication signal is shown by a proportional increase in L. machaerophorum (from about 5–20%). However, Thorsen and Dale (1997) showed a similar cyst signal to that from Sætre et al. (1997), although the fjord studied, Norda˚svannet near Bergen, was polluted by sewage effluent reportedly without appreciable industrial waste. This suggests that Norda˚svannet received pollution that was toxic, or light was reduced in the euphotic zone, or that eutrophication from sewage effluent may produce two very different signals—depending on the prevailing conditions of the system affected. Of the various cyst signals described by Dale (1996), two are particularly interesting for comparison with the eutrophication signal: the climatic signal (for reasons discussed below) and the coastal upwelling signal (also reflecting increased nutrients). Consideration of the climatic signal is directly relevant, since before concluding that cyst signals accompanying eutrophication do indeed represent eutrophication signals, we need first to consider other possible causes. Climate has changed during the time period of interest here (Jones, 1994), and its possible influence is therefore an important consideration. Furthermore, all three of the main cyst types involved in the eutrophication signal are also important for the climatic signal: O. centrocarpum as an indicator of environmental change, as here; L. machaerophorum as an important warmer water indicator for southern Scandinavia (Dale, 1996; Thorsen et al., 1995); and P. faeroense as a colder water indicator (Dale, 1977). The cyst signal here is clearly not climatic. If it were, this would indicate abrupt warming from the mid to late-1800s up to the mid-1900s, followed by a corresponding cooling to the 1990s. Warming after the 1800s may be explained by the final emergence from the ‘ Little Ice Age ’, but climatic records show warming into the 1990s. However, the pulses of increased cyst concentration seen most clearly in Phase 3, here (A , B and C in Figures 2–5), may represent another type of climatic signal that has not been previously noted. The cyst record shows clear periodicity of around 20–30 years in Phase 3. There may also be weaker indications of similar trends prior to this, shown by small pertubations in the record, in which case the Phase 3 pulses
may have been enhanced by eutrophication, and are therefore more prominent. Climate is one of the few mechanisms that may be invoked as a possible cause of such periodicity. It is interesting, therefore, to note that oceanographers have recently identified a decadal ‘ system ’ of North Atlantic Oscillation (NAO), that together with the El Nin˜o Southern Oscillation, may have accounted for much of the variance in Northern Hemisphere extratropical winter temperatures since 1935 (Sy et al., 1997; Dickson, 1997). The hydrographic records suggesting NAO only cover the past 30 years, but if this phenomenon has previously occurred regularly, it may be expected to have produced small-scale periodic effects on the local climate of NW Europe. There are pronounced differences between the eutrophication signal, here, and the coastal upwelling signal described by Dale (1996), reflecting major differences between these two types of nutrient enrichment. Strong coastal upwelling generally favours diatoms and other phytoplankton groups, rather than dinoflagellates. This is reflected in the cyst record by a coastal upwelling signal characterized by relatively low cyst productivity (compared with increased values in the eutrophication signal), and a massive dominance of heterotrophic species thought to prey on other groups (compared with insignificant amounts of heterotrophs in the eutrophication signal). However, shelf waters enriched by nearby coastal upwelling (e.g. in both California and NW Africa) produce a cyst signal heavily dominated by L. machaerophorum, as here, a signal of natural eutrophication.
Conclusions Cultural eutrophication in the inner Oslofjord, beginning in the mid to late-1800s, developing extensively from the early to mid-1900s, and diminishing from the mid-1970s to the present-day, was accompanied by corresponding changes in the dinoflagellate cyst record from bottom sediments which is considered to constitute a eutrophication signal. The signal comprises an approximately two-fold increase in cyst productivity, together with a marked increase of one species in particular, L. machaerophorum, from <5 to around 50% of the cyst assemblage. Acknowledgements We wish to thank Dr Jens Skei from NIVA for providing dating information on an earlier core from Bunnefjord, and colleagues at NIVA who provided logistical and financial support for the research project
Dinoflagellate cysts as indicators 381
including Core D90 used here. Financial support for dating of the other cores was kindly provided by the Nansen Fund. References Abdullah, M. I. & Danielsen, M. 1992 Chemical criteria for marine eutrophication with special reference to the Oslofjord, Norway. Hydrobiologia 235, 711–722. Alhonen, P. 1979 The sedimentary record of the cultural eutrophication and pollution of lakes in Finland Archiv fuer Hydrobiologie 86, 13–26. Alve, E. 1991 Foraminifera, climatic change, and pollution: a study of late Holocene sediments in Drammensfjord, southeast Norway. The Holocene 1, 243–61. Baden, S. P., Loo, L.-O., Pihl, L. & Rosenberg R. 1990 Effects of eutrophication on benthic communities including fish: Swedish west coast. Ambio 19, 113–122. Bakken, K. 1983 En miljørettet undersøkelse av resente dinoflagellat-cyster i sedimentprøver fra Oslofjorden. Unpublished cand. scient. thesis, University of Oslo Barss, M. S. & Williams, G. L. 1973 Palynology and nannofossil processing techniques. Geological Survey of Canada Paper 73-26, 1–25. Beyer, F. 1968 Zooplankton, zoobenthos, and bottom sediments as related to pollution and water exchange in the Oslofjord. Helgolander Wissenschaftliche Meeresuntersuchungen 17, 496–509. Beyer, F. & Føyn, E. 1951 Surstoffmangel I Oslofjorden. En kritisk situasjon for fjordens dyrebestand. Naturen 75 (10), 289–306. Braarud, T. & Bursa, A. 1939 The phytoplankton of the Oslofjord 1933–34. Hvalra˚dets Skrifter 19, 1–63. Dale, B. 1977 New observations on Peridinium faeroense Paulsen (1905), and classification of small orthoperidinioid dinoflagellates. British Phycological Journal 12, 241–253. Dale, B. 1983 Dinoflagellate resting cysts: ‘ benthic plankton ’. In Survival strategies of the algae (Fryxell, G. A., ed.). Cambridge University Press, New York, pp. 69–136. Dale, B. 1985 Dinoflagellate cyst analysis of Upper Quaternary sediments in core GIK 15530-4 from the Skagerrak. Norsk Geologisk Tidsskrift 65, 97–102. Dale, B. 1990 Eutrofi-situasjonen i Ytre Oslofjord 1989, Delprosjekt 4.2 Dinoflagellatcyster i Oslofjord-sedimenter. Unpublished report to The Norwegian Institute of Water Research (NIVA), 32 pp Dale, B. 1996 Dinoflagellate cyst ecology: Modelling and geological applications. In Palynology: principles and applications (Jansonius, J. & McGregor, D. C., eds). The American Association of Stratigraphic Palynologists Foundation, Publishers Press, Salt Lake City, pp. 1249–1276. Dale, B. & Nordberg, K. 1993 Possible environmental factors regulating prehistoric and historic ‘ blooms ’ of the toxic dinoflagellate Gymnodinium catenatum in the Kattegat-Skagerrak region of Scandinavia. In Toxic Phytoplankton Blooms in the Sea (Smayda, T. J. & Shimizu, Y., eds). Elsevier, Amsterdam, pp. 53–57. Dale, B. & Fjellsa˚, A. 1994 Dinoflagellate cysts as paleoproductivity indicators: State of the art, potential, and limits. In Carbon cycling in the glacial ocean: Constraints on the ocean’s role in global change (Zahn, R., Pedersen, T. F., Kaminski, M. A. & Labeyrie, L., eds). Springer-Verlag, Berlin, pp. 521–537. Dickson, B. 1997 From the Labrador Sea to global change. Nature 386, 649–650. Gaarder, T. & Gran, H. H. 1927 Investigations of the production of plankton in the Oslo Fjord. Rapports et Proces-Verbaux des Reunions Conseil International pour l’Exploration de la Mer 42, 1–48. Gade, H. G. 1968 Horizontal and vertical exchange and diffusion in the water masses of the Oslofjord. Helgolander Wissenschaftliche Meeresuntersuchungen 17, 462–475.
GESAMP 1991 The State of the Marine Environment. Oxford: Blackwell Gray, J. S. 1982 Pollution effects on marine ecosystems. Netherlands Journal of Sea Research 16, 424–443. Grindley, J. R. & Nel, E. A. 1970 Red water and mussel poisoning at Elands Bay, December 1966. South African Fisheries Bulletin 6, 36–55. Hansson, S. & Rudstam, L. G. 1990 Eutrophication and Baltic fish communities. Ambio 19, 123–125. Hickel, W., Mangelsdorf, P. & Berg, J. 1993 The human impact in the German Bight: eutrophication during three decades (1962–1991). Helgolander Wissenschaftliche Meeresuntersuchungen 47, 243–263. Jones, P. D., 1994 Hemispherical surface air temperature variations: a reanalysis and update to 1993. Journal of Climate 7, 1794–1802. Johannessen, T. & Dahl, E. 1996 Negative trends in oxygen saturation along the Norwegian Skagerrak coast, 1927–1993: a signal of ecosystem changes due to eutrophication? Limnology and Oceanography 41, 766–778. Lewis, J & Hallet, R. 1997 Lingulodinium polyedrum (Gonyaulax polyedra) a blooming dinoflagellate. Oceanography and Marine Biology: an Annual Review 35, 97–161. Madsen, A. 1990 Dinoflagellatcyster i sediment som eutrofieringsindikator i Bunnefjorden, indre Oslofjord. Unpublished cand. scient. thesis, University of Oslo. Magnusson, J. & Rygg, B. 1988 Eutrofisituasjonen i ytre Oslofjord. Rapport 338/88, Norsk institutt for vannforskning, Oslo. Mirza, F. B. & Gray, J. S. 1978 The fauna of benthic sediments from the organically enriched Oslofjord, Norway. Journal of Experimental Marine Biology and Ecology 54, 181–204. Morzadec-Kerfourn, M.-T. 1977 Les Kystes de dinoflagelle´s dans les se´diments Re´cents le long des coˆtes Bretonnes. Revue de Micropale´ontologie 20, 157–166. Munthe-Kaas, H. 1968 Surface pollution and light extinction in the Oslofjord. Helgolander Wissenschaftliche Meeresuntersuchungen 17, 476–488. Nixon, S. W. 1990 Marine eutrophication: A growing international problem. Ambio 19, 101. Nixon, S. W. 1995 Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41, 199–219. Paasche, E. & Erga, S. R. 1988 Phosphorus and nitrogen limitation of phytoplankton in the inner Oslofjord (Norway). Sarsia 73, 229–243. Pheiffer Madsen, P. & Sørensen, J. 1979 Validation of the lead-210 dating method. Journal of Radioanalytical Chemistry 54, 39–48. Richardson, K. & Heilman, J. P. 1995 Primary production in the Kattegat: past and present. Ophelia 41, 317–328. Risberg, J. 1990 Siliceous microfossil stratigraphy in a superficial sediment core from the northwestern part of the Baltic proper. Ambio 19, 167–172. Rosenberg, R., Elmgren, R., Fleischer, S., Jonsson, P., Persson G. & Dahlin, H. 1990 Marine eutrophication case studies in Sweden. Ambio 19, 102–108. Rosenberg, R., Gray, J. S., Josefson, A. B. & Pearson, T. H. 1987 Petersen’s benthic stations revisited. II. Is the Oslofjord and eastern Skagerrak enriched ? Journal of Experimental Marine Biology and Ecology 105, 219–251. Ruud, J. T. 1968a Introduction to the studies of pollution in the Oslofjord. Helgolander Wissenschaftliche Meeresuntersuchungen 17, 455–461. Ruud, J. T. 1968b Changes since the turn of the century in the fish fauna and the fisheries of the Oslofjord. Helgolander Wissenschaftliche Meeresuntersuchungen 17, 510–517. Rydberg, L., Edler, L., Floderus, S. & Graneli, E. 1990 Interaction between supply of nutrients, primary production, sedimentation and oxygen consumption in SE Kattegat. Ambio 19, 134–141. Simola, H. 1977 Diatom succession in the formation of an annually laminated sediment in Lovoja˚vi, a small eutrophicated lake. Annales Botanici Fennici 14, 143–148.
382 B. Dale et al. Smayda, T. 1990 Novel and nuisance phytoplankton blooms in the sea: evidence for a global epidemic. In Toxic Marine Phytoplankton (Graneli, E., Sundstrøm, B., Edler, L. & Anderson, D. A., eds). Elsevier, New York, pp. 29–40. Stockner, J. G. 1972 Paleolimnology as a means of assessing eutrophication. Verhhandlungen des Internationalen Vereiningung fuer Limnologie 18, 1018–1030. Stover, L. E., Brinckhuis, H., Damassa, S. P., de Verteuil, L., Helby, R. J., Monteil, E., Partridge, A. D., Powell, A. J., Riding, J. B., Smelror, M. & Williams, G. L. 1996: Mesozoic-Tertiary dinoflagellates, acritarchs and prasinophytes. In Palynology: principles and applications (Jansonius, J. & McGregor, D. C., eds). The American Association of Stratigraphic Palynologists Foundation, Publishers Press, Salt Lake City, pp. 641–750. Sy, A., Rhein, M., Lazier, J. R. N., Koltermann, K. P., Meincke, J., Putzka, A. & Bersch, M. 1997 Surprisingly rapid spreading of newly formed intermediate waters across the North Atlantic Ocean. Nature 386, 675–679.
Sætre, M. L. L., Dale, B., Abdullah, M. I. & Sætre, G.-P. 1997 Dinoflagellate cysts as possible indicators of industrial pollution in a Norwegian fjord. Marine Environmental Research 44 (2), 167–189. Thorsen T. A., Dale, B. & Nordberg, K. 1995 ‘ Blooms ’ of the toxic dinoflagellate Gymnodinium catenatum as evidence of climatic fluctuations in the late Holocene of southwestern Scandinavia. The Holocene 5, 435–446. Thorsen, T. A. & Dale, B. 1997 Dinoflagellate cysts as indicators of pollution and past climate in a Norwegian fjord. The Holocene 7 (4), 433–446. Walsh, J., Prmuzic, E. T. & Whitledge, T. E. 1981 Fate of nutrient enrichment of continental shelves as indicated by the C/N of bottom sediments. In Ecohydrodynamics (Nihoul, J. C. J., ed.). Elsevier, Amsterdam, pp. 13–50.
Dinoflagellate Cysts as Indicators of Cultural Eutrophication in the Oslofjord, Norway B. Dalea, T. A. Thorsena and A. Fjellsa˚b a b
Department of Geology, University of Oslo, PB 1047 Blindern, N-0316 Oslo, Norway Statoil, N-4035 Stavanger, Norway
Received 16 January 1998 and accepted in revised form 13 October 1998 Dinoflagellate cyst records were analysed from four sediment cores from the inner Oslofjord. The cores covered the pre-industrial period, and the most important period of human population growth associated with industrial development of the region, from the mid-1800s to the present, including the reported development of cultural eutrophication. Comparisons between the cyst records and the known history of eutrophication suggest cyst signals that should prove useful for tracing the development of eutrophication. The eutrophication signal consisted of a doubling of total cyst concentration, and a marked increase in one species in particular, Lingulodinium machaerophorum (from <5 to around 50% of the assemblages) with increased eutrophication. In the core considered most representative of general water quality in the inner fjord, these trends reversed back to pre-industrial levels during the 1980s and 1990s when improved sewage treatment took effect. 1999 Academic Press Keywords: eutrophication; marine pollution; sewage disposal; dinoflagellates; cysts; sedimentological tracers; fjords; Norway Coast
Introduction Eutrophication is an increase in the rate of supply of organic matter to an ecosystem (Nixon, 1995), termed cultural eutrophication when this results from human activities. Cultural eutrophication has been associated with harmful effects on marine ecosystems in different parts of the world (e.g. Nixon, 1990; Rosenberg et al., 1990; Smayda, 1990; GESAMP, 1991). However, there is no automatic threat to the marine environment from eutrophication. The full range of oligotrophic to hyperotrophic conditions is found in natural environments, determined by dynamic factors such as topography, hydrography, and climate that change naturally on time scales of tens to a few hundreds of years. Many coastal ecosystems may thus be presumed have a capacity for adapting to some degree of eutrophication. Identifying cultural eutrophication and its impact on ecosystems has proved difficult, mainly because it is a process involving changes over time. Its identification therefore requires an adequate time-series of observations. Ideally, these would include: (1) the human source of the problem (e.g. nutrients from sewage outfalls, agricultural run-off and air-borne pollution), (2) effects on the environment (e.g. levels of dissolved oxygen in the water) and (3) the ecosystem (e.g. primary productivity and benthos). In 0272–7714/99/030371+12 $30.00/0
reality, such efforts have been applied only when environmental deterioration is seen to be problematic by which time adequate observations are not available (e.g. Rydberg et al., 1990). Increased primary production produces eutrophication (Nixon, 1995), but the few long-term records suggest the need for caution in assuming a simple cause and effect relationship between increased nutrients from human activities and eutrophication (Rydberg et al., 1990, though see also Richardson & Heilmann, 1995; Hickel et al., 1993). The general lack of time-series data has prompted attempts to demonstrate marine eutrophication from present-day observations (e.g. from the benthic community (Gray, 1982)), and from chemical criteria (Abdullah & Danielsen, 1992). However, most reported cultural eutrophication is based on time-series observations of changes associated with or believed to be caused by eutrophication, including: the supply of nutrients (Rosenberg et al., 1990), oxygen concentration (Johannessen & Dahl, 1996), changes in benthic communities (Baden et al., 1990) and changes in fish communities (Hansson & Rudstam, 1990). There are few such long-term records, and there is a need to develop other methods, especially methods that may be applied retrospectively. The main approaches to retrospective evaluation suggested so far utilise the record of environmental 1999 Academic Press
372 B. Dale et al.
change archived in bottom sediments. Walsh et al. (1981) postulated that the geochemically determined C:N atomic ratio in sediment could be used as an indicator of eutrophication. Others have used microfossils, for example, diatoms have proved useful indicators of eutrophication in freshwater (Stockner, 1972; Simola, 1977; Alhonen, 1979), and brackish waters (Riseberg, 1990), and benthic foraminifera are useful indicators of oxygen concentration in bottom sediments (Alve, 1991). These methods have limitations, and a more robust future strategy for assessing eutrophication should therefore involve the development of as many such methods as possible, and applying these collectively. Work reported here investigates for the first time the possibility of using dinoflagellate cysts in bottom sediments as indicators of cultural eutrophication. Dinoflagellate cysts are an important group of microfossils, used extensively for biostratigraphy and palaeoecology of sediments from Mesozoic to recent ages (Stover et al., 1996; Dale, 1996). They are also proving increasingly useful as indicators of short-term environmental change caused by climate and human pollution (Dale & Nordberg, 1993; Dale & Fjellsa˚, 1994; Dale, 1996; Sætre et al., 1997; Thorsen & Dale, 1997). The cysts used here are recovered by palynological methods; they are acid-resistant and therefore not subject to dissolution problems sometimes affecting diatoms and foraminifera. As the fossilised remains of one of the major groups of phytoplankton, the cysts have an obvious potential for recording both quantitative and qualitative changes induced by cultural eutrophication. Cultural eutrophication in the Oslofjord The Oslofjord is recognized as having undergone eutrophication (Mirza & Gray, 1978; Abdullah & Danielsen, 1992), which may be traced to increased nutrient loading due to human population growth in the region. The population increase started in the mid-1800s, and particularly after the early 1900s, the fjord received increasing amounts of sewage disposal. The innermost fjord adjacent to the city of Oslo was affected the most, as local sewage treatment plants were established in the 1930s. Two are of particular interest here: Bekkelaget—established in 1963 and upgraded significantly in 1976 and since 1983; and VEAS—established in 1982 for improved treatment of most of the sewage previously treated elsewhere (Figure 1). Natural conditions in the Oslofjord are particularly favourable for the development of cultural eutrophication. The inner fjord basins, Vestfjord and
Oslo Bekkelaget
Bunnefjorden Vestfjorden
59°50'
×
VEAS
Core Water depth × B88 0–100 m D90 > 100 m B95 V95 Sill
59°40' 10°30'
10°40'
F 1. Map of the inner Oslofjord showing the core locations and the major sills.
Bunnefjord (both 160 m deep), are separated from the outer fjord by a relatively narrow channel, Drøbak Sound, with a maximum sill depth of only 19·5 m (Figure 1). This severely restricts circulation, exchange and renewal of waters in the inner fjord (Gade, 1968). During winter, mixing processes provide nutrient replenishment within the euphotic zone, often leading to a spring bloom of predominantly diatoms, while in summer, pronounced stratification in the water column may develop which favours blooms of dinoflagellates and other small flagellates. Ruud (1968a) summarized the main evidence for cultural eutrophication in the Oslofjord, including high phytoplankton populations in the innermost fjord first recorded in 1917 (Gaarder & Gran, 1927) and a pronounced effect from pollution (Braarud & Bursa, 1939). In 1950–1951, the deep waters of innermost Bunnefjord were found to be completely void of oxygen, and contained H2S from the bottom up to a depth of 75 m (Beyer & Føyn, 1951). Reports from the first comprehensive research project on the Oslofjord and its pollution problem include Ruud (1968a,b), Beyer (1968) and Munthe-Kaas (1968). Since the 1960s, The Norwegian Institute of Water Research (NIVA) has monitored the effects of
Dinoflagellate cysts as indicators 373 T 1. Core collection data
Core
Position (N/E)
Water depth (m)
Sampling date
Location
B88 D90 B95 V95
5946.95 /1043.30 5937.6 /1037.5 5950.23 /1042.48 5948.91 /1032.85
150 200 100 100
April 1988 1990 September 1995 September 1995
Bunnefjord (inner) Drøbak Sound Bunnefjord (outer) Vestfjord
pollution on the Oslofjord. Their main conclusion is that the inner fjord has experienced eutrophication, with a corresponding reduction of dissolved oxygen in bottom waters, though the negative effects of this seem to have been reduced as a result of improved sewage treatment from the mid 1970s onwards (summarized by Magnusson & Rygg, 1988). Supportive evidence for eutrophication of the inner fjord was also suggested by Rosenberg et al. (1987). Materials and methods The work reported here was carried out in three phases. Madsen (now Fjellsa˚) analysed a sediment core from Bunnefjord collected in 1988 (core B88, Table 1), in a first attempt to examine whether dinoflagellate cysts might provide useful signals for tracing the history of marine eutrophication (Madsen, 1990). The results were promising, and in the second phase of this work, in 1990, Dale and co-workers analysed four cores from various parts of the Oslofjord as part of a joint research project with NIVA, investigating the possibility of eutrophication in the outer fjord (Dale, 1990). Results from the outer fjord proved inconclusive, but results from a core in the Drøbak Sound, adjacent to the inner fjord (D90, Table 1), gave comparable signals to those recorded from the original core from Bunnefjord. The preliminary conclusions from these studies were included in a general assessment of the possibility of using cysts as palaeoproductivity indicators (Dale & Fjellsa˚, 1994), and in a review of cysts as environmental indicators (Dale, 1996). One important result from the Bunnefjord study was the indication that the eutrophication signal reversed towards pre-eutrophication levels in the very top of the core, possibly in response to improved water quality in the inner fjord as a result of improved sewage treatment (Dale & Fjellsa˚, 1994). In phase three of this work, therefore, Thorsen in 1995 analysed a new core from Bunnefjord (B95, Table 1) to examine whether this trend continued through the seven years since the first core was studied. He also
analysed a core from Vestfjord (V95, Table 1), geographically situated between Bunnefjord and Drøbak Sound. Together, these cores provided broad coverage of the inner fjord system, allowing us to better assess the possibility that cysts may be useful indicators of the development of eutrophication. The cores were all taken with standard gravity corers; details of core collection are given in Table 1, and the location of sites is shown in Figure 1. Core B88 was sampled as 1 cm-thick slices, taken from the top and every second cm throughout; Core D90 as 101 cm slices from 0–10 cm and 102 cm slices from 10–30 cm; Cores B95 and V95 were sampled as 1 cm slices throughout. From each slice of sediment, the outer edges were trimmed off to avoid contamination from the core barrel, leaving a sample representing about 2 cm2 from the centre. Samples were dried at 50 C, weighed and subjected to standard palynological treatment involving the digestion of minerals by cold HCl, followed by warm HF (similar to Barss & Williams, 1973). The remaining organic concentrate was gently sonified to disaggregate particles, sieved to retain the >25 ìm fraction, an aliquot portion of which was mounted in glycerine jelly on a slide, and counted for cysts using an optic microscope. The results of cyst analysis were expressed both qualitatively (% occurrence of species in the assemblage) and quantitatively (cysts/g dry sediment). The cyst nomenclature used here is the combination of biological and palynological names recommended by Dale (1983), to ease comparisons between this and earlier work. Synonyms for the three main cyst types discussed here are as follows: Peridinium faeroense (cyst first described by Dale, 1977, =Pentapharsodinium dalei Indelicato & Loeblich III 1986); Lingulodinium machaerophorum (=the cyst of Gonyaulax polyedra von Stein, 1883); and Operculodinium centrocarpum (=the cyst of Gonyaulax grindleyi Reinecke, 1967). The dating of cores for this study was based on the 210 Pb-method (Pheiffer Madsen & Sørensen, 1979). The initial dates inferred for Core B88 (in Dale & Fjellsa˚, 1994) were based on another core from the
374 B. Dale et al.
0
0
0
Cysts/g sediment
Phase
75 000 150 000
30 000
60 000
Percent 0
Cysts/g sediment
20
40
60
4 5 10
C B 3
15 A 20
Depth (cm)
25
2
30 35 40 45
1
50 55 60 L. machaerophorum O. centrocarpum P. faeroense Total cysts/g
F 2. Cyst data for Core B88, Bunnefjord: total cyst concentrations; concentration and percentage values of the three most important species; and phases of development of assemblage changes.
same area, dated in 1977. This is now superseded by more reliable dates obtained on material from the other three sites (though there is no marked difference between the overall timing of eutrophication inferred from these sources). For Core D90, coring was repeated immediately at the site to obtain a duplicate core that was sampled in the same way as D90 for dating. For Cores B95 and V95, duplicate samples from the same core were used for dating. Bulk sediment samples from all three cores were dated by the Danish Isotope Centre, in Copenhagen. Depth/age plots for B95 and V95 are shown in Figure 6.
Results Statistically viable assemblages of cysts recovered from all samples, included a total of 32 species. Three species, which dominated assemblages by up to 30–
60%, accounted for almost all of the variance in the data: L. machaerophorum, O. centrocarpum and P. faeroense. Their distributions in the cores is shown, together with total cyst concentrations, in Figures 2–5. Similar changes with time in both the percentage composition of these three species and the total cyst concentrations were recorded in all the cores. Core B88 from Bunnefjord (Figure 2) No samples from this core were available for dating, but estimates were inferred, particularly for the upper 20 cm, from a dated core taken nearby in 1977 by Dr Jens Skei, from NIVA (dates shown in Dale & Fjellsa˚, 1994, Figure 2). Based on comparisons with the other cores reported here, these estimated ages appear to have been too young. The cyst data suggest four distinct phases of development:
Dinoflagellate cysts as indicators 375 Cysts/g sediment Phase Cysts/g sediment 0
0
4 5
20 000 40 000
Percent 0
0
50 000 100 000
20
40
Dating 60
1980
C B
3
A
1900
10
Depth (cm)
2
15
1700
20 1 25
1500
30
35 L. machaerophorum O. centrocarpum P. faeroense Total cysts/g
F 3. Cyst data for Core B95, Bunnefjord: total cyst concentrations; concentration and percentage values of the three most important species; and phases of development of assemblage changes.
Phase 1. The lower 30 cm (58–30 cm, probably representing the 1700s to mid 1800s) contains relatively low cyst concentrations (<20 000 g 1) in the lower 15 cm, increasing to around 50 000 g 1 at 30 cm sediment depth. Assemblages are dominated by O. centrocarpum in the lower four samples and P. faeroense (between 40 and 60%) above this. Phase 2. From 30–20 cm (probably representing the mid to latest 1800s) cyst concentrations increase from around 50 000 g 1 to between 50 000 g 1 and 75 000 g 1. L. machaerophorum increases from <5% in the lower two samples to >10% in the upper sample of this phase. O. centrocarpum and P. faeroense continue to dominate at between 30% and 50%. Phase 3. From 20–4 cm (probably representing the earliest 1900 s to about 1980) cyst concentrations show three distinct pulses of increase (A, B and C in Figure 1), centered around 17 cm (up to 115 571 g 1), 11 cm (up to 115 593 g 1) and 6 cm (up to 156 042 g 1). These mainly comprise a
marked increase in L. machaerophorum (reflected by an increase from around 10% to between 30–40%), and to a lesser extent O. centrocarpum. Phase 4. The upper two samples (probably representing the 1980s up to 1988) show reduced cyst concentrations to the lowest levels recorded since the earliest phase 1 (25 000 g 1). L. machaerophorum and O. centrocarpum continue as the dominant species (about 30–40%).
Core B95 from Bunnefjord (Figure 3) The data suggest four distinct phases of development: Phase 1. The lower 19 cm (32–13 cm, representing the 1500s up to about the mid 1800s) contains relatively low cyst concentrations (25 000– 50 000 g 1), and assemblages dominated by O. centrocarpum and P. faeroense (between 30% and 55%).
376 B. Dale et al. Cysts/g sediment Phase Cysts/g sediment 0
0
D 5
C
10 000 20 000
Percent 0
0
30 000 60 000
20
40
Dating 60
1980 3
B 10
A
1900
Depth (cm)
2
15
20 1
25 1700
30 L. machaerophorum O. centrocarpum P. faeroense Total cysts/g
F 4. Cyst data for Core V95, Vestfjord: total cyst concentrations; concentration and percentage values of the three most important species; and phases of development of assemblage changes.
Phase 2. From 13–10 cm (representing about the mid-late 1800s) contains slightly higher cyst concentrations (just over 50 000 g 1), and shows a marked increase in L. machaerophorum (from <5% to >25%). O. centrocarpum is dominant (around 40–50%), while P. faeroense remains numerically important (around 20%).
Assemblages are dominated by O. centrocarpum and P. faeroense (between 20 and 45%).
Phase 3. From 10–4 cm (representing about 1900– 80) shows three distinct pulses of increase in cyst concentration (A, B and C in Figure 3), centered around 9 cm (up to 121 628 g 1), 7 cm (up to 102 813 g 1) and 5 cm (up to 94 938 g 1). These are mainly comprised of a marked increase in L. machaerophorum, which dominates assemblages in the middle of this phase (between 40 and 60%), together with O. centrocarpum (between 20 and 40%).
Phase 1. The lower 14 cm (28–14 cm, representing the 1700s to about the mid-1800s) contains relatively low cyst concentrations (generally between 15 000 and 30 000 g 1), and assemblages dominated by P. faeroense (between 35 and 55%) and O. centrocarpum (between 20 and 35%).
Phase 4. The upper four samples (1980s to 1995) show reduced cyst concentrations to the lowest levels recorded since Phase 1 (down to 38 250 g 1).
Core V95 from Vestfjord (Figure 4) The data suggest three phases of development:
Phase 2. From 14–10 cm (representing the mid-1800s to 1900) contains about the same cyst concentrations as Phase 1. There is a marked increase in L. machaerophorum (from <5 to >20%) in assemblages dominated by P. faeroense and O. centrocarpum, as in Phase 2 assemblages from the other cores studied.
Dinoflagellate cysts as indicators 377 Cysts/g sediment Phase Cysts/g sediment 0
15 000
3000
6000
Percent 0
0
0
7500
20
40
Dating 60
D 5 1980
C 2 B
Depth (cm)
10
A 15
20
1890
1 25
30 L. machaerophorum O. centrocarpum P. faeroense Total cysts/g
F 5. Cyst data for Core D90, Drøbak Sound: total cyst concentrations; concentration and percentage values of the three most important species; and phases of development of assemblage changes.
Phase 3. The upper nine samples (representing 1900– 95) contain increased cyst concentrations (generally between 30 000 and 60 000 g 1) in which three pulses comparable to those in cores from Bunnefjord may be distinguished (A, B and C in Figure 4), with an additional pulse (D) within the 1980s. There is a marked increase in L. machaerophorum, which dominates assemblages in the middle of this phase (between 30 and 40%), together with O. centrocarpum (20–35%) and P. faeroense (10–30%).
Phase 2. The upper 19 cm (representing 1900–90) contains generally higher cyst concentrations (mostly between 7500 and 12 500 g 1) with four distinct pulses (A, B, C, and D in Figure 5). There is a marked increase in L. machaerophorum in the lower two samples from this phase (from <5 to 40%) after which this species dominates the assemblages (around 40– 50%). O. centrocarpum remains the co-dominant species (around 30–40%). Discussion
Core D90 from Drøbak Sound (Figure 5) The data suggest two phases of development: Phase 1. The lower 11 cm (30–19 cm, representing the early to late-1800s) contains generally lower cyst concentrations (between 5000 and 7500 g 1), and assemblages heavily dominated by O. centrocarpum (around 60%), with around 15% P. faeroense and <5% L. machaerophorum.
The four cores studied here provide cyst records from the three main areas of the inner Oslofjord: the innermost Bunnefjord, the outermost Drøbak Sound and the intermediate Vestfjord (Figure 1). All these records cover the most important period of population growth associated with industrial development in the region, from the mid-1800s to the present, and they provide ample coverage of the period between the early 1900s and the 1970s, which is considered to
378 B. Dale et al. Year 2000 1975 1950 1925 1900 1875 1850 1825 1800 1775
0
Depth (cm)
4
8
Core B95 Core V95 12
F 6. Age/depth plots for and V95.
210
Pb datings of cores B95
have produced the most extensive cultural eutrophication. This allows us to compare the cyst records in the sediments with the known history of cultural eutrophication, to test for any consistent changes that may be utilized as signals for tracing the development of eutrophication. The eutrophication signal New results, here, support the main conclusion presented by Dale and Fjellsa˚ (1994) and Dale (1996) that the cyst record in the inner Oslofjord does provide a eutrophication signal. The signal comprises a combination of increased total cyst concentrations and a proportional increase in L. machaerophorum. The three cores from Bunnefjord and Vestfjord contain records from before the mid-1800s, prior to the human population increase accompanying industrial development in the region (Phase 1). These data provide pre-industrial background values for comparison with subsequent changes. In all three records, total cyst concentrations increased to about double their pre-industrial values during the period of exten-
sive cultural eutrophication (phase 3, 1900–80). A similar increase is also implied for the same period in the record from Drøbak, although the core did not recover pre-industrial sediments. That overall cyst concentrations increased with the development of eutrophication is not surprising. Though only about 10% of the over 2000 known dinoflagellate species may produce acid-resistant cysts (Dale, 1996), the results here suggest that the increase in primary producers during eutrophication included also the cystforming dinoflagellates. The extent to which cyst production reflects total productivity is presently unknown, but in the meantime the data suggest a useful signal that may be applied to show relative changes. In all four cores, a massive increase in L. machaerophorum accounts for much of the increased total cyst concentration associated with eutrophication in Phase 3. This is also a proportional increase, which elevates L. machaerophorum from a minor element of the pre-industrial assemblages (<5%) to the dominant species during eutrophication (around 40–50%). In Bunnefjord and Vestfjord, the increase in L. machaerophorum seems to have begun in the mid-to late-1800s (Phase 2). The suggested importance of L. machaerophorum to the eutrophication signal was surprising (Dale, 1996). Prior to work reported here, this species was established in the literature as an indicator of lower salinities, largely due to observed increases associated with present-day river estuaries along the French coast (Morzadec-Kerfourn, 1977). Recent work has revealed high amounts of this species in shelf sediments from nutrient-enriched waters associated with upwelling off California (Santa Barbara Basin) and NW Africa (Dale, unpublished work). This, together with its association with eutrophication here, strongly suggests an alternative explanation: that increased amounts in estuaries reflected increased nutrient loads from the rivers, rather than lower salinities. Interpreting the eutrophication signal While the main elements of the eutrophication signal are shown by all four cyst records, there are differences in details that most likely reflect local environmental differences between the various sites. Core B95 contains the best record for comparison with the other cores studied—including a particularly comprehensive record of the environmental recovery from the 1970s to 1995, from a location well suited to record the positive effects of relocating much of the city’s sewage treatment to VEAS in the outer Vestfjord in 1982 (Figure 1). In contrast, cores B88 and D90 contain less record from the recovery period (by about
Dinoflagellate cysts as indicators 379
7 and 5 years, respectively), while the waters at the sites of cores V95 and D90 may well have received local increases in nutrient levels from the new VEAS treatment plant after 1982. Core B95 shows the most robust eutrophication signal, details of which may be interpreted, to some extent, based on the known ecological requirements of the main species involved. Pre-industrial assemblages are characterized by co-dominance of approximately equal amounts of O. centrocarpum and P. faeroense (around 40%), with very little L. machaerophorum (<5%). Such assemblages are typically found today in the relatively unpolluted outer Oslofjord (Bakken, 1983), and similar locations from the southern Norwegian coast (Dale, unpublished records), implying the presence of similar conditions in the preindustrial inner fjord. Little is known regarding the ecological requirements of P. faeroense, but it is a colder water species found regularly in the Spring plankton of Oslofjord (Dale, 1977). The actual amounts of this species show very little variation throughout core B95 (generally between 10 000 and 20 000 g 1), strongly implying that it was not particularly affected by eutrophication. The first response to eutrophication (in Phase 2) is signalled by an increase in cyst concentration involving first O. centrocarpum, followed by L. machaerophorum. The main response (Phase 3) is a major increase in L. machaerophorum centred around peak B in Figure 3, and bracketed by two major increases in O. centrocarpum centered around peaks A and C. Both of these are bloom species (i.e. capable of forming large populations under certain conditions), with cosmopolitan distributions (Grindley & Nel, 1970; Lewis & Hallet, 1997). O. centrocarpum is the most cosmopolitan cyst type known, found in a wide variety of brackish to fully marine environments in polar to equatorial regions globally. Peak occurrences of O. centrocarpum, here, are considered indicative of an opportunistic reponse to changing environment, as in previous studies (Dale, 1985, 1996; Thorsen et al., 1995); the first peak (A) signals a change to marked eutrophication, the second (C) the change back to more normal levels. L. machaerophorum is the cyst of Gonyaulax polyedra, the known ecology of which is summarized by Lewis and Hallet (1997). L. machaerophorum is restricted to waters with summer temperatures above about 10 C, and its biogeographical boundary on the Norwegian coast occurs just North of Trondheim (Dale, 1996). It is thus probably restricted to summer plankton in the Oslofjord. The inner Oslofjord is considered to be nutrient limited (Paasche & Erga, 1988), with the amount of nutrients remaining or recycled after the
spring bloom being one of the main factors determining the extent of summer blooms. We suggest that the massive increase of L. machaerophorum accompanying eutrophication (phase 3), here, reflects elevated nutrient levels from pollution that, particularly in late summer, allowed more extensive blooms of this species than otherwise would have been sustained. This would also explain why the main cyst-producing species in the Spring plankton, P. faeroense, was seemingly unaffected by eutrophication—since Spring plankton would not have typically experienced nutrient limitation prior to eutrophication, and therefore would not have responded to the subsequently increased nutrient levels. The reversal back to preindustrial levels of L. machaerophorum, and the reestablishment of co-dominance of O. centrocarpum and P. faeroense in Phase 4, most likely reflect the general improvement of water quality in the inner fjord after the mid-1970s noted by NIVA, and particularly the improved sewage treatment at Bekkelaget after 1976. Differences between the B95 record and those from the other three cores suggest possible effects from local environments. The less complete record from B88 shows a reversal to pre-industrial levels of cyst concentrations in Phase 4, but percentage values of L. machaerophorum remain high. At this site, both maximum cyst concentrations and highest percentage values of L. machaerophorum appear to occur later than in B95 and V95. This may reflect a greater influence of local run-off from land in this long, narrow arm of the fjord. The lack of signal reversal in the upper parts of cores V95 and D90 may well be due to locally increased nutrient levels from the VEAS sewage treatment plant, from the 1980s to the present day, in effect counterbalancing the overall improvement in water quality. Most of the effluent is thought to mix with outflowing waters from the inner fjord that would be expected to affect site D90, but some probably impinges on the nearby V95 site. Fertilisation from VEAS since the early 1980s may also account for the peaks of cyst production (D in Figures 4 and 5) recorded at these two sites, but not from the innermost fjord. Comparison with other cyst signals Two other studies of cyst records from polluted fjords are particularly appropriate to compare with the eutrophication signal described here. Sætre et al. (1997) demonstrated cyst signals from a southern Norwegian fjord (Frierfjord) heavily polluted by industrial waste and sewage effluent. In contrast to the eutrophication signal, here, with increasing pollution,
380 B. Dale et al.
they showed decreasing cyst concentrations (possibly reflecting reduced production, at least of dinoflagellates), and a shift towards more heterotrophic species (possibly reflecting reduced light penetration in the euphotic zone, or increased production of prey for the heterotrophs). While the overall conclusion must be that pollution (especially toxic industrial waste) showed a negative effect on the cyst signal, a weaker eutrophication signal is shown by a proportional increase in L. machaerophorum (from about 5–20%). However, Thorsen and Dale (1997) showed a similar cyst signal to that from Sætre et al. (1997), although the fjord studied, Norda˚svannet near Bergen, was polluted by sewage effluent reportedly without appreciable industrial waste. This suggests that Norda˚svannet received pollution that was toxic, or light was reduced in the euphotic zone, or that eutrophication from sewage effluent may produce two very different signals—depending on the prevailing conditions of the system affected. Of the various cyst signals described by Dale (1996), two are particularly interesting for comparison with the eutrophication signal: the climatic signal (for reasons discussed below) and the coastal upwelling signal (also reflecting increased nutrients). Consideration of the climatic signal is directly relevant, since before concluding that cyst signals accompanying eutrophication do indeed represent eutrophication signals, we need first to consider other possible causes. Climate has changed during the time period of interest here (Jones, 1994), and its possible influence is therefore an important consideration. Furthermore, all three of the main cyst types involved in the eutrophication signal are also important for the climatic signal: O. centrocarpum as an indicator of environmental change, as here; L. machaerophorum as an important warmer water indicator for southern Scandinavia (Dale, 1996; Thorsen et al., 1995); and P. faeroense as a colder water indicator (Dale, 1977). The cyst signal here is clearly not climatic. If it were, this would indicate abrupt warming from the mid to late-1800s up to the mid-1900s, followed by a corresponding cooling to the 1990s. Warming after the 1800s may be explained by the final emergence from the ‘ Little Ice Age ’, but climatic records show warming into the 1990s. However, the pulses of increased cyst concentration seen most clearly in Phase 3, here (A , B and C in Figures 2–5), may represent another type of climatic signal that has not been previously noted. The cyst record shows clear periodicity of around 20–30 years in Phase 3. There may also be weaker indications of similar trends prior to this, shown by small pertubations in the record, in which case the Phase 3 pulses
may have been enhanced by eutrophication, and are therefore more prominent. Climate is one of the few mechanisms that may be invoked as a possible cause of such periodicity. It is interesting, therefore, to note that oceanographers have recently identified a decadal ‘ system ’ of North Atlantic Oscillation (NAO), that together with the El Nin˜o Southern Oscillation, may have accounted for much of the variance in Northern Hemisphere extratropical winter temperatures since 1935 (Sy et al., 1997; Dickson, 1997). The hydrographic records suggesting NAO only cover the past 30 years, but if this phenomenon has previously occurred regularly, it may be expected to have produced small-scale periodic effects on the local climate of NW Europe. There are pronounced differences between the eutrophication signal, here, and the coastal upwelling signal described by Dale (1996), reflecting major differences between these two types of nutrient enrichment. Strong coastal upwelling generally favours diatoms and other phytoplankton groups, rather than dinoflagellates. This is reflected in the cyst record by a coastal upwelling signal characterized by relatively low cyst productivity (compared with increased values in the eutrophication signal), and a massive dominance of heterotrophic species thought to prey on other groups (compared with insignificant amounts of heterotrophs in the eutrophication signal). However, shelf waters enriched by nearby coastal upwelling (e.g. in both California and NW Africa) produce a cyst signal heavily dominated by L. machaerophorum, as here, a signal of natural eutrophication.
Conclusions Cultural eutrophication in the inner Oslofjord, beginning in the mid to late-1800s, developing extensively from the early to mid-1900s, and diminishing from the mid-1970s to the present-day, was accompanied by corresponding changes in the dinoflagellate cyst record from bottom sediments which is considered to constitute a eutrophication signal. The signal comprises an approximately two-fold increase in cyst productivity, together with a marked increase of one species in particular, L. machaerophorum, from <5 to around 50% of the cyst assemblage. Acknowledgements We wish to thank Dr Jens Skei from NIVA for providing dating information on an earlier core from Bunnefjord, and colleagues at NIVA who provided logistical and financial support for the research project
Dinoflagellate cysts as indicators 381
including Core D90 used here. Financial support for dating of the other cores was kindly provided by the Nansen Fund. References Abdullah, M. I. & Danielsen, M. 1992 Chemical criteria for marine eutrophication with special reference to the Oslofjord, Norway. Hydrobiologia 235, 711–722. Alhonen, P. 1979 The sedimentary record of the cultural eutrophication and pollution of lakes in Finland Archiv fuer Hydrobiologie 86, 13–26. Alve, E. 1991 Foraminifera, climatic change, and pollution: a study of late Holocene sediments in Drammensfjord, southeast Norway. The Holocene 1, 243–61. Baden, S. P., Loo, L.-O., Pihl, L. & Rosenberg R. 1990 Effects of eutrophication on benthic communities including fish: Swedish west coast. Ambio 19, 113–122. Bakken, K. 1983 En miljørettet undersøkelse av resente dinoflagellat-cyster i sedimentprøver fra Oslofjorden. Unpublished cand. scient. thesis, University of Oslo Barss, M. S. & Williams, G. L. 1973 Palynology and nannofossil processing techniques. Geological Survey of Canada Paper 73-26, 1–25. Beyer, F. 1968 Zooplankton, zoobenthos, and bottom sediments as related to pollution and water exchange in the Oslofjord. Helgolander Wissenschaftliche Meeresuntersuchungen 17, 496–509. Beyer, F. & Føyn, E. 1951 Surstoffmangel I Oslofjorden. En kritisk situasjon for fjordens dyrebestand. Naturen 75 (10), 289–306. Braarud, T. & Bursa, A. 1939 The phytoplankton of the Oslofjord 1933–34. Hvalra˚dets Skrifter 19, 1–63. Dale, B. 1977 New observations on Peridinium faeroense Paulsen (1905), and classification of small orthoperidinioid dinoflagellates. British Phycological Journal 12, 241–253. Dale, B. 1983 Dinoflagellate resting cysts: ‘ benthic plankton ’. In Survival strategies of the algae (Fryxell, G. A., ed.). Cambridge University Press, New York, pp. 69–136. Dale, B. 1985 Dinoflagellate cyst analysis of Upper Quaternary sediments in core GIK 15530-4 from the Skagerrak. Norsk Geologisk Tidsskrift 65, 97–102. Dale, B. 1990 Eutrofi-situasjonen i Ytre Oslofjord 1989, Delprosjekt 4.2 Dinoflagellatcyster i Oslofjord-sedimenter. Unpublished report to The Norwegian Institute of Water Research (NIVA), 32 pp Dale, B. 1996 Dinoflagellate cyst ecology: Modelling and geological applications. In Palynology: principles and applications (Jansonius, J. & McGregor, D. C., eds). The American Association of Stratigraphic Palynologists Foundation, Publishers Press, Salt Lake City, pp. 1249–1276. Dale, B. & Nordberg, K. 1993 Possible environmental factors regulating prehistoric and historic ‘ blooms ’ of the toxic dinoflagellate Gymnodinium catenatum in the Kattegat-Skagerrak region of Scandinavia. In Toxic Phytoplankton Blooms in the Sea (Smayda, T. J. & Shimizu, Y., eds). Elsevier, Amsterdam, pp. 53–57. Dale, B. & Fjellsa˚, A. 1994 Dinoflagellate cysts as paleoproductivity indicators: State of the art, potential, and limits. In Carbon cycling in the glacial ocean: Constraints on the ocean’s role in global change (Zahn, R., Pedersen, T. F., Kaminski, M. A. & Labeyrie, L., eds). Springer-Verlag, Berlin, pp. 521–537. Dickson, B. 1997 From the Labrador Sea to global change. Nature 386, 649–650. Gaarder, T. & Gran, H. H. 1927 Investigations of the production of plankton in the Oslo Fjord. Rapports et Proces-Verbaux des Reunions Conseil International pour l’Exploration de la Mer 42, 1–48. Gade, H. G. 1968 Horizontal and vertical exchange and diffusion in the water masses of the Oslofjord. Helgolander Wissenschaftliche Meeresuntersuchungen 17, 462–475.
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Sætre, M. L. L., Dale, B., Abdullah, M. I. & Sætre, G.-P. 1997 Dinoflagellate cysts as possible indicators of industrial pollution in a Norwegian fjord. Marine Environmental Research 44 (2), 167–189. Thorsen T. A., Dale, B. & Nordberg, K. 1995 ‘ Blooms ’ of the toxic dinoflagellate Gymnodinium catenatum as evidence of climatic fluctuations in the late Holocene of southwestern Scandinavia. The Holocene 5, 435–446. Thorsen, T. A. & Dale, B. 1997 Dinoflagellate cysts as indicators of pollution and past climate in a Norwegian fjord. The Holocene 7 (4), 433–446. Walsh, J., Prmuzic, E. T. & Whitledge, T. E. 1981 Fate of nutrient enrichment of continental shelves as indicated by the C/N of bottom sediments. In Ecohydrodynamics (Nihoul, J. C. J., ed.). Elsevier, Amsterdam, pp. 13–50.